Matsuzaki et al. Progress in Earth and Planetary Science
https://doi.org/10.1186/s40645-019-0256-3(2019) 6:22

RESEARCH ARTICLE

Progress in Earth andPlanetary Science

Open Access

Paleoceanographic changes in the
Northern East China Sea during the last 400
kyr as inferred from radiolarianassemblages (IODP Site U1429)
Kenji M. Matsuzaki1,2* , Takuya Itaki3 and Ryuji Tada1

Abstract
The East China Sea (ECS) is a shallow marginal sea that is sensitive to glacio-eustatic sea-level changes and is
influenced by warm oligotrophic water of the Kuroshio Current (KC), the nutrient-rich Taiwan Warm Current, andfreshwater discharges from rivers in southern China during the East Asian summer monsoon season. In this area, local
paleoceanographic changes for times prior to 40 ka remain poorly studied because of high sediment accumulation
rates on the seafloor. During Integrated Ocean Drilling Program Expedition 346, long sediment cores representing thelast 400 kyr were retrieved from the northern part of the ECS (Site U1429). In these cores, radiolarians are abundant andwell-preserved, thus using the ecological properties of radiolarians, we analyzed how glacio-eustatic sea-level variations
have influenced the paleoceanography of the ECS over the last 400 kyr, with a focus on changes in water properties atintermediate depths. Additionally, the summer sea surface temperature (SST) and intermediate water temperature atabout 500 m were quantified by means of data on selected radiolarian species. The KC influenced the shallow water at
Site U1429 during each interglacial period over the last 400 kyr (marine isotope stages [MISs] 1, 5, 7, 9, and 11), causing
a high summer SST (about 27 °C), although inflow of the KC into the ECS was probably delayed until after the sea-level
maximum of interglacial MIS 1 and MIS 5. During this lag time, ECS shelf water was the dominant influence on thesystem. During glacial periods (MISs 2–4, 6, and 10), our data suggest that coastal conditions prevailed, probably
because of a sea-level drop of more than 90 m. At these times, the summer SST was colder, ca. 20 °C. Changes in therelative abundance of Cycladophora davisiana indicate that the most significant changes in the bottom water occurred
during MIS 6, when the bottom water likely became poorer in oxygen. An increase in the shallow-water primary
productivity during MIS 7 and MIS 6 was probably the key factor causing the oxygen-poor conditions.
Keywords: East China Sea, Kuroshio current, Changjiang River, Sea-level variations, Primary productivity, Bottom water,
Oxygen-poor seawater, Radiolarians

Introduction
The East China Sea (ECS) is a marginal sea of theNorthwest Pacific, and 70% of this sea lies over a continental shelf. The ECS is influenced by warm oligotrophic
water of the Kuroshio Current (KC), the nutrient-richTaiwan Warm Current (TWC), and discharges of freshwater from the Changjiang River (Chen et al. 1994). The* Correspondence: km.matsuzaki@aori.u-tokyo.ac.jp
1
Department of Earth and Planetary Science, Graduate School of Science,
The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan
2
Present address: Atmosphere and Ocean Research Institute, The Universityof Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan
Full list of author information is available at the end of the article

volume of discharge from the Changjiang River increases
during the East Asian summer monsoon (EASM), whichcauses high precipitation in southern China during summer and thus triggers greater freshwater discharges fromthe Changjiang River (e.g., Ichikawa and Beardsley 2002;
Kagimoto and Yamagata 1997; Tada et al. 2016). Thus,
the Changjiang River supplies a huge amount of freshwater into the northern ECS, and it mixes with the saline ambient water influenced by the TWC and KC toform the ECS continental shelf water (CSW; e.g., Ichikawa and Beardsley 2002). Moreover, upwelling of the
KC subsurface water and the North Pacific Intermediate© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, andreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made.

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

Water (NPIW) at the slope of the ECS continental shelfcontributes to the availability of a large number of nutrients in the shallow water of the ECS (e.g., Chen 1996;
Chen and Wang 1999; Ito et al. 1994; Matsuno et al.
2009).
Global climate during the Pleistocene is known to havebeen characterized by a series of alternating warm andcold (glacial and interglacial) periods, which were regulated and paced by the Milankovitch cycles, and signals
from these cycles are well-recorded in the oxygen isotope
ratio (δ18O) of benthic foraminifera (e.g., Berger andJansen 1994; Hays et al. 1976; Lisiecki and Raymo 2005;
Elderfield et al. 2012). Recently, Elderfield et al. (2012)
tried to separate the effects of temperature and global ice
volume on the deep-ocean foraminifera δ18O. The amplitude of the glacio-eustatic sea-level change (120 m, e.g.,
Yokoyama et al. 2001; Xie et al. 1995) are almost similar
in glacial-interglacial cycles for the past 700 kyr, except
for the MIS7/8 (300 ka). The Pleistocene is also known forbeing influenced by millennial-scale climatic instability,
the so-called Dansgaard-Oeschger (D-O) events, which
are abrupt climatic changes caused by periodic collapsesof continental ice sheets in the Northern Hemisphere andreductions in North Atlantic Deep Water formation (e.g.,
Bond et al. 1993; Dansgaard et al. 1993; Hodell andChannell 2016; Tada et al. 2018; Wary et al. 2016). These
events also caused variations in sea level.
Previous studies have shown that the ECS is sensitive tothe glacio-eustatic sea-level changes caused by the glacial/interglacial cycles because most of its surface water lies
above a continental shelf (< 200 m). Indeed, during glacial
periods over the last 40 kyr, about one-half of the ECS
continental shelf emerged and the mouth of the Changjiang River likely migrated southeastward toward the Okinawa Trough because of a sea-level drop of ca. 130 m(e.g., Ijiri et al. 2005; Kawahata and Ohshima 2004; Tada
et al. 2015; Xie et al. 1995). Such changes in the ECS landscape probably caused drastic changes in the local and regional paleoceanography. Several micropaleontologicaland geochemical studies have reconstructed changes inlocal hydrography of the shallow water over the past 40
kyr (e.g., Ijiri et al. 2005; Kawahata and Ohshima 2004;
Ujiie et al. 1991; Ujiié and Ujiié 1999; Xu and Oda 1999).
It was previously thought that during glacial periods, theKC did not enter the ECS and was deflected to the eastside of the Ryukyu Island Arc (e.g., Ujiie et al. 1991; Ujiié
and Ujiié 1999). At present, most studies agree that during
the Last Glacial Maximum, the KC likely flowed into thesouthern part of the ECS. However, in the northern ECS,
the KC probably shifted southeastward because of a stronger influence of coastal waters (e.g., Ijiri et al. 2005; Xie etal. 1995; Xu and Oda 1999). Recently, several geochemical
studies have also tried to estimate changes in summer sea
surface temperature (SST) and sea surface salinity (SSS)

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over the past 20 kyr to monitor and understand the linkage between changes in EASM intensity and ocean response at millennial and centennial scales with the goal ofquantifying and estimating the impact of the precipitation
related to the EASM on the local paleoceanography of the
ECS (e.g., Horikawa et al. 2015; Kubota et al. 2010, 2015a).
One of the concerns is that the paleoceanographic history of the ECS for periods older than 40 kyr is poorly
known because even long sediment cores (~ 33.65 mlong in Ijiri et al. 2005) only cover the past 40 kyr due tohigh sedimentation rates (~ 84.125 cm/kyr) in this area
(e.g., Ijiri et al. 2005; Huh and Su 1999; Su and Huh2002). Moreover, we still lack information about thechanges in intermediate water hydrography of the ECS,
such as the probable influence of the KC subsurface andthe NPIW on the local paleoceanography. To documenthydrographic changes of the subsurface and intermediate water is not easy in general because most paleoceanographic proxies relied on planktic and benthic
foraminifers, which have calcareous skeletons and inhabit only shallow water (< 300 m) and the seafloor, respectively (e.g., Gooday 2003; Fairbanks and Wiebe
1980; Kuroyanagi and Kawahata 2004). The microfossil
group of radiolarians is the only abundant group bearing
skeletons composed of amorphous silica (SiO2·nH2O)
and inhabiting deep to shallow water depths (e.g., Suzuki
and Aita 2011; Suzuki and Not 2015). Numerous studiesof radiolarians in the Northwest Pacific and its adjacentmarginal seas have demonstrated the suitability of thismicrofossil group as a paleoceanographic proxy (e.g.,
Itaki et al. 2007, 2009; Kamikuri et al. 2007; Matsuzaki
et al. 2014a, 2018; Okazaki et al. 2004). Recently, Integrated Ocean Drilling Program (IODP) Expedition 346,
which aimed to reconstruct changes in EASM intensity
since the Pliocene at high resolution, retrieved sedimentcores at Site U1429 in the Danjo Basin of the northern
ECS. These cores continuously cover the past 400 kyr
despite the high sedimentation rates in this area (Tadaet al. 2015; Sagawa et al. 2018).
Therefore, in this study, we reconstructed the hydrographic changes of the intermediate and shallow water
depths over the past 400 kyr based on the ecologicalproperties of selected radiolarian species at IODP Site
U1429. Our objective was to clarify how the orbitalparameters and their associated sea-level variations haveinfluenced the local and regional hydrography during
the last 400 kyr, with a particular focus on changes atintermediate water depths.

Oceanographic setting of the study area
The surface water of the ECS is influenced by warm, saline water from the KC and TWC (Tomczak andGodfrey 1994) (Fig. 1). The KC originates from theNorth Equatorial Current and transports warm-saline andMatsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

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Fig. 1 Map from Matsuzaki et al. (2016) modified for this study to show the location of site U1429 and the key oceanographic features of thestudy area. CDW means Changjiang diluted water and IODP means Integrated Ocean Drilling Program

oligotrophic water northward. Its flow volume throughthe East Taiwan Strait varies seasonally due to the influence of the EASM, and the highest flow of 24 Sv (1 Sv =106 m3/s) is recorded in summer, while lower flow occurs
in autumn (20 Sv) (e.g., Lee et al. 2001; Kagimoto and Yamagata 1997; Qu and Lukas 2003). In addition, dischargeof freshwater into the northwestern ECS from the Changjiang River causes the formation of a low-salinity seawaterby mixing with the Taiwan Warm Current, the so-called
Changjiang river diluted water (CDW) (Fig. 1) (e.g.,
Ichikawa and Beardsley 2002). The CDW flows southward
along the Chinese coast during winter, whereas during
summer, it flows as a southward coastal jet and has anorthward spread (e.g., Beardsley et al. 1985). The thickness of the CDW is around 30 m in the middle shelf area,
and it has a lower temperature and lower salinity than the
KC surface water (e.g., Isobe and Matsuno 2008). During
the summer, the SST and SSS of the shallow waters of thesouthern ECS water reach maxima of 28 °C and 34‰, respectively (Sun et al. 2005). In contrast, in the northernpart of the ECS, between China and Kyushu Island, theSST and SSS are relatively low, 26 °C and 32‰, respectively. This difference is a consequence of the CDW into
the northwestern ECS (Fig. 1; Ichikawa and Beardsley
2002). The total annual discharge of freshwater into thenorthwestern ECS from the Changjiang River reaches amaximum in summer (Beardsley et al. 1985). Therefore,
the SSS and SST of the northern ECS are greatly reduced
because of the CDW, which dominates the shallow continental shelf before being mixed with the warm, saline,
oligotrophic water of the KC and TWC in the northeastern ECS (Fig. 1).
The ECS shelf area is one of the most productive marine areas of the world because of Changjiang River freshwater discharges (9.24 × 1011 m3 year−1) (Tian et al. 1993)
and upwelling of the KC subsurface water from a water

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

depth of 200–300 m near the slope of the ECS continental
shelf (Wong et al. 1991; Chen and Wang 1999). These
Kuroshio subsurface waters are known for being rich innutrients such as nitrate (Chen and Wang 1999; Chen etal. 1999; Wong et al. 1991). Therefore, the nutrientsbrought up from the euphotic zone increases the local primary productivity (e.g., Chen 1996; Chen et al. 1999). The
contribution of this nutrient upwelling is higher than thatfrom the Changjiang and Yellow rivers (e.g., Chen andWang 1999). Additionally, in the ECS, when the Kuroshio
subsurface water upwells, although its influence is smaller,
some studies have suggested that the NPIW probably
mixes and upwells along the slope of the ECS continental
shelf and also contributes to the formation ofnutrient-rich shallow water (e.g., Chen 1996; Ito et al.
1994). The NPIW is formed in the Okhotsk Sea and ischaracterized by a salinity between 33.9 and 34.16‰ andan oxygen concentrations between 50 and 150 μmol kg−1
(e.g., Kaneko et al. 2001; Bostock et al. 2010). This watermass subducted into and below the thermocline of theKuroshio Extension before it enters subtropical gyres (e.g.,
Kaneko et al. 2001).

Materials and methods
Core samples and age model

In this study, we analyzed sediment core samples collected from Site U1429 during IODP Expedition 346.
Site U1429 is located in the northernmost part of the
ECS at a water depth of 732 m and coordinates 31°
37.04′ N and 128° 59.85′ E (Tada et al. 2015). This site
is located in the southern part of the Danjo Basin, inthe northern part of the Okinawa Trough (Tada et al.
2015). The cores are about 180 m long and characterized by calcareous-nannofossil-rich clay with diatoms
and foraminifera (Tada et al. 2015). The retrieved sediments are heavily bioturbated and contain tephra layersof various thicknesses, ranging from centimeters todecimeters (e.g., Tada et al. 2015; Sagawa et al. 2018).
This sedimentary succession was divided into two lithologic units (A and B) based on sediment composition(Tada et al. 2015). However, we did not analyze lithologic unit B because of heavy drilling disturbance andpoor recovery. Unit A spans the Holocene to Middle
Pleistocene (0 to 400 kyr) and consists of olive-gray tolight-greenish calcareous-rich clay with intercalation oftephra layers (Tada et al. 2015).
In this study, we used the core composite depth below
seafloor (CCSF-D) scale of Irino et al. (2018). The depths
in CCSF-D were then converted to ages (ka) following
the age model proposed by Sagawa et al. (2018), which
relies upon the oxygen isotope stratigraphy of benthic
foraminifer tuned to the LR04 benthic stack (Lisiecki
and Raymo 2005).

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Assemblage analysis

In this study, we analyzed changes in the radiolarian assemblage for 124 samples at about 0.5 to 1.5 m intervals
between 0 and 180 m CCSF-D. To monitor changes in
the northern ECS hydrography, changes in radiolarianassemblages and absolute abundances were analyzed fora continuum of the past 400 kyr. Additionally, we estimated the variation in summer SST and intermediatewater temperature at a depth of ca. 500 m by applying
the method proposed by Matsuzaki and Itaki (2017).
Two types of microscopic slides were mounted: faunalslides (F-slides) and quantitative slide (Q-slides). The
first preparation steps were similar for both types ofslide: the 124 samples were freeze-dried, treated with diluted hydrogen peroxide (H2O2) (15%, i.e., 50 ml of
H2O2 at a concentration of 30% diluted in 100 ml ofwater) and hydrochloric acid (15%) (40 ml of HCl at aconcentration of 35–37% diluted in 100 m of water) toremove organic and calcareous matter. The undissolved
residue in each sample was sieved through a 45-μm
screen following the method proposed in Tada et al.
(2015). Once the undissolved residue was washed, we
mounted slides following the procedures proposed by
Itaki et al. (2009). Then, we examined polycystine radiolarians under an optical microscope at magnifications of
× 100 to × 400 on both types of slide. All radiolarians
were identified and counted until at least 400 individual
tests were identified in each sample, or until the sample
material was exhausted (see the Additional file 1). The
identification followed the nomenclature of Itaki (2009),
Matsuzaki et al. (2015a), and Zhang and Suzuki (2017).
On average, we counted 435 specimens per slide.
We used changes in the entire radiolarian assemblage
over time to estimate species diversity because they canbe used to constrain changes in radiolarian productivity.
We used the software PAST 3 of Hammer et al. (2001)
to estimate the number of taxa (S), or species richness,
which is a count of species recorded in each sample; wealso determined the Shannon-Wiener index (H′), which
describes species diversity by accounting for the relative
proportion of each species within a sample as follows:X
H0 ¼ 
P i lnP i ;where Pi is the proportion of each species i in the sample (Shannon and Weaver 1949).
We also estimated species dominance (D), whichranges from 0 (all taxa are equally present) to 1 (onetaxon dominates the community completely), as follows:X
D¼
ðni =nÞ2 ;where ni is number of individuals of taxon i and n is thetotal number of samples (e.g., Harper 1999). The dominance is related to the Simpson index (D = 1 – Simpson

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

index); however, in this study, the use of D was more
useful for explaining our dataset.
From the full assemblage, where 144 species wereidentified in 124 samples (see the Additional file 1), we
selected 45 species with well-known geographic and vertical distributions for reconstructing the paleo-summer
SST and intermediate water temperature following thenomenclature of Matsuzaki and Itaki (2017). Then, toreconstruct the regional paleoceanography over the past
400 kyr, we selected ten species whose ecology is wellunderstood for the ECS based on the findings of Matsuzaki et al. (2016) (Figs. 2 and 3).
Sea surface and intermediate water temperature
estimation

We estimated the SST and intermediate watertemperature at a water depth of ca. 500 m by applying
the method proposed by Matsuzaki and Itaki (2017),
who used the transfer function of Imbrie and Kipp
(1971) on a dataset composed of 87 surface sediments
collected in the Northwest Pacific with a particular focus
on the seas surrounding Japan, including the northern
ECS, where more than 20 surface sediment samples wereanalyzed [see Matsuzaki and Itaki 2017 for details].
Briefly, modern summer SST and intermediate watertemperature at a water depth of ca. 500 m were attributed to each of the analyzed locations using the World
Ocean Atlas 2013 (Locarnini et al. 2013) and interpolated (with a 1 × 1° grid) onto the geographic position ofeach surface sediment station, as detailed in Matsuzaki
and Itaki (2017). Following the method of Matsuzaki
and Itaki (2017), we selected 28 species living in shallow
water (upper 200 m) for SST estimation and 17 species
living at intermediate water depths for the estimation ofintermediate water temperatures (Additional file 2: Table
S1 and Additional file 3: Table S2).
For the SST estimates, all the selected species shown
in Additional file 2: Table S1 overlap with a water depthof 0 m (e.g., Matsuzaki et al. 2016; Matsuzaki and Itaki
2017; Okazaki et al. 2004). Thus, we assumed that thereconstructed SST based on these selected shallow-water
species reflect a water depth of 0 m. However, in
Matsuzaki and Itaki (2017), the approach adopted by the
University of Bremen was used (i.e., http://www.geo.uni-bremen.de/geomod/ staff/csn/woa-sample.html), which
integrates the temperature data for the upper 10 m provided by the World Ocean Atlas. Therefore, the reconstructed SST corresponds to an average of the upper 10 mof the water column. In addition, as shown in Matsuzaki
and Itaki (2017), we assumed that the reconstructed SST
corresponds to the summer SST because the radiolarian
flux is generally low during winter in the Northwest Pacific (e.g., Itaki et al. 2008; Okazaki et al. 2005; 2008). For
the intermediate water temperature estimates, a similar

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assumption was adopted. The selected 17 intermediatewater species overlapped with water depths of 500 m, andthus we assumed that intermediate water temperatures reconstructed using these selected species corresponded tothose of water ca. 500 m deep. Then, intermediate watertemperatures at ca. 500 m provided by the World Ocean
Atlas were interpolated (i.e., Matsuzaki and Itaki 2017).
The relative abundance of the selected species was normalized using the procedures of Matsuzaki and Itaki(2017). The selected species and their normalized abundances are shown in Additional file 2: Table S1 andAdditional file 3: Table S2. The SST and intermediatewater temperature were then quantified using the PAST
software (Hammer et al. 2001), which implements the
CABFAC and REGRESS routines of the original methodof Imbrie and Kipp (1971) for Q-mode factor analysis (i.e.,
Matsuzaki and Itaki 2017).

Results
Radiolarian absolute abundances

We estimated 1.25 × 104 skel. g−1 to be the median absolute abundance of radiolarians at Site U1429 (Fig. 4). In
this study, we considered values higher than the median
to represent high radiolarian abundance. The interval
between 0 and 240 ka, which corresponds to MISs 1–7,
was characterized by high radiolarian absolute abundances. For this period, most of the estimated absoluteabundances were higher than the median and exceeded
2.5 × 104 skel. g−1 during interglacial periods (MISs 1, 5,
and 7; Fig. 4). During glacial periods (MISs 2, 4, and 6),
radiolarian absolute abundance was lower than the median in only a few intervals: at about 20 ka during MIS
2; at about 70 ka during MIS 4; and at about 130 and
190 ka during MIS 6 (Fig. 4). Therefore, radiolarianabundance was generally high between 0 and 240 ka,
with the highest absolute abundances attained during
warm interglacial periods. In contrast, the time interval
between 240 and 400 ka was characterized by lower
radiolarian absolute abundances (Fig. 4). Most of thevalues in this interval are lower than the median.
Radiolarian diversity

We estimated radiolarian diversity by analyzing the fullradiolarian assemblage (the list of taxa is provided in
the Additional file 1). We assumed that the number oftaxa (S) of radiolarian species and species groups canbe used as a diversity index. The median number of
species per sample was 57 (Fig. 4). The species diversity
was higher during interglacial periods, with a maximum
during MIS 5, when the number of radiolarian species
exceeded 90 (Fig. 4). Additionally, a drastic increase in
the number of radiolarian species was recorded at the
MIS 5/6 boundary (ca. 130 ka). Before the MIS 5/6
boundary, the number of radiolarian species (and thus

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Fig. 2 Key Spumellarian species encountered at Site U1429. 1–4 Actinomma leptodermum (Jørgensen) (sample 346-U1429A-7H6-27-29 cm); 5–6
Actinomma boreale Cleve (sample 346-U1429A-7H6-27-29 cm); 7 Actinomma medianum Nigrini (sample 346-U1429A-1H1-27-29 cm); 8-9 Spongodiscus
cf. resurgens Ehrenberg (sample 346-U1429A-1H1-27-29 cm); 10-11 Larcopyle weddelium Lazarus, Faust and Popova (sample 346-U1429A-7H6-2729 cm); 12 Spongosphaera streptacantha Haeckel (sample 346-U1429A-1H1-27-29 cm); 14 Druppatractus irregularis Popofsky (sample 346-U1429A-1H127-29 cm); 15-17 Phorticium polycladum Tan and Tchang (sample 346-U1429A-1H1-27-29 cm); 13 Larcopyle cf. buetschlii Dreyer (sample 346-U1429A7H6-27-29 cm); 18 Tetrapyle circularis Haeckel (sample 346-U1429A-7H6-27-29 cm); 19–21 Tetrapyle fruticosa (Tan and Chen)(sample 346-U1429A-7H6-27-29 cm)

the diversity index) was lower than or close to the median value of 57 and never exceeded 70 (Fig. 4). Thus,
radiolarian diversity was higher between 0 and 130 ka
than between 130 and 400 ka.

We also calculated the species dominance index (D) toassess the evenness of the radiolarian assemblages(Fig. 4). The median value of D was 0.05 during the past
400 kyr at Site U1429 (Fig. 4). High species dominanceMatsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

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Fig. 3 Key Nassellarian species encountered at Site U1429. 1–2 Botryostrobus auritus (Ehrenberg) (sample 346-U1429A-7H6-27-29 cm); 3–5
Cycladophora davisiana Ehrenberg (sample 346-U1429C-10H4-27-29 cm); 6–9 Arachnocorallium calvata Petrushevskaya group (sample 346-U1429A7H6-27-29 cm); 10, 14 Phormospyris spp. (10. sample 346-U1429C-10H4-27-29 cm, 11 sample 346-U1429A-7H6-27-29 cm); 11–13 Arachnocorys
castanoides Tan and Tchang (sample 346-U1429A-1H1-27-29 cm); 15–17 Pseudocubus obeliscus Haeckel (sample 346-U1429A-7H6-27-29 cm); 21-24
Lithomelissa setosa Jørgensen (sample 346-U1429A-7H6-27-29 cm); 18-19 Pseudodictyophimus gracilipes (Bailey) (sample 346-U1429C-10H4-27-29 cm);
20 Plectacantha oikiskos (Jørgensen) (Sample 346-U1429A-7H6-27-29 cm); 26 Dimelissa thoracites (Haeckel) (sample 346-U1429A-1H1-27-29 cm);
25 Phormacantha hystrix Jørgensen

is recorded at the MIS 6/7 boundary, with several successive values higher than the median (Fig. 4). However,
the highest values of D were recorded between MIS 2
and late MIS 5, with the maximum value being

approximately 0.20 (Fig. 4). This result suggests thatduring MISs 2–4, the radiolarian assemblage was likely
dominated by a single species, and thus ecological conditions enabling this dominance prevailed.

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

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Fig. 4 Radiolarian absolute abundance. The number of taxa (S), dominance index (D), and Shannon-Wiener diversity index (H′) are shown overtime and compared to the benthic foraminifera isotope curve of Sagawa et al. (2018). Red lines indicate median values

The last species diversity index that we calculated was
the Shannon–Wiener index (H′). The median value of
this index is 3.43 (Fig. 4). In general, between mid-MIS 6

and MIS 11, H′ was close to the median value; however,between mid-MIS 6 and MIS 1, except for MIS 2, theindex value was slightly higher, close to 3.8. This result

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

suggests higher species diversity for the mid-MIS 6 to
MIS 1 time interval, except for MIS 2. During intervals ofhigh species dominance (MISs 2–4 and at the MIS 6/7
boundary), H′ was at a minimum, with values close
to 2.6 (Fig. 4).
In general, the values of the diversity index suggestthat radiolarian species diversity increased after 130 ka(MISs 1 and 5).

Relative abundances of selected species

We selected ten species or species groups that are usefulfor reconstructing the paleo-hydrography of the northern ECS over the past 400 kyr from the full radiolarianassemblage (Fig. 5). Species selection was conductedwith reference to Matsuzaki et al. (2016): in that study,
radiolarians collected from plankton tows were analyzed
to clarify the regional spatial and vertical radiolarian distributions (see Matsuzaki et al. (2016) for details). The
raw data of the present study are available in the Additional file 1.
In the northern ECS (Site U1429), the occurrenceof the Tetrapyle circularis/fruticosa group (Fig. 5b)
sensu Zhang and Suzuki (2017) was high during eachinterglacial period (i.e., MISs 1, 5, 7, 9, and 11; Fig.
5). The highest abundance of the T. circularis/fruticosa group (> 22%) was recorded during MIS 9 (300–337 ka). Recently, it has been proven that all species
belonging to the Tetrapyle genus have algal symbionts
and inhabit warm shallow water (Zhang et al. 2018).
In addition, this species group has been found inareas influenced by warm-water currents (e.g., the KC
and its related branches), such as the northern ECS,Japan Sea, and Japan’s Pacific coast (e.g., Lombari and
Boden 1985; Itaki et al. 2004, 2007, 2010; Motoyama
and Nishimura 2005; Kamikuri et al. 2008; Itaki 2009,2016; Boltovskoy et al. 2010; Matsuzaki et al. 2014a,
2015a, 2015b, 2016; Botovskoy and Correa 2016; Matsuzaki and Itaki 2017). Therefore, the high abundanceof T. circularis/fruticosa during interglacial periods
implies an influence of the KC at Site U1429 (Fig. 5).
Additionally, the maximum abundance of the T. circularis/fruticosa group and its fluctuation patternchanged between MISs 6 and 7. For MISs 1 and 5,
an increase in T. circularis/fruticosa abundance occurred after a sea-level rise, whereas for MISs 7 and
9, increases in T. circularis/fruticosa abundance were
almost synchronous with a sea-level rise (Fig. 5).
Didymocyrtis tetrathalamus (Haeckel) (Fig. 5g) is also
known to inhabit shallow warm water (e.g., Lombari and
Boden 1985; Boltovskoy et al. 2010; Botovskoy and Correa 2016; Matsuzaki and Itaki 2017). However, at the
study site, D. tetrathalamus exhibited no significant variations in abundance in response to glacial–interglacial

Page 9 of 21

cycles, and its relative abundance rarely exceeded 2% of
the assemblage (Fig. 5).
The species Lithomelissa setosa Jørgensen (Fig. 5c)
was almost absent from Site U1429 during interglacial
periods; in contrast, it dominated the radiolarian assemblages during glacial periods, with relative abundances greater than 30% of the total assemblage,
except during MIS 8 (Fig. 5). L. setosa is a transitional–subarctic species, and it is abundant along thecoasts of the Sea of Okhotsk and northeastern Japan(e.g., Itaki et al. 2008; Matsuzaki and Itaki 2017). In
the northern Atlantic, L. setosa is dominant in fjord
areas (Bjørklund et al. 1974). Additionally, Itaki et al.
(2008) suggested that this species is probably characteristic of nutrient-rich coastal areas. Therefore, ourdata suggest that during MISs 2–4, 6, and 10, Site
U1429 was influenced by relatively cold, nutrient-richcoastal water.
At present, Pseudocubus obeliscus Haeckel (Fig. 5d) isan abundant species in the northern ECS (Matsuzaki etal. 2016). In our data, this species exhibited higher relative abundances, with values close to 10% of the assemblage, when the sea level was rising or falling, such as at
MIS boundaries (Fig. 5).
The species Arachnocorallium calvata Petrushevskaya (Fig. 5e) is associated with the shallow water ofthe ECS continental shelf and is probably characteristic of ECS continental shelf water (Matsuzaki et al.
2016). In our data, the relative abundances of A. calvata were slightly higher for the period between 0
and 170 ka, for which a relative abundance higher
than 6% was recorded (Fig. 5).
The species Actinomma medianum Nigrini (Fig. 5f)
exhibited low abundance throughout the core, except
during MIS 10 (337–375 ka), in which the relative abundance of this species exceeded 5% of the total assemblage (Fig. 5). At present, this species is associated withtransitional waters of the Northwest Pacific, where the
KC and Oyashio Current mix (Matsuzaki and Itaki2017). This distribution suggests that MIS 10 probably
was warmer than other glacial periods. In addition,
Lithomelissa setosa was less abundant during MIS 10(Fig. 5), consistent with this interval being warmer.
The species group Actinomma boreale/leptodermum
sensu Itaki et al. (2004) showed higher relative abundances between 100 and 290 ka, which corresponds to
MISs 5–9 (Fig. 5h). Two high-abundance peaks (> 20%of the total assemblage) were recorded during MIS 6 at
ca. 140 and 180 ka (Fig. 5). Additionally, the relative
abundance of this species was nearly 10% of the total
assemblage almost continuously between 190 and 290
ka (Fig. 5). This species is a subarctic species (e.g., Kling
1979; Okazaki et al. 2004; Kamikuri et al. 2008), and in
the modern ECS, it dominates the assemblage at

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

Page 10 of 21

Fig. 5 Relative abundances of key radiolarian species encountered at Site U1429 over time, with comparison to the benthic foraminifer isotope
curve of Sagawa et al. (2018)

intermediate water depths (Matsuzaki et al. 2016).
However, Pseudodictyophimus gracilipes (Bailey) had
its highest abundance during MIS 10 (337–375 ka;
Fig. 5i). Pseudodictyophimus gracilipes is also a
subarctic species that lives at intermediate water
depths in the ECS (Matsuzaki et al. 2016), although

it inhabits shallow to subsurface water depths at
higher latitudes (e.g., Kling 1979; Okazaki et al.
2004). High abundances of these species may suggest
a greater influence of subarctic water at intermediatewater depths in the ECS from 100 to 290 ka andfrom 337 to 375 ka.

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

The Botryostrobus auritus/australis (Ehrenberg) group
showed high abundance during the earliest stages of MIS
9 (300–337 ka), when its relative abundance exceeded
10% of the total assemblage (Fig. 5j). The ecology of thisspecies at that time is largely unknown, but Matsuzaki
and Itaki (2017) found that this species is probably related
to the intermediate water of southern Japan.
The abundance of Cycladophora davisiana Ehrenberg (Fig. 5k) was more than 5% of the total assemblage between ca. 160 and 400 ka. The ecology ofthis species is well understood: its presence implies
cold, oxygen-rich intermediate water (e.g., Boltovskoy
and Riedel 1987; Kling and Boltovskoy 1995; Okazaki
et al. 2003; Itaki and Ikehara 2004; Abelmann and
Nimmergut 2005; Itaki et al. 2009; Matsuzaki et al.
2014b; Matsuzaki and Itaki 2017). Therefore, our data
indicate that, the intermediate water depth of the

Page 11 of 21

ECS was likely cold and well ventilated at 160–400ka.
Summer SST and intermediate water temperature variations
over the past 400 kyr

By applying the dataset and method proposed by Matsuzaki and Itaki (2017), we estimated the paleo-summer
SST and intermediate water temperature at ca. 500 m
based on the selected radiolarian species using the transfer function of Imbrie and Kipp (1971) with an error
margin of 0.9 °C for paleo-summer SST and 1.2 °C forintermediate water temperature (Fig. 6 and Additional
file 4: Table S3; see Matsuzaki and Itaki 2017 fordetails).
Our reconstruction shows that the paleo-summer SST
at Site U1429 fluctuated between 18.1 and 28.3 °C, withan error margin of 0.9 °C (Fig. 6). During eachFig. 6 Radiolarian-based estimates for intermediate water temperature and SST over time and compared to the benthic foraminifera isotope
curve of Sagawa et al. (2018). Dashed curves indicate modern median temperatures. Also shown are the summer SST estimated using the Mg/Ca
ratio of planktic foraminifera (Kubota et al. 2010) in the northern Okinawa Trough and bottom water temperature estimated using the Mg/Ca
ratio of benthic foraminifera in the southern Okinawa Trough (Kubota et al. 2015b)

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

interglacial period, the summer SST exceeded 26 °C, witha maximum of 28.3 °C at 1.5 ka (MIS 1), whereas during
glacial periods, the summer SST was between 18 and
22 °C, with a minimum of 18.1 °C at 263 ka (MIS 8; Fig.
6). During interglacial periods, our reconstructed summer
SST values are close to the modern summer SST (27 °C)
at Site U1429; the values for glacial periods are between
those of modern winter and spring SSTs (17–21 °C;
Locarnini et al. 2013; Fig. 6).
The reconstructed intermediate water temperature atca. 500 m fluctuated between 3.9 and 8.0 °C, with an error
margin of 1.2 °C (Fig. 6). These temperatures correspondto the modern intermediate water temperature at ca.
500 m water depth at Site U1429 (ca. 7 °C) and thetemperature at ca. 500 m off northern Japan (ca. 4 °C;
Locarnini et al. 2013). The maximum value of 8.0 ± 1.2 °C
was recorded at 180 ka (during MIS 6); the minimum of
3.9 ± 1.2 °C was recorded at ca. 60 ka (MIS 4; Fig. 6). Although the glacial to interglacial variation is within theerror range of the method, the reconstructed intermediatewater temperature at ca. 500 m seems to indicate
warmer temperatures during interglacial periods andcolder temperatures during glacial periods between 0
and 130 ka (MISs 1–5; Fig. 6). However, for older
time intervals, there appears to be no correlation withglacial–interglacial cycles.

Discussion
Comparison of radiolarian-based summer SST andintermediate water temperatures

We compared our SST data with the results of Kubota etal. (2010), who estimated summer SSTs on the basis ofvariations in the Mg/Ca ratio of the planktic foraminifer
Globigerinoides ruber (D’Orbigny). The radiolarian-based
summer SST and Mg/Ca variation-based summer SST are
similar for interglacial periods, confirming the suitabilityof our method. However, there are some discrepancies between the two sets of results for glacial periods (Fig. 6):
radiolarian-based summer SSTs are ca. 2 °C colder thanthose inferred from foraminifera. Although there is noclear explanation for this pattern at this time, wehypothesize that for glacial periods, our summer SST
values do not reflect the temperature near the water
surface but rather the temperature at ca. 100 m. During
glacial periods, the dominant radiolarian species was
Lithomelissa setosa (Additional file 2: Table S1), which inhabits the subsurface (e.g., Bjørklund et al. 1974; Itaki
2004; Matsuzaki et al. 2016). Therefore, our glacial-period
SST values may reflect the subsurface sea temperatures,
whereas during interglacial periods, because of the highabundances of KC species that prefer the upper 25 m of
the water column in the northern ECS (Matsuzaki et al.
2016), it is likely that we obtained information on the partof the environment similar to the habitat of G. ruber (0–Page 12 of 21

50 m, Kuroyanagi and Kawahata 2004). However, because
the ECS is strongly affected by local and regional influences, such as the EASM, which causes freshwater andsediment discharges into the ECS, it is also possible that
the Mg/Ca ratio of foraminifera was influenced by suchfactors. To test this hypothesis, the radiolarian-based SST
should be compared again with the SST estimated from
Mg/Ca ratios in foraminifera and, if possible, thealkenone-based SST in an area less subject to such regional influences, such as the open ocean.
We also compared our reconstructed intermediate
temperature data with those of Kubota et al. (2015b),
who estimated the seawater temperatures at 1100 m
depth in the southern Okinawa Trough from variations
in benthic foraminifera Mg/Ca ratios. Our intermediatewater temperature curve fluctuates in a manner similar
to that of the temperature estimated using benthic
foraminifera Mg/Ca over the last 15 kyr (Fig. 6). Although we note a discrepancy of ca. 3 °C, it can easily be
explained by the effect of water depth. Indeed, ourtemperature estimates correspond to a water depth ofca. 500 m, whereas those of Kubota et al. (2015b) are forwater depths of ca. 1100 m, and it is reasonable to record warmer temperatures at shallower depths.
Evolution of local shallow water over the last 400 kyr

The hydrography of the ECS shallow water is sensitive
to glacio-eustatic sea-level changes caused by glacial–interglacial cycles (Figs. 5, 7, and 8). Based on the paleoceanographic changes inferred from our radiolarian data,
as described in the “Results” section, an overview of ECS
shallow-water hydrography during each of the three
sea-level regimes that have prevailed during the past 400
kyr is provided in Fig. 8.
Evolution of local shallow water during interglacial periods

The fluctuations of the radiolarian-based summer SST
curve are generally synchronous with those of the oxygen isotope curve of benthic foraminifera at Site U1429(Sagawa et al. 2018). The summer SST values were close
to the modern summer SST during interglacial periods(ca. 27 °C) (Fig. 6). This increase in SST was caused by
the presence of the KC at Site U1429. Indeed, the radiolarians Tetrapyle circularis/fruticosa and Didymocyrtis
tetrathalamus, which are markers of KC water in the
Northwest Pacific (e.g., Lombari and Boden 1985;
Boltovskoy et al. 2010; Hernández-Almeida et al. 2017;
Matsuzaki and Itaki 2017), showed relative abundanceshigher than 15% during MISs 1, 5, 7, 9, and 11 (Fig. 7).
This finding suggests that KC water influenced the shallow water of the northern ECS during each interglacial
period of the past 400 kyr (Fig. 7). This result is inagreement with previous studies suggesting that the KC
influenced the northern ECS during interglacial periods

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

Page 13 of 21

Fig. 7 Temporal fluctuation of various radiolarian abundances: a benthic foraminifera isotope curve of Sagawa et al. (2018), b radiolarian absoluteabundance, c insolation at 65° N (Paillard et al. 1996), d coastal water species (%), e KC-related species (%), and f continental shelf species (%)(Xie et al. 1995; Xu and Oda 1999; Ijiri et al. 2005; Shi etal. 2014). Our study also demonstrates that the path of
the KC was probably similar to the modern path during
every interglacial period of the past 400 kyr.
However, for MIS 1 and MIS 5, the SST and therelative abundances of KC species increased after thebenthic foraminiferal δ18O values reached a low point,
which indicates a sea-level maximum (Figs. 5 and 7).
Furthermore, the abundance of Arachnocorallium
calvata increased at those times (Fig. 7). This species isknown to inhabit the ECS shelf water (Matsuzaki et al.
2016); thus, our data imply that when the sea-level roseand reached a maximum, shelf water expanded eastwards
and influenced our study site. Therefore, the KC only influenced our site and the northern ECS after the rise in
sea level. These MIS transitions correspond to maxima ofsummer insolation at 65° N. In the ECS, and Asia in general, maxima of summer insolation at 65° N are associatedwith maxima of EASM intensity, which causes an increasein precipitation. Thus, during these maxima, discharges offreshwater into the ECS are higher (e.g., Wang et al. 2001,
2008). Therefore, in the ECS, it is probable that intensification of the EASM and the related southeastwards
expansion of ECS shelf water weakened the KC inflow thatpasses across the northern ECS at the MIS 1/2 and MIS
5/6 transitions (Fig. 8).
Evolution of local shallow water during glacial periods

During the last glacial period (MIS 2), the ECS continental shelf was exposed, which triggered eastward migration of the coastlines and river mouths of the main
Chinese rivers (Xie et al. 1995; Xu and Oda 1999; Kawahata and Ohshima 2004; Ijiri et al. 2005). However, thepaleoceanography of older glacial periods has remained
unknown because of the lack, until now, of sedimentcores covering time intervals prior to 40 ka. Based on

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

Page 14 of 21

Fig. 8 Postulated hydrographic evolution of the northern ECS over the last 400 kyr

our data, the paleoceanographic conditions during MISs
2–4, 6, and 10 were likely very similar, although MIS 10
was probably warmer because Actinomma medianum, atransitional species of the North Pacific, exhibited
relative abundances of about 5% (Figs. 5 and 7). Thus, asimilar sea-level drop probably occurred during MISs 2–
4, 6, and 10 (Fig. 8). This scenario is consistent with arecent study that attempted to separate the effects oftemperature and global ice volume on deep-ocean
foraminiferal δ18O values (Elderfield et al. 2012). The
radiolarian Lithomelissa setosa, a coastal-water species,
dominated the assemblage with relative abundances exceeding 40% during these glacial periods (Fig. 7). In themodern era, L. setosa dominates the coastal environmentof northern Japan and is absent offshore (Kamikuri et al.
2008; Matsuzaki and Itaki 2017). Additionally, thisspecies is probably associated with nutrient-richcoastal water created by suspension of lithogenic matter (Itaki et al. 2008). Therefore, our data suggest thatduring MISs 2–4, 6, and 10, nutrient-rich coastal
water prevailed because of probable higher input of
terrigenous matter and consequent eastward migration of the coastline.
For MISs 2–4 and 6, high variability in Lithomelissa
setosa abundance and radiolarian absolute abundance
are observed, whereas the benthic foraminiferal δ18O

curve does not show such variability (Fig. 7). During thepast 1500 kyr, the climate at high latitudes of the Northern Hemisphere was influenced by millennial-scale D-O
events (e.g., Bond et al. 1993; Dansgaard et al. 1993,
Hodell et al. 2016; Tada et al. 2018). These high-latitude
climate changes likely affected the EASM and paleoceanography of seas adjacent to Asia, such as the Sea ofJapan, by influencing the path of the westerly jet (e.g.,
Tada et al. 1999; Tada 2004; Itaki et al. 2007; Kido et al.
2007; Nagashima et al. 2007, 2011; Ikehara and Oshima2009). As argued by Oba et al. (1991) and Tada et al.
(1999), the ECS is the only source of the surface waterin the Sea of Japan. Therefore, the high variability in L.
setosa abundance and radiolarian absolute abundance
recorded at site U1429 was probably related to the influence of D-O events, but our sampling interval precludes
further discussion here.
The MIS 8 glacial period stands out as different fromother glacial periods during the past 400 kyr. Indeed, although coastal species dominated during other glacial
periods, during MIS 8, continental shelf species (A. calvata and Pseudocubus obeliscus) and KC species showed
high abundances during the later and earlier parts of thestage, respectively (Fig. 7). During early MIS 8, the benthic foraminiferal δ18O values were close to those of
MIS 5 (Sagawa et al. 2018), suggesting that early MIS 8

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

was distinguished by warmer deep water, a smaller
sea-level drop, or both (Fig. 8). Indeed, the estimates ofElderfield et al. (2012) also imply a relatively smaller
glacio-eustatic sea-level drop during MIS 8; thus, it isprobable that the warming recorded during early MIS 8
in the northern ECS was related to the sea level beingslightly higher than during other glaciations. The causesof this higher sea level are not understood at this time.
In other areas, unexpected warming was recorded forthe northern Japan Pacific coastal areas (off the Shimokita Peninsula) based on radiolarian data (Matsuzaki etal. 2014a), whereas the time interval corresponding to
MIS 8 is missing (hiatus) from sediment cores retrieved
at sites C0001 and C0002 during IODP Expedition 315
on the Pacific side of the Honshu Island coast off the Kii
Peninsula, Japan (Matsuzaki et al. 2015b). In the Northwest Pacific (Shatsky Rise ODP Site 1209), calcareous
nannofossil data suggest an increase in primary productivity during MISs 8–12 (Bordiga et al. 2013). Additionally, planktic foraminiferal and calcareous nannofossil
data suggest that a modern water-mass structure wasestablished in the Northwest Pacific (Shatsky Rise ODP
1210) at ca. 300 ka (MIS 8; Chiyonobu et al. 2012).
Therefore, MIS 8 appears to have been different fromother glacial maxima, but this difference cannot currently be explained based on our data and other available multi-proxy data available for this stage.
Evolution of local primary productivity and its consequences
for bottom water
Evolution of local primary productivity based on radiolarians

Ocean acidification can drastically affect biomineralization by calcareous micro-organisms (e.g., Kawahata et al.
2018), but such effects are not well understood forpolycystine radiolarians. Indeed, we just know that theskeletons of polycystine radiolarians are composed ofamorphous (opaline) silica, and undersaturation of opal
in sea water causes opal to dissolve at the seafloor (e.g.,
Takahashi 1981). These observations imply that the absolute abundance of radiolarians in sediment is affectedby changes in both primary productivity and dissolution
at the seafloor. At Site U1429, the preservation of radiolarian skeletons has been reported to be moderate togood (Tada et al. 2015), which was confirmed by our observations. Specifically, no signs of strong dissolution
were recognized because most species were identifiable
and only slight damage to individual specimens was observed. Such minor changes in radiolarian preservation
may be related to changes in sedimentation rates because at Site U1429 the sedimentation rates varied from30 to 40 cm/kyr during interglacial periods to ca. 60–
80 cm/kyr during glacial periods (Sagawa et al. 2018).
Therefore, we assume that dissolution is not the main
factor regulating radiolarian absolute abundances. In

Page 15 of 21

addition, most of the radiolarian species inhabiting shallow water in tropical to subtropical areas of the NW Pacific bear algal symbionts (Suzuki and Not 2015; Zhang
et al. 2018). This fact suggests that radiolarians contribute, in part, to primary ocean productivity, at least inwarm areas (De Wever et al. 2001; Suzuki and Not 2015;
Zhang et al. 2018). In Fig. 9, we plotted total radiolarianabsolute abundances and absolute abundances of species
bearing algal symbionts following Zhang et al. (2018).
Both curves fluctuate in a similar manner, suggestingthat radiolarian absolute abundance is likely related toocean primary productivity, at least in warm areas. Additionally, modern observations have indicated that the
maximum radiolarian standing stock occurs at the water
depths in which the chlorophyll-a concentration is at a
maximum (e.g., Kling 1979; Matsuzaki et al. 2016).
However, there is a discrepancy between radiolarianabundance and other primary productivity indicatorssuch as total organic carbon (TOC %) and diatom
abundance (Tada et al. 2015; Fig. 9). The TOC and diatom data show that primary productivity at this site did
not alter in association with glacial and interglacial cycles; instead, the primary productivity seems to havechanged during the time interval between 130 to 220 ka(Fig. 9). This discrepancy can be explained by considering that two factors control ocean primary productivity:
sunlight and nutrients. Radiolarians related to the KC
bear algal symbionts because they inhabit oligotrophic
waters and thus have to obtain energy from photosynthesis. This fact explains why the absolute abundancesof algal-symbiont-bearing radiolarians were higher during interglacial periods, and suggests that the absoluteabundances of algal-symbiont-bearing species can beused as a primary productivity index for interglacial periods. However, this index cannot be used to compare
primary productivity between interglacial and glacial
periods. Indeed, our data show that the KC did not influence our site during glacial periods; thus, the absolute abundances of algal-symbiont-bearing species
decreased. In contrast, the percentage abundances ofcoastal species increased during glacial periods becauseof the sea-level drop and consequent southeastward migration of the coastlines and river mouths of the main
Chinese rivers, which might have led to a marked increase in the nutrient levels in shallow water. This finding indicates that, although we detected a drastic
decrease in the abundances of species that bear algal
symbionts, high nutrient levels were available in theshallow water during glacial periods, and thus theocean primary productivity should have been also highduring those times. Therefore, to compare and discusschanges in ocean primary productivity during glacial
periods, abundances of coastal species (such as Lithomelissa setosa) should be used.

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

Page 16 of 21

Fig. 9 Temporal fluctuation of the local primary productivity: a benthic foraminifera isotope curve of Sagawa et al. (2018), b radiolarian absoluteabundance, c radiolarian absolute abundance of species bearing algal symbiosis based on Zhang et al. 2018 (A. vinculata, B. scutum, L. hispida, P.
obeliscus, P. praetextum, P. clausus, A. lappacea/spinosa, D. tetrathalamus, D. muelleri, P. pylonium group, S. resurgens, S. streptacantha, Tetrapyle
circularis/fruticosa group, L. reticulata, Heliodiscus spp., D. elegans), d C. davisiana (%), e continental shelf species (%), f total organic carbon (TOC)(%), and g diatom abundances

In this context, the absolute abundance of radiolarians
that bear algal symbionts indicate higher primary productivity for the interglacial periods MISs 1, 5, and 7, but
not MISs 9 and 11 (Fig. 9). In contrast, the abundancesof coastal species were higher during MISs 2–4 and 6
than during MIS 8 and 10 (Fig. 9). Combining bothtypes of radiolarian data, our results suggest an increasein local primary productivity from the MIS 6 to MIS 7(130–220 ka). The data on TOC (%) and diatom abundances of Tada et al. (2015) suggest a similar trend, witha higher TOC (%) around late MIS 6 and an increase indiatom abundance during early MIS 7 (Fig. 9).
The increases in primary productivity during MISs 2–
4 and 6 are difficult to explain, but the amplitude ofsea-level drop and/or changes in wind intensity may
have been the cause(s). In contrast, the increase in primary productivity during interglacial periods is probably
related to KC dynamics. Previous studies showed thatthe productivity and nutrient content of the northern
ECS are controlled by upwelling of the KC subsurface
water on the slope of the ECS continental shelf because
this subsurface water is rich in nutrients such as nitrate(Wong et al. 1991; Chen and Wang 1999; Chen et al.
1999). Although the mechanism causing upwelling ofKC subsurface water is debated, Chen and Wang (1999)
and Chen (2000) suggested that advection of freshwater
discharged from rivers by estuarine circulation allowed
KC subsurface water to well up to the shelf. This

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

upwelling supplied nutrients to the continental shelf ofthe ECS, which increased the local primary productivity(e.g., Chen 1996; Chen et al. 1999). Therefore, wehypothesize that local productivity may have been lower
during MIS 9 than in later interglacial periods becauseof weaker upwelling of KC subsurface water at the slopeof the ECS.
Primary productivity and changes in intermediate water
oxygenation

The intermediate water of the ECS was probably lesssensitive than the shallow water to the glacio-eustatic
sea-level changes forced by orbital parameters. The reconstructed intermediate water temperature at ca.
500 m was apparently lower for the time interval frommid-MIS 6 to MIS 11 (> 160 ka) compared to later MISs
(Fig. 6). This finding is based on the occurrence of
Cycladophora davisiana, which had a relative abundance
of 5% or more of the total assemblage between mid-MIS
6 and MIS 11, whereas for the interval between MIS 1
and mid-MIS 6, its relative abundance was approximately 0% (Figs. 5 and 9).
Previous studies demonstrated that Cycladophoradavisiana dominates the radiolarian assemblage of the
Okhotsk Sea Intermediate Water (OSIW), which has
cold, oxygen-rich water masses (Okazaki et al. 2003,
2004; Hays and Morley 2004; Itaki and Ikehara 2004;

Page 17 of 21

Abelmann and Nimmergut 2005; Matul 2011). In the
North Pacific, C. davisiana dominates assemblages inareas where the NPIW is formed (young NPIW), particularly in the northern Japan Oyashio area, where
the OSIW mixes with water of the North Pacific (Talley 1993; Yasuda 1997, 2004; Okazaki et al. 2003;
Itaki and Ikehara 2004; Abelmann and Nimmergut
2005; Itaki et al. 2009; Matul 2011; Matsuzaki et al.
2014b; Matsuzaki and Itaki 2017). In other areas of
the North Pacific, particularly at middle to low latitudes, the relative abundance of C. davisiana is much
lower, even in areas influenced by the NPIW (e.g.,
Boltovskoy and Riedel 1987; Kling and Boltovskoy
1995; Matsuzaki and Itaki 2017). Therefore, we canassume that C. davisiana is abundant in areas directly
and/or indirectly influenced by the OSIW and that
this species is related to cold, oxygen-rich water
masses. In addition, based on studies conducted in
the modern ECS, C. davisiana generally inhabitswater depths below 500 m, although its abundance islow (< 1.5%; Fig. 10; Matsuzaki and Itaki 2017).
Therefore, we can infer that, as our site is ca. 730 m
below present-day sea level, the abundance of C.
davisiana is indicative of the bottom-water environmental conditions. Therefore, our data imply that thebottom water was moderately oxygenated and relatively cold between 160 and 400 ka, whereas afterFig. 10 Current vertical distribution of C. davisiana in the ECS based on the dataset of Matsuzaki and Itaki (2017)

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

than 160 ka, the bottom water was oxygen-poorer
and also probably warmer (Fig. 7).
Changes in Cycladophora davisiana abundance cannot
be explained by plausible changes in the NPIW
influence, because the NPIW is characterized by low
oxygen content in the ECS, and C. davisiana prefers an
oxygen-rich environment (e.g., Kaneko et al. 2001).
Thus, we attribute changes in bottom-water oxygenation
to local factors. Indeed, from our data and other onboard data of Tada et al. (2015) discussed above, thetime interval between MIS 1 and MIS 7 (0–220 ka) was
probably characterized by higher primary productivity inshallow waters (Fig. 9). This finding implies that the
deep-sea sediments collected from site U1429 becamericher in organic carbon after 220 ka (Fig. 9). Therefore, it
is likely that the inferred increase in the primary productivity of shallow waters during MIS 6 and MIS 7 enhanced
the production of organic matter (carbon), which sank tothe sea bottom and increased the amount of organic carbon in deep-sea sediments. This organic carbon accumulated at the seafloor and was oxidized, which consumed
the available oxygen at these depths (e.g., Ruddiman2001). Therefore, an increase in the shallow-water productivity reduced the amount of available oxygen in thebottom water and thus decreased the bottom-water oxygenation, which probably caused the lowering of C. davisiana abundance.

Conclusions
Analysis of radiolarian assemblages collected from Site
U1429 enabled us to reconstruct the paleoceanographic
history of the northern ECS over the last 400,000 years.
We conclude that radiolarians in the ECS were sensitive
to environmental changes caused by glacio-eustatic
sea-level variations and regional climatic events in thefollowing ways.
1. Although the similarity of radiolarian assemblagesfor MISs 1, 5, 7, and 9 suggests that the modern KC
flow was not significantly altered during previous
interglacial periods, during MIS 1 and MIS 5 our data
implies that the KC influenced the ECS after the sea
level had risen. The radiolarian assemblages suggestthat the shelf water of the ECS probably influenced
the study site during sea-level maxima. This effect
was probably related to the high solar insolation at
65° N during those times and probable intensificationof the EASM, which intensified freshwater discharge
into the ECS.
2. During glacial periods (MISs 2–4, 6, and 10), becauseof a sea-level drop of ca. 90 m, the ECS continental
shelf emerged. In this context, our radiolarian assemblages imply that coastal conditions prevailed at siteU1429, although MIS 10 was probably warmer.

Page 18 of 21

Additionally, our data suggest that the shallow water
was likely rich in nutrients due to injection of lithogenic matter into the shallow water precipi1tated byeastward migration of the Chinese coastline.
3. The intermediate water temperature at a water
depth of ca. 500 m reconstructed from ourradiolarian assemblages fluctuated roughly
synchronously with the interglacial–glacial period
cycle between 0 and 130 ka (MIS 5/6 boundary).
For older periods, the water temperature at ca.
500 m was probably not related to these cycles.
4. The data on radiolarian assemblages suggest thatthe bottom-water oxygenation changed at siteU1429 around 160 ka. Oxygen-poor conditions appear to have prevailed after mid-MIS 6 (ca. 160kyr), whereas the interval between mid-MIS 6 andMIS 11 was relatively richer in oxygen. This change
was probably caused by increased shallow-waterproductivity, which resulted in larger amounts ofsinking organic matter; oxidation of this additionalorganic matter led to increased oxygen
consumption.

Additional files
Additional file 1: Counts of radiolarians species at Site U1429 (IODP346). (XLSX 118 kb)
Additional file 2: Table S1. Relative abundance (%) of selected shallow
water species after the normalization of Matsuzaki and Itaki (2017) toestimate the paleo-summer SST at site U1429 (PDF 37 kb)
Additional file 3: Table S2. Relative abundance (%) of selectedintermediate water species after the normalization of Matsuzaki and Itaki(2017) to estimate the paleo intermediate water temperature at ca.
500 m at site U1429 (PDF 32 kb)
Additional file 4: Table S3. Reconstructed paleo-summer SST and intermediate water temperature at ca. 500 m at site U1429 with margins oferror (PDF 21 kb)
Abbreviations
CCSF-D: Core composite depth below sea floor; CDW: Changjiang river
diluted water; CSW: Continental shelf water; D-O events: DansgaardOeschger events; EASM: East Asian summer monsoon; ECS: East China Sea;
IODP: Integrated Ocean Drilling Program; KC: Kuroshio Current; MIS: Marine
isotopic stage; NPIW: North Pacific Intermediate Water; OSIW: Okhotsk Sea
Intermediate Water; SSS: Sea surface salinity; SST: Sea surface temperature;
TOC: Total organic carbon; TWC: Taiwan Warm Current
Acknowledgments
We would like to thank IODP Expedition 346 for providing us with the samples
and the curators of the Kochi Core Center for their sampling assistance. We also
wish to thank Dr. Li Lo (Guangzhou Institute of Geochemistry) and Dr.
Tomohisa Irino (Hokkaido University) for helpful advice. Lastly, we wish to thanktwo anonymous reviewers for helpful comments, advice, and criticisms which
helped to improve our manuscript significantly.
Funding
This research was financially supported by the Japan Society for the Promotionof Science (JSPS) Grant-in-Aid for Young Scientists (B), number 15 K17782
awarded to MKM. This work was also partially financed by IODP Exp. 346 After
Cruise Research Program, JAMSTEC awarded IT and JSPS KAKENHI Grant
Number 16H04069 to Yusuke Okazaki (Kyushu University).

Matsuzaki et al. Progress in Earth and Planetary Science(2019) 6:22

Availability of data and materials
The radiolarian data used in this study are available in the appendix, which is
attached to this study as supplementary material.
Competing interests
The authors declare that they have no competing interest.
Authors’ contributions
MKM conducted treatment and analysis on 124 samples from Site U1429, drew
figures, tables, interpreted the data, and wrote the manuscript. IT and TR
assisted with data interpretation, proposed the topic, and designed the study.
Authors’ information
MKM is assistant professor at the University of Tokyo; IT is a senior researcher
at the Geological Survey of Japan, AIST; and TR is a professor of the
University of Tokyo and was the host researcher of MKM until 2018.08 andthe co-chief of IODP Exp. 346.

Publisher’s NoteSpringer Nature remains neutral with regard to jurisdictional claims inpublished maps and institutional affiliations.
Author details
1
Department of Earth and Planetary Science, Graduate School of Science,
The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-0033, Japan.
2
Present address: Atmosphere and Ocean Research Institute, The Universityof Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan. 3Geological
Survey of Japan, AIST, Marine Geology Research Group/Institute of Geology
and Geoinformation, Tsukuba Central 7, 1-1-1 Higashi, Tsukuba, Ibaraki
305-8567, Japan.
Received: 11 March 2018 Accepted: 7 January 2019

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