Global and Planetary Change 72 (2010) 131–140

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Global and Planetary Change
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / g l o p l a c h a

Climatic and hydrologic variability in the East China Sea during the last 7000 years
based on oxygen isotope records of the submarine cavernicolous micro-bivalve
Carditella iejimensis
Nagisa Yamamoto a,⁎, Akihisa Kitamura a, Tomohisa Irino b, Tomoki Kase c, Syu-ichi Ohashi daInstitute of Geosciences, Shizuoka University, Shizuoka 422-8529, Japan
Faculty of Environmental Earth Science, Hokkaido University, N10W5 Sapporo 060-0810, Japanc
National Science Museum, 3-23-1, Hyakunincho, Shinjyuku-ku, Tokyo 169-0073, Japand
Kaiyo Planning Co. Ltd., 1732-12, Maeda, Urasoe, Okinawa 901-2102, Japanba r t i c l e

i n f oArticle history:
Received 3 August 2009
Accepted 25 January 2010
Available online 1 February 2010
Keywords:
East China Sea
Middle–Late Holocene
submarine cavernicolous micro-bivalve
oxygen isotope
East Asian monsoon

a b s t r a c t
The micro-bivalve Carditella iejimensis inhabits the sediment surface within submarine caves at Ie Island,
Okinawa, Japan. A comparison of the δ18O values (δ18Oaragonite) of empty and living shells indicates that theshell is formed over several seasons, and that the main cause of mortality is low water temperature.
According to this hypothesis, it is likely that the shells with heaviest δ18Oaragonite values (− 0.4‰) among therecent dataset formed under or close to the lower limit of growth temperature for the species. Assuming an
unchanging temperature tolerance of the species during the Holocene, samples with δ18Oaragonite values
heavier than − 0.4‰ indicate unusually low temperatures and enrichment of δ18O of sea water (δ18Oseawater).
The δ18Oaragonite record of C. iejimensis from sediment cores recovered from Daidokutsu cave shows no clear
long-term trend in sea surface temperature or δ18Oseawater in the East China Sea during the past 7000 years,
and indicates anomalously cool and dry events (enrichment in δ18Oseawater) at around 6300 and 5550 cal.
years BP. These events may have been related to changes in the activity of the East Asian monsoon, related inturn to weakening solar activity. In contrast, these anomalies appear to be obscured during the last1000 years, including a weak Asian summer monsoon event during the Little Ice Age, thereby indicating thatthe mode of the East China Sea climatic and hydrologic response to decadal- to centennial-scale variability inthe intensity of East Asian monsoon has varied over the past 7000 years.
© 2010 Elsevier B.V. All rights reserved.

1. Introduction
The magnitude of natural climate change during the Holocene is
one of the key factors in estimating the current and future effects ofanthropogenic climate change (e.g., Bond et al., 1997, 2001;
deMenocal, 2001; Cronin et al., 2003; Mayewski et al., 2004; Wanget al., 2005; Wanner et al., 2008). It is necessary to undertake suchstudies in many regions of the world, not only because of regional
differences in ecosystems and the lifestyle of human populations, but
because of spatial variations in the nature and degree of climatechange. East Asia, which is home to approximately one-third of theworld's population, is strongly inﬂuenced by the East Asian monsoon(Fig. 1), which is driven by differential heating between the Asian
continent and the surrounding seas and Northwest Paciﬁc.
Precisely dated stalagmite oxygen isotope records from southern
China reveal that Holocene weakening in the summer monsoon
corresponds to an orbitally induced reduction in summertime solar⁎ Corresponding author. Tel.: +81 54 238 4798; fax: +81 54 238 0491.
E-mail address: seakita@ipc.shizuoka.ac.jp (N. Yamamoto).
0921-8181/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.gloplacha.2010.01.025

insolation in the Northern Hemisphere (e.g., Dykoski et al., 2005;
Wang et al., 2005). On a decadal–century scale, weak Asian summer
monsoon events correspond to periods of reduced solar activity (e.g.,
Neff et al., 2001; Jung et al., 2002; Gupta et al., 2003; Wang et al.,2005). However, Maher (2008) suggested that stalagmite δ18O
records reﬂect the declining Holocene inﬂuence of isotopically lighter,
Indian-monsoon-sourced moisture over China and consequent increase in the proportion of isotopically heavy rainfall, sourced fromthe relatively oceanic East Asian monsoon. This view was proposed
because stalagmite records do not match other East Asian proxy
rainfall records based on the magnetic properties of loess/palaeosol(Maher and Hu, 2006) and intercomparisons of cave oxygen isotope
data (Hu et al., 2008).
The winter monsoon has no such signature in the hydrologicalcycle, and is reconstructed mainly from changes in dust ﬂux. Wanget al. (1999) and Lim et al. (2005) reported that the winter monsoon
weakened at 4000–3000 years BP in response to increasing winterinsolation. Yancheva et al. (2007) claimed that the strengths of thesummer and winter monsoons are anti-correlated on a decadal timescale; however, this hypothesis has been challenged by Zhang and Lu(2007) and Zhou et al. (2007). Other studies have argued that

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N. Yamamoto et al. / Global and Planetary Change 72 (2010) 131–140

Fig. 1. Spatial distributions of observed mean surface wind (vectors) in East Asia for the periods June–August and December–February. Modiﬁed from Kitoh (2005).

centennial-scale variations in the winter monsoon (intensiﬁcation)
are inﬂuenced by solar activity (weakening) (Lim et al., 2005; Xiao
et al., 2006; Yancheva et al., 2007). Although there is intense debate
regarding the nature of Holocene changes in the Asia monsoon,
analyses of continental climate records have greatly improved ourunderstanding in this regard. In contrast, few studies have considered
the relationship between the East Asian monsoon and the oceanography of the East China Sea, which borders China and Japan.
Previous studies have examined Holocene oceanographic changes
in the East China Sea based on geochemical analysis of the planktonic
foraminifera Globigerinoides ruber recovered from deep-sea sedimentary cores (Jian et al., 2000; Ijiri et al., 2005; Sun et al., 2005; Lin et al.,2006). Jian et al. (2000) proposed that a decrease in sea surface
temperature (SST) during the period 4600–2700 cal. years BP was
related to an intensiﬁcation of the winter monsoon. In addition, theauthors argued that this decrease in SST may have caused aremarkable decrease in the abundance of the planktonic foraminifera
Pulleniatina obliquiloculata (i.e., the Pulleniatina Minimum Event),
which is regarded as the Kuroshio Current indicator species by Jianet al. (1996), Li et al. (1997), and Ujiié and Ujiié (1999). In contrast, Linet al. (2006) reported no change in SST or sea surface salinity during
the Pulleniatina Minimum Event. This discrepancy among different
studies may reﬂect the varying quality of data obtained from manydifferent individuals of G. ruber.
Globigerinoides ruber remains at water depths of 2–50 m during its
life cycle (Fairbanks et al., 1982; Hemleben et al., 1989; Lin et al.,2004), and thrives in the East China Sea during autumn, spring, andsummer when SST is high and the water column is well stratiﬁed(Xu et al., 2005). During the summertime development of thermal
stratiﬁcation, sea temperatures vary from 28–29 °C at 0 m depth
to 25 °C at 50 m (Xu et al., 2005). Because a single sample
for geochemical analysis requires 20–40 individuals of G. ruber(Jian et al., 2000; Ijiri et al., 2005; Sun et al., 2005; Lin et al., 2006),
each sample represents a mixture of individuals that lived during
different years and at different depths.
To reconstruct climatic and hydrologic variability in the East China
Sea during the Holocene, there exists the need for other long,continuous records of paleoceanographic change. To this end,
Kitamura et al. (2007b) and Yamamoto et al. (2008) measured theδ18Oaragonite values of empty (dead) and whole shells of thecavernicolous micro-bivalve C. iejimensis, which lives in surface
sediment within the submarine cave Daidokutsu (meaning large
cave in Japanese; 29 m water depth; 26°43′N, 127°44′E) of Okinawa,
Japan (Fig. 2). Their data reveal that the δ18O-derived temperature
represents the springtime water temperature for each year, and that
there exists no signiﬁcant millennial-scale trend in the δ18Oaragonite

record over the past 3000 years. Because the mixed surface layer wasless than 2 cm-thick during the deposition of calcareous mud in the
cave, time-averaging of the fossil specimens was less than 100 years(Yamamoto et al., 2008). Thus, the δ18Oaragonite records of C. iejimensis
provide unique data for reconstructing Holocene oceanographic
changes in the East China Sea. However, Yamamoto et al. (2009b)
found no systematic ontogenetic variations in the δ18Oaragonite valuesof empty shells from surface sediment within Daidokutsu cave, whichis inconsistent with previous interpretations (Kitamura et al., 2007b;
Yamamoto et al., 2008).
In the present study, we re-evaluate the potential of δ18Oaragonite
values of C. iejimensis as a tool for reconstructing Holocene
oceanographic change. Based on our revised interpretation, we
reconstruct climatic and hydrologic variability in the East China Sea
during the last 7000 years based on new data. The results provide
information on the evolution of the mode of the climatic andhydrologic response of the East China Sea to the East Asian monsoon.

2. Study area and water temperature conditions
The entrances to the submarine caves Daidokutsu and Shodokutsu(meaning small cave in Japanese) lie in about 20 m water depth on thefore-reef slope of Ie Island, off the Motobu Peninsula of Okinawa
Island (Fig. 2a). Daidokutsu is 40 m long, dark inside, and deepens
inward to its deepest point at 29 m below sea level, while Shodokutsu
cave is more than 30 m long, dark inside, and has a horizontal cave
ﬂoor (Fig. 2b and c). The ﬂoors of both caves are covered by calcareousmud (Hayami and Kase, 1993; Kitamura et al., 2003, 2007a).
Kitamura et al. (2007b) and Kitamura and Yamamoto (2009)
measured hourly water temperature data in Daidokutsu cave from 26
July 2003 to 6 July 2004, and from 27 August 2007 to 19 September
2008 (Fig. 3), revealing seasonal changes from 29 °C in August–
September to 21 °C in February. Yamamoto et al. (2009b) reported nosigniﬁcant difference in salinity and δ18Oseawater value inside the cave(salinity = 34.3 psu, δ18Oseawater = 0.3 ± 0.1‰) and at 30 m depth
outside the cave (salinity = 34.2 psu, δ18Oseawater = 0.4 ± 0.1‰) during early July, which is the summer monsoon season. These data
reveal that underground water did not ﬂow into Daidokutsu caveduring the observation period and that patterns of seasonal change inwater temperature and salinity within the cave are similar to thosemeasured outside the cave at 30 m water depth (mean monthly
values) around Okinawa for the period 1906–2003 (Japan Oceanographic Data Center; J-DOSS; 1 × 1 grid cells, 26–27°N latitude and
127–128°E longitude) (Fig. 3a and d). In this study, we measured
water conditions in Shodokutsu cave (Fig. 4).

N. Yamamoto et al. / Global and Planetary Change 72 (2010) 131–140

133

Fig. 2. (a) Location maps of Daidokutsu and Shodokutsu submarine caves at Ie Island, off Okinawa Japan, the locations of drill cores A7 (Sun et al., 2005; Xiang et al., 2007) and MD403(Lin et al., 2006), and Dongge cave, China. NEC: North Equatorial Current; KC: Kuroshio Current. (b) Simpliﬁed cross-section of Daidokutsu cave, showing the location of core sample 19.
(c) Simpliﬁed cross-section of Shodokutsu cave.

3. Material

sediments within Daidokutsu cave (n = 47, r = − 0.37, p b 0.05)(Fig. 5a), and calculated the following relationship:

3.1. Shells
18

Carditella iejimensis, which measures less than 3.5 mm in height andlength (Fig. 5d), is a shallow infaunal suspension feeder with a shell of
100% aragonite. The species is only found in Daidokutsu andShodokutsu caves (Fig. 2) among many caves in the Ryukyu Islands,
Bonin Islands, Philippine Islands, Saipan, Palau, and Guam (Hayami andKase, 1993, 1996). No previous study has investigated the ecology of thespecies. Our preliminary study found only four living specimens in
Daidokutsu cave, whereas numerous living specimens were found on
the surface sediment within Shodokutsu cave (Hayami and Kase, 1993).
Kitamura et al. (2007b) measured the δ18Oaragonite values of 30
empty and whole shells of C. iejimensis picked from the N1 mm
fractions of surface sediments (uppermost 5 cm of sediment, representing the past 250 years) within Daidokutsu cave, and obtained astatistically signiﬁcant correlation between shell size and δ18Oaragonite(r = − 0.55, p b 0.01). Yamamoto et al. (2008) added to this dataset theδ18Oaragonite values of 17 empty and whole shells collected from surface

δ Oaragonite = –0:10H–0:63

ð1Þ

Using the above equation and the palaeothermometry equation
presented by Grossman and Ku (1986) and Goodwin et al. (2001), we
have
h

i
18
18
Tð BCÞ = 20:6–4:34 δ Oaragonite = VPDB – δ Owater = VSMOW –0:2 :ð2Þ

Kitamura et al. (2007b) and Yamamoto et al. (2008) estimated theδ18O-derived temperature for the period during the precipitation ofsmall shells (shell height of 1 mm) and the outer portions of large
shells (3.0 mm or more from the umbo), yielding values of 23.8 °C and26.1 °C, respectively. Given that these values correspond to monthly
mean water temperatures during May and July, respectively, Kitamura
et al. (2007b) and Yamamoto et al. (2008) proposed the followinginterpretation: the δ18O-derived temperature obtained from the shells

Fig. 3. Observed temperatures within Daidokutsu cave. The observation period was from 26 July 2003 to 6 July 2004, and from 27 August 2007 to 19 September 2008.

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N. Yamamoto et al. / Global and Planetary Change 72 (2010) 131–140

of C. iejimensis indicates water temperature between May and July ofeach year. Because the mixed surface layer was less than 2 cm-thickduring the deposition of calcareous mud in Daidokutsu cave (thereby
indicating that the time-averaging of the fossil specimens was lessthan 100 years; Yamamoto et al., 2008), the δ18Oaragonite records of
C. iejimensis provide high-resolution data for reconstructing millennial-scale oceanographic change in the East China Sea. A previous
analysis of δ18Oaragonite values of C. iejimensis from three sedimentcores from Daidokutsu cave (Cores 02, 04 and 05; Fig. 6) showed nosigniﬁcant millennial-scale trend over the past 3000 years, suggestingthat both springtime temperature and δ18Oseawater at 30 m depth
around the Okinawa Islands (Yamamoto et al., 2008).
However, Yamamoto et al. (2009b) found no systematic ontogenetic variations in the δ18Oaragonite values of 19 empty shells, which isinconsistent with previous interpretations that the δ18O-derived
temperature obtained from the shells of C. iejimensis indicates watertemperature between May and July of each year (Kitamura et al.,2007b; Yamamoto et al., 2008). The authors proposed that the species
may grow over several seasons, but did not speculate on the reason forthe size dependence of δ18Oaragonite in the empty shells.
3.2. Cored sediments
As noted above, Yamamoto et al. (2008) obtained δ18Oaragonite
values for C. iejimensis over the past 3000 years, from three sedimentcores recovered from Daidokutsu cave. To extend this earlier study,in the present study we collected additional measurements fromwhole shells within core 19 (6 cm in diameter and 233 cm in length),which was collected from Daidokutsu cave during September 2007
(Yamamoto et al., 2009a).
The sediment in the core shows a ﬁning-upward trend, and isdivided into a lower, gray calcareous sand (233–178 cm depth) and an
overlying gray calcareous mud (178–0 cm depth) (Fig. 6) (Yamamoto
et al., 2009a). Based on 14C age data, the cored sediments preserve a
record of fossils and sedimentation over the past 7000 years. The
sedimentation rate is estimated to be 28.6 cm/kyr between 233 and211 cm depth, 49.2 cm/kyr between 211 and 153 cm depth, and28.9 cm/kyr between 153 and 0 cm depth (Fig. 6). Based on temporalchanges in the abundance of debris derived from a red soil layer andtemporal changes in cavernicolous bivalve assemblages, Yamamoto
et al. (2009a) proposed that the ﬁlling of cavities within the reefal
foundations of the cave has continued over time, resulting in a
progressive decrease in the ﬂux of water between the interior andexterior parts of the cave over at least the past 6500 years.
4. Methods
4.1. Water conditions and analysis of δ18Oseawater
We used an Alec Electronics ACT-HR self-registering temperature–salinity meter to measure water temperature and salinity every hourin the innermost part of Shodokutsu cave, from 3 June 2007 to 31 July2009 (Fig. 2c). Unfortunately, records of water temperature within
the cave were not obtained between 25 September 2007 and 19
September 2008 due to malfunction of the temperature–salinity
meter. Water samples for oxygen isotope analysis were collected
within Shodokutsu cave and upon the reef slope at 30 m water depth
on 2 July 2007. δ18Oseawater analyses were performed at the GeoScience Laboratory in Nagoya, Japan, using a Finnigan MAT delta S.
δ18Oseawater values are reported relative to VSMOW; analyticalprecision (1 SD) was better than ± 0.1‰.
4.2. Analyses of δ18Oaragonite of micro-shell specimens
To examine the cause of the size dependence of δ18Oaragonite
values for empty shells of C. iejimensis, we compared δ18Oaragonite
between living and empty specimens from Shodokutsu cave. For thispurpose, samples of 5-cm-thick surface sediment were collected fromthe middle part of Shodokutsu cave (Fig. 2c) on 3 June 2009 and 29
July 2009.
Twenty-nine living individuals and 54 empty specimens of
C. iejimensis were picked from the N1 mm fractions. We also picked
160 specimens of C. iejimensis from the N1 mm fractions of 1-cm-thicksamples from core 19 (i.e., from 233 sediment samples).

Fig. 4. (a) Observed temperatures within Shodokutsu cave. The observation period was from 3 June 2007 to 24 September 2007 and from 20 September 2008 to 31 July 2009.
(b) Observed salinities within Shodokutsu cave. The observation period was from 3 June 2007 to 24 September 2007 and from 20 September 2008 to 31 July 2009. Seasonal variations insalinity (monthly mean values) at 30 m depth for the period 1906–2003 (1 × 1 grid cells; 26–27°N latitude and 127–128°E longitude). Error bars represent one standard deviation (1σ).

N. Yamamoto et al. / Global and Planetary Change 72 (2010) 131–140

All samples received no additional thermal or chemical treatment
prior to stable isotope analysis. δ18Oaragonite values of whole shells of
C. iejimensis were determined using a Finnigan MAT 251 mass
spectrometer at Hokkaido University, Japan. Individual samples
were reacted with 100% phosphoric acid at 60 °C. Isotope ratios arereported relative to VPDB, and analytical precision (1 SD) was better
than ±0.08‰.
5. Results
5.1. Water conditions and δ18Oseawater
The results show that water temperature within Shodokutsu cavevaried between 20 °C and 29 °C (Fig. 4a). Salinity within the cave
showed seasonal change, ranging from 33.5 to 34.5 (Fig. 4b).
The salinity values from 3 June 2007 to 24 September 2007 are thesame as mean monthly salinity measured at 30 m depth in the opensea (J-DOSS, Fig. 4b). On the other hand, the salinity values from
October 2008 to July 2009 are 0.4 lower than the mean monthly
salinity. For the measurement day (2 July 2007), we found no
signiﬁcant difference in salinity or δ18Oseawater between inside the135cave (salinity = 33.9 psu, δ18Oseawater = 0.3 ± 0.1‰) and outside thecave at 30 m depth (salinity = 34.2, δ18Oseawater = 0.4 ± 0.1‰). The
obtained δ18Oseawater–salinity relationship is similar to the linear
relationship reported by Abe et al. (2009), who measured δ18Oseawaterand salinity within surface water at Ishigaki Island (24°20.2′N,
124°9.8′E), Okinawa, Japan, every 10 days from 1998 to 2004
(δ18Oseawater = −10.3 (±0.5) + 0.31 (±0.01) S, where S = salinity).
Based on the δ18Oseawater–salinity relationship and our salinity data,
δ18Oseawater values within the cave are estimated to be 0.3 ± 0.1‰
throughout the year.
The mean daily temperatures within Shodokutsu cave were higher
by b2 °C than those in Daidokutsu cave during summer, while thewater temperatures in other seasons were similar between the caves.
5.2. δ18O values of living and empty specimens from surface sediments
The shell heights of living specimens from surface sediments in
Shodokutsu cave range from 1.2 to 3.5 mm (Fig. 5b, Table 1). The
δ18Oaragonite values of living specimens collected in early June and late
July ranged from − 1.0 to − 1.5‰ and from − 1.1 to − 1.5‰,
respectively (no signiﬁcant difference). There was no signiﬁcantFig. 5. Relationship between δ18O and the shell height of C. iejimensis. Error bars represent one standard deviation of a single δ18O analysis. Note that the vertical axes are inverted sothat higher temperatures (lower δ18O) are toward the top. (a) Empty shells from surface sediment within Daidokutsu cave; (b) living shells from surface sediment within
Shodokutsu cave; (c) empty shells from surface sediment within Shodokutsu cave; (d) empty shells from core 19 within Daidokutsu cave.

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N. Yamamoto et al. / Global and Planetary Change 72 (2010) 131–140

Table 1Results of oxygen isotope analyses of living specimens of C. iejimensis from Shodokutsu
cave.
Collected in 2009/6/3

Collected in 2009/7/29

Height(mm)

δ18O

Height
(mm)

δ18O

3.5
3.3
2.9
2.7
2.5
2.1
1.7
1.7
1.5
1.5
1.4
1.3
1.3
1.2
1.2

− 1.25− 0.98− 1.37− 1.28− 1.46− 1.31− 1.51− 1.25− 1.22− 1.08− 1.34− 1.36− 1.22− 1.25− 1.08

2.7
2.6
2.5
2.3
2.3
2.2
2.2
2.2
2.2
2.1
2.1
2.0
1.9
1.6

− 1.32− 1.33− 1.25− 1.40− 1.18− 1.50− 1.41− 1.25− 1.17− 1.44− 1.17− 1.14− 1.29− 1.30correlation between shell size and δ18Oaragonite. The mean and 1σdeviation for δ18Oaragonite values were −1.28 ± 0.13‰.
δ18Oaragonite values obtained for empty specimens ranged between−1.3 and −0.6‰, and show a size dependence (n = 54, r = −0.42,
p = 0.002) (Fig. 5c, Table 2). The obtained relationship is as follows:18

δ Oaragonite = –0:11H–0:69

ð3Þ

where H is shell height. The slope of the regression line is similar tothat obtained for empty shells from Daidokutsu cave (−0.10, Fig. 5a;
Yamamoto et al., 2008).
5.3. δ18Oaragonite values of specimens from cored sediments
We obtained the δ18Oaragonite values of 160 specimens from coredsediments (Table 3). Kitamura et al. (2007b; core 01) and Yamamoto
Table 2
Results of oxygen isotope analyses of empty specimens of C. iejimensis from surface
sediments in Shodokutsu cave.
Height(mm)

δ18O

Height
(mm)

δ18O

1.2
1.2
1.2
1.3
1.3
1.3
1.3
1.4
1.4
1.4
1.4
1.4
1.4
1.5
1.5
1.5
1.5
1.5
1.5
1.5
1.6
1.6
1.7
2.1
2.1
2.1
2.2

− 1.02− 0.76− 0.69− 0.96− 0.91− 0.85− 0.76− 1.03− 0.95− 0.91− 0.91− 0.77− 0.65− 0.87− 0.84− 0.80− 0.79− 0.63− 0.62− 0.59− 0.82− 0.64− 0.78− 1.14− 1.07− 0.85− 1.21

2.2
2.2
2.2
2.2
2.3
2.3
2.3
2.4
2.4
2.4
2.5
2.5
2.5
2.6
2.6
2.7
2.8
2.8
2.9
2.9
3.0
3.0
3.0
3.0
3.0
3.0
3.5

− 1.16− 1.03− 0.99− 0.88− 1.03− 1.00− 0.86− 1.33− 1.07− 0.80− 1.01− 0.95− 0.90− 0.96− 0.95− 1.20− 1.17− 0.80− 1.03− 0.99− 1.13− 1.10− 0.95− 0.93− 0.91− 0.76− 0.75et al. (2008; cores 02, 04, and 05) reported the δ18Oaragonite values ofC. iejimensis from cored sediments from Daidokutsu cave. We sorted
these previous data, and our data, into right and left valves (Fig. 7).
The δ18Oaragonite values range from − 2.1 to 1.7‰, with most being
between −1.0 and −0.5‰ (Fig. 5d). The δ18Oaragonite records showthat the long-term trend in δ18Oaragonite has been stable for the past
7000 years, although anomalously heavy δ18Oaragonite values areobserved at 6500 and 5000 cal. years BP (Fig. 7).
We found a statistically signiﬁcant correlation between δ18Oaragonite
and shell height for empty shells from core 19 (Fig. 5d), as follows:
18

ð4Þ

18

ð5Þ

δ Oaragonite = –0:35H + 0:06 ðright valvesÞ
δ Oaragonite = –0:48H + 0:30 ðleft valvesÞ

The slopes of the regression lines for right and left valves (−0.35
and −0.48, respectively) are much steeper than those for empty
shells within surface sediments from Daidokutsu and Shodokutsu
caves. Most of the shells with heavy δ18Oaragonite values are less than
1.5 mm in height and are concentrated in periods dated between 6500
and 5000 cal. years BP.
6. Discussions
6.1. Potential of C. iejimensis as an archive of Holocene palaeoceanography
There is no signiﬁcant difference in salinity or δ18Oseawater between
inside Shodokutsu cave and outside the cave at 30 m depth, thereby
indicating that δ18Oaragonite of C. iejimensis in the cave is not inﬂuenced
by the inﬂow of underground water.
In Shodokutsu cave, the mean water temperature during June is24.9 °C, and about 2 °C lower than values during July (Fig. 4a). Basedon the temperature equations for aragonitic molluscan shells
presented by Grossman and Ku (1986) and Carré et al. (2005), adifference in water temperature of 2 °C would cause a 0.5‰ variationin the δ18Oaragonite value of shell. However, in the living specimens,
there is no signiﬁcant difference in δ18Oaragonite among datasets
obtained in early June and late July. Moreover, small individuals arefound in late July. These ﬁndings are consistent with Yamamoto et al.
(2009b) hypothesis that the species may be able to grow over several
seasons, but are inconsistent with a previous interpretation that shell
deposition begins in early April and ends in July (Kitamura et al.,2007b; Yamamoto et al., 2008). We propose that the size dependenceof δ18Oaragonite of empty shells arises mainly because of thetemperature dependence of mortality rate during the juvenile stage.
Mortality in bivalves is caused by biotic and abiotic factors. Kaseand Hayami (1994) suggested that predators are sparse in Shodokutsu cave and that their activities are infrequent, based on an
analysis of the frequency of drilling predation on cavernicolous microbivalves. Hayami and Kase (1993) noted that C. iejimensis makes up
more than 90% of living individuals from the bottom sediments of
Shodokutsu cave. In fact, we found several tens of living individuals of
the species, but few living individuals of other bivalve species. This
dominance of C. iejimensis indicates that intraspeciﬁc competition,rather than interspeciﬁc competition, is the main cause of mortality inthe species.
The main abiotic agents of mortality are temperature, salinity,
oxygen concentration, siltation, and waves (e.g., Dame, 1996). Basedon our data and observations, we consider that temperature is the
only important abiotic agent of mortality for C. iejimensis. Consequently, among all the agents of mortality for this species, we proposethat temperature is especially important, and we consider that thesize dependence of δ18Oaragonite of empty shells of C. iejimensis iscaused mainly by the high mortality rate of juveniles duringexceptionally cold periods. During such periods, the probability of

N. Yamamoto et al. / Global and Planetary Change 72 (2010) 131–140

137

Table 3Results of oxygen isotope analyses of empty specimens of C. iejimensis from core 19 in Daidokutsu cave.
Depth
(cm)

Valve

Height
(mm)

δ18O

Depth
(cm)

Valve

Height
(mm)

δ18O

Depth
(cm)

Valve

Height
(mm)

δ18O

Depth
(cm)

Valve

Height
(mm)

δ18O

3.5
4.5
17.5
18.5
26.5
33.5
37.5
38.5
49.5
50.5
57.5
59.5
64.5
67.5
69.5
70.5
78.5
84.5
85.5
85.5
89.5
90.5
90.5
91.5
103.5
104.5
106.5
107.5
109.5
110.5
111.5
112.5
113.5
114.5
114.5
114.5
115.5
117.5
117.5
118.5

R
L
L
R
L
R
L
L
R
R
R
R
L
R
L
R
R
R
L
R
L
R
L
R
R
L
L
L
R
L
L
R
R
L
L
R
L
L
R
L

2.5
3.3
3.0
2.0
3.0
2.3
2.5
1.4
1.1
2.7
1.2
1.0
2.2
1.9
2.9
2.7
1.3
2.0
1.4
2.5
2.5
1.2
2.2
1.7
2.6
2.8
1.2
3.1
2.7
1.4
2.3
1.9
2.0
1.2
1.3
1.6
2.2
1.4
1.5
1.7

− 0.73− 0.84− 2.10− 0.64− 0.69− 0.24− 0.74− 0.480.03− 0.75− 0.400.16− 0.73− 1.17− 0.59− 0.670.43− 1.03− 1.86− 0.87− 0.69− 0.81− 1.020.14− 0.90− 0.910.21− 0.89− 0.80− 1.08− 0.84− 0.82− 0.53− 0.61− 0.22− 0.84− 0.71− 0.79− 0.48− 0.59

118.5
119.5
120.5
121.5
122.5
122.5
124.5
124.5
125.5
126.5
126.5
127.5
127.5
127.5
128.5
130.5
130.5
132.5
133.5
134.5
135.5
136.5
137.5
137.5
137.5
138.5
139.5
143.5
146.5
146.5
147.5
147.5
147.5
148.5
149.5
150.5
150.5
150.5
151.5
152.5

R
R
R
R
L
L
R
R
R
R
R
R
L
R
L
R
R
L
L
R
L
R
R
R
R
R
R
L
R
L
R
L
R
R
R
L
R
R
L
L

1.9
2.9
1.8
2.1
2.8
3.0
1.3
2.9
1.2
1.4
2.7
1.9
2.3
3.0
3.0
1.9
2.3
1.1
2.1
2.4
2.1
1.0
1.2
3.0
3.1
1.1
2.0
2.0
1.7
2.4
1.0
1.2
2.8
2.4
1.7
0.9
2.2
2.9
2.0
2.7

− 1.02− 0.59− 0.44− 1.27− 0.71− 0.65− 0.68− 0.420.04− 0.86− 0.61− 1.07− 0.79− 0.64− 0.93− 0.69− 0.950.15− 0.78− 0.77− 0.56− 0.25− 0.72− 0.74− 0.55−0.35− 0.66− 0.79− 0.53− 1.06− 1.170.12− 0.56− 0.88− 0.570.75− 0.91− 0.71− 0.90− 0.67

154.5
155.5
156.5
156.5
156.5
157.5
158.5
158.5
159.5
159.5
160.5
162.5
163.5
164.5
165.5
167.5
168.5
169.5
170.5
171.5
171.5
171.5
172.5
173.5
174.5
174.5
175.5
177.5
178.5
178.5
178.5
179.5
179.5
179.5
179.5
179.5
180.5
181.5
181.5
183.5

R
L
R
L
L
L
L
L
R
R
L
R
L
R
R
R
L
L
L
L
R
R
R
R
L
R
L
R
R
R
R
L
R
R
R
R
L
L
R
L

2.1
1.0
1.1
1.7
2.4
1.4
1.3
1.4
2.5
2.8
2.7
1.5
1.1
1.2
1.0
2.6
1.4
1.6
2.2
0.7
2.2
2.7
1.7
2.4
1.2
2.2
1.4
1.2
1.3
1.4
1.9
1.2
1.2
1.3
2.0
2.2
2.8
1.5
1.5
1.4

− 0.881.08− 0.63− 0.84− 0.99− 0.69− 0.81− 0.87− 1.14− 0.72− 0.83− 0.06
0.39
0.08
0.89
− 0.76− 0.40− 0.70− 0.890.29− 0.97− 0.74− 0.59− 0.90− 0.61− 0.83− 0.75− 0.45− 0.62− 0.97− 1.00− 0.71− 0.440.54− 0.960.19− 0.88− 0.65− 0.60− 1.70

185.5
186.5
186.5
187.5
188.5
189.5
190.5
190.5
191.5
192.5
192.5
193.5
194.5
194.5
195.5
196.5
196.5
197.5
198.5
199.5
199.5
200.5
201.5
202.5
203.5
203.5
204.5
204.5
205.5
205.5
206.5
208.5
209.5
210.5
212.5
215.5
216.5
217.5
218.5
226.5

L
L
R
R
L
R
R
R
L
R
R
R
L
L
L
R
L
L
L
L
R
L
L
R
L
L
R
R
L
L
L
L
L
R
L
R
L
L
R
R

2.5
1.1
1.2
2.5
2.5
2.3
1.8
2.6
1.7
1.6
2.8
2.2
1.4
1.5
2.5
1.3
2.3
2.3
2.0
1.1
2.0
2.3
1.3
1.7
1.0
2.2
1.0
2.2
1.1
1.4
1.4
2.2
1.8
1.5
1.5
2.2
1.1
2.1
2.4
1.3

− 0.59− 0.800.30− 0.88− 0.84− 1.05− 0.70− 0.73− 0.97− 0.65− 0.89− 1.12− 0.78− 0.94− 0.84− 0.29− 0.74− 0.96− 0.850.65− 2.00− 0.80− 0.37− 0.740.40− 0.851.34− 0.931.72− 0.880.20− 0.80− 1.11− 0.64− 0.63− 0.761.03− 0.72− 0.77− 0.49ﬁnding a dead immature individual (empty, small shell) within thedeath assemblage would be much higher than that during periods ofnormal water temperature. As a result, the proportion of specimens in
the death assemblage with high δ18Oaragonite would be lower in thesubgroup of larger specimens.
If the above interpretation is correct, it is likely that shells with theheaviest δ18Oaragonite value (− 0.4‰) among the recent dataset grewunder or close to the lower limit of growth temperature. Many
δ18Oaragonite values heavier than −0.4‰ are found within sedimentdeposited between 6500 and 5000 cal. years BP. Given the widely
accepted view that the environmental tolerance of marine invertebrate species is likely to remain largely constant over a period ofseveral thousand years, we consider that the δ18Oaragonite values
heavier than −0.4‰ indicate unusually low temperature and enrichment of δ18Oseawater (dry conditions).
6.2. Reconstruction of paleoceanographic variations over the past
7000 years
We found no clear long-term trend in the δ18Oaragonite records
during the last 7000 years, except for frequent centennial-scale
ﬂuctuations. The absence of a long-term trend is consistent with theﬁndings of Sun et al. (2005) and Lin et al. (2006), who estimated SST
and δ18Oseawater based on an analysis of the Mg/Ca and δ18O values ofthe planktonic foraminifera G. ruber from deep-sea sediment cores
recovered from the East China Sea (Figs. 2 and 6). The authors foundno clear insolation-related trend of decreasing intensity in thesummer monsoon since the early–middle Holocene, which ischaracteristic of terrestrial records from monsoon regions (An, 2000;
Fleitmann et al., 2003; Wang et al., 2005). This observation of a lack of
any long-term trends in SST, δ18Oseawater, or sea surface salinity (SSS)over the past 6000 years is also supported by other paleoceanographic
studies (Ijiri et al., 2005) and simulations of paleoclimate (Kitoh et al.,2006; Oppo et al., 2007). Sun et al. (2005) and Lin et al. (2006)
proposed that the absence of long-term trends reﬂects the complexityof hydrographic processes, as hydrographic conditions were inﬂuenced by water originating from both high and low latitudes, which
experienced contrasting SST histories during the Holocene. Our study,
as well as that of Lin et al. (2006), detected no distinctive, consistentanomalies in the climatic and hydrologic variability associated with
the Pulleniatina Minimum Event.
As noted above, it is likely that δ18Oaragonite values heavier than
−0.4‰ indicate occurrences of unusually low temperatures and dry
conditions. Thus, our records show anomalously cool and dry events
at about 6300 and 5550 cal. years BP. These events closely coincidewith weak Asia summer monsoon events (Neff et al., 2001; Wanget al., 2005; Selvaraj et al., 2007), and the older event corresponds toone of three summertime cold events (which occurred at about 1700,
2300–4600, and 6200 cal. years BP) inferred from the planktonic
foraminiferal record of the East China Sea (Xiang et al., 2007).
Therefore, we consider that unusually cool and dry events in the East
China Sea may have been related to weak summer monsoon events.
Abe et al. (2009) detected interannual variation of δ18Oseawater ofsurface water (+0.007‰year− 1) based on continuous records from138

N. Yamamoto et al. / Global and Planetary Change 72 (2010) 131–140

Fig. 6. Stratigraphic columns compiled for cores 01, 02, 04, 05, and 19 recovered from within Daidokutsu cave, showing the stratigraphic distribution of Daidokutsu pumice. Also
shown is a map of the distribution of surface sediment facies within the cave. Facies 1, gray calcareous sand; Facies 2, gray calcareous mud; Facies 3, calcareous sand containing theskeletons of partly encrusted coralline sponges.

1998 to 2004 at Ishigaki Island, and proposed that both a reduction in
wintertime northeasterly winds and summertime southwesterly
winds caused a decrease in precipitation and consequent enrichmentof δ18Oseawater around the island. This interpretation is based on thefact that the vapor source for the island is evaporation from the surfaceof the northern East China Sea in winter and the tropics in summer(Fig. 1). If these processes are applicable to decadal- to centennialscale variability in the intensity of East Asian monsoon, a weaksummer monsoon may result in enrichment of δ18Oseawater around thepresent study area. A strong winter monsoon (anomalously low airtemperature) may cause a decrease in δ18Oseawater by transporting
large amounts of vapor and producing anomalous low SSTs, resulting
in heavy δ18Oaragonite values. As noted above, although there has been
considerable debate regarding the nature of variability in the wintermonsoon, Yancheva et al. (2007) reported that the strengths of thewinter and summer monsoons are anti-correlated on a decadal timescale. In such a case, a strong winter monsoon may have contributed tothe anomalously cool and dry events in the East China Sea at about
6300 and 5550 cal. years BP.
As noted above, a weak summer monsoon and strong wintermonsoon occur during times of weak solar activity (Neff et al., 2001;
Fleitmann et al., 2003; Lim et al., 2005; Wang et al., 2005; Xiao et al.,2006; Yancheva et al., 2007). Two anomalously cool and dry events inthe East China Sea took place during the interval of Bond event 4,
which is an ice-rafting event in the North Atlantic (Bond et al., 2001)(Fig. 7). These ﬁndings indicate that these cool and dry events may berelated to weak solar activity.
It is noteworthy that in the present data, the occurrence of heavy
δ18Oaragonite values appears to be obscured after 1000 cal. years BP,
even though a weak Asian summer monsoon event occurred during

the Little Ice Age (Wang et al., 2005). Sixty δ18Oaragonite values fall
between 6500 and 5500 cal. years BP, while 32 values fall in the period
between 1000 years BP and the present. Therefore, it appears to be
difﬁcult to explain the absence of anomalously heavy δ18Oaragonite
values after 1000 cal. years BP in terms of sampling intervals. In
addition, Lin et al. (2006) reported that summertime δ18Oseawater
values in the East China Sea during the early Holocene oscillated
between 0.7‰ and −0.2‰, but the magnitudes of the oscillations
decreased to ∼0.5‰ in the middle Holocene and ∼0.2‰ during 2–1 ka(Fig. 7). These observations may indicate that the mode of the East
China Sea climatic and hydrological response to decadal- tocentennial-scale variability in the intensity of East Asian monsoon
has varied during the past 7000 years. An examination of the cause ofthis mode shift is required to further understand natural climatechange around the East China Sea and East Asia.
7. Conclusions
1. This study found no relationship between shell size and theδ18Oaragonite values of living specimens of the submarine cavernicolous
micro-bivalve C. iejimensis, indicating that the species forms its shellover several seasons. Accordingly, the size dependence of theδ18Oaragonite values of empty shells is well explained by the highmortality rate of juveniles during exceptionally cold periods.
2. Based on our interpretation that the main cause of mortality in thespecies is exceptionally low temperature, we consider that the shells thatformed at the lower limit of growth temperature represent the heaviest
δ18Oaragonite values (−0.4‰). It is therefore likely that the δ18Oaragonite
values heavier than −0.4‰ indicate occurrences of unusually low
temperatures and enrichment of δ18Oseawater (i.e., dry conditions).

N. Yamamoto et al. / Global and Planetary Change 72 (2010) 131–140

139

Fig. 7. Comparison of δ18O values of C. iejimensis from cored samples (present study) with the δ18Oseawater record from the East China Sea (Lin et al., 2006), stalagmite δ18O record
from Dongge cave in southeast China (Wang et al., 2005), and record of ice-rafted debris from the North Atlantic (Bond et al., 2001). Note that the axes are inverted so that higher
temperatures (lower δ18O) are toward the top.

3. The obtained δ18Oaragonite values indicate no clear long-term
trend in SST or δ18Oseawater in the East China Sea during the middle–
late Holocene, and reveal the occurrence of unusually cool and dry
events at around 6300 and 5550 cal. years BP. These events were
probably related to decadal- to centennial-scale variability in theintensity of the East Asian summer monsoon, which was linked inturn to weakened solar activity.
4. The absence of heavy δ18Oaragonite values after 1000 cal. year BP
indicates that the mode of the East China Sea climatic and hydrologic
response to decadal- to centennial-scale variability in the intensity of
East Asian summer monsoon has varied over the past 7000 years.
Acknowledgements
We thank Shigemitu Kinjo and Koushin Yasumura for collecting
samples, and A. Stallard for improving the English in the manuscript.
This study was funded by Grants-in-Aid (16340159 and 19540492)
awarded by the Japan Society for Promotion of Science, The Japan
Science Society, a Sasakawa Scientiﬁc Research Grant, and a Grant-in-Aid
from the Fukada Geological Institute.
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