Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54
https://doi.org/10.1186/s40645-018-0204-7

Progress in Earth andPlanetary Science

RESEARCH ARTICLE

Open Access

Paleoceanographic history of the Japan Sea
over the last 9.5 million years inferred fromradiolarian assemblages (IODP Expedition
346 Sites U1425 and U1430)
Kenji M. Matsuzaki1,2* , Takuya Itaki3, Ryuji Tada1 and Shin-ichi Kamikuri4

Abstract
Previous studies showed that the evolution of the Japan Sea paleoceanography since the Miocene has been
influenced by the regional tectonism (e.g., opening/closing of the connecting seaways) and regional/global climate.
In the Japan Sea, Expedition 346 of the Integrated Ocean Drilling Program (IODP) retrieved core sediments datingback to the Miocene at two sites (U1425 and U1430). In this study, we reconstruct shallow-to-deep-water hydrographyof the Japan Sea during the Mio-Pliocene based on radiolarian assemblages at Sites U1425 and U1430 considering the
local tectonism and changes in global/regional climate. Our data suggest that glacioeustatic sea-level changes haveprobably had an influence on the local paleoceanography between 9.5 and 7.0 Ma. Indeed, warm water probably
flowed from the North Pacific into the Japan Sea when sea level was high via shallow central and eastern seaways.
In addition, the sill depth of the northern seaway was probably close to 1000 m between 9.5 and 7.8 Ma and had
probably allowed inflow of oxygen minimum zone water from the North Pacific to the Japan Sea when sea level
was high. In contrast, our data imply that Cycladophora nakasekoi, an endemic species to the Japan Sea, dominatedbetween 9.5 and 7.3 Ma when sea level was low. Our data also suggest a progressive shoaling of the sill for the period
since 7.8 Ma and that global climatic events such as such the late Miocene cooling (7.5–5.5 Ma) and the early Pliocene
warmth have had a sustained influence on the Japan Sea. During the mid-Pliocene, a deep cooling of the subsurface
to intermediate water of the Japan Sea likely occurred because species related to subarctic subsurface to intermediatewaters were dominant between 5 and 3.8 Ma. The Northern Hemisphere Glaciation (ca. 3.0–2.7 Ma) and Mid-Pleistocene
Transition (1.2–0.8 Ma) have both likely intensified the cooling of the Japan Sea.
Keywords: Japan Sea, Integrated Ocean drilling program, Paleoceanography, Sea-level changes, Sill depths, Oxygen
minimum zone, Radiolarians

Introduction
The Japan Sea is a back-arc basin opened by continental
rifting during the late Oligocene to middle Miocene
Epoch, ca. 28–13 million years ago (Ma) (e.g., Tamaki etal. 1992; Jolivet et al. 1994). Currently, the Japan Sea isconnected to neighboring seas by four shallow straits: theTsushima Strait (sill depth of 130 m) connecting to 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

East China Sea, the Tsugaru Strait (sill depth of 130 m)
connecting to the Pacific, and the Soya and Mamiya
Straits (sill depths of 55 and 12 m, respectively) connecting to the Sea of Okhotsk (Fig. 1). Therefore, water exchanges are restricted only to the surface waters of theEast China Sea, Northwest Pacific, and Sea of Okhotsk,
and intrusion of intermediate and deep waters is prevented (e.g., Gamo et al. 2014). This semi-isolation of theJapan Sea leads to formation of its own deep water, theso-called Japan Sea Proper Water, by cooling of the Tsushima Warm Current (TWC) (e.g., Gamo et al. 2014). The
Japanese islands and Sakhalin Island, which bound theeastern margin of the Japan Sea, are characterized by© The Author(s). 2018 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.

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Fig. 1 Location of the study sites and the local oceanographic setting of the Japan Sea. The map was generated by the software Ocean Data
View 4 of Schlitzer (2016)active tectonism, which drastically modified the Japan Sea
paleogeography, such as the sill depths of the key straits
during the Neogene (e.g., Iijima and Tada 1990; Jolivet etal. 1994; Kosaka et al. 1992; Kano et al. 1991; Suzuki 1989;
Taira 2001).
During the middle Miocene, a sedimentary basin called
the Fossa Magna was formed in central Japan because of
back-arc rifting associated with the opening of the Japan
Sea (e.g., Iijima and Tada 1990). The paleobathymetry ofthis basin evolved from deep water depths in the middle
Miocene (middle bathyal sedimentary facies) to shallow
water depths in the late Miocene (shallow-water sedimentary facies) (e.g., Fujii et al. 1992; Iijima and Tada 1990;
Kobayashi and Tateishi 1992; Kosaka et al. 1992). The beginning of a compressional stress regime in Northeast
Japan due to the collision of the Izu-Bonin Arc since themiddle Miocene may have caused the shoaling and closureof this seaway ca. 8–7 Ma (e.g., Sato 1994; Sato et al. 2004;

Iijima and Tada 1990; Yoshida et al. 2013). In addition, during the late Miocene, a few shallow seaways (about 200 mdeep) probably existed in Northeast Japan because of subsidence of the Tohoku-Hokkaido area during the late Miocene (Sato 1994; Yoshida et al. 2013). However, thesesubsided areas were also likely uplifted because of the compressional stress regime, which started ca. 8–7 Ma (Sato
1994; Yoshida et al. 2013) (Fig. 2). At the same time, thesouth of the Japan Sea was likely isolated by land from theNorth Pacific because no marine fossils and microfossils
were recorded from the late Miocene (ca. 10 Ma) to theearly Pliocene (ca. 4 Ma) along the eastern edges of the Yellow and South China seas (e.g., Iijima and Tada 1990; Kano
et al. 1991; Wang et al. 2014) (Fig. 2). In the northern Japan
Sea (corresponding to the southern to central part of
Hokkaido Island), several geological studies suggested thata bathyal environment prevailed since the beginning of thelate Miocene until the late Pliocene (e.g., Fukusawa 1988;

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Fig. 2 Evolution of the Japan Sea since 10.5 Ma and its paleomaps (based on Fukusawa 1988; Fujii et al. 1992; Iijima and Tada 1990; Sato 1994;
Kano et al. 1991; Kharakhinov 2010; Kobayashi and Tateishi 1992; Kosaka et al. 1992; Sagayama, 2002; Yahata 2002; Yoshida et al. 2013). The baselines of the coasts and hydrography came from http://d-maps.com

Iijima and Tada 1990; Itaki 2016; Kosaka et al. 1992; Kano
et al. 1991; Sagayama 2002; Suzuki 1989; Ogasawara 1994;
Yahata 2002) (Fig. 2). At the northernmost Japan Sea, in thearea presently around the Sakhalin and Tatar straits, tectonic studies suggested that a neritic environment prevailed
from the middle Miocene to the end of the late Miocene(Kharakhinov 2010) (Fig. 2). A southward shift of the
Okhotsk plate likely caused a southward migration of theKuril basin and a progressive shoaling and closure of the
Sakhalin seaways during the early to late Pliocene (Takeuchi
et al. 1999; Kharakhinov 2010).
Paleoceanographic conditions in the Japan Sea are
known to have been sensitive to orbital and suborbital
forcings and glacioeustatic sea-level changes during the
middle to late Pleistocene (e.g., Tada et al. 1999; Itaki etal. 2007; Kido et al. 2007). Currently, the TWC is theunique current flowing into the Japan Sea and controlling its oceanographic condition (Gamo et al. 2014)(Fig. 1). After entering, the TWC bifurcates into threebranches at the southwestern part of the Japan Sea near
the Tsushima Strait (Hase et al., 1999) (Fig. 1). The firstbranch of the TWC (TWC B1) flows along the west
coast of Honshu Island (Fig. 1). The second branch of
the TWC (TWC B2) flows along the Korean peninsula
before rejoining TWC B1, and the third branch of the
TWC (TWC B3) flows along the Korean Peninsula
northward to form the Leman Cold Current (LCC in
Fig. 1). During the Pleistocene, the amplitude of glacioeustatic sea-level variations caused by orbital cycles
was about 100 m (e.g., Miller et al. 2005; Siddall et al.

2003; Yokoyama et al. 2001; Itaki 2007; Itaki et al. 2004).
Because the Tsushima Strait has a shallow sill depth(about 130 m), a sea-level variation of about 100 m restricted flow of the TWC into the Japan Sea, leading to adecrease in surface water salinity and drastically reducing the local deep-water ventilation, which resulted in
euxinic bottom-water conditions (e.g., Kido et al. 2007;
Oba et al. 1991; Tada et al. 1999).
For the Mio-Pliocene, Tada (1994) compiled the published sedimentological and diatom data of Koizumi(1992a, 1992b) and Tada and Iijima (1992) related to thepaleoceanographic history of the Japan Sea and discussed
the sill depth of the connecting straits that could have influenced exchanges between the Japan Sea and the North
Pacific. Tada (1994) suggested that sediment deposition in
the Japan Sea began at ca. 20 Ma, and the sea was open to
the south, east, and north until ca. 10.5 Ma. Warm surface
water and relatively oxic bottom water conditions prevailed
until ca. 15–14 Ma, when a drastic cooling was recorded.
Mollusca fossil records also suggest this kind of coolingand indicate that temperate water prevailed since ca.
13 Ma (Chinzei 1978; Ogasawara 1994). According to recent studies, this cooling is closely related to the mid-Miocene global cooling events (15–14 Ma), including the East
Antarctic Ice Sheet expansion and stabilization (Holbournet al. 2013, 2014; Zachos et al. 2001, 2008). The southernstrait closed ca. 10.5 Ma, which enhanced the cooling of
the Japan Sea (Tada 1994; Ogasawara 1994). In contrast,
sedimentary, microfossil facies, and chemical data suggestthat the Japan Sea bottom water was oxygen-deficient from

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

18 to ca. 6.5 Ma (Hanagata 2003, 2006; Tada 1994; Yamamoto et al. 2005). Tada (1994) suggested that the origin of
the oxygen-poor water was related to inflow of oxygen
minimum zone (OMZ) water of the adjacent North Pacific.
The presence of this OMZ in the North Pacific during the
Miocene may be controvertible. However, Woodruff and
Savin (1989) used measurement of δ13C in the benthic foraminifer Cibicidoides to report a very low δ13C value for
the North Pacific between latitudes 20° and 40° at water
depths between ca. 1000 and 3000 m during the middle
and late Miocene. This implied the presence of a layer withlow dissolved oxygen content in the North Pacific between
1000 and 3000 m at that time (e.g., Woodruff and Savin1989). Additionally, radiolarian studies were conducted in
the context of the Deep-Sea Drilling Program (DSDP) andOcean Drilling Program (ODP) (namely, legs 31, and 127
and 128). These studies mainly produced biostratigraphic
reports (Alexandrovich 1992; White and Alexandrovich
1992; Ling 1992). Kamikuri and Motoyama (2007) showed
that, at DSDP Site 302, radiolarian species related to theNorth Pacific deep water occurred in the Japan Sea between 8 and ca. 3 Ma, which suggests inflow of deep waterof the North Pacific into the Japan Sea. These findings
showed that the hypothesis proposed by Tada (1994) forthat time is plausible, although some concern remains
about the ecology of the radiolarian species associated with
the North Pacific deep water. For the late Pliocene, few
studies have reconstructed paleoceanographic conditionsof the Japan Sea. Most of them agree that, during the late
Pliocene, cold surface water prevailed in the northern partof the Japan Sea, while warm water from the southernstrait (Tsushima Strait) influenced the sea only during
interglacial periods (e.g., Kitamura and Kimoto 2006;
Kitamura et al. 2001).
Problem addressed here

Our knowledge about global and regional climatic events
has improved greatly. Recent studies stressed the importance of the monsoon on the global climate andocean and also stressed the importance of the uplift of
the Tibetan-Himalayan Plateau at the Oligocene/Miocene boundary in establishing the monsoon (e.g., Betzler
et al. 2017; Clift 2017; Holbourn et al. 2018; Tada et al.
2016). The monsoon has an influence on the carbon
cycle by controlling chemical weathering and thus
strongly affecting the global climate (Raymo and Ruddiman 1992; Tada et al. 2016). During the late Miocene
between 7 and 5.5 Ma, a period of global cooling was reported for the middle to high latitudes of both hemispheres, the so-called late Miocene cooling event(Herbert et al. 2016). Recent studies suggested that theEast Asian winter monsoons (EAWM) were probably
stronger at that time, and thus the EAWM probably
played an important role in the late Miocene cooling

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event (Holbourn et al. 2018). Recent studies suggested
that the beginning of the shoaling of the Panama Isthmus to a few hundred meters of water depth probably
caused changes in the meridional deep ocean circulation(Butzin et al. 2011). Then, during the Pliocene, the final
closure of the Panama Isthmus caused drastic changes
in ocean salinity/heat distributions that may have triggered the Northern Hemisphere Glaciation (NHG) (e.g.,Cortese et al. 2004; Haug et al. 2001; Karas et al. 2017;
Motoi et al. 2005; Sandoval et al. 2017; Steph et al. 2006;
Raymo 1994; Stroynowski et al. 2015). These changes
may have caused an episodic strong Atlantic meridional
overturning circulation between 4.5 and 3.8 Ma (Karaset al. 2017). In addition, although it remains under
debate, between 16.4 and 8 Ma, the Indonesian seaway,
which allowed water mass exchanges between the
Northern Pacific and the Indian Ocean, closed progressively and probably caused the formation of a
proto-Kuroshio Current (e.g., Kennett et al. 1985;
Ogasawara et al. 2008).
Consequently, the reconstruction of changes in theJapan Sea paleoceanography during the Mio-Pliocene is
crucial for a better understanding of how the Japan Sea
was affected by these global tectonic and climatic events.
Objective and strategy

In this study, we analyzed deep-sea sediments of the JapanSea collected during Expedition 346 of the Integrated
Ocean Drilling Program (IODP) to reconstruct pasthydrographic conditions of the Japan Sea during the
Mio-Pliocene. Sediment cores were collected from sevensites covering wide latitudinal and depth ranges in theJapan Sea. We selected samples collected at Sites U1425
and U1430 in the central and southcentral parts of theJapan Sea during IODP Expedition 346 because hemipelagic sediments covering the middle Miocene to Pliocene
were retrieved (Tada et al. 2015a, 2015b). We analyzed
154 sediment core samples collected at Site U1425 (about
2000 m deep) and 51 samples collected at Site U1430(about 1000 m deep) to reconstruct past paleoceanography of the Japan Sea since the late Miocene. In the Japan
Sea, the present calcite compensation depth (CCD) isabout 2000 m, and dissolution of planktic foraminifera begins at a depth of about 1400 m (Ujiie and Ichikura 1973).
Lee et al. (2000) reported that the CCD was likely shallower during the Mio-Pliocene. These data show that theuse of paleoceanographic proxies based on calcareous microfossils is not necessarily suitable for the Japan Sea, particularly for sites with water depths deeper than 1000 m(Sites U1425 and U1430). Consequently, the use of assemblages of siliceous microfossils appears to be a unique alternative to reconstructing oceanographic conditions of
the shallow to deep waters. Because radiolarians are aunique siliceous microfossil group inhabiting shallow toMatsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

deep waters, we analyzed their assemblages and changes
over time to reconstruct hydrographic changes of theshallow to deep waters since the Miocene.

Methods/experimental
Sites studied

In this study, we analyzed sediment core samples collected from Sites U1425 and U1430 drilled during IODP
Expedition 346 (2013). However, because a hiatus is present
between 7.2 and ca. 4.5 Ma at Site U1430 (Kamikuri et al.
2017; Tada et al. 2015b), most of the analysis was conducted on samples from Site U1425. In this study, weonly used data from Site U1430 to provide supporting
information.
Site U1425 is located in the central part of the Japan
Sea, in the middle of the Yamato Bank (1909 m water
depth) at 39° 29.44′ N and 134° 26.55′ E (Tada et al.
2015a). The drilling at Site U1425 recovered a total of
417.5 m of sediment (recovery rate of 98%). The description of the sediment core lithology at Site U1425 given
below follows that of Tada et al. (2015a).
The lithology of Mio-Pliocene sediments at this site
can be divided into three major lithological units, andeach is subdivided into two subunits (e.g., IA and IB)

Page 5 of 33(Figs. 3 and 4). Unit III is the older and deeper lithological unit (> 262 m CCSF-D; > 7.419 Ma) (CCSF-D isan abbreviation for core composite depth below seafloor). This unit consists of clay, diatom-rich clay, anddiatom ooze. This unit can be divided into two subunits
based on the degree of lithification (IIIA and IIIB). Subunit IIIB corresponds to the depth interval deeper than
356 m CCSF-D (> 9.528 Ma), and it is characterized bygray siliceous claystone with occasional parallel laminations and burrows. Lithological subunit IIIB is not discussed in this study, because it contained no biogenic
silica. Subunit IIIA corresponds to the depth interval between ca. 356 and 262 m CCSF-D (9.528–7.419 Ma)(Figs. 3 and 4). This subunit is characterized by decimeter- to meter-scale cyclic alternation of dark gray diatom ooze and moderate to heavily bioturbated clayey
diatomaceous ooze. A fine lamination of diatom ooze
occurring within a dark organic-rich layer extending to a
thickness of about 1.5 m has been recognized at 275 m
core depth below seafloor (CSF-A) (Tada et al. 2015a),which corresponds to about 287 m CCSF-D (Irino et al.
2018). Based on the age model of Kamikuri et al. (2017),
these laminations occurred about 8 Ma. Lithological unit
II corresponds to a depth interval between ca. 262 andFig. 3 Radiolarian absolute abundance (AB) (skel/g) and relative abundance (%) of selected radiolarian species (1/2) at Site U1425 plotted by age(Ma) (Kamikuri et al. 2017 depth age model) and compared to the lithological units of Tada et al. (2015a). Narrow red shading on the AB curve
corresponds to the mean AB for each lithological subunit

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Fig. 4 Radiolarian absolute abundance (AB) (skel/g) and relative abundance (%) of selected radiolarian species (2/2) at Site U1425 plotted by age(Ma) (Kamikuri et al. 2017 depth age model) and compared to the lithological units of Tada et al. (2015a). Narrow red shading on the AB curve
corresponds to the mean AB for each lithological subunit

99 m CCSF-D (7.419–2.722 Ma) (Figs. 3 and 4). This
unit consists of diatomaceous clay and diatomaceous
ooze that is moderately to heavily bioturbated. Unit II
can be distinguished from unit III by a decrease in terrigenous matter. This unit is divided into two subunits(IIA and IIB) based on the diatom content and intensityof bioturbation. Subunit IIB (ca. 262–137 m CCSF-D;
7.419–4.200 Ma) is dominated by brownish diatom ooze.
Diatom content (70–90% of the smear slide) is a key
component for the recognition of this subunit. Subunit
IIA (ca. 137–99 m CCSF-D; 4.200–2.722 Ma) mainly
consists of brownish-greenish diatom-rich clay. In general, the sediments of subunit IIA are heavily bioturbated. Unit I corresponds to a depth interval between ca.
99 and 0 m CCSF-D (since 2.722 Ma) (Figs. 3 and 4).
Unit I consists of clay and silty clay with small amountsof diatom-rich clay, while foraminifer-bearing clay israre. This unit is divided into two subunits (IA and IB)
based on the frequency of the color alternations (darkand light layer) and the intensity of bioturbation. Subunit IB (ca. 99–51 CCSF-D; 2.722–1.244 Ma) consists oflight greenish gray clay with a low frequency of dark andlight color alternation. Subunit IA (ca. 51–0 m CCSF-D;
since 1.244 Ma) is dominated by clay, small amounts ofdiatomaceous-bearing clay, and tephras. This subunit isalso characterized by a pronounced decimeter-scale alternation of light and dark layers.
Site U1430 is located on the southern slope of theeastern South Korean Plateau (1083 m below sea level)at 37° 54.16′ N and 131° 32.25′ E. As above, the lithology of the sediment cores at Site U1430 is describedfollowing Tada et al. (2015b) (Fig. 5). The lithology ofthis site consists of clayey silt, silty clay, nannofossil
ooze, diatom ooze, claystone, and sandstone. This site
can be divided into four units (I to IV), and each of units
I to III is further divided into two subunits based on
sediment composition and relative abundances of biosiliceous and siliciclastic fractions. However, subunit IIB
and unit IV correspond to glauconite sandstone intervals
with no biogenic silica, so these units are not discussed
further. Subunit IIIA corresponds to the depth interval
between ca. 256 and 103 m CCSF-D (11.714–7.891 Ma)(Fig. 5). This subunit is characterized by decimeter- tometer-scale alternating layers of heavily bioturbated,
relatively dark gray diatomaceous ooze and very darkgray diatom-rich clay. Lithological unit II corresponds to
a depth interval between ca. 103 and 60 m CCSF-D(7.891–3.003 Ma) (Fig. 5). This unit consists of green
silty clay, olive gray diatom-rich silty clay, and dark olive-gray diatom ooze. This unit is divided into two subunits (IIA and IIB) based on the diatom content.
Preliminary studies using biostratigraphic data suggestthat subunit IIB (103–76 m CCSF-D; 7.891–4.100 Ma)
corresponds to a hiatus (Tada et al. 2015b; Kamikuri etal. 2017). Subunit IIA (ca. 76–60 m CCSF-D; 4.100–
3.003 Ma) mainly consists of meter-scale alternating
heavily bioturbated dark olive-gray diatom-bearing clay
and very dark gray diatom ooze. Unit I differs from unitMatsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

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Fig. 5 Relative abundance (%) of selected radiolarian species at Site U1430 plotted by age (Ma) (Kamikuri et al. 2017 depth age model) and comparedto the lithological units of Tada et al. (2015b)

II by a decrease in biosiliceous content. This unit consists of alternating interbedded clayey silt, silt clay, foraminifer-rich diatom-bearing clayey silt, nannofossil ooze,
and tephras. As for Site U1425, this unit is also divided
into two subunits (IA and IB) based on the frequency ofthe color alternations and the intensity of bioturbation.
Subunit IB (60–46 m CCSF-D; 3.003–1.839 Ma) consistsof a low-frequency dark and light color alternation andincreasing dominance of light gray clayey silt. Subunit IA(< 46 m CCSF-D; since 1.839 Ma) consists of terrigenous
grains, biogenic matter, pumice, and volcanic glass.
Assemblage analysis

In this study, we used the depth scale of Irino et al.
(2018), who defined the splice and composite depths ofall sediment cores retrieved during IODP Expedition
346 (CCSF-D patched-Ver. 2) (see details in Irino et al.
2018). Then, we analyzed changes in the radiolarian assemblage for 154 samples collected at about 3-m intervals from cores drilled at Site U1425 between 0 and
250 m CCSF-D and at about 2-m intervals between 250
and 360 m CCSF-D. To monitor changes in the Japan
Sea hydrography, changes in the radiolarian assemblage
and radiolarian absolute abundance (AB, in skel/g) areuseful tools for reconstructing hydrographic changes

throughout the past 10 My. Two types of microscopic
slides were prepared: a faunal slide (F-slide) for analyzing changes in the assemblage and a quantitative slide(Q-slide) for accurately estimating the AB of radiolariansin 1 g of dried sediment.
The 154 samples were freeze-dried and treated withdiluted hydrogen peroxide (15%) and hydrochloric acid(15%) to remove organic and calcareous matter. The undissolved residue in each sample was washed over asieve with 45 μm mesh size. For mounting a Q-slide, we
followed the procedure proposed by Itaki (2009) andMatsuzaki and Itaki (2016), which starts with transferring the washed undissolved residue to a beaker with
100 mL of water. The obtained solution is homogenizedby mixing to settle the radiolarians randomly, after
which a 0.5-mL sample is withdrawn (Itaki 2009) andmounted onto an 18 × 24-mm cover slip to make amicroscopic slide. All specimens visible on each Q-slide
are counted. The AB of radiolarians is calculated as follows (Itaki 2009): A = 100a/0.5g, where A is the estimated radiolarian AB (skel/g), a is the number ofradiolarian skeletons counted in the Q-slide, and g is theweight of the freeze-dried sample. The remaining undissolved residue in the beaker was also homogenized bymixing to settle the radiolarians randomly and thenMatsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

P1

mounted onto a 22 × 40-mm cover microscopic slide(F-slide) following the procedure of Itaki (2003). Examination of polycystine radiolarians was carried out underan optical microscope at total magnifications of 100–
400×. Sample examination continued until at least 400
radiolarians were identified in each sample, or until thesample material was exhausted. The identification
followed the nomenclature of Itaki (2009), Matsuzaki etal. (2015a), and Zhang and Suzuki (2017) for extant species. For extinct species, we mainly followed the taxonomic nomenclature of Nigrini and Lombari (1984),
Motoyama (1996), and Kamikuri (2010). Microphotographs of selected species are shown in Plate 1. Whensimilar paleoceanographic responses were empiricallyknown for similar species, these radiolarians weregrouped for paleoceanographic analysis, as described
below. We calculated the relative abundances of the encountered species as a percentage of all radiolarians inthe sample. In this study, an average of 412 specimens
was counted per sample. We also analyzed the radiolarian assemblage of 51 samples collected at 3.5-m intervals
from Site U1430. However, because a hiatus of 2.7 Myr
was encountered between 7.2 and ca. 4.5 Ma (Tada et al.
2015b; Kamikuri et al. 2017), only F-slides were
mounted, and selected taxa were counted to strengthen
the significance of the data obtained from Site U1425.
As mentioned above, a few aspects hamper the paleoceanographic reconstruction when it is based on changes in
the microfossil assemblage for a time interval older than
the Pleistocene, especially when including extinct species.
Generally, knowledge of the vertical and geographical distributions of extinct species is limited. Fortunately, until thelate Miocene, there are a few extant radiolarian species
whose vertical and geographical distributions are known.
Additionally, a few previous studies have clarified geographical distribution of Mio-Pliocene radiolarian species, which
helped our reconstruction (Oseki and Suzuki 2009). In thiscontext, we selected 21 extant/extinct species with known
geographical distribution from the total assemblage in thisstudy (Figs. 3, 4, and 5).
Age model

We followed the age-depth model of Kamikuri et al. (2017)
for Sites U1425 and U1430 for the Mio-Pliocene and theage-depth model of Tada et al. (2018) for the Pleistocene,
which relies on correlation of dark and light layers and estimates ages using tephras and magnetostratigraphic events.
Details about the tie points and the sedimentation rates
used in this study are shown in Tables 1 and 2.

Results
At both sites (U1425 and U1430), the preservation ofradiolarian fossils fluctuated between good to moderate
for the time interval between the late Miocene and late

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Pliocene. During the Pleistocene, the preservation of radiolarians fluctuated between poor and good. A similar
observation was also made by Kamikuri et al. (2017) andTada et al. (2015a, 2015b).
Site U1425
Polycystine radiolarian absolute abundance (skel/g)

Because the skeletons of polycystine radiolarians arecomposed of amorphous opaline silica, their AB can beused to constrain changes in opaline silica (e.g., De
Wever et al. 2001) (Figs. 3 and 4).
In lithological subunit IIIA (9.52–7.41 Ma), the mean
radiolarian AB is 2.24 × 104 skel/g and the standard deviation (SD) is 1.18 × 104 skel/g (N = 54), while the means ofradiolarian AB in lithological subunits IIB (7.41–4.20 Ma)
and IIA (4.20–2.72 Ma) are 3.26 × 104 skel/g (SD = 1.10 ×
104 skel/g; N = 46) and 2.50 × 104 skel/g (SD = 1.41 × 104
skel/g; N = 25), respectively (Figs. 3 and 4). These data
imply that although the mean radiolarian AB is lower insubunit IIIA than in subunits IIB and IIA, the radiolarian
AB of subunit IIIA has a higher variability (subunit
IIIASD > subunit IIASD > subunit IIBSD). These subunits
are all characterized by a diatom ooze or diatom-rich clayey
silt, suggesting high biogenic silica content. However, subunit IIIA, which has a lower mean value and higher SD, ischaracterized by a higher content of terrigenous matter(Tada et al. 2015a). Therefore, it is probable that the higher
content of terrigenous matter reduced radiolarian productivity between 9.52 and 7.41 Ma (subunit IIIA). In addition,in subunit IIB (7.41–4.20 Ma), which is characterized by
the highest radiolarian AB mean values and lowest SD, thesediments are strongly bioturbated (Tada et al. 2015a).
Previous studies demonstrated that highly bioturbated sediments imply oxic bottom water conditions in the Japan Sea
during the Pleistocene (e.g., Watanabe et al. 2007). Therefore, it is probable that oxic bottom water conditions prevailed in the Japan Sea between 7.4 and 4.2 Ma, which
probably allowed high productivity of radiolarians.
Lithological subunits IA and IB (1.2–0 Ma), which consistof clay and silty clay with small amounts of diatom-richclay, are characterized by the lowest radiolarian AB. Indeed,
the means of radiolarian AB are 1.27 × 104 skel/g (SD =1.62 × 104 skel/g; N = 11) and 2.01 × 104 skel/g (SD = 2.00 ×
104 skel/g; N = 18) for subunits IB and IA, respectively(Figs. 3 and 4). However, the SD estimated for subunit IA(since 1.2 Ma) is the highest since 9.5 Ma, which suggests
high variability in radiolarian productivity since 1.2 Ma,
which may be related to the glacioeustatic sea-level variation caused by glacial/interglacial cyclic climate changes(e.g., Elderfield et al. 2012; Lisiecki and Raymo 2005).
Relative abundances of dominant species

We have defined a species or species group as dominant
if their relative abundance exceeded 30% of the total

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 9 of 33

Plate 1 Photomicrographs of select radiolarian species used in this study: 1. Dictyocoryne profunda Ehrenberg (sample 346-U1425D-1H1-12–
14 cm), 2. Larcopyle buetschlii Dreyer (sample 346-U1425D-1H1-12–14 cm), 3. Lithelius barbatus Motoyama (sample 346-U1425B-47H1-91-93 cm), 4.
Larcopyle weddellium Lazarus, Faust and Popova-Goll (sample 346-U1425B-47H1-91-93 cm), 5. Lithelius minor Jørgensen group (sample 346U1425B-29H1-81–83 cm), 6–7. Spongodiscidae juvenile (sample 346-U1425B-23H5-129-131 cm), 8. Spongopyle osculosa Dreyer (sample 346U1425B-23H5-129–131 cm), 9. Stylodictya tenuispina Jørgensen group, 10. Phorticium spp. (sample 346-U1425B-6H5-11–13 cm), 11–12. Tetrapyle
spp. (Fig. 11: sample 346-U1425B-6H5–11–13 cm, Fig. 12: sample 346-U1425B-34H4–46-48 cm), 13. Lychnocanoma magnacornuta Sakai (sample
346-U1425B-51HCC-24-29 cm), 14. Lipmanella redondoensis (Campbell and Clark) (sample 346-U1425D-29H1–45-47 cm), 15. Peripyramis circumtexta
Haeckel group (sample 346-U1425B-47H1–91-93 cm), 16. Cornutella profunda Ehrenberg group (sample 346-U1425B-47H1–91-93 cm), 17–18.
Stichocorys peregrina /delmontensis group (sample 346-U1425B-34H4-46–48 cm), 19–20. Siphocampe arachnea/lineata (Ehrenberg) group (sample
346-U1425B-21H6-19–21 cm), 21–22. Lithomelissa setosa Jørgensen (sample 346-U1425B-5H6-81–83 cm), 23–24. Amphimelissa setosa (Cleve)(sample 346-U1425B-3H4-51–53 cm), 25. Pseudodictyophimus gracilipes (Bailey) (sample 346-U1425B-5H6-81–83 cm), 26. Lychnocanoma parrallelipes
Motoyama (sample 346-U1425B-34H4-46–48 cm), 27. Cycladophora nakasekoi Motoyama (sample 346-U1425B-47H1-91–93 cm), 28. Cycladophorasphaeris (Popofsky) (sample 346-U1425B-21H6-19–21 cm), 29. Cycladophora davisiana (Ehrenberg) (sample 346-U1425B-6H5-11–13 cm), 30.
Carpocanistrum papillosum (Ehrenberg) group (sample 346-U1425B-34H4-46–48 cm), 31. Ceratospyris borealis Bailey (sample 346-U1425B-3H5-12–14 cm)

assemblage at the site. Six species or species groups
dominated at Site U1425: Amphimelissa setosa (Cleve),
Cycladophora davisiana (Ehrenberg), Ceratospyris borealis Bailey, Siphocampe lineata/arachnea sensu Nigrini(1977), Cycladophora nakasekoi Motoyama, and theLithelius barbatus Motoyama group (Figs. 3 and 4).
Changes in their relative abundances are described
below with their inferred paleoceanographic conditions.
The species A. setosa is an extant species inhabiting
subsurface water depths (50–300 m) in the Arctic Ocean(Bjørklund et al. 2015; Ikenoue et al. 2016; Itaki 2003;
Matul and Abelmann 2005). However, this species disappeared from the subarctic North Pacific between marine
isotope stages (MISs) 4 and 5 (0.07–0.05 Ma) (e.g.,
Matul and Abelmann 2005; Ikenoue et al. 2016; Matul etal. 2002; Matsuzaki and Suzuki 2018). In addition, thefirst occurrence of this species is recorded at 1.48 Ma in
the Northeast Pacific (Matsuzaki and Suzuki 2018). In
the Japan Sea, this species occurred between 1.47 and0.05 Ma, although our sampling resolution is relatively

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 10 of 33

Table 1 Samples used, biostratigraphic tie points, and related sedimentation rates at IODP Site U1425 (cm/ky)
Exp Site

Hole Core Type Sect A/W Offset
CCSF-A (m) CCSF-D_Patched Age (Ma) Sedimentation Comments(cm) Mid (Tada et al. (Irino et al. 2018)
rates (cm/ky)
2015a)

346 U1425 D

1

H

1

W

13

0.130

346 U1425 D

1

H

1

W

103

1.030

1.03

0.017

346 U1425 D

1

H

3

W

3

3.030

3.03

0.051

6.22

0.105

Tie point of Tada et al. (2018)

0.13

0.002

346 U1425 B

1

H

5

W

99

6.992

6.99

0.121

346 U1425 D

2

H

2

W

14

8.005

8.00

0.143

346 U1425 D

2

H

3

W

64

10.0055.924

We used the Tephra & Pmag
age of Dark layer No. 1–6(Additional file 3)

10.00

0.185

Tie point of Tada et al. (2018)

10.55

0.197

4.707

We used the Tephra & Pmag
age of Dark layer No. 2–5(Addional file 3)

Tie point of Tada et al. (2018)

14.13

0.292

3.776

We used the Tephra & Pmag
age of Dark layer No. 3–2(Additional file 3)

16.01

0.342

Tie point of Tada et al. (2018)

17.66

0.386

3.735

We used the Tephra & Pmag
age of Dark layer No. 4–2(Additional file 3)

Tie point of Tada et al. (2018)

21.71

0.483

4.188

We used the Tephra & Pmag
age of Dark layer No. 5–3(Additional file 3)

3.002

We used the Tephra & Pmag
age of Dark layer No. 6–3(Additional file 3)

4.026

We used the Tephra & Pmag
age of Dark layer No. 7–2(Additional file 3)4.251

We used the Tephra & Pmag
age of Dark layer No. 9–1(Additional file 3)

4.346

We used the Tephra & Pmag
age of Dark layer No. 11–1
(Additional file 3)3.869

We used the Tephra & Pmag
age of Dark layer No. 13–3
(Additional file 3)3.001

We used the Tephra & Pmag
age of Dark layer No. 15–2
(Additional file 3)346 U1425 B

2

H

5

W

65

16.006346 U1425 D

3

H

5

W

42

22.012

22.01

0.493

346 U1425 B

3

H

4

W

52

24.904

24.90

0.589

25.46

0.608

Tie point of Tada et al. (2018)

346 U1425 B

3

H

5

W

113

27.014

Tie point of Tada et al. (2018)

27.01

0.647

29.18

0.700

346 U1425 D

4

H

3

W

28

30.008

30.01

0.720

346 U1425 D

4

H

5

W

28

33.008

33.01

0.790

33.21

0.795

35.81

0.855

38.16

0.909

Tie point of Tada et al. (2018)

346 U1425 D

4

H

7

W

8

35.808

Tie point of Tada et al. (2018)

346 U1425 B

4

H

7

W

32

39.034

39.23

0.937

346 U1425 D

5

H

3

W

15

40.016

40.21

0.962

41.75

1.002

43.21

1.050

44.97

1.109

Tie point of Tada et al. (2018)

346 U1425 D

5H

Tie point of Tada et al. (2018)

5

W

15

43.016

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 11 of 33

Table 1 Samples used, biostratigraphic tie points, and related sedimentation rates at IODP Site U1425 (cm/ky) (Continued)
Exp Site

Hole Core Type Sect A/W Offset
CCSF-A (m) CCSF-D_Patched Age (Ma) Sedimentation Comments(cm) Mid (Tada et al. (Irino et al. 2018)
rates (cm/ky)
2015a)

346 U1425 D

5

H

6

W

65

45.016

45.21

1.116

346 U1425 B

5

H

5

W

32

46.026

46.32

1.146

47.98

1.192

48.32

1.204

Tie point of Tada et al. (2018)

346 U1425 B

5

H

6

W

82

48.026346 U1425 D

6

H

3

W

134

50.990Tie point of Tada et al. (2018)

346 U1425 B

6

H

2

W

62

53.017

Tie point of Tada et al. (2018)

51.28

1.306

51.43

1.311

53.31

1.391

54.8

1.455

346 U1425 B

6

H

3

W

112

55.017

55.31

1.468

346 U1425 B

6

H

5

W

12

57.017

57.31

1.517

346 U1425 D

7

H

2

W

82

60.013

60.30

1.592

64.115

64.63

1.700

65.013

65.30

1.750

Tie point of Kamikuri et al. (2017)346 U1425 D

7

H

5

W

132

346 U1425 B

7

H

5

W

104

68.016

68.31

1.972

346 U1425 D

8

H

2

W

99

69.996

70.29

2.119

346 U1425 D

8

H

4

W

143

73.006

73.30

2.342

346 U1425 B

8

H

3

W

138

76.007

76.30

2.564

346 U1425 B

8

H

5

W

138

Tie point of Kamikuri et al. (2017)79.007

79.30

2.787

80.005

80.62

2.885

346 U1425 B

8

H

7

W

39

81.017

81.57

2.905

346 U1425 B

9

H

3

W

5

85.002

85.55

2.992

346 U1425 B

9

H

4

W

55

87.002

87.55

3.035

346 U1425 D

10

H

2

W

65

88.007

88.56

3.057

346 U1425 D

10

H

4

W

65

91.007

91.56

3.122

346 U1425 D

10

H

6

W

66

94.017

93.75

3.170

346 U1425 B

10

H

5

W

94

96.013

95.74

3.213

346 U1425 D

11

H

3

W

133

99.003

98.73

3.278

346 U1425 D

11

H

5

W

133

102.003101.73

3.343

346 U1425 B

11

H

5

W

62

106.008

105.74

3.430

346 U1425 D

12

H

3

W

75

109.005

108.73

3.495

346 U1425 D

13

X

2

W

71

112.011111.86

3.563

346 U1425 B

14

H

3

W

59

115.014114.86

3.628

3.635

We used the Tephra & Pmag
age of Dark layer No. 17–1
(Additional file 3)

2.892

We used the Tephra & Pmag
age of Dark layer No. 19–1
(Additional file 3)

2.344

We used the Tephra & Pmag
age of Dark layer No. 21–2
(Additional file 3)

4.013

We used the Last Occurrenceof A. acquilonium (Radiolaria),
which occurred at the mid
depth of 64,115 m CCSF-A.
This bioevent has noerror margin.

1.350

We used the Last Occurrenceof H. parviakitaense (Radiolaria),
which occurred at the mid
depth of 80,005 m CCSF-A.
This bioevent has an error
margin of 0,015 Ma.

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 12 of 33

Table 1 Samples used, biostratigraphic tie points, and related sedimentation rates at IODP Site U1425 (cm/ky) (Continued)
Exp Site

Hole Core Type Sect A/W Offset
CCSF-A (m) CCSF-D_Patched Age (Ma) Sedimentation Comments(cm) Mid (Tada et al. (Irino et al. 2018)
rates (cm/ky)
2015a)

346 U1425 B

14

H

5

W

56

118.014117.86

3.694

346 U1425 B

14

H

6

W

106

120.014119.86

3.737

346 U1425 D

14

H

2

W

59

122.009121.86

3.780

346 U1425 D

14

H

3

W

109

124.009123.86

3.824

346 U1425 B

17

H

2

W

124

125.003124.85

3.845

346 U1425 D

15

H

3

W

23

127.011126.86

3.889

346 U1425 D

15

H

4

W

73

129.011128.86

3.932

346 U1425 D

15

H

6

W

73

132.011131.863.997

134.43134.284.050

Tie point of Kamikuri et al. (2017)346 U1425 D

16

H

2

W

4

136.013135.86

4.089

346 U1425 D

16

H

4

W

2

139.013138.86

4.164

346 U1425 D

16

H

6

W

2

142.013141.86

4.238

346 U1425 B

21

H

2

W

21

144.030

143.88

4.289

346 U1425 B

21

H

4

W

20

147.020146.874.363

148.51148.36

4.400

Tie point of Kamikuri et al. (2017)346 U1425 B

21

H

6

W

20

150.020149.87

4.480

346 U1425 D

18

H

5

W

7

151.996151.84

4.584

346 U1425 D

18

H

6

W

60

154.026

153.87

4.691

346 U1425 B

22

H

3

W

111

156.990156.84

4.848

346 U1425 B

22

H

5

W

11

158.990158.844.954

160.815160.66

5.050

Tie point of Kamikuri et al. (2017)346 U1425 D

19

H

3

W

127

161.021160.87

5.054

346 U1425 D

19

H

5

W

128

164.031163.88

5.111

346 U1425 B

23

H

3

W

130

167.020

166.87

5.167

346 U1425 B

23

H

5

W

130

170.020169.87

5.224

346 U1425 D

20

H

4

W

97

172.014171.86

5.262

346 U1425 D

20

H

5

W

146

174.004173.85

5.299

346 U1425 B

24

H

2

W

145

176.002175.85

5.337

346 U1425 D

21

H

2

W

37

178.013177.86

5.375

346 U1425 D

21

H

3

W

87

180.013179.86

5.413

346 U1425 D

21

H

5

W

87

183.013182.86

5.470

346 U1425 B

25

H

2

W

91

185.001

184.85

5.507

4.606

We used the Last Occurrenceof D. bullatus (Radiolaria),
which occurred at the
mid depth of 134.43 m
CCSF-A. This bioevent has
an error margin of 0.25 Ma.

4.023

We used the First Occurrenceof D. bullatus (Radiolaria),
which occurred at the
mid depth of 148.51 m
CCSF-A. This bioevent has
an error margin of 0.1 Ma.

1.893

We used the Last Occurrenceof L. redondoensis (Radiolaria),
which occurred at the mid
depth of 160,815 m CCSF-A.
This bioevent has an error
margin of 0.05 Ma.

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 13 of 33

Table 1 Samples used, biostratigraphic tie points, and related sedimentation rates at IODP Site U1425 (cm/ky) (Continued)
Exp Site

Hole Core Type Sect A/W Offset
CCSF-A (m) CCSF-D_Patched Age (Ma) Sedimentation Comments(cm) Mid (Tada et al. (Irino et al. 2018)
rates (cm/ky)
2015a)

346 U1425 B

25

H

4

W

92

188.011187.86

5.564

346 U1425 D

22

H

5

W

62

193.011

192.86

5.659

346 U1425 D

22

H

6

W

112

195.011194.86

5.696

346 U1425 D

23

H

2

W

77

198.007

197.86

5.753

346 U1425 D

23

H

4

W

77

201.007200.86

5.810

346 U1425 D

23

H

6

W

77

204.007203.86

5.867

346 U1425 B

27

H

4

W

28

207.014206.86

5.923

346 U1425 B

27

H

6

W

27

210.004

209.85

5.980

346 U1425 D

24

H

5

W

6

212.008211.86

6.018

346 U1425 D

24

H

6

W

56

214.008

213.86

6.056

346 U1425 B

28

H

3

W

148

217.010216.866.112

219

218.85

6.150

Tie point of Kamikuri et al. (2017)346 U1425 B

29

H

1

W

82

222.021221.996.267

346 U1425 B

29

H

3

W

82

225.021224.996.378

346 U1425 B

29

H

5

W

83

228.031228.00

6.489

346 U1425 D

27

H

1

W

123

231.023231.006.600

346 U1425 B

30

H

3

W

32

233.012234.23

6.720

346 U1425 B

30

H

5

W

32

236.012237.236.831

237.66239.09

6.900

Tie point of Kamikuri et al. (2017)346 U1425 D

28

H

4

W

90

238.009239.23

6.903

346 U1425 D

28

H

6

W

90

241.009242.23

6.968

346 U1425 D

29

H

1

W

46

243.011244.23

7.012

346 U1425 D

29

H

2

W

96

245.011246.23

7.055

346 U1425 B

33

H

3

W

40

247.002248.22

7.099

346 U1425 B

33

H

4

W

90

249.002250.22

7.142

346 U1425 B

33

H

5

W

139

250.992

252.21

7.186

346 U1425 B

33

H

6

W

91

252.012253.23

7.208

346 U1425 D

30

H

5

W

76

255.009256.237.273

255.58257.46

7.300

Tie point of Kamikuri et al. (2017)346 U1425 B

34

H

4

W

47

258.010259.23

7.342

346 U1425 B

34

H

5

W

97

260.010262.23

7.413

346 U1425 D

31

H

2

W

118

261.012265.23

7.484

5.290

We used the Last Occurrenceof L. parallelipes (Radiolaria),
which occurred at the
mid depth of 219.00 m
CCSF-A. This bioevent has
an error margin of 0.25 Ma.

2.699

We used the Rapid Increaseof L. barbatus (Radiolaria),
which occurred at the
mid depth of 237.66 m
CCSF-A. This bioevent has
an error margin of 0.10 Ma.

4.593

We used the First Occurrenceof L. barbatus (Radiolaria),
which occurred at the
mid depth of 255.58 m
CCSF-A. This bioevent has
an error margin of 0.10 Ma.

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 14 of 33

Table 1 Samples used, biostratigraphic tie points, and related sedimentation rates at IODP Site U1425 (cm/ky) (Continued)
Exp Site

Hole Core Type Sect A/W Offset
CCSF-A (m) CCSF-D_Patched Age (Ma) Sedimentation Comments(cm) Mid (Tada et al. (Irino et al. 2018)
rates (cm/ky)
2015a)

346 U1425 D

31

H

4

W

118

264.012267.23

7.531

346 U1425 B

35

H

3

W

48

266.008268.23

7.555

346 U1425 B

35

H

3

W

148

267.008270.23

7.602

346 U1425 B

35

H

5

W

48

269.008274.23

7.697

346 U1425 D

32

H

4

W

6

273.007275.23

7.720

346 U1425 D

32

H

4

W

106

274.007277.23

7.768

346 U1425 D

32

H

6

W

6

276.007280.23

7.839

346 U1425 B

37

H

1

W

129

279.011281.24

7.863

346 U1425 B

37

H

2

W

80

280.021281.26

7.863

346 U1425 D

33

H

4

W

3

282.014283.23

7.910

346 U1425 B

38

H

1

W

102

283.006

284.22

7.933

346 U1425 D

35

H

2

W

48

287.003288.22

8.028

346 U1425 B

39

H

2

W

126

290.011291.23

8.099

346 U1425 B

39

H

4

W

61

291.991293.21

8.146

346 U1425 B

40

X

2

W

59

293.998294.22

8.170

346 U1425 B

40

X

3

W

10

295.008296.22

8.217

346 U1425 D

37

H

1

W

144

297.010298.36

8.268

346 U1425 D

37

H

2

W

94

298.010299.36

8.292

346 U1425 D

37

H

4

W

95

300.010301.36

8.339

346 U1425 D

37

H

5

W

45

301.010302.36

8.363

346 U1425 B

42

H

3

W

67

306.015307.36

8.481

346 U1425 D

38

H

2

W

127

307.006

308.35

8.505

346 U1425 D

39

H

1

W

57

310.003311.35

8.576

346 U1425 D

39

H

2

W

107

312.003313.35

8.623

346 U1425 D

39

H

3

W

57

313.003314.35

8.647

346 U1425 B

44

H

2

W

77

314.012315.36

8.670

346 U1425 B

44

H

4

W

5

316.012317.36

8.718

346 U1425 D

40

H

2

W

60

318.013319.36

8.765

346 U1425 D

40

H

3

W

10

319.013320.36

8.789

346 U1425 D

40

H

3

W

110

320.013321.36

8.812

346 U1425 B

46

H

1

W

53

321.027321.85

8.824

346 U1425 D

41

H

2

W

109

323.018323.85

8.871

346 U1425 D

41

H

4

W

37

325.008

325.84

8.918

346 U1425 B

47

H

1

W

92

326.016326.84

8.942

346 U1425 B

47

H

2

W

42

327.016327.84

8.966

346 U1425 B

47

H

2

W

143

328.026

328.85

8.990

346 U1425 B

47

H

3

W

92

329.016329.84

9.013

346 U1425 D

43

H

2

W

28

331.016331.849.061

332.68333.51

9.100

Tie point of Kamikuri et al. (2017)

4.225

We used the First Occurrenceof L. barbatus (Radiolaria),
which occurred at the
mid depth of 255.58 m
CCSF-A. This bioevent has
no an error margin.

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 15 of 33

Table 1 Samples used, biostratigraphic tie points, and related sedimentation rates at IODP Site U1425 (cm/ky) (Continued)
Exp Site

Hole Core Type Sect A/W Offset
CCSF-A (m) CCSF-D_Patched Age (Ma) Sedimentation Comments(cm) Mid (Tada et al. (Irino et al. 2018)
rates (cm/ky)
2015a)

346 U1425 D

43

H

3

W

78

333.016333.84

9.106

346 U1425 D

43

H

4

W

28

334.016

334.84

9.123

346 U1425 D

43

H

4

W

128

335.016335.84

9.140

346 U1425 D

43

H

6

W

28

337.016

337.84

9.173

346 U1425 B

49

H

2

W

30

338.016

338.84

9.190

346 U1425 B

49

H

2

W

130

339.016

339.84

9.207

346 U1425 D

44

H

2

W

31

341.014341.84

9.241

346 U1425 B

50

H

2

W

67

343.994344.82

9.291

346 U1425 B

50

H

3

W

118

346.004

346.83

9.325

346 U1425 D

45

H

2

W

41

347.010347.84

9.342

346 U1425 D

45

H

2

W

141

348.010348.84

9.359

346 U1425 D

46

H

1

W

76

349.73350.56

9.393

346 U1425 D

46

H

2

W

76

351.23352.06

9.423

346 U1425 D

46

H

4

W

4

353.23354.06

9.462

346 U1425 D

48

H

1

W

26

358.63359.469.568

382.925

383.75

9.950

Tie point of Kamikuri et al. (2017)

low for the Pleistocene (Fig. 3). During this time interval(1.47–0.05 Ma), the mean of A. setosa relative abundance is 10.6% (SD = 18.3; N = 22). The highest abundance of this species is 80.55% recorded at 0.34 Ma(Fig. 3 and Additional file 1).
The species C. davisiana and C. borealis are bothsubarctic, abundant in areas influenced by the Oyashio Current and in the Sea of Okhotsk (e.g., Matsuzaki and Itaki 2017; Matsuzaki et al. 2014a, 2014b;
Okazaki et al. 2004). In the Japan Sea, C. davisiana
is related to the Japan Sea deep water formed bycooling of the TWC, that is, the Japan Sea Proper
Water (Itaki 2003; Itaki et al. 2007), while C. borealis
prefers cold surface and subsurface water (50–200 m) (Itaki 2003; Itaki et al. 2007; Okazaki et al.
2004). C. davisiana is recorded at Site U1425 between 3.21 and 0 Ma, with a mean relative abundance of 6.4% (SD = 13.1; N = 37), while C. borealis isrecorded between 3.56 and 0 Ma with a mean relative abundance of 8.4% (SD = 15.2; N = 42) (Fig. 3
and Additional file 1).
The species group S. lineata/arachnea is an extant
species inhabiting water between 300 and 1000 m deepin the North Pacific (Kling and Boltovskoy 1995). Higher
abundances of this species are recorded in the arctic to5.911

We used the First Occurrenceof C. nakasekoi (Radiolaria),
which occurred at the
mid depth of 382.925 m
CCSF-A. This bioevent has anerror margin of 0.25 Ma.

subarctic areas of the North Pacific (e.g., Boltovskoy andCorrea 2016; Kling and Boltovskoy 1995; Takahashi1991). Additionally, Boltovskoy and Correa (2016)
showed that this species is restricted to the Northern
Hemisphere high latitudes. Therefore, we assume
that this species group is related to the intermediatewater of the Northern Hemisphere high latitudes. At
Site U1425, this species is encountered intermittently
between 9.5 and 0 Ma, with a mean relative abundance of 4.3% (SD = 11.4; N = 154) (Additional file 1).
This species dominates the radiolarian assemblage(> 30%) between 4.9 and 4.0 Ma (Fig. 4 andAdditional file 1).
The L. barbatus group is an extinct group (e.g.,
Motoyama 1996; Kamikuri et al. 2004, 2007) and was
described as having relatively wide variation of morphological forms by Motoyama (1996). This species grouphas been encountered in areas related to the subarctic
gyre of the North Pacific (e.g., Motoyama 1996;
Kamikuri et al. 2004, 2007), whereas this species groupis absent in areas influenced by the subtropical gyre
(Kamikuri 2017; Kamikuri et al. 2009). Therefore, we assumed that this species is related to water masses oftransitional to subarctic areas. At Site U1425, this species is encountered between 7.55 and 5.51 Ma, with aMatsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

mean relative abundance of 11.6% (SD = 12.9; N = 32)(Fig. 4 and Additional file 1). This species’ relative
abundance is higher than the mean value between
7.01 and 5.75 Ma, and it dominates the radiolarianassemblage between 6.11 and 6.02 Ma (> 30%)
(Fig. 4).
Finally, C. nakasekoi is an extinct species endemic to
the Japan Sea (Motoyama 1996; Kamikuri et al. 2004,
2007), but its related ecology, such as depth of its habitatand preferred climatic condition, is unknown. This
species is recorded between 9.57 and 7.41 Ma at Site
U1425, with a mean relative abundance of 20.0%(SD = 12.7; N = 55) (Fig. 4 and Additional file 1). The
relative abundance of C. nakasekoi fluctuates
between high (> 30%) and low relative abundances(< 10%) (Fig. 4). Interestingly, the sediments collected
at Site U1425 spanning the time interval between
9.57 and 7.41 Ma correspond to lithological subunit
IIIA, composed of alternating dark gray diatom ooze
and heavily bioturbated clayey diatomaceous ooze
(Tada et al. 2015a).
Relative abundance of abundant species

We have defined a species or species group as abundant
when its relative abundance is between 10 and 30% of
the total assemblage at least once at the site. At Site
U1425, abundant species are Lithomelissa setosa
Jørgensen, Spongodiscidae juvenile, Pseudodictyophimus
gracilipes (Bailey), Cycladophora sphaeris (Popofsky),Phorticium spp., Tetrapyle spp., Lithelius minor
Jørgensen group, Stylodictya tenuispina Jørgensen group,
Stichocorys delmontensis (Campbell and Clark), Stylochlanydium venustum/bensoni group, Larcopyle polyacantha group (Campbell and Clark), and Stichocorys
peregrina (Riedel) (Figs. 3 and 4). The last two species are grouped as Stichocorys delmontensis/peregrina in Fig. 4.
Species such as L. setosa, Spongodiscidae juvenile, andP. gracilipes are well-known extant species related tosubarctic areas. Based on previous studies, we know that
L. setosa is related to the shallow water of subarctic toarctic areas of the Northern Hemisphere (Atlantic andPacific oceans) (Boltovskoy and Correa 2016; Matsuzaki
and Itaki 2017; Okazaki et al. 2004). At Site U1425, thisspecies was recorded between 3.69 and 0 Ma, and its
mean relative abundance is 1.7% (SD = 3.3; N = 44) (Fig. 3
and Additional file 1). P. gracilipes is related to theupper intermediate water of areas influenced by the
Oyashio Current (300–500 m). Young forms of Spongodiscidae, whose taxonomy is still unsettled, are often
named as Spongodiscus resurgens Ehrenberg group (e.g.,
Itaki 2009; Matsuzaki et al. 2015a). However, whichever
name is used, this form is likely related to the shallow
subsurface waters of transitional subarctic areas in the

Page 16 of 33

Northwest Pacific (e.g., Kamikuri et al. 2008; Matsuzaki
and Itaki 2017; Okazaki et al. 2004). In our study, boththe species and species group were found at Site U1425
throughout the period since 9.5 Ma. The mean relative
abundance of P. gracilipes is 1.2% (SD = 2.2; N = 154),
while the mean relative abundance of Spongodiscidae
juvenile is 5.2% (SD = 6.2; N = 154) (Fig. 3 and Additional file 1). For P. gracilipes, relative abundance higher
than the mean value is recorded intermittently between
3.85 and 2.79 Ma, 1.75 and 1.12 Ma, and 0.65 and0.49 Ma (Fig. 3 and Additional file 1). For juvenile Spongodiscidae, progressive increases in its relative abundance are recorded since 7.34 Ma, where its relative
abundance exceeds the mean value for the first time
(12.47%). From 4.2 and 0.49 Ma, relative abundance
higher than 11% is constantly recorded (Fig. 3 andAdditional file 1).
C. sphaeris is an extinct species, but it likely inhabitedwater of transitional-subarctic to subarctic areas of theNorth Pacific (e.g., Kamikuri et al. 2007; Motoyama
1996; Oseki and Suzuki 2009). In our study, this species
occurred between 7.93 and 3.06 Ma at Site U1425 andthe mean relative abundance is 9.3% (SD = 6.9; N = 79)(Fig. 3 and Additional file 1). Highest abundance of thisspecies was recorded in the late Pliocene at 3.34 Ma(36.62%) (i.e., Fig. 3 and Additional file 1).
Phorticium spp. and Tetrapyle spp. are extant species
groups, both known as a marker of warm shallow waterin the North Pacific (e.g., Lombari and Boden 1985; Itaki
et al. 2010; Kamikuri et al. 2008; Matsuzaki et al 2014b;
Matsuzaki et al. 2015b; Matsuzaki et al. 2016; Matsuzaki
and Itaki 2017). However, the main difference between
the two species groups is that while Tetrapyle spp. are
restricted to the low-middle latitudes, Phorticium spp.
are also common in temperate areas (Kamikuri et al.
2008; Romine 1985). According to Zhang and Suzuki(2017), our Phorticium spp. and Tetrapyle spp. mightalso include morphotypes from different genera because
for the Miocene, the taxonomy of both genera is poorly
settled and accurate taxonomic study of both genera isrequired for this period. However, most of the extant
taxa, which potentially belong to these two species
groups, bear algal symbionts and inhabit warmer shallow
waters (Zhang et al. 2018). Therefore, this taxonomic
concern does not affect our paleoceanographic reconstruction. At Site U1425, both species groups are recorded continuously since 9.5 Ma, although Tetrapyle
spp. seem to be absent from 5.05 to 3.06 Ma (Fig. 4 andAdditional file 1). Phorticium spp. have a mean relative
abundance of 5.3% (SD = 6; N = 154), while Tetrapyle
spp. have a mean relative abundance of 1.9% (SD = 3.1;
N = 154) (Fig. 4 and Additional file 1). Tetrapyle spp.
have a relative abundance twice as high as the meanvalue for the periods between 9.57 and 7.06 Ma andMatsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 17 of 33

Table 2 Samples used, biostratigraphic tie points, and related sedimentation rates at IODP Site U1430 (cm/ky)
Exp Site

Hole Core Type Sect A/W Offset CCSF-A (m) CCSF-D_
Age (Ma)(cm) (Tada et al. PatchedMid
2015b)(Irino et al. 2018)

346 U1430 A

1

H

CC

W

0

3.68

Tie point of Tada et al. (2018)

346 U1430 A

2

H

4

W

69

9.14

Tie point of Tada et al. (2018)

346 U1430 A

11.24

0.197

5.677

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

3.407

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

Tie point of Tada et al. (2018)

18.78

0.408

3.708

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

19.28

0.421

22.57

0.504

3.981

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

23.65

0.530

26.88

0.608

4.128

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

29.59

0.678

Tie point of Tada et al. (2018)

30.43

0.700

3.855

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

Tie point of Tada et al. (2018)

32.28

0.795

1.945

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

33.75

0.842

36.11

0.909

3.537

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

39.23

0.998

Tie point of Tada et al. (2018)

39.36

1.002

3.502

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

Tie point of Tada et al. (2018)

42.42

1.109

2.852

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

43.69

1.145

45.39

1.192

3.587

We used the Tephra& Pmag age of Dark

69

13.52

0.160

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

0.292

W

0

9.14

5.714

0.264

4

W

0.105

14.46

H

CC

6

13.52

3

H

0.064

Tie point of Tada et al. (2018)

346 U1430 A

2

3.68

Sedimentation Comments
rates (cm/ky)

19.28

Tie point of Tada et al. (2018)

346 U1430 A

3

H

CC

W

0

23.65

Tie point of Tada et al. (2018)

346 U1430 A

346 U1430 A

4

4

H

H

4

CC

W

W

69

0

29.59

33.75

Tie point of Tada et al. (2018)

346 U1430 A

346 U1430 A

5

5

H

H

Tie point of Tada et al. (2018)

4

CC

W

W

69

0

39.23

43.69

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 18 of 33

Table 2 Samples used, biostratigraphic tie points, and related sedimentation rates at IODP Site U1430 (cm/ky) (Continued)
Exp Site

Hole Core Type Sect A/W Offset CCSF-A (m) CCSF-D_
Age (Ma)(cm) (Tada et al. PatchedMid
2015b)(Irino et al. 2018)

Sedimentation Comments
rates (cm/ky)
layer No. 1–6(Additional file 3)

Tie point of Tada et al. (2018)

346 U1430 A

6

H

4

W

69

49.15

Tie point of Tada et al. (2018)

48.23

1.311

49.15

1.366

50.66

1.455

346 U1430 A

6

H

CC

W

0

53.56

53.56

1.841

346 U1430 A

7

H

4

W

69

59.2

59.2

2.592

61.41

61.41

2.885

Tie point of Kamikuri et al. (2017)

2.381

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

1.689

We used the Tephra& Pmag age of Dark
layer No. 1–6(Additional file 3)

0.751

We used the Last Occurrenceof H. parviakitaense(Radiolaria), which occurredat the mid depth of
61.41 m CCSF-A. Thisbioevent has an error marginof 0.015 Ma.

1.174

We used the First Occurrenceof D. bullatus (Radiolaria),
which occurred at the mid
depth of 75.08 m CCSF-A.
This bioevent has an error
margin of 0.25 Ma.

346 U1430 A

7

H

CC

W

0

63.61

63.61

3.073

346 U1430 A

8

H

4

W

69

69.22

69.22

3.551

346 U1430 A

8

H

CC

W

0

73.67

73.67

3.931

346 U1430 A

9

H

1

W

69

74.33

74.33

3.987

75.08

75.08

4.050

75.83

75.83

HiatusWe defined this depths
interval as a hiatus following
the findings of Tada et al.
(2015b), Kamikuri et al. (2017)

80.06

80.06

7.300

We used the First Occurrenceof L. parallelipes (Radiolaria),
which occurred at the mid
depth of 80.06 m CCSF-A.
This bioevent has an error
margin of 0.10 Ma.

Tie point of Kamikuri et al. (2017)346 U1430 A

9

H

2

W

69

Tie point of Kamikuri et al. (2017)346 U1430 A

9

H

5

W

71

80.35

80.35

7.3075186054

346 U1430 A

9

H

6

W

71

81.85

81.85

7.3457488021

346 U1430 A

9

H

CC

W

0

83.22

83.22

7.3806657152

346 U1430 A

10

H

1

W

71

84.75

84.75

7.4196605159

346 U1430 A

10

H

2

W

71

86.25

86.25

7.4578907126

346 U1430 A

10

H

3

W

69

87.73

87.73

7.4956111734

346 U1430 A

10

H

4

W

69

89.23

89.23

7.5338413702

346 U1430 A

10

H

5

W

71

90.75

90.75

7.5725813029

346 U1430 A

10

H

6

W

71

92.25

92.25

7.6108114996

346 U1430 A

10

H

CC

W

0

93.55

93.55

7.6439443368

346 U1430 A

11

H

4

W

69

99.35

99.35

7.7917677643

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 19 of 33

Table 2 Samples used, biostratigraphic tie points, and related sedimentation rates at IODP Site U1430 (cm/ky) (Continued)
Exp Site

Hole Core Type Sect A/W Offset CCSF-A (m) CCSF-D_
Age (Ma)(cm) (Tada et al. PatchedMid
2015b)(Irino et al. 2018)

346 U1430 A

11

H

CC

W

0

103.71103.717.9028902029

346 U1430 A

12

H

4

W

69

109.56109.568.0519879702

346 U1430 A

12

H

CC

W

0

114.02114.02

8.1656590886

346 U1430 A

13

H

4

W

69

119.82119.828.3134825161

346 U1430 A

13

H

CC

W

0

124.17124.178.4243500867

346 U1430 A

14

H

4

W

69

129.73129.738.5660566826

346 U1430 A

14

H

CC

W

0

134.19134.198.679727801

346 U1430 A

15

H

4

W

69

139.65

139.658.8188857172

346 U1430 A

15

H

CC

W

0

144.11144.118.9325568356

346 U1430 A

16

H

1

W

71

145.44145.448.9664542767

346 U1430 A

16

H

2

W

71

146.94146.949.0046844734

346 U1430 A

16

H

3

W

71

148.44148.449.0429146702

346 U1430 A

16

H

4

W

71

149.94149.949.081144867

150.68150.68

9.100

Tie point of Kamikuri et al. (2017)346 U1430 A

16

H

5

W

69

151.42151.42

9.117

346 U1430 A

16

H

6

W

71

152.94152.94

9.151

346 U1430 A

16

H

CC

W

0

154.41

154.41

9.184

346 U1430 A

17

H

1

W

71

156.81156.81

9.239

346 U1430 A

17

H

2

W

71

158.31158.31

9.273

346 U1430 A

17

H

3

W

69

159.79159.799.306

346 U1430 A

17

H

4

W

71

161.33161.33

9.341

346 U1430 A

17

H

5

W

69

162.83162.83

9.375

346 U1430 A

17

H

6

W

71

164.33

164.33

9.409

346 U1430 A

17

H

CC

W

0

165.78165.789.442

188.24188.24

9.950

Tie point of Kamikuri et al. (2017)from 1.20 to 0 Ma, while Phorticium spp. have relative
abundances twice as high as the mean value between
7.27 and 3.28 Ma (Fig. 4 and Additional file 1).
The L. minor group and S. tenuispina group are extant
species, although their ecology is not well understood.
The L. minor group, which has an unsettled taxonomy
and is often named as Lithelius minor Jørgensen (e.g.,
Matsuzaki et al. 2015a), likely inhabits intermediatewater in the subtropical North Pacific (e.g., Matsuzaki etSedimentation Comments
rates (cm/ky)

3.924

We used the Last Occurrenceof L. magnacornuta(Radiolaria), which occurredat the mid depth of 150.68 m
CCSF-A. This bioevent has noerror margin.

4.418

We used the Last Occurrenceof L. magnacornuta(Radiolaria), which occurredat the mid depth of
188.24 m CCSF-A. Thisbioevent has an error marginof 0.25 Ma

al. 2016). This species is also related to subtropical-transitional areas of the North Pacific (Motoyama and Nishimura 2005). The vertical distribution of S. tenuispinagroup is not well understood, but this species is probably
related to transitional to subarctic areas in the Northwest Pacific, according to Kamikuri et al. (2008)(named as Stylodictya stellata Bailey in Kamikuri etal. 2008). Both species occurred sporadically since
9.5 Ma and their mean relative abundances are 2%

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

(SD = 3.6; N = 154) and 1.8% (SD = 2.8; N = 154) for
the S. tenuispina and L. minor groups, respectively(Fig. 4 and Additional file 1).
The S. venustum/bensoni groups are extinct, but they
probably inhabited the middle to high latitudes of theNorth Pacific during the Neogene (Kamikuri 2010). The
L. polyacantha group dominated the radiolarian assemblage between about 15 and 7 Ma at ODP Site 884(south of the Bering Sea), Site 887 (southern Gulf of Alaska), and Site 1151 (off Northeast Japan) (Kamikuri etal. 2004, 2007), and therefore, this species is also probably related to the middle to high latitudes of theNorth Pacific during the Neogene. S. venustum/bensoni groups occurred throughout the last 9.5 Ma andtheir mean relative abundance is 1.5% (SD = 3.1; N =154), with highest relative abundance between 5.3 and3.06 Ma (Fig. 3 and Additional file 1). The L. polyacantha group occurred between 9.57 and 2.3 Ma, andits mean value is 1.6% (SD = 2.1; N = 127) (Fig. 3 andAdditional file 1).
S. delmontensis/peregrina are extinct species that were
widely distributed in the North Pacific during the Mio-Pliocene (Motoyama 1996; Kamikuri 2012; Kamikuri etal. 2007; Oseki and Suzuki 2009; Romine 1985). S. delmontensis/peregrina only occur sporadically between
9.57 and 3.89 Ma and their mean relative abundance is
1.5% (SD = 4.4; N = 106) (Fig. 4 and Additional file 1).
Relative abundance higher than the mean value only
occurs between 9.57 and 7.21 Ma (Fig. 4 and Additional file 1). These species are abundant in sedimentcore samples from the North Pacific (e.g., Romine 1985),
while they have only sporadic occurrence in the Japan
Sea. The ecology of these species is also under debate.
Romine (1985) showed that despite a wide distribution
in the North Pacific, these species were probably related
to temperate-subarctic areas. Casey (1982) suggested
that these species may have inhabited shallow water athigh latitudes and intermediate water at low latitudes,
while Kamikuri (2012) reported that each species had its
own high-latitude and low-latitude forms, which makethe diagnostic use of S. delmontensis/peregrina problematic. However, Motoyama (1996) suggested that S. delmontensis/peregrina are probably a marker of warm
water in the Northwest Pacific. In addition, previous
studies in the Japan Sea showed that the relative abundances of S. delmontensis/peregrina covaried together
with those of Collosphaera spp. (Kamikuri andMotoyama 2007). Collosphaera spp. belong to the order
Collodaria, which includes species inhabiting shallow
water of subtropical to temperate areas (Suzuki and Not
2015; Biard et al. 2016, 2017). Therefore, in this study,
we assumed that the presence of S. delmontensis/peregrina suggests subtropical-temperate water of theNorth Pacific.

Page 20 of 33

Relative abundance of minor species

We have defined species or species groups as minor
when their relative abundance is between 0 and 10% of
the total assemblage. These minor species are Spongopyle osculosa Dreyer; Larcopyle weddellium Lazarus,
Faust, and Popova-Goll group; and Cornutella profunda
Ehrenberg and Carpocanistrum papillosum (Ehrenberg)
group (Figs. 3 and 4).
The species S. osculosa is a transitional-subarctic to
subarctic species inhabiting intermediate water depths in
the North Pacific (Kling and Boltovskoy 1995; Kamikuri
et al. 2008; Matsuzaki and Itaki 2017). This species has asporadic occurrence at Site U1425 and its mean relative
abundance is 1% (SD = 1.4; N = 154). This species’ relative abundance is higher than the mean value between 4
and 3 Ma, with a maximum of 10.5% at 3.56 Ma (Fig. 3
and Additional file 1).
The species L. weddellium is known as a subarctic-arctic species in the North Pacific (Tanaka and Takahashi
2008; Kamikuri et al. 2008; Matsuzaki and Itaki 2017).
At the middle to low latitudes of the North Pacific, thisspecies is less abundant and inhabits intermediate water
depths only (Matsuzaki et al. 2016). This species has also
been abundant at high latitudes of the Southern Hemisphere since 10 Ma (i.e., ODP Sites 689–690 in the
Weddell Sea) (Lazarus et al. 2005). Therefore, this species is likely related to subpolar-polar areas of bothhemispheres (bi-polar species). This species’ mean relative abundance is 1.6% (SD = 1.8; N = 154), although its
relative abundance never exceeds 1.0% after 1.47 Ma(Fig. 4 and Additional file 1). This species’ relative abundance is generally higher than the mean value between
7.91 and 5.05 Ma (Fig. 4 and Additional file 1).
C. profunda is an extant species that inhabits water
deeper than 300 m (Renz 1976; Casey et al. 1979; Takahashi 1991; Takahashi and Honjo 1981), while C. papillosum, which is also an extant species, inhabits water
deeper than about 1000 m in the North Pacific (Takahashi 1991; Takahashi and Honjo 1981). At Site U1425, C.
profunda occurs between 9.57 and 2.56 Ma, and its
mean relative abundance is 1.8% (SD = 1.7; N = 126).
The C. papillosum group occurs between 9.57 and3.89 Ma, and its mean relative abundance is 0.9% (SD =1.5; N = 106) (Fig. 4 and Additional file 1). C. papillosum
has a higher relative abundance exceeding 2% between
9.57 and 7.91 Ma (Fig. 4 and Additional file 1). Additionally, the species C. profunda shows relative abundance of 1–8% from 9.57 to 2.79 Ma (Fig. 4 andAdditional file 1).
Site U1430

According to Tada et al. (2015b) and Kamikuri et al.
(2017), a hiatus is present at Site U1430 in the upper
part of unit IIB (about 83 m CCFS-D according to Tada

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

et al. 2015b) and the stratigraphic interval between theD. bullatus (4.3–3.8 Ma) and L. parallelipes zones (6.8/
7.0 Ma to 7.2/7.4 Ma) is missing (e.g., Kamikuri et al.
2017). Therefore, we only describe the abundance ofspecies that can support the data obtained at Site U1425
for the reconstruction of the paleoceanography of the
Pleistocene and late Miocene (Fig. 5). Species related toarctic and subarctic areas, such as A. setosa, C. borealis,and C. davisiana, occur since 3 Ma (Fig. 5). The mean
relative abundance of A. setosa is 4.04% (SD = 5.03; N =11), while the means of C. borealis and C. davisiana are
7.98% (SD = 9.1; N = 14) and 9.27% (SD = 23.41; N = 14),respectively (Fig. 5 and Additional file 2). Relative abundances of C. sphaeris and the S. lineata/arachnea group
could not be estimated between 7.4 and ca. 4 Ma because of the hiatus (Fig. 5). Abundances of Phorticium
spp. and Tetrapyle spp., which are warm-water index
species (see above), are also affected by this hiatus. The
mean relative abundances of Phorticium spp. and Tetrapyle spp. are respectively 1.13% (SD = 2.9; N = 51) and
0.68% (SD = 1.48; N = 51) (Fig. 5 and Additional file 2).
Tetrapyle spp. has a relative abundance higher than themean value for the periods between 9.24 and 9.15 Ma,
8.93 and 8.68 Ma, 7.64 and 7.54 Ma, and 1.15 and 0 Ma
(Fig. 5 and Additional file 2). The S. delmontensis/peregrina group occurs only sporadically between 8.41 and8.31 Ma and 7.38 and 7.30 Ma, with an abundance peakexceeding 30% of the total assemblage (Fig. 5 and Additional file 2). C. nakasekoi occurs continuously between
9.44 and 7.38 Ma, and its mean relative abundance is
11.58% (SD = 8.60; N = 32) (Fig. 5 and Additional file 2).
C. papillosum occurs between 9.44 and 7.38 Ma, and its
mean relative abundance is 1.57% (SD = 2.29; N = 33),
while C. profunda occurs between 9.44 and 2.52 Mawith a mean relative abundance of 0.84% (SD = 1.50;
N = 40) (Fig. 5 and Additional file 2).

Discussion
During the Mio-Pliocene, the local paleoceanography of
the Japan Sea was closely related to regional tectonic activity and the progressive uplift of the Japanese islands.
During the Miocene until 10.5 Ma, the Japan Sea wasconnected to the North Pacific Ocean via seaways located around the edges of the East China and Yellow
seas, Fossa Magna basin, the subsided Tohoku area at
mid-latitudes, between northern Honshu and southern
Hokkaido islands, and around Sakhalin Island (e.g.,
Fukusawa 1988; Fujii et al. 1992; Iijima and Tada 1990;
Sato 1994; Kano et al. 1991; Kharakhinov 2010; Kobayashi and Tateishi 1992; Kosaka et al. 1992; Sagayama
2002; Yahata 2002; Yoshida et al. 2013). Between ca. 10.5
and 7 Ma, the Japan Sea was connected to the North Pacific via relatively shallow seaways around the Fossa
Magna, subsided Tohoku area, and Sakhalin Island,

Page 21 of 33

where neritic sedimentary facies (< 200 m) are recognized (e.g., Iijima and Tada 1990; Sato 1994; Yoshida etal. 2013; Kharakhinov 2010; Fukusawa 1988). However, arelatively deep seaway was reported between the northern Honshu and southern Hokkaido islands (e.g., Fukusawa 1988; Iijima and Tada 1990). Tada (1994) suggested
that the sill depth of this seaway would have been between 500 and 1000 m based on the sediments and fossil
facies reported in Iijima and Tada (1990). Around 8 and
7 Ma, the northeast Japan Islands uplifted because of
tectonic activity, which probably closed the Tohoku andFossa Magna seaways, and thus the Japan Sea was only
connected to the North Pacific via seaways locatedaround the southern Hokkaido and Sakhalin islands
until 3.1 Ma (e.g., Iijima and Tada 1990; Kano et al.
1991; Sato 1994; Yoshida et al. 2013; Kharakhinov 2010;
Fukusawa 1988). At 3.1 Ma, most studies agree that theseaway around the East China and Yellow seas re-opened (Itaki 2016; Kitamura and Kimoto 2006; Kitamura
et al. 2001; Tada 1994; Wang et al. 2014). In the discussion below, we propose to reconstruct the paleoceanography of shallow to deep waters with each connecting
seaway configuration taken into account.
In the following discussion, we use the following nomenclature: southern seaway is the seaway locatedaround the edge of the East China and Yellow seas, central seaway is the Fossa Magna basin, eastern seaway is
the subsided Tohoku area at mid-latitudes, northern seaway is the area between northern Honshu and southern
Hokkaido islands, and northernmost seaway is the areaaround Sakhalin Island.
Evolution of the sill depth of the northern seaway since
9.5 MaAccording to Iijima and Tada (1990), whose paleobathymetrical estimation relied upon sedimentological, micropaleontological (benthic foraminifera), and macrofossil(e.g., bivalves) analyses, the sill depths of the Japan Sea
northern seaway are estimated as middle to upper
bathyal water depths (500–1000 m) during the late Miocene (ca. 10–6 Ma). Our new dataset provides additional
constraints on the estimation of the northern strait sill
depths. At Sites U1425 and U1430, the time interval between ca. 9.5 and 7.8 Ma is characterized by occurrencesof C. profunda inhabiting water below 300 m and C.
papillosum inhabiting water between 1000 and 3000 m
deep in the North Pacific (Figs. 4, 5 and 6) (Takahashi
and Honjo 1981; Takahashi 1991). These species are absent in the modern Japan Sea (e.g., Itaki 2003; Itaki
2016; Motoyama et al. 2016a). Itaki (2016) suggested
that the absence of these species in the modern Japan
Sea is due to the geographical isolation of the intermediate and deep water of the Japan Sea from the North Pacific and thus suggested that these species are related toMatsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 22 of 33

Fig. 6 Details of the late Miocene paleoceanography of the Japan Sea (10–5 Ma). We compare relative abundances of C. nakasekoi, Tetrapyle spp.,
and C. papillosum from Sites U1425 and U1430 between 9.5 and 7 Ma. The interval between 7.0 and 5.0 Ma shows relative abundance of Phorticium
spp. and species related to subarctic water (the selected species are listed at the upper right in the figure). These data are compared to oxygen andcarbon isotope data for planktic and benthic foraminifer obtained from the South China Sea (ODP 1146, Holbourn et al. 2018)

the deep water of the North Pacific. Therefore, in thisstudy, we assumed that C. profunda and C. papillosum
are indicators of deep water of the North Pacific. Thus,
our data imply that between 9.5 and 7.8 Ma intermediate
to deep water of the North Pacific probably flowed into
the Japan Sea through the northern seaway, which had
water depths between 500 and 1000 m, because otherseaways open at that time (central, east, and northernmost) were too shallow (< 200 m) to enable deep-waterexchanges. Although the passive upwelling of deep-water

current may have also had an influence on these inflows
of deep water, because our radiolarian data are in agreement with other sedimentological data estimating the sill
depth of the northern seaway (e.g. Iijima and Tada
1990), we can consider that the effect of the passive upwelling is minor. Therefore, our new data, combinedwith the previous data of Iijima and Tada (1990), suggestthat the sill depth of the northern seaway was likely close
to 1000 m between 9.5 and 7.8 Ma. The very low abundance or absence of C. papillosum and the progressive

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

decrease in C. profunda relative abundance since 7.8 Ma
implies a probable shoaling of the northern seaway between 7.8 and 3 Ma, with the northern seaway probably
having a sill depth shallower than 300 m at ca. 3 Ma. Thisis likely related to regional tectonic activity and progressive uplift of the Japanese islands since 8–7 Ma, when the
stress regime in the Japanese islands and eastern JapanSea changed from extensional to compressional (e.g.,
Jolivet et al. 1994; Sato 1994; Yoshida et al. 2013).
Paleoceanography of the Japan Sea between 9.5 and
7.0 MaDuring this interval, the Japan Sea was connected to theNorth Pacific via shallow seaways at the central, east,and northernmost Japan Sea and via a deep seaway inthe north. Our data show intermittent high abundancesof Tetrapyle spp. and S. delmontensis/peregrina at Sites
U1425 and U1430 and, thus, relatively warm shallow
water probably prevailed intermittently (Fig. 6). Because
S. delmontensis/peregrina had a relatively wide geographical distribution and their ecology remains controvertible, we use mainly Tetrapyle spp. to discuss the
local paleoceanography.
Tetrapyle spp. occur episodically at ODP Site 302 inthe central Japan Sea (Kamikuri and Motoyama 2007)
and thus support our findings that the Japan Sea was influenced by warm water of the North Pacific between
9.5 and 7.0 Ma. Taking into account that only the northernmost, northern, eastern, and central seaways wereopen between 10 and 7 Ma (e.g. Iijima and Tada 1990;
Kano et al. 1991; Kharakhinov 2010; Sagayama 2002;
Sato 1994), warm current must have flowed into theJapan Sea through one of these seaways. Previous studies
did not report Tetrapyle spp. flowing the northern Japan
outcrops (Motoyama 1992; Motoyama 1993), middle-highlatitudes of the Northwest Pacific (ODP Sites 1151/1152)(Kamikuri et al. 2004), the Bering south of Sea/Gulf of
Alaska (ODP Sites 884–887) (Kamikuri et al. 2007), or
Hokkaido area outcrops (e.g., Shinzawa et al. 2009;
Motoyama and Nakamura 2002; Motoyama et al. 2016b).
As extant Tetrapyle spp. live in warm water and always
bear algal symbionts at the subfamily level (e.g., Zhang etal. 2018), shallow-warm waters were not flowing in theseregions. Thus, warm water of the North Pacific probably
did not flow into the Japan Sea via the northern andnorthernmost seaways, and the eastern and central Japan
Sea seaways are the most plausible pathways for enabling
the inflow of warm water into the Japan Sea from theNorth Pacific. Interestingly, the abrupt decrease in Tetrapyle spp. abundances at ca. 7 Ma also corresponds to thetiming of emergence of lands in the Tohoku area and theclosure of the central seaway (e.g., Fujii et al. 1992; Sato
1994; Yoshida et al. 2013). In consideration of the intermittent occurrence of Tetrapyle spp. between 9.5 andPage 23 of 33

7 Ma, we point out that the northern limit of Tetrapyle
spp. was probably around the Tohoku area (eastern seaway) during the late Miocene, and thus warm water probably flowed intermittently via the central and easternseaways between 9.5 and 7 Ma (Fig. 7).
The time interval between 9.5 and 7.0 Ma is alsocharacterized by high abundance of C. nakasekoi (about
30–60%) and intermittent abundance of C. papillosum
fluctuating between 1 and 10% (Fig. 6). The intermittent
fluctuation pattern for C. papillosum is roughly similar
to those of Tetrapyle spp. (Fig. 6). We know that C.
papillosum inhabits water depths between 1000 and3000 m in the North Pacific and its presence implies
that the sill depth of the northern seaway was probably
about 1000 m. Previous studies based on measurementof δ13C in benthic foraminifera imply that a layer withlow dissolved oxygen content existed in the North Pacific between 1000 and 3000 m, the so-called OMZ(Woodruff and Savin 1989). If we assume that the habitat zone of C. papillosum was similar throughout the
Neogene, C. papillosum may have inhabited the OMZ
water during the late Miocene. This hypothesis is
strengthened by the fact that laminations of diatom ooze
occurring within a dark organic-rich layer extending to a
thickness of about 1.5 m were recognized at about
287 m CCSF-D, which corresponds to an age of ca.
8 Ma (Irino et al. 2018; Kamikuri et al. 2017). Interestingly, the highest relative abundance (about 10%) of C.
papillosum is recorded at ca. 8 Ma at Sites U1425 andU1430 (Fig. 6), when the thickest lamina were deposited(Tada et al. 2015a). Other laminations are also recorded
at depths below 287 m CCSF-D; however, these were
not as thick, so their positions were not reported in Tada
et al. (2015a). Interestingly, the relative abundance of C.
papillosum was also intermittent before 8 Ma, but its
relative abundance was much lower (Fig. 6). Therefore,
it is possible that the occurrence of C. papillosum is related to the deposition of laminas. Based on Watanabe
et al. (2007), laminas are deposited in the Japan Sea
when the bottom water is poor in oxygen. Therefore, itis probable that the C. papillosum abundance implies
oxygen-poor bottom water in the Japan Sea. Thus, when
C. papillosum abundance is high, it is probable thatOMZ water from the North Pacific was flowing into theJapan Sea, while when the C. papillosum relative abundance was lower or close to 0%, OMZ water probably
was not flowing. To explain this intermittent fluctuationin C. papillosum, one plausible explanation is the glacioeustatic sea-level variation, which was already proposed by Tada (1994), who assumed that orbitally paced
glacioeustatic sea-level changes probably caused shoaling
and deepening of the northern seaway (ca. 1000 m), although a shoaling/deepening of the OMZ itself cannot
be neglected (Fig. 7). However, as said above, theMatsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 24 of 33

Fig. 7 Suggested hydrography of the deep water and shallow water of the Japan Sea between 9.5 and 7.0 Ma

intermittent fluctuation of Tetrapyle spp. is roughly synchronous to that of C. papillosum. We have alreadyshown that warm water of the North Pacific probably
flowed into the Japan Sea via the eastern and northeastern seaways, which had relatively shallow water depths.
Therefore, it is probable that changes in the sill depthsof the connecting seaways (northern, eastern, and central) in relation to the glacioeustatic sea-level changes

influenced OMZ and warm water inflow from the North
Pacific into the Japan Sea at that time.
In contrast, the relative abundance C. nakasekoi increased when C. papillosum and Tetrapyle spp. had alow relative abundance. The concern is that C. nakasekoi
is a species reported in the Japan Sea only between ca.
10 and 7 Ma (Kamikuri and Motoyama 2007; Kamikuri
et al. 2004; Motoyama 1996), and its ecology remains

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

unknown. Previous studies reported that C. nakasekoi isabsent in the North Pacific Ocean and only constituted
about 1% of the total assemblage in samples from outcrops in Hokkaido Island, while this species exceeded
20% of the total assemblage in the Japan Sea (e.g., Kamikuri et al. 2004; Motoyama et al. 2016b; Shinzawa et al.
2009; this study). As we assumed that the sill depth of
the northern seaway was ca. 1000 m between 9.5 and
7.8 Ma, one plausible explanation is that C. nakasekoi
lived in waters deeper than 1000 m, and thus C. nakasekoi would have been trapped in the Japan Sea. However,it seems that high abundance of C. nakasekoi occurred
when the relative abundances of Tetrapyle spp. and/or
Phorticium spp. were low (Fig. 6). This implies that theC. nakasekoi relative abundance increased when therelative abundances of species related to warm water decreased. Therefore, although the specific distribution of
C. nakasekoi suggests that this could be an intermediate-to-deep-water species restricted to the Japan Sea, wecannot assume that this species is not related to a cold
marine environment. In fact, the more probable explanation is that C. nakasekoi is related to poorly stratified
water conditions. Indeed, Tada (1994) suggested that the
OMZ was nutrient-rich and probably had a high salinity
based on the interpretation of the value of δ13C reported
by Woodruff and Savin (1989). However, warm water isknown for having a low density (e.g., Ruddiman 2001).
Therefore, when the OMZ and warm water flowed fromthe North Pacific into the Japan Sea, the water column
was likely well stratified (Tada 1994). In such a context,
we observed low relative abundance of C. nakasekoi(Figs. 6 and 7). In contrast, when there was no inflow of
OMZ and warm water from the North Pacific, it is likelythat the water masses in the Japan Sea were less stratified, and Tada (1994) suggested that the paleoceanographic condition would have been more or less similar
to the present Japan Sea, where deep water is well ventilated because of a vertical mixing of water masses(Fig. 7). Therefore, it is probable that C. nakasekoi developed in the Japan Sea when the water column was probably relatively well mixed, and thus it seems that C.
nakasekoi prefers water masses that are well oxygenated(Figs. 6 and 7).
Paleoceanography of the Japan Sea during the late
Miocene and early Pliocene with only the northern strait
open (ca. 7–5.0 Ma)

From 7 to 5 Ma, the northern and northernmost seaways were the only gateways enabling water exchanges
between the Japan Sea and the North Pacific. As suggested above, the sill depth of the northern strait was
likely shallower than 1000 m but deeper than 300 m
between ca. 7.8 and 3 Ma because of the presence ofC. profunda (> 300 m) and low relative abundance/orPage 25 of 33

absence of C. papillosum (> 1000 m) (Fig. 6). This suggests that only intermediate to shallow water could havebeen exchanged between the Japan Sea and North Pacific at that time. Radiolarian data at Site U1425 suggest
enhanced cooling conditions in the Japan Sea between
7.0 and 5.8 Ma, which was characterized by an increasein abundances of the subarctic-transitional species, exceeding 30% of the total assemblage during this interval(Fig. 5). Our data therefore suggest that a cold marine
environment prevailed in the Japan Sea at that time.
Recently, Herbert et al. (2016) used the alkenone unsaturation index to show that a synchronous cooling occurred in shallow water at high latitudes in the Northern
Hemisphere between ca. 7.5 and 5.5 Ma. This cooling
was interpreted as a transient glaciation of the Northern
Hemisphere and is called the late Miocene cooling (Herbert et al. 2016). Other studies suggested that during thiscooling, an increase in C4 plants was recorded, and thus
the climate likely became drier (e.g., Cerling et al., 1997;
Holbourn et al. 2018; Huang et al., 2007). Additionally,
recent analysis of Asian eolian dust from the Japan Sea
also suggested a temporal drying of Central Asia ca. 8–
7 Ma (Shen et al. 2017). Holbourn et al. (2018) used
δ18O and δ13C to measure benthic and planktic foraminifera at ODP Site 1146 (South China Sea) and suggested
a cooling at that time because of enhanced EAWM,
which probably increased the biological pump anddrastically modified the carbon cycle. In Fig. 6, we compare our radiolarian data to the isotope data of Holbourn et al. (2018). The cooling implied by radiolarianassemblages is synchronous with the shift recorded in
isotope data from the South China Sea, and thus thecooling implied by radiolarian assemblages is likely related to the late Miocene cooling and the enhanced
EAWM. Cooling at high latitudes is generally associated with a southward shift of the subarctic front (e.g.,
McClymont et al., 2008), while enhanced EAWM generally strengthened winds blowing from north to south
because of a Siberian high and Aleutian low (e.g., Tada
et al. 2016). Therefore, rather than a local increase incold radiolarian species productivity because of a cooling climate, it is likely that the influence of cold water
currents was stronger during the late Miocene cooling,
and thus a larger amount of cold water was transported
from high latitudes to the marginal sea. This implies
that this cold current influenced the Japan Sea via thenorthern and northernmost seaways located between
northern Honshu and southern Hokkaido islands andaround Sakhalin Island because other seaways wereclosed at that time (Fig. 8).
In this study, at Site U1425, abundances of subarctic-transitional species drastically decreased between 5.8
and 5.2 Ma, while abundances of species related to shallow water of transitional-subtropical (Phorticium spp.)

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

areas increased (by about 20%) (Fig. 6). Radiolarian data
imply that cold water continued to flow into the Japan
Sea from the northernmost seaway (Sakhalin area) because the relative abundance of transitional-subarctic
species was still fluctuating between 10 and 20% (Fig. 6).
However, relatively warm water probably flowed at thesame time from the northern seaway (northern Honshu
and Southern Hokkaido islands) because the relative
abundance of subtropical-transitional species was about
20%, while their abundance was less than 5% between 7
and 5.8 Ma (Fig. 8). Previously published data for mollusca fossils confirmed our hypothesis by showing thattemperate conditions prevailed in the Japan Sea duringthat time (Ogasawara 1994). Around 5 Ma (early Pliocene), Earth experienced a warm climate with relatively
high atmospheric pCO2 (e.g., Fedorov et al. 2013). At
the same time, the tropical warm pool likely expanded(e.g., Brierley et al. 2009). Therefore, considering that
we have used an age model relying on biostratigraphyof radiolarians and an error margin of ca. 0.2 Myr(Kamikuri et al. 2017), the higher abundances of transitional-subtropical species between ca. 5.8 and 5.2 Ma
are probably related to the warm conditions prevailingthroughout the Earth, which plausibly caused an expansion of the tropical warm pool and a northward shift ofthe subtropical front, enabling inflow of relatively temperate-warm water into the Japan Sea through thenorthern strait.

Page 26 of 33

Drastic cooling of the subsurface and intermediate waters
during the mid-Pliocene (ca. 5.0–3.8 Ma)

Our radiolarian data from the Japan Sea show that the S.
arachnea/lineata group, an intermediate-water species
restricted to the polar to subpolar areas of the Northern
Hemisphere (e.g., Boltovskoy and Correa 2016), dominates our assemblages between ca. 5.0 and 3.8 Ma(Fig. 9). The S. arachnea/lineata group reported in previous paleoceanographic and biostratigraphic studies
showed a low abundance (< 5%) because this group isrelatively small (about 50 μm), and most of the previous
studies processed the sediments with 63-μm mesh sieves(e.g., Motoyama 1996; Kamikuri et al. 2004, 2007, 2009).
Despite this technical issue, increases and decreases in
the abundance of this group have been reported off thenortheastern Japanese coast and in the subarctic North
Pacific south of the Bering Sea (ODP Sites 1151 and884) at ca. 4.7 and 4.0 Ma (appendix of Kamikuri et al.
2004, 2007). In the southern Gulf of Alaska (ODP Site
887) and in the Equatorial Pacific (ODP Sites 845 and1241), this species was absent (Kamikuri et al. 2007;
Kamikuri et al. 2009). These findings, combined with
our data, suggest that a drastic cooling occurred in thesubsurface to intermediate waters of the Japan Sea andthe Northwest and Central North Pacific almost simultaneously during the mid-Pliocene. This may have beencaused by a southward flow of subarctic subsurface tointermediate water from high latitudes of the Northwest

Fig. 8 Connections between the Japan Sea and the North Pacific during the late Miocene to late Pliocene

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 27 of 33

Fig. 9 Details of the paleoceanography of the Japan Sea between 5 and 0 Ma. We compare relative abundances of S. arachnea/lineata group,
Phorticium spp., and species related to subarctic and arctic areas (the selected species are listed at the upper right in the figure) from Site U1425.
These data are compared to Mg/Ca ratio data for plankton of the South Pacific and Atlantic (ODP 516/590, Karas et al. 2011, 2017) and benthic
oxygen isotopes (Lisiecki and Raymo 2005)

Pacific. At that time, only the northern seaway, which ata water depth deeper than 300 m was deep enough toenable inflow of subsurface to intermediate water of theNorth Pacific, because S. lineata/arachnea inhabitswater depths between 300 and 1000 m in the North Pacific (Kling and Boltovskoy 1995). Therefore, we suggestthat such intermediate water influenced the Japan Sea
via the northern Strait between 5.0 and 3. 8 Ma (Fig. 8).
However, causes and mechanisms are difficult to explain.
A re-estimation of S. arachnea/lineata group presence
using 45-μm mesh sieves at other DSDP/ODP sites andcomparison with geochemical data would probably provide clarification.

Although it is just speculation, numerous studies havesuggested a close link between changes in the North Pacific paleoceanographic conditions and the final shoalingof the Panama Isthmus ca. 5–4 Ma (e.g., Cortese et al.
2004; Haug et al. 2001; Steph et al. 2006; Stroynowski etal. 2015). Steph et al. (2006) showed that the δ18O measured in Globigerinoides sacculifer (Brady) (planktic foraminifera) at sites between the Eastern Equatorial Pacificand the Caribbean Sea began to diverge between ca. 4.7
and 4.2 Ma. This was interpreted as a reduced exchangeof water masses through the Panama Isthmus, inhibitingexchanges of shallow water between the North Pacificand North Atlantic (Steph et al. 2006). A coupledMatsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Page 28 of 33

atmosphere-ocean climate model experiment by Motoi
et al. (2005) suggested that the closure of the Panama
Isthmus not only inhibited the export of warm waterfrom the North Atlantic to the North Pacific but also
disturbed the water mass density (salinity) balance ofboth oceans. In addition, Karas et al. (2017) reconstructed temperatures based on the planktic foraminifera
Mg/Ca ratio and found a synchronous cooling of theSouth Atlantic and South Pacific between 5 and 4 Ma.
Further, they associated this cooling with an episodic enhanced Atlantic meridional overturning circulation due
to water mass density disturbance initiated by the final
closure of the Panama Isthmus. In Fig. 9, we plot ourradiolarian data against the Mg/Ca ratio obtained by
Karas et al. (2017) in the South Atlantic and South Pacific. It seems that the interval where the radiolarian assemblage of the Japan Sea is dominated by the S.
arachnea/lineata group corresponds to the cooling
event reported by Karas et al. (2017). Therefore, it ispossible that the cooling recorded in the Japan Sea andNorthwest Pacific intermediate water is related to theclosing of the Panama Isthmus and its related watermass density perturbation, which may have affected theglobal thermohaline circulation episodically.

diatom Td’-based sea surface temperature (SST) of theJapan Sea (ODP Site 797) was colder than that recordedin the North Pacific (ODP Site 436) at a similar latitude
despite the opening of the seaway into the southern
Japan Sea at ca. 3.1 Ma (Iijima and Tada 1990; Tada
1994; Ogasawara 1994). To explain this observation,
Itaki (2016) suggested the possibility that subarctic waterfrom the Sea of Okhotsk influenced the Japan Sea via astrait west of Hokkaido Island during the Pliocene. Considering the local geological context, we know that until
ca. 3 Ma the area around Sakhalin Island was still characterized by shallow neritic facies, implying that cold
water of the high latitudes could still influence the JapanSea via the northernmost seaway of the Japan Sea (Kharakhinov 2010). Therefore, we can infer that transitional-subarctic species probably continued to enter the JapanSea via a shallow strait between the Sakhalin Islands andthe Japan Sea until its closure between 3 and 2 Ma
(Kharakhinov 2010), while transitional-subtropical species probably entered through the northern strait, as
during the early Pliocene (Figs. 8 and 9).

Paleoceanography of the Japan Sea during the late
Pliocene (ca. 3.8–2.7 Ma)

At 2.7 Ma, the NHG began, which marked the beginningof the Pleistocene (e.g., Haug et al. 1999; Raymo 1994).
At Site U1425, our data show that relative abundancesof arctic species increased from 2.7 Ma, while transitional-subarctic species and subtropical-transitional species
abundances decreased (Fig. 9). In addition, species related to deep water of the North Pacific disappeared(Figs. 3 and 4). This implies a drastic cooling of theJapan Sea due to the NHG, and the absence of Pacificdeep-water species suggests that the deep water of theJapan Sea was isolated from the North Pacific because
the sill depth of the northern seaway was too shallow.
This shoaling is probably due to the sea-level fall causedby the NHG and tectonic uplift of northeastern Japan(e.g., Kamikuri and Motoyama 2007; Itaki 2016).
The Pleistocene is characterized by cyclical glaciation(e.g., Lisiecki and Raymo 2005), and the relationship between the amplitude of glaciations caused by orbital forcing was not linear (e.g., Lisiecki and Raymo 2005;
Elderfield et al. 2012). During the early Pleistocene(2.58–1.2 Ma), weak glaciations with a periodicity of
41 ky characterized the glacial-interglacial cycles, whilestrong glaciations were repeated with a periodicity ofnearly 100 ky since the middle Pleistocene (0.8 Ma)(Lisiecki and Raymo 2005; Elderfield et al. 2012). This
periodicity shift, called as the mid-Pleistocene transition(MPT) (Berger and Jansen 1994), occurred from 1.2 to
0.8 Ma. During this event, our data show high abundance peaks of species related to arctic shallow water

The late Pliocene is characterized by a progressive global
cooling until the beginning of the NHG (e.g., Haug et al.
1999; Raymo 1994). Abrupt emergence of land is suggested for the Hokkaido and Sakhalin archipelagic water
regions based on recent geological studies because of thecooling related to the NHG between 3 and 2 Ma (e.g.,
Sagayama 2002; Yahata 2002; Kharakhinov 2010). Thus,
the exchange of subarctic water via the northernmost
seaway would have been affected (Sagayama 2002;
Yahata 2002; Kharakhinov 2010). For this interval (3.5–
2.7 Ma), our data show that the transitional-subarctic
species and transitional-subtropical species had relative
abundances varying between 20 and 40% and 10 and
20%, respectively (Fig. 9). Between 3.8 and 2.7 Ma, ourdata imply that the Japan Sea was probably still influenced by transitional-subarctic and transitional-subtropical water at that time.
Previous studies suggested that the opening of thesouthern strait at ca. 3 Ma caused only a restricted andlocalized warming to the southernmost part of the Japan
Sea because the channel was probably very narrow andinsufficient to supply significant amounts of warm water(e.g., Iijima and Tada 1990; Itaki 2016; Kitamura andKimoto 2006; Kitamura et al. 2001). Therefore, transitional-subtropical water probably did not flow into theJapan Sea from the southern strait. Koizumi and Yamamoto (2016) showed that at the same latitude, thePaleoceanography of the Japan Sea during the
Pleistocene (ca. 2.5–0 Ma)

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

between 1.3 and ca. 1.0 and Ma and thus imply that the
MPT and its related strong glaciation probably intensified the cooling of the Japan Sea. Additionally, the Mid-Brunhes Event (MBE) occurring between 0.45 and
0.3 Ma (Jansen et al. 1986) corresponds to a period
when Earth eccentricity was close to 0 (Berger 1978).
This likely caused lower pCO2 and caused a colder
spring-summer season, while the autumn/winter season
was warmer (Lüthi et al. 2008; Yin and Berger 2010).
Our data show high abundance peaks of species related
to arctic shallow water between 0.5 and ca. 0.3 Ma(Fig. 9). This suggests intensification of the cooling of
the Japan Sea shallow water during these times. Interestingly, this orbital event fit well with our second coolingof the shallow water and thus suggests that the MBE
probably intensified the cooling of the Japan Sea.

Page 29 of 33

of the tropical warm pool likely occurred(e.g., Fedorov et al. 2013; Brierley et al. 2009).
7. The Japan Sea subsurface to intermediate water
drastically cooled between 5.0 and 4.0 Ma andsimilar cooling likely occurred in the subarctic areaof the Northwest Pacific almost synchronously. The
reasons and mechanisms of this cooling remain
unknown, but because the timing of this cooling
was almost simultaneous with the formation of the
Panama Isthmus, they may be related.
8. The NHG and Pleistocene major climatic events,
such as the MPT and MBE, intensified the coolingof shallow water in the Japan Sea.

Additional files
Additional file 1: Raw data (%) of the species used in this study(U1425). (XLSX 84 kb)

Conclusions
Radiolarian assemblages analyzed at Sites U1425 andU1430 enabled us to reconstruct the evolution of theJapan Sea hydrographic system since 9.5 Ma. We canconclude that radiolarians in the Japan Sea were sensitive to environmental changes caused by regional tectonism, as well as global climatic events:
1. During the late Miocene, the sill depth of thenorthern strait was likely close to 1000 m until ca.
7.8 Ma and probably enabled inflow of OMZ waterfrom the North Pacific when the sea level was high.
Since 7.8 Ma, a progressive shoaling of the northernstrait is implied by the radiolarian data, and at
about 3 Ma, the sill depth of the northern strait wasprobably 300 m. This shoaling is likely due toenhanced tectonic activity on the Japan islands.
2. The central and eastern seaways were likely the keystraits enabling inflow of warm-shallow water of theNorth Pacific into the Japan Sea between 9.5 and
7 Ma, when sea level was high.
3. Our data suggest that C. papillosum is probably
related to OMZ water of the North Pacific.
4. Although the habitat zone of C. nakasekoi remains
difficult to assess, it is possible that C. nakasekoi
was related to poorly stratified water masses formed
when the sea level was low during the late Miocene
because the inflow of OMZ and warm water wereprevented.
5. The Japan Sea recorded a deep cooling between 7
and 5.5 Ma. This cooling is probably related to thelate Miocene cooling of Herbert et al. (2016) andenhanced EAWM.
6. A moderate warming occurred between 5.6 and
5.2 Ma in the Japan Sea, and it was probably related
to the early Pliocene warming, when an expansion

Additional file 2: Raw data (%) of the species used in this study(U1430). (XLSX 42 kb)
Abbreviations
AB: Absolute abundance; CCD: Calcite compensation depth; CCSF: Core
composite depth below sea floor; DSDP: Deep-Sea Drilling Program;
EAWM: East Asian winter monsoons; F-slide: Faunal slide; IODP: Integrated
Ocean Drilling Program; MBE: Mid-Brunhes Event; MIS: Marine isotope stage;
MPT: Mid-Pleistocene Transition; NHG: Northern Hemisphere Glaciation;
ODP: Ocean Drilling Program; OMZ: Oxygen minimum zone; Q-slide: Quantitative
slide; SD: Standard deviation; SST: Sea surface temperature; TWC: Tsushima Warm
Current
Acknowledgements
We would like to thank the Integrated Ocean Drilling Program (IODP)
Expedition 346 for providing us the samples. We also wish to thank the
Kochi Core Center (KCC) and its curators for their sampling assistance.
We also wish to thank Mr. Shunsuke Kurokawa for discussions about themanuscript and Mr. Yasuaki Chiba for his help in analyzing samples from
Site U1430.
Funding
This work was supported by the Japan Society for the Promotion of Science(JSPS) Research Fellowship for Young Scientists, grant 16J02142 (MKM) andpartly founded by the JSPS grant 18H01279 attributed to Takuya Sagawa(Kanazawa University). This work was also partially financed by the IODP
Expedition 346 After Cruise Research Program, JAMSTEC.
Availability of data and materials
The radiolarian data used in this study are available in Additional files 1 and 2,
which are attached to this study as supplementary materials.
Authors’ contributions
MKM conducted the treatment and analysis on 154 samples from Site
U1425, drew figures and tables, and wrote the manuscript. IT and TR
proposed the topic and co-designed the study. KSI conducted analysis
on samples from Site U1430. All authors read and approved the final
manuscript.
Authors’ information
MKM is a JSPS Research Fellow at the University of Tokyo and now assistantprofessor at Atmosphere and Ocean Research Institute of the university ofTokyo; IT is a senior researcher at the Geological Survey of Japan, AIST; TR isa professor of the University of Tokyo, the host researcher of MKM, and theco-chief of IODP Expedition 346; KSI is an associate professor at Ibaraki
University.

Matsuzaki et al. Progress in Earth and Planetary Science (2018) 5:54

Competing interests
The authors declare that they have no competing interests.

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. 4Faculty of Education, Ibaraki University, 2-1-1 Bunkyo,
Ibaraki 310-8512, Japan.
Received: 15 February 2018 Accepted: 14 August 2018

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