Asami et al. Progress in Earth and Planetary Science
https://doi.org/10.1186/s40645-020-00329-z(2020) 7:15

Progress in Earth andPlanetary Science

RESEARCH ARTICLE

Open Access

Evaluation of geochemical records as apaleoenvironmental proxy in thehypercalcified demosponge Astrosclera
willeyana
Ryuji Asami1*, Akira Kinjo2, Daiki Ohshiro2, Tohru Naruse3, Masaru Mizuyama4, Ryu Uemura5, Ryuichi Shinjo2,
Yuji Ise6, Yoshihisa Fujita7 and Takashi Sakamaki8

Abstract
The geochemistry of the calcium carbonates of marine organisms is an excellent proxy for reconstruction of thepaleoceanographic history. However, previous studies of hypercalcified demosponges (sclerosponges) areconsiderably fewer than those of corals, foraminifers, and bivalves. Here, we investigated stable oxygen (δ18O) andcarbon (δ13C) isotopes and minor and trace element (Mg, Sr, Ba, Pb, and U) to Ca ratios of 36 living sclerosponges(Astrosclera willeyana) collected from Kume Island in the Ryukyu Islands, southwestern Japan, to evaluate the utilityof geochemistry as a paleoenvironmental proxy. The δ18O, δ13C, and Sr/Ca deviations of the coevally precipitatedskeleton were extremely small and almost constant at all skeletal portions, strongly suggesting that within-skeletal
variations in the chemical components are negligibly small for non-symbiotic sclerosponges. Mean δ18O, δ13C, and
Sr/Ca values (N = 36), falling within a quite narrow range, showed no significant evidence for intraspecific (interspecimen) variations in the sclerosponges. The sclerosponges δ18O and δ13C were consistent with those of thearagonites precipitated in isotopic equilibrium with seawater at the growth site. The sclerosponge Sr/Ca was close
to that of inorganically precipitated aragonite, and the estimated partition coefficient of 1.1 (almost unity) is
identical to previously reported values for different species (Ceratoporella nicholsoni). Consequently, these results
suggest that A. willeyana sclerosponge, having little vital effects on the geochemistry, is a robust indicator of
paleocean environments (seawater δ18O, temperature, and dissolved inorganic carbon δ13C). Further, our evaluation
study documents that sclerosponges living in deeper ocean environments can support the reconstruction of spatial
and vertical paleoceanographic changes in conjunction with coral proxy records. The sclerosponge U/Ca showed
little within-skeletal and intraspecific variations, but the heterogeneity and individual difference of the Mg/Ca, Ba/Ca,
and Pb/Ca were relatively large, the reasons of which still remain unresolved.
Keywords: Sclerosponge, Astrosclera willeyana, Oxygen and carbon isotopic composition, Minor and trace elements,
Isotope equilibrium, Paleoenvironmental proxy* Correspondence: ryuji.asami.b5@tohoku.ac.jp1
Institute of Geology and Paleontology, Graduate School of Science, Tohoku
University, Aobayama, Sendai 980-8578, Japan
Full list of author information is available at the end of the article© The Author(s). 2020 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
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Asami et al. Progress in Earth and Planetary Science(2020) 7:15

Introduction
The hypercalcified demosponges (“sclerosponge” hereinafter), members of the earliest branching metazoan
taxon (Porifera), have been dominant reef-building marine organisms throughout the Phanerozoic (e.g., Vacelet
1985; Reitner and Engeser 1987; Wood 1990; Reitner
1992). The taxon Astrosclera is present in the fossil record
from the Late Triassic (Vacelet 1979, 1985). In modern
coral reefs, the sclerosponges can be found in cryptic
niches of low-light environments, unlike zooxanthellatescleractinian corals (e.g., Wörheide 1998). Sclerosponges,
commonly mushroom-shaped in form, deposit a CaCO3
skeleton at a very slow growth rate of mostly less thanabout 2 mm/year and can grow for up to several hundredyears (e.g., 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 the processes underpinning climate change
and global warming, environmental proxy archives such as
trees, sediments, and corals for documenting air and sea
surface temperature variation over the last millennia areneeded (PAGES 2 k Consortium 2013; Abram et al. 2016).
The stable oxygen (δ18O) and carbon (δ13C) isotope records of sclerosponges are a useful proxy for reconstructing
seawater temperature and salinity (e.g., Wörheide 1998;
Böhm et al. 2000; Moore et al. 2000; Rosenheim et al.
2005a) and dissolved inorganic carbon δ13C of seawater(e.g., Böhm et al. 1996; Swart et al. 2010) for the past. Results of previous studies have shown that, like corals, theδ18O and δ13C values of sclerosponges have respectively
reflected interannual climate variability (Swart et al. 2002;
Grottoli 2006; Grottoli et al. 2010; Wu and Grottoli 2010)
and increasing fossil fuel CO2 in seawater (Böhm et al.
2002; Swart et al. 2010). Moreover, other minor and traceelements and isotopes can be a proxy for monitoring ocean
environments and chemistry (e.g., Lazareth et al. 2000;
Fallon et al. 2005; Rosenheim et al. 2005b; Ohmori et al.
2014). Some studies showed that sclerosponge strontium/
calcium (Sr/Ca) can offer a potential for paleotemperature
determination of seawater (e.g., Rosenheim et al. 2004;
Waite et al. 2018).
Importantly, sclerosponges can live in environmentswith less sunlight (ex. reef caves and overhangs) and at
greater water depths of up to several hundred meters in
the Indo-Pacific tropical regions (e.g., Hartman 1980)
and in the Atlantic and Caribbean regions (e.g., Druffel
and Benavides 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 vertical variations of physical and chemical parameters of seawater and generating their several-century-longtime series that overlap with and extend beyond the instrumental climate data. Nevertheless, sclerosponge-based

Page 2 of 18

reconstruction studies are extremely few (especially in the
North Pacific) relative to those of other marine CaCO3 organisms such as corals, foraminifers, and mollusks. Furthermore, evaluation and calibration studies of sclerosponges
for fidelity as a paleoenvironmental proxy are few and they
were only based on time series analyses along the growth
direction (Böhm et al. 2000; Rosenheim et al. 2005b, 2009).
Therefore, distribution (homogeneity/heterogeneity) andintraspecific difference of chemical composition in thesclerosponge skeleton should be evaluated for further robust application to paleoenvironmental reconstruction.
We investigated 36 specimens of living sclerosponges
collected in Kume Island, southwestern part of Japan in
the North Pacific to clarify (1) within-skeletal variationsin the δ18O, δ13C, and elements/Ca ratios (magnesium/
Ca (Mg/Ca), Sr/Ca, barium/Ca (Ba/Ca), lead/Ca (Pb/Ca),and uranium/Ca (U/Ca)) and (2) their intraspecific variations (individual difference = inter-specimen variations). In
addition, to evaluate the fidelity as a paleoenvironmental
proxy, we compared the isotopic values of the sclerosponge
samples to theoretically calculated values of aragonites
precipitated close to isotope equilibrium with seawaterat the living site and estimated partition coefficients forelements/Ca between seawater and aragonitic skeleton.
Knowledge acquired through the results of our evaluation study can contribute to the expansion of applications of multi-proxy reconstructions for climate andocean environmental changes and can provide insight
into a better understanding of calcium carbonate biomineralization for marine organisms.

Materials and methods
Study site and environment

The study site (26°20′12–17′′ N, 126°43′40–49′′ E) islocated off the western coast of Kume Island in the
Ryukyu Islands, southwestern Japan (Fig. 1). The climateof this region is subtropical, with atmospheric temperatures of 17–29 °C and an annual mean of 23 °C (Japan
Meteorological Agency 2016). The average annual precipitation is ca. 2100 mm/year. The warm Kuroshio
current (the western North Pacific current) flows into
the East China Sea and passes northeastward along the
Ryukyu Islands. It allows the development of coral reefs
with a high bio-diversity at Kume Island (e.g., Naruse
et al. 2012).
In situ seawater temperature and salinity at the studysite in water depths of 34–40 m were measured every 1 hfrom the 5th of October 2015 through the 13th ofNovember 2016 using data loggers (Infinity CTW; JFE
Advantech Co., Ltd. and HOBO Tidbit v2; Onset Computer Corp.). The observation data were calibrated withactual temperature and salinity measurements of seawater collected at the study site using a calibration
thermometer and a conductivity meter (CM-41X: DKK-Asami et al. Progress in Earth and Planetary Science(2020) 7:15

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Fig. 1 Maps showing Kume Island and study site locations

TOA Corp.). The in situ data for 2015–2016 are fundamentally consistent with monthly average data at a
depth of 30 m, available from the Japan Oceanographic
Data Center (JODC) for 1906–2003 (26°–27° N, 126°–
127° E; http://www.jodc.go.jp/) (Fig. 2). The seawatertemperature and salinity vary respectively, as 20 °C–
31 °C and 33.6–35.0 (psu) with annual means of 25.4 °C
and 34.6 (psu).

using a multipurpose XRD device (RINT Ultima/PC;
Rigaku Corp.) to test for the presence of calcite. Powdered samples were mounted on well-cleaned glass
slides with HCl, ethanol, and milli-Q water and were analyzed using Cu Kα radiation (40 kV, 30 mA) by scanning from 20 to 37° at a 2θ angle at 0.02° steps. SEM
imaging of the skeleton was conducted using a microscope (TM3030; Hitachi High-Tech. Corp.).

Samples

Stable isotope analyses

The hypercalcified demosponges (Astrosclera willeyana
Lister 1900) examined in this study were growing on theceiling or wall in dark submarine caves, crevasses, oroverhung of reef outer edge. In October 2015 andNovember 2016, 36 living sclerosponge samples werecollected by scuba diving. Specifically, 6 samples (KMJ40), 4 samples (KMJ-34), and 26 samples (KMJ-38) werecollected respectively at water depths of 40 m, 34 m, and
38 m (Table 1 and Fig. 3). The surfaces of samples aremostly light-to-dark brown and/or orange. The samples,
which were from 5.4 mm × 5.0 mm × 2.5 mm to 24.9mm × 18.0 mm × 11.6 mm, were rinsed three times
ultrasonically with milli-Q water (resistance = 18.2 mΩ;Millipore Corp.) and were then dried in a desiccator.
To check the mineralogy and preservation state of theskeleton, five selected sclerosponges (KMJ-38-14, KMJ38-20, KMJ-38-22, KMJ-38-25, and KMJ-38-26) were
examined using X-ray diffraction (XRD) analysis andscanning electron microscopy (SEM) (Fig. 4). At the
University of the Ryukyus, XRD analysis was conducted

For stable isotope analyses, powdered subsamples (1–20
subsamples per sclerosponge) were taken from the skeleton surface along the X-axis (= long axis) and Y-axis (=short axis) directions (see Fig. 4), to evaluate withinskeleton variations in the isotope values. The top of thesample is regarded as the coordinate origin (X = 0, Y = 0).
A subsample (Φ, 1 mm; depth, ca. 1.5 mm) was taken atintervals of 1–4 mm from the coevally precipitated skeleton using a pre-cleaned diamond drill. The common
skeletal growth rates of A. willeyana scleroponges are estimated to be about 0.2–1.9 mm/year (e.g., Wörheide 1998;
Moore et al. 2000; Fallon and Guilderson 2005; Fallon
et al. 2005; Grottoli et al. 2010). The tissue layer in A. willeyana can occupy upwards of about 5 mm and the time
between initial deposition and secondary infilling of aragonite skeleton appears to be several years (Fallon et al.
2005; Allison et al. 2012). Furthermore, the skeletal density of A. willeyana increases gradually with depth. That in
the surface living zone is about half that of inner structures, which is indicative of continual thickening ofAsami et al. Progress in Earth and Planetary Science(2020) 7:15

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Fig. 2 Monthly mean climatology and logging data of seawater temperature and salinity at the study site. Data are derived from the Japan
Oceanographic Data Center (JODC) for 1906–2003 (26°–27° N, 126°–127° E; http://www.jodc.go.jp/) and in situ observations made during October
2015 to November 2016 using loggers in this study. Error bars represent monthly maximum and minimum values in the past. Salinity of seawater
samples collected at the site was also measured for cross-validation

aragonite throughout the living tissue layer (Fallon et al.
2005). Considering such characteristics of skeletal growth,
the subsampling portion (Φ, ~ 1 mm; depth, ~ 1.5 mm)
probably corresponds to an increment during about a few
years, assumed to be the years 2013–2016 in this study.
Stable oxygen (δ18O) and carbon (δ13C) isotope analyses of calcium carbonate (0.14–0.16 mg) were conducted using a continuous flow isotope ratio mass
spectrometer attached to a Gasbench II and a GC-PAL
auto-sampler (Delta V Advantage; ThermoFisher Scientific Inc.) at the University of the Ryukyus, following themethod presented by Asami et al. (2015). The seawater
δ18O was measured using a cavity ring-down spectroscopy (CRDS L2130-i; Picarro Inc.) at the University of
the Ryukyus, following the method reported by Uemura
et al. (2012). Isotopic ratios were reported in the conventional δ notation relative to Vienna Pee Dee Belemnite(VPDB) for carbonate and Vienna Standard Mean Ocean
Water (VSMOW) for seawater. External precision (1σ)
throughout the entire analysis was ± 0.07‰ (δ18O) and± 0.05‰ (δ13C) for carbonate and ± 0.08‰ (δ18O) forseawater. Accuracy of the measurements of sclerosponge
samples was evaluated based on replicates of GSJ/AIST
JCp-1 (aragonite; Okai et al. 2004), yielding average δ18O
and δ13C values of − 4.65 ± 0.07‰ and − 1.59 ± 0.06‰(N = 42), which show excellent agreement with previously reported values of − 4.71‰ and − 1.63‰(Nakayama et al. 2008), respectively.
Elements/Ca analyses

Elements/Ca ratios (Mg/Ca, Sr/Ca, Ba/Ca, Pb/Ca, U/Ca)
were analyzed using an inductively coupled plasma-mass
spectrometer (XSeries II, Thermo Fisher Scientific) at
the University of the Ryukyus, basically following themethod reported by Asami et al. (2009, 2013). Eachsclerosponge powder sample (~ 0.15 mg) was dissolved
in 4.5 mL of 0.5 mol/L high-purity HNO3 diluted withultrapure Milli-Q water. Each seawater sample of 125 μL
was diluted 80 times with high-purity HNO3 and ultrapure Milli-Q water. Internal standard elements (Sc, Y,
and Yb) were added to all of the solutions to produce
equal concentrations to control matrix effect and to correct for instrumental noise. Solutions were analyzed for24
Mg, 43Ca, 44Ca, 45Sc, 87Sr, 88Sr, 89Y, 137Ba, 138Ba, 172Yb,
208
Pb, and 238U. Measurements were conducted in triplicate. Calibrations of the five gravimetric standard solutions yielded high correlation coefficients of r > 0.99998
for Ca, Mg, and Sr and of r > 0.99995 for Ba, Pb, and U.
A reference solution, gravimetrically matched to the Caconcentration of the average sclerosponge sample

(2020) 7:15

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Table 1 Details of sclerosponge samples and analytical results of geochemistry
δ13C (‰)

δ18O (‰)

Mg/Ca
Sr/Ca
Ba/Ca
Pb/Ca
U/Ca
(mmol/mol) (mmol/mol) (μmol/mol) (μmol/mol) (μmol/mol)

Avg. SD(1σ)

Avg. SD(1σ)

Avg. SD(1σ)

Avg. SD(1σ)

Avg. SD(1σ)

Avg. SD(1σ)

Avg. SD(1σ)

93.49 0.07-1.08 0.07

1.45 0.36

9.42 0.17

0.59 0.70

0.45 0.28

3.26 0.04

4.8

8

3.40 0.05-1.16 0.10

1.49 0.64

9.36 0.11

1.06 0.64

0.51 0.17

3.23 0.03

11.8

5.5

9

3.43 0.05-1.00 0.17

2.11 0.61

9.41 0.11

1.39 0.76

0.71 0.17

3.13 0.06

19.0

15.5

8.9

14 3.42 0.06

-1.00 0.11

1.59 0.25

9.52 0.15

1.90 1.02

0.63 0.15

3.25 0.02

KMJ-405

24.9

18.0

11.6

13 3.47 0.08

-1.01 0.13

1.85 0.36

9.42 0.16

2.74 0.77

N/A

3.24 0.06

KMJ-406

21.0

18.6

12.6

14 3.51 0.08

-0.75 0.12

1.33 0.38

9.58 0.19

2.97 0.69

N/A

3.21 0.07

10.3

10.2

5.9

13 3.51 0.05

-0.98 0.07

1.45 0.47

9.63 0.13

1.96 0.44

0.71 0.11

3.17 0.04

KMJ-342

12.4

11.3

6.0

12 3.45 0.09

-0.88 0.06

1.26 0.23

9.76 0.09

2.06 0.40

0.81 0.13

3.12 0.04

KMJ-343

13.9

10.8

6.8

14 3.42 0.12

-1.02 0.09

1.47 0.39

9.52 0.09

2.04 0.44

0.74 0.12

3.17 0.07

KMJ-344

15.2

13.8

11.4

17 3.44 0.07

-1.07 0.12

1.61 0.37

9.43 0.14

1.86 0.43

0.73 0.12

3.27 0.05

3.454 ±
0.024

-0.995 ±0.072

1.560 ±
0.160

9.503 ±
0.077

1.857 ±
0.451

0.663 ±
0.086

3.205 ±
0.033

SampleID

Collection
Date

Water
Depth
(m)

Size

40

9.4

8.8

6.0

KMJ-402

11.4

7.9

KMJ-403

12.3

KMJ-404

KMJ-40- 6-Oct-15
1

KMJ-34- 7-Oct-15
1

34

N

X
Y
H
(mm) (mm) (mm)ALL (KMJ-34 and -40): 95%
CL
KMJ-38- 13-Nov-16 38
1

14.7

13.2

8.8

16 3.41 0.05

-0.98 0.06

1.31 0.32

9.15 0.17

1.44 0.94

N/A

3.27 0.14

KMJ-382

17.7

12.5

10.5

18 3.40 0.05

-1.01 0.16

1.29 0.34

9.27 0.28

1.47 1.11

N/A

3.24 0.12

KMJ-383

5.4

5.0

2.5

1

3.37

-1.17

2.14

9.26

N/A

N/A

3.36

KMJ-384

6.0

5.7

2.0

1

3.48

-0.95

1.40

9.29

N/A

0.08

3.27

KMJ-385

6.0

6.0

3.0

1

3.44

-0.99

1.45

9.55

N/A

0.53

3.42

KMJ-386

7.2

6.9

3.5

5

3.36 0.02-0.89 0.10

1.78 0.51

9.43 0.28

0.59 1.07

N/A

3.29 0.10

KMJ-387

7.8

7.1

3.0

5

3.38 0.03-0.95 0.08

1.67 0.17

9.45 0.16

0.75 0.99

N/A

3.40 0.15

KMJ-388

7.7

7.2

4.0

5

3.34 0.05-1.02 0.09

1.33 0.20

9.35 0.12

0.31 0.29

N/A

3.54 0.08

KMJ-389

9.7

8.7

4.0

5

3.38 0.04-1.00 0.09

0.95 0.10

9.74 0.08

N/A

2.32 1.64

3.35 0.06

KMJ-3810

10.0

9.9

6.0

5

3.41 0.05-0.93 0.03

1.07 0.129.80 0.15

0.43 0.97

0.98 0.75

3.34 0.14

KMJ-3811

11.0

10.3

7.0

15 3.40 0.06

-1.09 0.11

0.90 0.06

9.33 0.09

0.12 0.33

2.53 1.16

3.37 0.10

KMJ-3812

11.4

8.9

5.1

12 3.42 0.05

-0.99 0.08

0.96 0.28

9.41 0.08

0.09 0.31

3.53 1.37

3.30 0.07

KMJ-3813

12.8

8.9

7.3

11 3.44 0.05

-0.94 0.06

1.03 0.18

9.51 0.09

0.09 0.20

4.55 2.49

3.48 0.07

KMJ-3814

12.3

10.8

7.0

14 3.37 0.04

-0.90 0.05

1.08 0.12

9.73 0.40

2.41 0.85

3.20 1.36

3.11 0.07

KMJ-38-

12.7

11.8

6.4

13 3.40 0.03

-1.06 0.09

1.14 0.22

9.44 0.25

1.59 1.14

3.82 2.70

3.18 0.06

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Table 1 Details of sclerosponge samples and analytical results of geochemistry (Continued)
SampleID

Collection
Date

Water
Depth
(m)

Size

N

X
Y
H
(mm) (mm) (mm)δ13C (‰)

δ18O (‰)

Mg/Ca
Sr/Ca
Ba/Ca
Pb/Ca
U/Ca
(mmol/mol) (mmol/mol) (μmol/mol) (μmol/mol) (μmol/mol)

Avg. SD(1σ)

Avg. SD(1σ)

Avg. SD(1σ)

Avg. SD(1σ)

Avg. SD(1σ)

Avg. SD(1σ)

Avg. SD(1σ)

15
KMJ-3816

15.9

15.5

8.8

16 3.39 0.06

-1.17 0.05

1.02 0.21

9.28 0.09

1.20 0.82

3.01 1.55

3.22 0.06

KMJ-3817

17.1

15.1

8.8

14 3.41 0.05

-1.07 0.11

1.19 0.31

9.56 0.15

0.84 0.95

N/A 3.80

3.21 0.07

KMJ-3818

15.6

12.8

8.0

12 3.34 0.06

-1.12 0.12

1.09 0.16

9.36 0.25

1.86 1.03

2.24 0.87

3.16 0.05

KMJ-3819

14.8

13.6

9.0

15 3.37 0.06

-0.94 0.07

1.22 0.49

9.30 0.17

2.24 0.45

1.50 0.44

3.22 0.05

KMJ-3820

18.2

15.9

9.5

19 3.38 0.04

-1.01 0.09

1.04 0.14

9.38 0.09

1.01 0.71

N/A 3.49

3.24 0.04

KMJ-3821

20.0

16.8

10.0

20 3.39 0.05

-1.00 0.07

1.10 0.12

9.41 0.25

1.46 0.86

3.19 1.64

3.20 0.05

KMJ-3822

18.5

18.2

9.0

15 3.41 0.03

-1.02 0.07

1.10 0.27

9.32 0.19

1.31 0.90

2.37 1.37

3.20 0.07

KMJ-3823

20.5

15.8

9.0

14 3.35 0.06

-0.95 0.09

1.23 0.20

9.74 0.31

1.75 0.92

1.43 0.61

3.20 0.05

KMJ-3824

21.6

16.2

10.0

17 3.37 0.06

-0.96 0.11

1.15 0.07

9.43 0.18

2.13 0.44

0.79 0.18

3.17 0.04

KMJ-3825

19.8

19.7

10.2

18 3.39 0.05

-1.02 0.11

0.99 0.14

9.38 0.20

2.15 0.47

0.77 0.39

3.22 0.06

KMJ-3826

21.6

19.1

11.8

20 3.39 0.06

-1.01 0.08

0.86 0.09

9.24 0.18

1.55 0.79

0.72 0.12

3.25 0.06

3.392 ±
0.012

-1.006 ±0.029

1.211 ±
0.114

9.428 ±
0.067

1.217 ±
0.312

2.086 ±
0.611

3.277 ±
0.041

ALL (KMJ-38): 95% CL

solutions, was measured at intervals of three samples tocorrect for instrumental drift. Based on replicate measurements of the solution of aragonite reference material
JCp-1 coral (Okai et al. 2002), external precisions for
Mg/Ca, Sr/Ca, Ba/Ca, Pb/Ca, and U/Ca determinations
were better than 0.43%, 0.31%, 1.1%, 4.0%, and 0.82%
relative standard deviations (N = 150) and the measurement values of samples were calibrated using the widely
accepted values of Hathorne et al. (2013).

diagenetic alteration such as overgrowth of inorganically
precipitated secondary cements, traces of dissolution, or
bioerosion. Consequently, these results indicate that A.
willeyana samples used for this study can retain pristineskeletons with original values of isotope compositionand elemental concentrations.

Results and discussion

Biological carbonates are known to precipitate out of
13
C and 18O equilibrium with seawater attributable tokinetic and metabolic isotope effects (e.g., McConnaughey 1998, 2003). For a photosynthetic scleractinianaragonitic coral with symbiotic algae, McConnaughey(1989) showed that the δ13C and δ18O variations (1σ) of
the coeval skeletal increments were significantly different
between sunshine side samples (± 0.17‰ and ± 0.04‰,
respectively) and shade side samples (± 0.47‰ and ±0.49‰, respectively). Furthermore, a strong positive correlation (r = 0.90) between coral δ13C and δ18O wasfound for the shade side. These results suggest that theisotopic composition is different depending on the skeletal portion of CaCO3 in photosynthetic corals.

Skeletal structures and preservation

The results of XRD analysis indicate that the skeleton
samples of Astrosclera willeyana consist exclusively ofaragonite (> 99.9%), with no detection of calcite. The
SEM images of skeletal samples also reveal no evidenceof the existence of calcite (Fig. 5). Skeletal aspects of oursclerosponge samples closely resemble those found in
earlier studies (e.g., Wörheide 1998; Jackson et al. 2010;
Gilis et al. 2013), clearly showing a typical macrostructure of reticulate skeletal organization with branches
composed of aragonitic spherulitic structural elements(Ayling 1982; Reitner 1992; Allison et al. 2012). Pristine
aragonite crystals were observed without evidence ofWithin-skeleton variations
Oxygen and carbon isotopes

Asami et al. Progress in Earth and Planetary Science(2020) 7:15

Page 7 of 18

Fig. 3 Photographs of sclerosponge samples

The average and standard deviation (1σ) of δ13C andδ O in an A. willeyana specimen were estimated fromvalues of sub-samples (N < 20) collected at the coevally
precipitated skeleton (Table 1; Fig. 4). The δ13C andδ18O records are almost similar among KMJ-40, KMJ34, and KMJ-38. The δ13C and δ18O variations (standard
deviations, 1σ) of the coeval skeleton were quite small:from ± 0.02 to ± 0.12‰ and from ± 0.03 to ± 0.17‰, respectively. To identify within-skeletal variations of all
samples, the respective deviations relative to the average18(differences between isotopic values and the average) in
an individual specimen are depicted in Fig. 6. The wholestandard deviation (2σ) of the isotopic differences was
small (± 0.11‰ for δ13C and ± 0.19‰ for δ18O) and almost constant at all skeletal portions, with no significant
variations and trends (Fig. 6). These results show thatthe within-skeletal variations in the isotopic composition
are negligibly slight for the species A. willeyana.
The distribution of correlation coefficients among respective samples in within-skeleton showed little

Asami et al. Progress in Earth and Planetary Science(2020) 7:15

Page 8 of 18

Fig. 4 Example showing the sub-sampling method conducted on a sclerosponge specimen. Subsamples for geochemical analyses (red) and for
XRD analysis and SEM observation (blue) were collected

systematic relationships and trends (Fig. 7). Only 5 sclerosponge samples showed positive relations between theδ13C and δ18O with high r values of 0.6–0.8, but theseare expected to be arbitrary in consideration of the veryslight within-skeletal variation of ± 0.03–0.06‰ for δ13C
and ± 0.08–0.11‰ for δ18O and considering analyticalerrors (Table 1). It is considered that the homogeneity of
the isotopic composition in the coevally skeleton for A.
willeyana is due to little kinetic fractionation effect because the species has no symbiont and a very slow
growth rate of the CaCO3 precipitation.
Elements/Ca ratios

Despite δ13C and δ18O records, only a few studies havereported minor and trace elements/Ca ratios of sclerosponges (e.g., Fallon et al. 2005; Rosenheim et al. 2005b;
Allison et al. 2012). The Sr/Ca and U/Ca records in thecoevally precipitated skeletons of A. willeyana samples
are almost similar among KMJ-40, KMJ-34, and KMJ-38(Table 1). Overall, the Mg/Ca, Sr/Ca, and U/Ca variations(1σ) of the coeval skeleton were small, ranging respectively
from ± 0.06 to ± 0.64 mmol/mol, ± 0.08 to ± 0.40 mmol/
mol, and from ± 0.02 to ± 0.15 μmol/mol. The sclerosponge Ba/Ca and Pb/Ca had large fluctuations with respective standard deviations of ± 0.20–1.14 μmol/mol and± 0.11–3.80 μmol/mol. The deviations (2σ) relative to theaverage for an individual were almost constant at all skeletal
portions (± 0.55 mmol/mol for Mg/Ca, ± 0.37 mmol/mol
for Sr/Ca, ± 1.45 μmol/mol for Ba/Ca, ± 2.45 μmol/mol for

Pb/Ca, and ± 0.13 μmol/mol for U/Ca), with no significant
variations and trends (Fig. 6). These results show that theelements are homogeneously distributed in coeval skeletonof A. willeyana sclerosponge, whereas the relative standard
deviations of Sr/Ca (3.9%) and U/Ca (4.2%) were quite
smaller than those of Mg/Ca (45%), Ba/Ca (97%), and Pb/
Ca (138%), which can be partially caused by the differencein elemental concentrations and respective analytical errors.
Therefore, our results suggest that the within-skeletal variations of Sr/Ca and U/Ca in A. willeyana sclerosponge areso slight as to be ignored.
The distribution of correlation coefficients among
respective samples in within-skeleton showed little
systematic relationships and trends, showing thatmost of the r values fell within a range from − 0.4 to
0.4 (Fig. 7). The relationships mostly explain only <20% of the covariance among respective geochemicalcomposition, thereby indicating that the within-skeletal
geochemistry for A. willeyana can be less influenced bykinetic fractionation effect. It is known that sclerosponges are composed of two key crystal structures inthe skeleton at a micro-scale resolution: fused aragonitic spherulites (formed intracellularly and fused together at the surface) and epitaxial backfill (deposited
extracellularly at the base of the sponge tissue). Highresolution spatial analyses showed that elements/Ca ratios were highly variable in and among these structures(Allison et al. 2012), probably indicating a heterogeneityof chemical composition in the sclerosponge skeleton.

Asami et al. Progress in Earth and Planetary Science(2020) 7:15

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Intraspecific variations
Oxygen and carbon isotopes

Fig. 5 Scanning electron micrograph images of sclerosponges. A
well-preserved pristine aragonite skeleton is visible (a, b KMJ-38-14;
c KMJ-38-25)

On the other hand, our data showed that withinskeletal Sr/Ca and U/Ca of A. willeyana sclerosponges
were quite small and constant (Table 1 and Fig. 6).
These suggest that the chemical components in thesclerosponge skeleton are commonly homogeneous at
millimeter-scale resolution and annually resolved reconstruction of ocean environmental changes can beapplied.

The average δ13C (δ18O) values of A. willeyana samples
collected in October 2015 and November 2016 fellwithin quite narrow ranges from 3.40 to 3.51‰ (from −0.75 to − 1.16‰) and from 3.35 to 3.48‰ (from − 0.89
to − 1.17‰), respectively (Table 1 and Fig. 8). The respective averages of the δ13C and δ18O with 95% confidence levels were 3.45 ± 0.02‰ and − 0.99 ± 0.07‰ for
KMJ-40 and KMJ-34 samples (N = 10) and 3.39 ±0.01‰ and − 1.01 ± 0.03‰ for KMJ-38 samples (N =26) (Table 1). No significant difference was found between the two population averages for δ18O (0.01 ±0.08‰). The δ13C average for KMJ-38 samples (presumably 2014–2016) was slightly lower than that for KMJ-40
and KMJ-34 samples (presumably 2013–2015) with asignificant difference of 0.06 ± 0.03‰, which may reflect
the Suess Effect widely accepted as a result of the burning of 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 mid-20th
century because of the accelerated increase of anthropogenically derived CO2 with isotopically low δ13C values
into the ocean from the atmosphere, results of which arerecorded in corals and sclerosponges (e.g., Böhm et al.
2002; Asami et al. 2005; Swart et al. 2010). The difference is roughly consistent with decreasing δ13C rates of− 0.03‰/year for 2000–2016 (atmospheric CO2 at Hawaii: derived from Scripps CO2 Program initiated in1956 by Keeling CD) and − 0.07‰/year for 2000–2010(coral data in the Ryukyu Islands; Asami et al. unpublished data).
Cross plots of δ13C and δ18O records of our 36 sclerosponge samples converged respectively to the averagesof 3.41‰ and − 1.00‰ with very slight standard deviations of ± 0.04‰ and ± 0.08‰ (Fig. 8). The relationshipbetween average δ13C and δ18O values of all samples
yielded a very weak correlation coefficient of 0.27 (p >0.01, Table 2), which is unlike those found in photosynthetic marine organisms. Therefore, one can reasonably
infer that the intraspecific δ13C and δ18O variations (individual difference) for the species A. willeyana are quite
small and hardly influenced by vital effects because thesclerosponges grow without the need for light and symbiotic algae.
Elements/Ca ratios

The average Sr/Ca (U/Ca) ratios of A. willeyana samples
collected in October 2015 and November 2016 fellwithin quite narrow ranges from 9.36 to 9.76 mmol/mol(from 3.12 to 3.27 μmol/mol) and from 9.15 to 9.80
mmol/mol (from 3.11 to 3.54 μmol/mol), respectively(Table 1 and Fig. 8). The respective Sr/Ca and U/Ca averages with 95% confidence levels were 9.50 ± 0.08

Asami et al. Progress in Earth and Planetary Science(2020) 7:15

Page 10 of 18

Fig. 6 Within-skeleton variations in a δ18O and b δ13C values and c–g elements/Ca ratios of sclerosponges. Deviations to the average in
an individual sample are shown. Horizontal lines and dotted lines
respectively represent zero and standard deviation (2σ)

mmol/mol and 3.21 ± 0.03 μmol/mol for KMJ-40 and
KMJ-34 samples (N = 10) and 9.43 ± 0.07 mmol/mol
and 3.28 ± 0.04 μmol/mol for KMJ-38 samples (N = 26)(Table 1). No significant difference was found between
the two population averages for Sr/Ca (0.08 ± 0.10
mmol/mol) and U/Ca (0.07 ± 0.05 μmol/mol). Furthermore, the Sr/Ca and U/Ca records are in agreement withthose of the same species from other regions in the
Pacific Ocean (Table 3). Consequently, these results
strongly suggest that intraspecific variations are negligibly small for Sr/Ca and U/Ca of A. willeyana.
The mean values of within-skeletal Mg/Ca, Ba/Ca, and
Pb/Ca ratios fall within 1.33–2.11 mmol/mol, 0.59–
2.97 μmol/mol, and 0.45–0.81 μmol/mol for KMJ-40 and
KMJ-34 samples (collected in 2015) and 0.86–2.14
mmol/mol, 0.09–2.41 μmol/mol, and 0.08–4.55 μmol/
mol for KMJ-38 samples (collected in 2016), respectively(Table 1 and Fig. 8). The respective Mg/Ca and Ba/Ca
averages with 95% confidence levels were 1.56 ± 0.16
mmol/mol and 1.86 ± 0.45 μmol/mol for KMJ-40 and
KMJ-34 and 1.21 ± 0.11 mmol/mol and 1.22 ±0.31 μmol/mol for KMJ-38 (Table 1). The differences between the two population averages for Mg/Ca (0.35 ±0.20 mmol/mol) and for Ba/Ca (0.64 ± 0.55 μmol/mol)were statistically significant but not so large (Fig. 8). The
respective Pb/Ca averages with 95% confidence levels
were 0.66 ± 0.09 μmol/mol for KMJ-40 and KMJ-34 and2.09 ± 0.61 μmol/mol for KMJ-38, the difference of
which is significant (1.42 ± 0.62 μmol/mol). The intraspecific variations for Mg/Ca, Ba/Ca, and Pb/Ca may be
due to an individual difference in biological controls onskeletal partitioning of the trace elements.
For Mg/Ca, the mechanisms of magnesium incorporation into aragonite are very complicated: loosely boundin the crystal lattice, bound to metal sites of organic
compounds, and/or adsorbed onto crystal surface (Amielet al. 1973). The intraspecific Mg/Ca variations may be
due to individual differences in organic phases and themetal binding capacity of sclerosponge tissue layers. For
Ba/Ca, the mode of incorporation of barium into the sclerosponge skeleton remains unknown (e.g., Rosenheim et al.
2005b; Allison et al. 2012). Sclerosponges contain a large
amount of bacteria living within their tissue (Wörheide
1998). One possibility to explain the intraspecific Mg/Caand Ba/Ca variations found in this study is that the physiological processes associated with these bacteria may havean effect on the incorporation of Mg2+ and Ba2+ for calcification at a micro-environmental level (Rosenheim et al.
2005b). Further, the intraspecific variation indicates that

Asami et al. Progress in Earth and Planetary Science(2020) 7:15

Page 11 of 18

Fig. 7 Frequency distributions (histograms) of correlation coefficients among geochemical records of sclerosponges. The Y-axis represents thenumber of individuals (sample number: N). The r values are divided into nine classes in the X-axis. A trend of the respective relations of two
within-skeleton geochemical components is visualized. High frequency with r values of − 0.4–0.4 indicates a little significant relationship in
within-skeletal geochemistry

the efficiency for transporting elements into the calcification site may be different among individuals because of thelarge discrepancy in the cationic radii of Mg2+ and Ba2+
relative to Ca2+ unlike Sr2+ (Gaetani and Cohen 2006).
The Pb/Ca profiles along a growth direction shows historical changes associated with environmental lead

pollution (e.g., Lazareth et al. 2000; Swart et al. 2002;
Ohmori et al. 2014). Skeletal Pb/Ca in a Acanthochaetetes
wellsi (high-Mg calcite) collected from the same locality as
our study (Kume Island, Japan) varied roughly from 200
to 1000 nmol/mol for 2000–2007 (Ohmori et al. 2014)
and that in a Ceratoporella nicholsoni (aragonite) from theAsami et al. Progress in Earth and Planetary Science(2020) 7:15

Page 12 of 18

Fig. 8 Scatter plot of a δ18O and δ13C and b elements/Ca ratios of sclerosponges. Data are shown as averages with 1σ standard deviations inindividual samples, which show intraspecific variations in sclerosponge geochemistry. Red (EQ1) and gray (EQ2) areas are shown respectively as
estimated ranges of isotopically equilibrium aragonite precipitated at the study site using a relation between seawater δ18O and salinity by Oba(1990) and Abe et al. (2009)

analyses carried out in this study smoothed the heterogeneity of skeletal geochemistry, which results in a smoothingof environmental signals to no small extent through the living tissue layer. Meanwhile, there significantly exist weakcorrelations between Sr/Ca and δ18O (r = 0.47), Mg/Ca and
Pb/Ca (r = − 0.56), and Ba/Ca and U/Ca (r = − 0.69), but
their relationships can explain only 22–48% in the respective variance. The former may reflect a difference in skeletal
growth rate among the individual samples because bothsclerosponge Sr/Ca and δ18O strongly correlated negatively
with seawater temperature. At this point, no clear reason
underlying the latter two can be inferred. However, thenegative relation between Mg/Ca and Pb/Ca found in thisstudy can be explained by an indication that sclerosponges
would acquire more Mg2+ nutritionally with a decrease inpumping of ambient water and particulates with adsorbed
Pb species (Willenz and Hartman 1989; Rosenheim et al.
2005b). The significant negative correlation of the comparatively high r value of − 0.69 between Ba/Ca and U/Ca in

Caribbean Sea varied roughly from 90 to 120 nmol/mol
for 1999–2001 (Rosenheim et al. 2005b). Considering the
Pb/Ca averages of our samples (1648 ± 421 nmol/mol), interspecific variations are large. Sclerosponges incorporate~ 10 times higher Pb than corals because pumping and filtering particulates, which absorb heavy metal species, arethe only source of nutrition for sclerosponges (e.g., Hartman and Goreau 1966; Willenz and Hartman 1989).
Therefore, it is inferred that the amounts, size, and/or species of filtered particles may be considerably different
among individuals and species.
Differences in the geochemistry among micro-scale skeletal structures may reflect variations in the composition of
the precipitation fluid, the incorporation of ions into theskeleton, and/or kinetic effects (Gabitov et al. 2008). In
most cases, apparent relationships among elements/Ca andisotope data of all samples were not founded, yielding avery weak correlation coefficient ranging from − 0.38 to
0.29 (Table 2). This may indicate that the millimeter scale

Table 2 Correlations between average values of sclerosponge geochemistry*
δ C
13

δ18O
Mg/Ca
Sr/Ca

δ18O

Mg/Ca

0.27

0.22

0.17

0.22

-0.35

-0.11

-0.06

0.47

0.29

-0.04

-0.06

-0.11

0.18

-0.56

0.02

0.16

-0.01

-0.12

-0.38

-0.69

Sr/Ca

Ba/Ca

Ba/Ca
Pb/Ca
*

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

Pb/Ca

U/Ca

0.19

(2020) 7:15

Asami et al. Progress in Earth and Planetary Science

Page 13 of 18

Table 3 Average elemental ratios and partition coefficients for aragonite sclerosponges
Species

Site

Depth
(m)

Mg/Ca (mmol/
mol)

Sr/Ca (mmol/
mol)

Ba/Ca (μmol/
mol)

Pb/Ca (nmol/
mol)

U/Ca (μmol/
mol)

A.
willeyana

Kume Is., Japan30-40

1.31 ± 0.11

9.45 ± 0.05

1.42 ± 0.26

1648 ± 421

3.26 ± 0.03

3.62-4.27 x 10-4

1.09-1.11

0.007-0.017

0.85-0.92

9.45-9.89

3.60-4.14

1.81 x 10

1.10

0.098

0.77-0.90

10.15-10.74

1.6 x 10

This study
Avg. (95% CL)
DMe, Arag

2.28-2.35

Rosenheim et al. (2005)
Avg. (±1σ)
DMe, Arag
Average (±1σ)
DMe, AragC.
Jamaicanicholsoni

22

C.
Bahamasnicholsoni

143

-4

-4

8.13-91.9

3.20-3.37

3.16-3.66

52.10-289

3.07-3.28

1.17

0.86

171.85

2.98

Fallon et al. (2005)
Avg. (1980-1994)

A.
willeyana

Otta Island,
Micronesia

25

0.9-1.2

9.5-12.0

2.7-4.1

Avg. (-2004, several A.
yrs)
willeyana

Nomuka Ika,
Tonga

9.5

0.3-1.1

8.5-12.5

2.5-8.0

3.1-3.6

Allison et al. (2012)

our sclerosponge samples possibly reflects a significant
positive relation between Ba/Ca and sample size (a parameter presumably related to biological and skeletal growthrate) (Fig. 9) and the significant negative relationship between U/Ca and seawater carbonate ion concentration (relating to pH and aragonite saturation degree) for deep-sea
azooxanthellate corals (Anagnostou et al. 2011).
Compared with equilibrium aragonite for stable isotopes

To evaluate the fidelity of A. willeyana as apaleoenvironmental proxy, we compared our data withthe δ13C and δ18O values of aragonites that are inorganically precipitated in isotopic equilibrium with seawaterat the sclerosponge growth site: “equilibrium aragonite.”

The δ18O values were calculated using an equation(1000 × ln α = 17.88(103/T) − 31.14) derived from laboratory synthesis experiments of aragonite at watertemperatures of 0–40 °C (Kim et al. 2007). Therein, α isthe fractionation factor between aragonite and water; T
is in degrees Kelvin. Although showing good consistency
with the climatological data products (Fig. 2), the in situ
observational data of this study (October 2015 to November 2016) are temporally limited relative to thegrowth periods (a few years) of investigated skeletal portions. Based on skeletal growth characteristics for A.
willeyana reported from earlier works (see the “Materials and methods” section), for this study, the investigated skeletal increments of our sclerosponges were

Fig. 9 Relationship between sample size and a δ18O and δ13C and b elements/Ca ratios of sclerosponges

Asami et al. Progress in Earth and Planetary Science(2020) 7:15

assumed to be precipitated for 2013–2016. Consequently, the annual mean seawater temperature (25.4 °C)
and the variation (± 0.9 °C, 2σ) for 2013–2016 were estimated from JODC and Integrated Global Ocean Services
System gridded data (26°–27° N, 126°–127° E: Reynolds
et al. 2002). The seawater δ18O values of 0.26 ± 0.05‰
or 0.43 ± 0.08‰ were estimated respectively from JODC
salinity data using a relation for the East China Sea –Kuroshio Current region (Oba 1990) (case 1) or for Ishigaki Island in the southern Ryukyus (Abe et al. 2009)(case 2). These estimations are consistent with δ18O
values (0.18‰ in November 2009, 0.25–0.29‰ in October 2015, 0.35‰ in March 2016) of seawater samples
collected at water depths of 34–40 m in this study area.
Consequently, the δ18O values of equilibrium aragonites
precipitated at the study site for 2013–2016 are expected
to fall within a range of − 0.92‰ to − 1.37‰ (case 1:
shown as EQ1 in Fig. 8) or from − 0.73‰ to − 1.23‰(case 2: shown as EQ2 in Fig. 8) at 95% confidence
intervals.
The δ13C values of the equilibrium aragonites were estimated using DIC δ13C of seawater, the carbon-isotope
fractionation factors among CO2 species (Zhang et al.
1995), and the aragonite–HCO3− enrichment factor (2.7
± 0.6‰; Romanek et al. 1992). Because of the lack ofdata on DIC δ13C of seawater around the study site, theannual δ13C value of DIC at a water depth of 40 m is assumed to be the medium value (0.68‰) between November and August estimated using two significant
relations established west of Okinawa Island (r2 = 0.810;
Takayanagi et al. 2012) and southeast of Okinawa Island(r2 = 0.997; Suzuki et al. 2009). Consequently, the δ13C
values of the equilibrium aragonites are expected to beroughly 3.0–4.2‰ (Fig. 8). It is noteworthy that the estimated δ13C values are approximate because of the limitations and uncertainty of the dataset.
The skeletal δ13C and δ18O values in our 36 sclerosponge samples almost fell within the probable ranges(case 1 and case 2) of the equilibrium aragonites precipitated at the living site (Fig. 8). This result strongly showsthat the δ13C and δ18O of A. willeyana is not be influenced isotopically by vital physiological effects. Furthermore, no strong correlation exists between the isotope
composition and the sclerosponge sample size (r = 0.076
for δ13C and r = 0.150 for δ18O, p > 0.01) (Fig. 9), unlike
symbiont corals for which the isotopic variations (thedegree of disequilibrium) are related to the skeletal
growth rate (e.g., McConnaughey 1989; Felis et al. 2003).
δ13C and δ18O values of corals with symbiotic algae are
well known to differ greatly from those of equilibrium
aragonite because of kinetic and metabolic fractionation
effects (e.g., Aharon 1991; McConnaughey 2003). We
therefore suggest that the fractionation effects have little
influence on the isotopic composition of A. willeyana

Page 14 of 18

because the skeletal growth is expected to constant at avery slow rate. Our results are supported strongly by evidence from earlier studies showing that δ18O values ofliving sclerosponges (seven C. nicholsoni from the Caribbean Sea and a A. willeyana from the Great Barrier Reef)
are in good agreement with published values from synthetic aragonite and near-equilibrium values of mollusks
and foraminifers (Böhm et al. 2000) and that sclerosponges (three C. nicholsoni from the Caribbean Sea anda A. wellsi from New Caledonia) precipitate CaCO3 skeletons close to isotopic equilibrium for δ13C values(Böhm et al. 1996).
Partition coefficients of elements/Ca

Partition coefficients, apparent distribution coefficients(DMe, Arag), were estimated using element/Ca ratios between seawater and aragonitic skeleton of sclerosponge,
except for Pb/Ca (Table 3). As it is known that the DSr,
Arag of inorganic aragonite depends on water temperature(e.g., Kinsman and Holland 1969; DeCarlo et al. 2015),
sclerosponge Sr/Ca can be useful for a proxy of seawatertemperature (e.g., Rosenheim et al. 2004; Haase-Schramm
et al. 2005; Waite et al. 2018). The DSr, Arag from our A.
willeyana samples was 1.09–1.11 (almost unity), which isconsistent with that of C. nicholsoni from the Caribbean
Sea (Rosenheim et al. 2005b) (Table 3) and experimentally
precipitated abiogenic aragonite (Gaetani and Cohen
2006; DeCarlo et al. 2015). The average Sr/Ca of ~ 9.5mmol/mol in our sclerosponges was identical to an estimation of inorganic aragonite of 9.42–9.50 mmol/mol at
25.4 ± 0.9 °C calculated by using the experimentally established relationship (Gaetani and Cohen 2006) and almost
consistent with previously reported values for the same
species in the Pacific Ocean (Fallon et al. 2005; Grottoli
et al. 2010; Allison et al. 2012). Furthermore, highresolution Sr/Ca records of aragonitic skeleton for A. willeyana (Fallon et al. 2005) and C. nicholsoni (Rosenheim
et al. 2004) using LA-ICP-MS have been shown to be seasonal variations, yielding significant calibrations for seawater temperature. Therefore, these lines of evidence
suggest that A. willeyana sclerosponge Sr/Ca can be a robust indicator of seawater temperature.
The value of DMg, Arag estimated from our samples
shows that A. willeyana sclerosponge Mg/Ca ratios areseveral orders (10-3 to 10-4) of magnitude smaller thanthose of seawater (Table 3). The value is about twicethat of the species C. nicholsoni (Rosenheim et al.
2005b), but about one order of magnitude less than experimentally precipitated inorganic aragonite (Gaetani
and Cohen 2006). The DBa, Arag estimated from our samples shows that Ba/Ca ratios in A. willeyana sclerosponge are variable and about two orders of magnitudeless than those of seawater. The DBa, Arag value estimatedin this study is about several orders (10-1 to 10-2) ofAsami et al. Progress in Earth and Planetary Science(2020) 7:15

magnitude less than those for the species C. nicholsoni(Rosenheim et al. 2005b) and inorganic aragonite (Gaetani and Cohen 2006; Mavromatis et al. 2018). Rosenheim et al. (2005b) also reported that C. nicholsoni
sclerosponges showed large variations in their DBa, Aragvalues of about 0.1–0.9 (Table 3). Such a small DBa, Aragvalue of < 1 for sclerosponge samples can be reasonably
explained by the lower incorporation of an incompatible
trace metal because of the large difference of ~ 25% inionic radius between Ba2+ and Ca2+, as was true also forother aragonite materials such as synthetic aragonite(Mavromatis et al. 2018), speleothems (e.g., Wassenburg
et al. 2016), bivalves (e.g., Poulain et al. 2015), and fish
otoliths (e.g., Bath et al. 2000) in contrast to corals,
which were greater than unity (e.g., Gonneea et al.
2017). However, such a different value of ~ 0.01 to ~ 0.9(Table 3) indicates that physiological processes for theincorporation of Ba2+ into aragonitic sclerosponges for
calcification differ greatly not only among individuals
but also among species. Perhaps for this reason, significant correlations exist between the Ba/Ca and the sclerosponge sample size found in this study (r = ~ 0.6, p <0.01) (Fig. 9). Furthermore, results of a study of element
partitioning during aragonite precipitation suggest thatthe calcifying fluid from which coral skeleton precipitates is depleted in Mg and Ba, unlike Sr. Results alsosuggest that seasonal fluctuations exist in the mass fraction of aragonite precipitated from the fluid (precipitation efficiency) (Gaetani and Cohen 2006), which canqualitatively explain our results showing lower DMg, Aragand DBa, Arag values and a value of DSr, Arag that is almost
equal to unity for A. willeyana sclerosponge. Quantitative verification of these results requires additional experimental work.
For U/Ca, the average value (~ 3.3 μmol/mol) of our
A. willeyana sclerosponges was consistent with those of
the same species (Fallon et al. 2005) and with C. nicholsoni (Rosenheim et al. 2005b) (Table 3). The value of
DU, Arag (2.3–2.4) estimated in this study was slightly
lower than that (2.98) reported for C. nicholsoni (Rosenheim et al. 2005b) and much higher than the experimentally determined value (0.31 ± 0.06) of inorganic
aragonite precipitation at 25.5 °C (DeCarlo et al. 2015).
Degradation of tissue layers and/or bacteria can influence the pH and carbonate species system of the calcifying fluid, thereby altering the U/Ca ratios insclerosponge skeleton at different levels, which possibly
caused differences in U/Ca among sclerosponge species.
Although coralline aragonite U/Ca records are apparently correlated with temperature (e.g., Min et al. 1995;
Shen and Dunbar 1995), several recent studies demonstrated that the U/Ca ratios of azooxanthellate deep sea
coral (Anagnostou et al. 2011) and experimentally precipitated aragonite from seawater (DeCarlo et al. 2015)

Page 15 of 18

have significant negative correlation with carbonate ion
concentrations because the aqueous chemistry of uranium is influenced by the carbonate ion, which forms
complexes with the uranyl ion (Langmuir 1978). The
sclerosponge U/Ca is about 2–3 times higher than thatof zooxanthellate corals, which may be related to lowering of pH and carbonate ion concentrations in the calcifying fluid. These lines of implication might bring higher
DU, Arag values in aragonitic sclerosponges than that ofsynthetic aragonite. Although the complicated mechanism
for the incorporation of uranyl complexes into calcium
carbonate has not been resolved, the slight intraspecificvariations (± 0.03 μmol/mol, the relative variation is 0.9%)
of sclerosponge U/Ca for the A. willeyana species examined in this study (Fig. 8) support the possibility of its use
as a proxy for ocean environments.

Conclusions
Results of this study are important scientific findings forthe hypercalcified demosponge Astrosclera willeyana; (1)within-skeletal variation is quite small for δ13C, δ18O,
Sr/Ca, and U/Ca (namely, little heterogeneity in thecoevally precipitated skeleton); (2) intraspecific variations are quite small for δ13C, δ18O, Sr/Ca, and U/Ca
(namely, little individual difference); (3) the aragonite
skeleton is precipitated in or very close to isotopic equilibrium with seawater at the living site; (4) the isotopic
composition of the skeleton is scarcely affected by kinetic and biological effects; (5) the partition coefficient of
Sr/Ca is consistent with that for different species andclose to inorganic aragonite.
We believe that sclerosponge U/Ca may be a
paleoenvironmental proxy although there are still unknowns relating to uranium into the aragonitic skeleton.
Relatively large variations and individual differences inthe sclerosponge Mg/Ca, Ba/Ca, and Pb/Ca were shownin this study. To clarify the reasons for controlling factors of incorporation (distribution) of the elements into
the sclerosponge aragonite skeleton, further investigations such as ultra-high resolution analyses and culture
experiments are needed. Importantly, we suggest that A.
willeyana δ18O (δ13C) is very suitable as an environmental proxy to reconstruct seawater temperature and δ18O
(DIC δ13C) for the past. Coupled determination of Sr/Caand δ18O in a sclerosponge can potentially enable theconstruction of independent time series for both seawater temperature and δ18O (≒ salinity) at near-annual
resolution by using a millimeter-scale sampling protocol
for widely used and convenient methods. Furthermore,in combination with the geochemistry of marine calcified organisms living in shallow waters, such as corals
and giant clams, long-lived sclerosponge-based reconstruction of deeper ocean environments can generate along time series of spatial and vertical changes in coralAsami et al. Progress in Earth and Planetary Science(2020) 7:15

reef environments for the past few hundred years, extending beyond the observation data. This study alsopresents the important implication that even if only afew skeletal fragments and a few sclerosponge samples
are collected, one can reconstruct annual average paleoceanographic conditions using well-preserved fossils thathave not been altered diagenetically. Regarded fromthese viewpoints, our results can support contributions
toward broad applications not only to climatology andoceanography but also to geology and biogeochemistry.
Abbreviations
JODC: Japan Oceanographic Data Center; VPDB: Vienna Standard Pee Dee
Belemnite; VSMOW: Vienna Standard Mean Ocean Water
Acknowledgements
We are grateful to a chief editor (Prof. H. Kawahata) and two anonymous
reviewers for their helpful and valuable suggestions and comments on the
manuscript. We also thank M. Kondo (Okinawa Institute of Science andUnderwater Technology) for help with field surveys and Dr. H. Fujimura, M.
Chinen, and Y. Akamine (University of the Ryukyus) for help withexperiments.
Authors’ contributions
RA designed the study, analyzed the samples and data, and wrote themanuscript. TN, MM, YI, YF, and TS collaborated with RA in the fieldwork andsampling. AK, DO, RU, and RS collaborated with RA in the chemical analyses.
The authors read and approved the 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
Please contact the corresponding author for data requests.
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, Aobayama, Sendai 980-8578, Japan. 2Department of Earth Science,
Faculty of Science, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa
903-0213, Japan. 3Tropical Biosphere Research Center, Iriomote Station,
University of the Ryukyus, 870 Uehara, Taketomi, Okinawa 907-1541, Japan.
4
Department of Chemistry, Biology, and Marine Science, Faculty of Science,
University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa 903-0213, Japan.
5
Division of Earth and Environmental Sciences, Graduate School ofEnvironmental Studies, Nagoya University, Furo-cho, Chikusa-ku, Nagoya
464-8601, Japan. 6Centre for Marine and Coastal Studies (CEMACS), Universiti
Sains Malaysia, 11800 USM, Penang, Malaysia. 7Okinawa Prefectural Universityof Arts, 1–4 Shuri-Tounokura, Naha, Okinawa 903-8602, Japan. 8Department
of Civil and Environmental Engineering, Graduate School of Engineering,Tohoku University, 6-6-06 Aramaki-Aza-Aoba, Sendai 980-8579, Japan.
Received: 26 November 2019 Accepted: 15 April 2020

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