Millennial-scale fluctuations in water volume transported by the Tsushima Warm Current in the Japan Sea during the Holocene

Millennial-scale fluctuations in water volume transported by the Tsushima Warm Current in the Japan Sea during the Holocene

Global and Planetary Change 183 (2019) 103028 Contents lists available at ScienceDirect Global and Planetary Change journal homepage: www.elsevier.c...

3MB Sizes 0 Downloads 39 Views

Global and Planetary Change 183 (2019) 103028

Contents lists available at ScienceDirect

Global and Planetary Change journal homepage: www.elsevier.com/locate/gloplacha

Research article

Millennial-scale fluctuations in water volume transported by the Tsushima Warm Current in the Japan Sea during the Holocene

T



Keiji Horikawaa, , Tomohiro Kodairab, Ken Ikeharac, Masafumi Murayamad, Jing Zhanga a

Graduate School of Science and Engineering for Research, University of Toyama, Gofuku 3190, Toyama 930-8555, Japan Graduate School of Science and Engineering for Education, University of Toyama, Gofuku 3190, Toyama 930-8555, Japan c Research Institute of Geology and Geoinformation, Geological Survey of Japan, AIST, Tsukuba Central 7, 1-1-1 Higashi, Tsukuba, Ibaraki 305-8567, Japan. d Center for Advanced Marine Core Research, Kochi University, B200 Monobe, Nankoku 783-8502, Japan b

A R T I C LE I N FO

A B S T R A C T

Keywords: Neogloboquadrina incompta Mg/Ca-derived sea-surface temperature The Japan Sea Tsushima Warm Current Holocene Solar forcing

Cyclic changes in volume transport of the Tsushima Warm Current (TWC) have been argued from diatom records in the southern Japan Sea off the Japanese islands during the Holocene. Although this phenomenon has not yet been confirmed by various proxy data, determining whether or not these oceanographic changes occurred is crucial for clarifying the nature of oceanographic changes in the southern Japan Sea. Here, we conducted a coupled analysis of Mg/Ca ratios and oxygen isotopes (δ18O) in shallow-dwelling Neogloboquadrina incompta from 13 core-top sediments in southern Japan, and developed a new equation for Mg/Ca temperature calibration (Mg/Ca = 0.311 × exp (0.07 × T)) as a proxy for spring sea surface temperature (SST). Using the newly developed, species-specific Mg/Ca-paleothermometry, we reconstructed SST variability for the past 6800 years from core YK10-7-PC09 in the southern Japan Sea. The Mg/Ca-derived SST record clearly represented five warmer periods at 6200–6000, 4900–4500, 4200–3800, 2600–2100, and 900–400 cal. year BP, almost consistent with previously published diatom records. These warmer events also corresponded to the periods in which warm molluscan assemblages increased at the northern end of the TWC, suggesting that periods of higher SST can be seen as reflecting the increased volume transport of the TWC. We interpreted the results of a model study showing that higher solar irradiance provoked positive Arctic Oscillation (AO)-like spatial patterns and the negative phase of the Pacific Decadal Oscillation (PDO) to mean that increased (reduced) TWC volume transport on the multi-centennial to millennial time scales was caused by high (low) solar insolation via a potential link between AO and PDO. Given that larger and more frequent volcanic eruptions occurred in the mid Holocene than in the late Holocene, volcanic forcing on the TWC volume transport changes would have been more significant during the former, as seen in the highly variable SST from this period and distinct decreases in SST around ~5900 cal. year BP and ~6400 cal. year BP. The millennial-scale fluctuations seen in SSTs in the southern Japan Sea would have had a large impact on the evolution of vegetation and human adaptation in the northern Japanese islands, adjacent to the Japan Sea, over the last 6800 years.

1. Introduction A growing number of high-resolution Holocene climate records have highlighted that sea surface temperature (SST), precipitation, and the latitudinal position of the westerly jet have oscillated over centennial to millennial timescales (Jo et al., 2017; Mayewski et al., 2004; Nagashima et al., 2013; Sagawa et al., 2014; Wang et al., 2005; Wanner et al., 2008). These climate proxy records have been used to analyze the spatiotemporal patterns in climate variability and their relationship with natural modes of variability (e.g. the El Niño Southern Oscillation

(ENSO), Pacific Decadal Oscillation (PDO), and Arctic Oscillation (AO)), and to natural forcing factors (i.e. orbital insolation, solar irradiance, and volcanic eruptions) (Koutavas and Joanides, 2012; Mayewski et al., 2004; Sigl et al., 2015; Wanner et al., 2011). Orbital insolation has strongly influenced spatiotemporal climate patterns throughout the Holocene (Wanner et al., 2008). The redistributed insolation energy has led to a progressive southward shift of the summer position of the Intertropical Convergence Zone (ITCZ) in the Northern Hemisphere (NH), and weakened the Asian and African monsoon systems from the mid to late Holocene (Clement et al., 2000;



Corresponding author. E-mail addresses: [email protected] (K. Horikawa), [email protected] (K. Ikehara), [email protected] (M. Murayama), [email protected] (J. Zhang). https://doi.org/10.1016/j.gloplacha.2019.103028 Received 22 November 2018; Received in revised form 19 July 2019; Accepted 5 September 2019 Available online 05 September 2019 0921-8181/ © 2019 Elsevier B.V. All rights reserved.

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

at multiple sites in the southern Japan Sea since 8000 years ago, arguing the volume transport changes in the TWC on the millennial timescale. However, the temporal resolution of diatom records is not extensive enough for use in discussing its relevance to changes in modes of natural variability and natural forcing factors. Further, alkenonederived SST record that was reported in the northern Japan Sea exhibited a different SST variability on the millennial timescale (Bae et al., 2014), requiring a reason for the discrepancy between different SST records. A previous study in the western North Pacific proposed that solar activity could be the principal climate forcing in the East Asian Monsoon system (Sagawa et al., 2014). However, the linkage between oceanographic changes, natural variability modes (e.g. ENSO, PDO, and AO), and natural forcing factors (solar irradiance and volcanic eruption) on multi-centennial to millennial timescales still remains unclear. There are no Holocene Mg/Ca-derived SST records from planktonic foraminifera in the Japan Sea so far, although planktonic foraminiferal Mg/Ca thermometry has been applied to many oceanic sediments, for use as a robust SST proxy (Cléroux et al., 2008; Mashiotta et al., 1999). In this study, first we established a new Mg/Ca-temperature calibration for Neogloboquadrina incompta, using core-top sediments collected from shallow depths (< 1500 m water depth) near the Japanese islands. Then, we generated high-resolution Mg/Ca-derived SSTs for the past 6800 years in the southern Japan Sea as a new record for the western North Pacific. We also analyzed volume transport changes in the TWC at millennial timescales, and examined how such volume transport change might be correlated with natural variability modes and natural forcing factors.

Koutavas and Joanides, 2012). In addition, solar irradiance and explosive volcanic eruptions might have had a large influence on the appearance of decadal to multi-centennial climate variations during the Holocene (Sigl et al., 2015; Wang et al., 2005; Wanner et al., 2008). With the sun being the energy source for the Earth's climate system, small changes in solar activity can induce a relatively large modulation of solar ultraviolet output and alter the radiative balance in the stratosphere through ozone feedback processes, subsequently leading to changes in tropospheric circulation (Gray et al., 2010). Climate model simulations show that solar minima drive spatial patterns in atmospheric pressure and temperature that resemble the negative phase of the AO (Ineson et al., 2011). On the other hand, large volcanic eruptions emit sulfate aerosols into the troposphere and stratosphere (20–25 km). These aerosols remain for longer periods of time, and their efficient adsorption of incoming solar radiation causes regional to global cooling for 2–3 years, weakening the Asian and African summer monsoons due to continental cooling and a reduction of the land-sea temperature contrast (Robock, 2015; Sigl et al., 2015). Multiple large volcanic eruptions separated by several decades could cause decadal to centennial cooling in the NH (Sigl et al., 2015). Although solar irradiance forcing, at its peak amplitude, is roughly an order of magnitude smaller than volcanic forcing, the lower-frequency nature of solar irradiance forcing results in a substantially larger impact (Mann et al., 2005). The Japan Sea (also called as the Sea of Japan) is a semi-closed marginal sea under the influence of the East Asian Summer Monsoon (EASM). Today, the Japan Sea is dominated by inflow of the Tsushima Warm Current (TWC) from the East China Sea (ECS) through the shallow Tsushima Strait (sill depth = 130 m) (Fig. 1a). Koizumi (1989) and Koizumi (2008) found that the abundance of TWC-related diatom species, Fragilariopsis doliolus, has largely fluctuated at 1500-yr intervals

Fig. 1. (a) Map showing the Tsushima Warm Current (TWC, red arrows) and the Liman Current (blue arrows) (Mooers et al., 2005) in the Japan Sea and the locations of core-top samples (open circles). At Site YK10-7-PC09 (star), piston core and core-top samples were obtained. Closed squares denote the localities for sediment cores (L-3, C-GC-8, and MR0604-PC03B) previously published (Bae et al., 2014; Koizumi, 2008; Oba et al., 1995). The colour map shows the annual mean SST, and the bathymetric contours (1000 and 2000 m) are also shown. (b) Map showing the locations B-3GC (Jian et al., 2000), Mulyoungari (Park et al., 2016), MD01-2421 (Isono et al., 2009), BN-1 (Jo et al., 2017), Mt. Logan (Fisher et al., 2008), and V21–30 (Koutavas and Joanides, 2012), which are selected Holocene climate archives used in this study. (c) Monthly changes in temperature and salinity at water depths of 20 m and 50 m near Site PC09. 20 m (S) and 20 m (T) denote salinity and temperature data at the water depth of 20 m. The light blue bar presents the dominant habitat season for Neogloboquadrina incompta. 2

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

2. Oceanographic setting

past can be inferred from SST reconstructions, if they record the spring, winter, or annual means.

2.1. Oceanographic setting in the southern Japan Sea 2.2. Neogloboquadrina incompta The semi-closed Japan Sea can only exchange surface waters with the open oceans through the Tsushima, Tsugaru, Soya, and Mamiya Straits (< 130 m water depth) (Fig. 1a). The surface water (0–200 m depth) in the Japan Sea is occupied by the TWC, which flows through the Tsushima Strait and flows out through the Tsugaru and Soya Straits (Na et al., 2009) (Fig. 1a). Maximum throughflow in the Tsushima Strait (2.5 ± 0.5 Sv) (1 Sv = 106 m3 s−1) takes place in spring to fall and minimum throughflow in winter, which occurs synchronously in the Tsugaru and Soya Straits (Kida et al., 2016; Takikawa et al., 2005). The TWC forms three branches in the Japan Sea (Kawabe, 1982). The nearshore branch of the TWC feeding from the eastern channel of the Tsushima Strait flows along the Japanese coast, and the second branch feeding from the western channel of the Tsushima Strait flows along the continental shelf break and slope along the Japanese coast (Hase et al., 1999) (Fig. 1a). The nearshore and the second branches develop throughout the year and spring to fall, respectively (Hase et al., 1999). The northern Japan Sea is dominated by the Liman Current, which consists of Amur River water and sea-ice meltwater (Fig. 1a). The Liman Current flows from northeast to southwest along the Russian coast (Martin and Kawase, 1998), and then meets the TWC at ~40° N, in the central Japan Sea, forming the Polar Front. The TWC consists of the admixture of three water masses (Che and Zhang, 2018); (1) Changjiang River diluted water in the ECS, (2) a branch of the Kuroshio Current, and (3) the Taiwan Warm Current. The proportional contribution from each water mass changes seasonally, thereby changing the water properties of the TWC. From summer to autumn, the summer monsoon increases the Changjiang River discharge into the ECS, and increases the volume transport of the TWC. Consequently, warm and low-salinity waters are delivered from the ECS to the Japan Sea (Fig. 1c), and the southern Japan Sea undergoes a stratified surface condition. In contrast, during the winter and spring seasons, the volume transport of the TWC decreases, which reduces heat and freshwater transport to the southern Japan Sea, leading to the decreases in SST and increases in sea-surface salinity (SSS) (Fig. 1c). The change in the TWC volume transport is also attributed to seasonal changes in the atmospheric pressure over the Japan Sea, the along-strait wind stress at the Tsushima Strait, and the sea-level differences along the straits (Lyu and Kim, 2005). Indeed, the nearshore branch of the TWC intensifies in response to the intensification of the southwesterly winds during the summer monsoon seasons, when the North Pacific High is located further west (Takikawa et al., 2017). Further, the decadal variation in the upper ocean heat content (50–125 m) has been documented in the eastern part of the Japan Sea, which is considered to be a result of the TWC variability at decadal timescales (Na et al., 2012). An increased TWC volume transport through the Tsushima Strait occurred during the 1970s when the PDO was in its negative phase, implying that changes in the TWC volume transport might be affected by internal climate variability (Senjyu et al., 2010). Due to the shallow sill depth of the Tsushima Strait, the TWC extends horizontally in the southern Japan Sea. Therefore, the Japan Meteorological Agency (JMA) presumes that changes in the TWC volume transport can be inferred from a horizontal extent of the warm water mass in the southern Japan Sea. The JMA defines the area where SST > 10 °C at 100 m water depth as the Tsushima Current Area, which can be regarded as an indicator of the TWC volume transport. The changes in the TWC volume transport correlate highly with spring SST anomalies in the central Japan Sea (R = 0.69), but not with the summer SST anomalies (R = 0.17) (Fig. 2). The annual mean and winter SST anomalies also showed significant correlations with the Tsushima Current Area (not shown, R = 0.68 and 0.69, respectively). These data suggest that changes in the TWC volume transport in the

Neogloboquadrina incompta (N. incompta) is an asymbiotic species that dwells in subpolar, temperate, and transitional water masses of the North Atlantic, Southern Ocean, northeastern North Pacific, and northwestern North Pacific, including the Japan Sea (Bolton and Marr, 2013; Field, 2004; Iwasaki et al., 2017; Kuroyanagi and Kawahata, 2004; Sagawa et al., 2014). Darling et al. (2006) proposed adaptation of the widely recognized name of Neogloboquadrina incompta for the rightcoiling Neogloboquadrina pachyderma, and although there are a few exceptions due to genetic mutation of the coiling direction, we chose to adopt this proposal herein. The depth habitat of N. incompta is strongly dependent on maximum chlorophyll a concentrations in the water column (Kuroyanagi and Kawahata, 2004; Oda and Yamasaki, 2005). Furthermore, this species prefers shallow and warmer (> 8 °C) surface waters compared to N. pachyderma (sin.), which is shown by the evidence that N. incompta represents lighter δ18Oc than N. pachyderma (sin.) (Kim et al., 2000; Schiebel et al., 2001; Takei et al., 2002). According to the plankton tow study in the subarctic North Pacific, peaks in the vertical distributions of N. incompta have been observed at depths of 0–50 m, and the average temperature for the water where the peaks in standing stocks were seen was 13.1 ± 1.6 °C (Iwasaki et al., 2017). In the southern Japan Sea, numerous eddies mix the TWC and cold Japan Sea subsurface water, forming a transitional water mass. In the transitional water mass, N. incompta accounts for 50–80% of the total planktonic foraminiferal abundance (Domitsu and Oda, 2005; Kuroyanagi and Kawahata, 2004). Analyses of sediment cores in the southern Japan Sea show that N. incompta has been the dominant planktonic species since ~8000–7000 cal. year BP, which is interpreted as the result of the inflow of the TWC and the formation of a transitional water mass in response to the full opening of the Tsushima Strait (Domitsu and Oda, 2008). 3. Materials and methods 3.1. Core-top sediments in the southern Japan Sea To develop an N. incompta Mg/Ca-temperature calibration, we used thirteen core-top sediments, obtained by a multiple corer, a pilot corer, and a grab sampler, from the southern Japan Sea (Fig. 1a). Given the relatively shallow saturation horizon of calcite in the Japan Sea (1500–1700 m) (Park et al., 2006), we collected core-top samples at water depths ranging from 220 m to 1500 m under the nearshore and second branches of the TWC (Fig. 1a; Table 1). All sediment cores contain well preserved oxic surface layers at the top surface, suggesting that the seafloor sediments were completely recovered. All sediment cores included abundant N. incompta for measurements. Although we do not measure 14C dates for each core-top sediment, the existence of N. incompta indicates the dates of sediment deposition might be within the Holocene (< 8000 years ago). Shallow marginal areas near the Japanese islands are marked by high sedimentation rates (> 10 cm/kyr) due to high riverine input during the late Holocene (Domitsu and Oda, 2006; Domitsu and Oda, 2008; Koizumi, 2008). Based on the shallower depths of these core sites and the preservation of the oxic surface layers, we assume that the core-top sediments are from the late Holocene. The N. incompta from the core-top sediments can be paired with modern hydrographic data to develop the Mg/Ca-temperature calibration. If foraminifera tests grew during the warmer or colder periods during the late Holocene, we would expect the Mg/Ca ratios to be mirrored in the δ18Oc that are used to determine calcification temperatures. Using the paired geochemical approach, the warmer or colder periods are embedded similarly in Mg/Ca and δ18Oc temperature 3

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

Fig. 2. Correlation between Tsushima Current Area and the SST anomaly in spring (left) and in summer (right). The Tsushima Current Area is defined by the area that has SST > 10 °C at 100 m water depth. The SST anomaly was calculated as the deviation from the averaged SST in the central Japan Sea between 1981 and 2010. Tsushima Current Area and SST anomaly data are from the JMA (http://www. jma.go.jp/jma/indexe.html).

(Koizumi, 2008). However, the sedimentation rate for the upper part of the piston core seems to be unusually lower than that of core C-GC-8 and the sedimentation rates of the middle–lower parts of core PC09 (18.6–77.8 cm/kyr) (Fig. 3a). Furthermore, the downcore δ18Oc and Mg/Ca values of N. incompta between the pilot and the piston cores did not match within the overlapped time period, and L* data from the pilot and piston cores also did not match (Fig. 3b, c, d). Since core images, visual core descriptions, and L* data do not show severe coring disturbance in the upper part of the piston core, we interpreted this to mean that the 14C age for the topmost piston core sediments is unreliable, due to contamination of the younger 14C record. In summary, we excluded the 14C date (1030 ± 35 14C year BP) at the 15.5-cm core depth from the topmost piston core, and applied the sedimentation rate of 16.4 cm/kyr, estimated from the pilot core, to the upper part of the piston core. Consequently, the sedimentation rates for core PC09 resulted in the range from 16.4 to 77.8 cm/kyr for the past ~7000 years (Fig. 3a). According to this age model, the first continuous occurrence of N. incompta was estimated to take place at 6800 cal. year BP. In the eastern and southern areas of the Japan Sea, the first continuous occurrence of N. incompta is considered to take place from 6800 to 8300 cal. year BP (Domitsu and Oda, 2008; Takei et al., 2002), demonstrating that our age model is reliable.

proxies (Morley et al., 2017).

3.2. Piston core YK10-7-PC09 Piston-core (762.5 cm long) and pilot-core (31.5 cm long) sediments were obtained at Site PC09 (38° 36.89′ N, 138° 56.34′ E, 738 m water depth) from the foot-of-slope in the southern Mogami Trough off central Japan during the YK10-07 cruise of R/V Yokosuka (the cruise report can be found in http://www.godac.jamstec.go.jp/darwin/cruise/ yokosuka/yk10-07/e) (Fig. 1a). This site is under the influence of the nearshore branch of the TWC. The pilot core preserved the oxic surface sediment, but the piston core did not contain the sediment (Fig. 3b). The lack of the seafloor sediments in the piston core can be compensated for by using the pilot core sediments. Although piston core PC09 recovered sediments from the LGM to the present, this study only focused on the Holocene section of the upper part of the core (0–170 cm core depth), which contained N. incompta. This Holocene section was mainly composed of olive-black bioturbated clayey silt, without any significant disturbance. For this Holocene section, we have measured the 14C ages of mixed planktonic foraminifera at eight stratigraphic horizons (one from the pilot core and seven from the piston core) to construct a combined-age model for piston and pilot cores at YK10-7-PC09 (Fig. 3a; Table 2). Our 14C age control points in the Holocene section are marked by the largest number among previous studies, which will allow us to further determine the timing of SST changes (Domitsu and Oda, 2006; Domitsu and Oda, 2008; Koizumi, 2008; Takei et al., 2002). We used Neogloboquadrina incompta, Neogloboquadrina dutertrei, and Globigerinoides ruber for 14C dates, which were picked up from the > 180-μm-size fraction. The foraminifera shells were roughly crushed to open all chambers and ultrasonicated with ultrapure water (18 MΩ·cm) and methanol to remove adherent clay particles (super special grade, Wako Pure Chemical Industries, Ltd.). After confirming that all dirt had been removed, the shell fragments were washed with ultrapure water three times and dried in an oven at 40 °C. The 14C ages were measured by accelerator mass spectrometry (AMS) at the National Ocean Sciences AMS facility (NOSAMS) at Woods Hole Oceanographic Institution (Table 2). Conventional 14C ages were converted to calendar ages using the CALIB 7.1.0 program and Marine13 (Reimer et al., 2013; Stuiver et al., 2017). For this calculation, we used 60 ± 29 years as the local reservoir age (ΔR) that was reported in the Japan Sea (Kuzmin et al., 2001; Yoneda et al., 2007). Although we did not find a 14C age reversal among the measured 14 C data, we required a consideration for making an association between the pilot and piston cores. The 14C date at the bottom (29.6 cm) of pilot core was 2270 ± 50 14C year BP, while the 14C date at a piston core depth of 15.5 cm was 1030 ± 35 14C year BP (Table 2). If we apply these two dates to making an association between the pilot and piston cores, we find a large difference in the sedimentation rates for the pilot and the upper part of the piston cores (16.4 cm/kyr and 4.7 cm/kyr, respectively) (Fig. 3a). The sedimentation rate for the pilot core was comparable with that of nearby core C-GC-8 (21 cm/kyr)

3.3. Analyses of δ18Oc and metal/Ca ratio For core PC09, we subsampled 1-cm-thick sediments throughout a core depth of 0–170 cm, whereas for the core-top samples, we subsampled top centimeter sediments of multiple cores, pilot cores, or grab sediments (Table 1). These sediments were wet-sieved, with a mesh size of 63-μm, and the residues were then dried in an oven at 50 °C. Approximately 30 to 50 specimens of well-preserved N. incompta were handpicked from the 180–250-μm size fraction from each sample for measurements of the oxygen isotopic composition (δ18Oc) and metal/Ca ratio of calcite. > 20 specimens were used for the metal/Ca measurement, and the remains were used for the δ18Oc measurement. Foraminifera samples were gently crushed and sonicated with ultrapure water and methanol three times (super special grade, Wako Pure Chemical Industries, Ltd.), to remove adherent clay particles. The foraminifera samples for metal/Ca measurements were further cleaned according to a reductive cleaning procedure (Boyle and Keigwin, 1985; Rosenthal et al., 1997). Briefly, the samples were treated with hot reducing (hydrazine/ammonium citrate) and oxidizing (hydrogen peroxide buffered by sodium hydroxide) solutions, transferred into new acid-leached 1.5-mL centrifuge tubes, and finally leached with a dilute ultrapure nitric acid solution (0.001-M HNO3, TAMAPURE-AA-100 from Tama Chemicals Co., Ltd.). Cleaned samples were dissolved with 2% ultrapure nitric acid, which included scandium as an internal standard, and diluted to obtain a calcium concentration of 10 ± 1 μg·g−1 to reduce the matrix effect on metal/Ca ratios (de Villiers et al., 2002). The metal/Ca ratios were determined with a Thermo Scientific ELEMENT 2 sector field inductively coupled plasma mass spectrometer (ICP-MS) at the University of Toyama (Horikawa 4

Global and Planetary Change 183 (2019) 103028

Pilot core Pilot core Multiple core Pilot core Multiple core Push core (ROV HyperDolphin) Grab core Grab core Multiple core Grab core Grab core Grab core Grab core 11.7 10.8 10.6 13.1 11.9 13.4

12.3 12.8 12.1 11.3 10.8 12.4 11.3

Type of core Apparent calcification temperature (°C)

36 25 98 103 119 110 98

4.1. Core-top δ18Oc and Mg/Ca values for N. incompta

0.03

0.04

0.02

±

±

0.75 0.78 0.74 0.64 0.70 0.76 0.72

±

4 1 2 1 1 1 2

Core-top δ18Oc values for N. incompta ranged from 0.65 to 1.37‰ (Table 1), which were within the range of δ18Oc values of N. incompta and reported as N. pachyderma (dex.) at southern Japan Sea sites (Domitsu and Oda, 2006; Kim et al., 2000; Oba et al., 1995; Takei et al., 2002; Yokoyama et al., 2007). The highest value was observed at Site H-1, and the lowest value were observed at Sites HPD1559 and PC01. In general, the southwestern sites (132, Oki-2, 308, 47, and 118) and offshore sites (PC09, PC05, H-1, and J-1) presented heavier values (> 1.0‰), compared with the nearshore sites (HPD1559, PC01, b6, and d6) (Fig. 1a; Table 1). The core-top Mg/Ca ratios for N. incompta showed a narrow range from 0.64 to 0.78 mmol·mol−1. The highest value was observed at Site HPD1559, and the lowest value was observed at Site 118. In general, the sites near the coast of Japan exhibited relatively higher Mg/Ca ratios, with lower δ18Oc values, and vice versa at the offshore sites, such as Sites PC05, H-1, 118, and 132. The Mg/Ca ratios showed a good correlation with δ18Oc values (Mg/Ca = −0.14 × δ18Oc + 0.86, r2 = 0.54, p = .004), suggesting that Mg/Ca ratios for N. incompta are potentially useful as a thermometry method in the southern Japan Sea. However, it is noteworthy that the Mg/Ca ratios in the southern Japan Sea were significantly lower than those of N. incompta, reported in the Sothern Ocean, Atlantic Ocean, and northeast Pacific (0.8–2.1 mmol·mol−1) (Bolton and Marr, 2013; Friedrich et al., 2012; Martinez-Boti et al., 2011; Morley et al., 2017). This issue will be discussed in a later section (Section 5.2.2).

0–3 0–3 0–1 0–3 0–3 0–3 0–3 1.4 −0.1 −6.5 5.3 48.9 17.4 14.2 450 580 1157 406 223 303 330

0.89 0.77 1.07 1.22 1.37 1.00 1.24

31 47 45 13 48 18 2 3 1 1 1 1 0.01 0.04 ± ± 0.67 0.66 0.66 0.72 0.72 0.78 2–3 0–3 8–10 4–8 5–6 0–4 −1.8 −1.3 −10.6 0.4 −4.9 −5.9

4.2. Holocene δ18Oc and Mg/Ca records for N. incompta Over the past 6800 years, we measured N. incompta δ18Oc (n = 148) and Mg/Ca ratios (n = 123) from the pilot (ca. 30 cm core depth) and piston cores (0–170 cm core depth). One-centimeter-thick subsamples and high temporal resolution analysis allow us to identify detailed oceanographic responses on a multi-centennial timescale. The downcore variations in δ18Oc and Mg/Ca ratios for N. incompta are shown in Fig. 3 (Table 3). The δ18Oc data exhibited high variability from 0.6 to 1.6‰, with an average of 1.03‰ (Fig. 3c), while the Mg/Ca ratios varied from 0.6 to 0.9 mmol·mol−1 with an average of 0.74 mmol·mol−1 (Fig. 3d). Fig. 4 shows the temporal changes in δ18Oc and Mg/Ca values with the age model. The δ18Oc variability represents the close consistency with the low-resolution δ18Oc record from Site L3 on Oki Ridge (Oba et al., 1995) (Fig. 4a). We also showed the 250-year running mean for

36°49.80′ 36°49.89′ 36°39.33′ 37°16.70′ 36°33.97′ 35°57.55′ 36°13.15′ NN337-b6 NN382-d6 NN371-Oki-2 GH88–118 GH86–2-132 GH87–2-308 GH87–2-47

137°09.60′ 137°33.52′ 133°52.30′ 136°09.57′ 133°18.07′ 134°26.90′ 135°01.65′

38°36.89′ 38°12.59′ 38°07.69′ 37°41.50′ 37°34.00′ 37°26.63′ YK-10-7-PC09 YK-10-7-PC05 NN371-H-1 YK-10-7-PC01 NN371-J-1 NT-13-17-HPD1559

138°56.34′ 136°55.45′ 137°26.36′ 138°29.93′ 137°57.70′ 137°47.70′

738 690 1515 536 1010 1103

1.09 1.33 1.37 0.65 1.04 0.65

Apparent calcification depth (m) N Mg/Ca (mmol/mol) δ18Oc (‰ VPDB) Core depth (cm) [ΔCO32−] (μmol/ kg) Water Depth (m) Latitude (N)

Longitude (E)

et al., 2015). We measured 24Mg, 26Mg, 43Ca, 44Ca, and 88Sr, and 55Mn was measured to monitor contamination by clay minerals and diagenetic coatings. Element counts were converted into molar ratios by the intensity ratio method based on a series of matrix-matched standard solutions. The accuracy and precision of the Mg/Ca ratio were confirmed by measurements of carbonate reference material BAM RS3. BAM RS3 was analyzed for every five unknown samples, and the average of these standard runs was compared to the recommended value to determine a correction factor for each of the samples analyzed on that day. The repeated measurements in the study period gave an averaged Mg/Ca ratio of 0.786 ± 0.009 mmol·mol−1 (1σ, n = 140), which was within the reported value (0.791 ± 0.03) (Greaves et al., 2008). Samples that show high Mn/Ca ratios (> 80 μmol·mol−1) were rejected in this study, due to the presence of diagenetic coatings. δ18Oc values were measured using a Finnigan MAT 253 mass spectrometer at the Center for Advanced Marine Core Research, Kochi University. Measured isotope ratios were calibrated with an NBS-19 standard, and expressed as ‰ VPDB. The standard deviation of these measurements was better than ± 0.07‰ (1σ) for δ18Oc. 4. Results

Site ID

Table 1 Details of the surface sediment samples, the Mg/Ca ratios, and the δ18Oc values from Neogloboquadrina incompta. Errors were obtained by repeated analyses of different solution samples (1σ).

K. Horikawa, et al.

5

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

Fig. 3. (a) An age model for core YK10-7-PC09. Open squares present the age control points by AMS 14C dates (Table 2). A gray square presents the rejected data from the age model. The sedimentation rate was calculated by the linear sedimentation rates between the age control points. (b) Reflectance L* data from the pilot and piston cores. (c and d) Depth profiles of δ18Oc value and Mg/Ca ratio for N. incompta from pilot and piston cores. Analytical errors of δ18Oc and Mg/Ca measurements are shown by error bars (1σ).

(Fig. 4a). Furthermore, the period from 6800 to ~3700 cal. year BP was marked by highly variable, heavier δ18Oc values. The Mg/Ca ratios also exhibited high variability from 6800 to 3000 cal. year BP and exhibited a long-term slightly decreasing trend over the last 6800 years (Fig. 4c). Unlike the core-top data set, the downcore Mg/Ca ratios did not show a linear correlation with δ18Oc values (r2 < 0.01) for the past 6800 years, suggesting that the relative proportions of temperature and seawater δ18O in the δ18Oc changed during the past 6800 years (Fig. 4).

Table 2 The AMS 14C dates from core YK10–7-PC09 and the calibrated calendar ages. The local reservoir age of ΔR = 60 ± 29 year was applied. Core

Depth (cm)

14 C age (yr B.P.)

Pilot Piston Piston Piston Piston Piston Piston Piston

29.6 15.5 30.0 48.5 63.5 101.5 142.5 193

2270 1030 3810 4010 4610 5440 5920 6730

a

±1 σ

Calendar age (cal. yr B.P.)

+1 σ

−1 σ

Lab code

50 35 50 30 50 55 35 40

1808 566a 3682 3941 4747 5751 6278 7203

79 41 85 76 68 74 61 50

67 41 82 57 85 89 40 49

OS-91844 OS-91847 OS-100417 OS-100418 OS-91852 OS-100419 OS-92353 OS-92354

5. Discussion 5.1. Apparent calcification depth and calcification temperature for N. incompta

The data was not used to construct the age model.

To develop an Mg/Ca-temperature calibration for N. incompta, we first calculated calcification temperatures using data from thirteen core tops. Shell compositions, such as δ18Oc and Mg/Ca ratios, of planktonic foraminifera records calcification temperatures at the average calcification depth during their ontogeny (Anand et al., 2003; Regenberg et al., 2009). The apparent calcification depth can be assumed by the depth in which the measured foraminifera δ18Oc value matched the

both δ Oc and Mg/Ca records to filter the decadal-scale variability and to emphasize the multi-centennial to millennial-scale fluctuations. The millennial-scale fluctuations demonstrated that there are pronounced heavier δ18Oc periods (> 1.2‰) at ~4200 cal. year BP and at ~400 cal. year BP, and the lighter δ18Oc periods (< 0.8‰) at ~2600 cal. year BP 18

6

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

Table 3 (continued)

Table 3 Down-core profile of δ18Oc and Mg/Ca ratios of N. incompta and the calculated δ18Osw from core YK10–7-PC09. The SSTs for the last 6.8 kyrs were calculated by using Eq. (3) in the text. Mid Depth (cm)

Age (cal. kyr B.P.)

δ18Oc (‰ VPDB)

Mg/Ca (mmol/ mol)

Mg/Caderived SST (°C)

δ18OSW (‰ VPDB)

Pilot core 2.5 5.5 6 6.5 7.5 8.5 9.5 10.5 11.5 12.5 13.5 14.5 15.5 16.5 17.5 18.5 19.5 20.5 21.5 22.5 23.5 24.5 25.5 26.5 27.5 29.6

0.15 0.34 0.37 0.4 0.46 0.52 0.58 0.64 0.7 0.76 0.83 0.89 0.95 1.01 1.07 1.13 1.19 1.25 1.31 1.38 1.44 1.5 1.56 1.62 1.68 1.81

1.09

0.67 0.77

11 12.9

−0.29

0.71 0.73 0.75 0.81 0.65 0.83 0.73 0.71 0.76 0.66 0.73 0.7 0.65 0.72 0.57 0.69 0.72 0.65 0.65 0.66 0.73 0.74 0.72

11.7 12.3 12.6 13.7 10.4 14 12.2 11.9 12.8 10.8 12.2 11.5 10.5 11.9 8.7 11.4 12.1 10.5 10.5 10.7 12.3 12.3 11.9

Piston core 1 2.5 3 4.5 5.5 6.5 7.5 8 8.5 9.5 10 10.5 11.5 12 12.5 13.5 15.5 17.5 18.5 19.5 20.5 21.5 22.5 23.5 24.5 25.5 26.5 27.5 28.5 30 31.5 32.5 33.5 34.5 35.5 36.5 37.5 38.5 39.5 40.5 41.5

1.91 2 2.03 2.12 2.19 2.25 2.31 2.34 2.37 2.43 2.46 2.49 2.55 2.58 2.61 2.67 2.8 2.92 2.98 3.04 3.1 3.16 3.22 3.28 3.34 3.41 3.47 3.53 3.59 3.68 3.7 3.72 3.73 3.74 3.76 3.77 3.79 3.8 3.81 3.83 3.84

0.96

0.74 0.71 0.74 0.77 0.81 0.77 0.8 0.86

12.4 11.8 12.4 12.9 13.6 12.9 13.5 14.5

0.78 0.79 0.82

13.1 13.4 13.8

0.79 0.88 0.71 0.72 0.69 0.82 0.76 0.68 0.73 0.61 0.76 0.68 0.83 0.72 0.8 0.74 0.76 0.63 0.67 0.68 0.8 0.67 0.62 0.76 0.87 0.78 0.77 0.74

13.3 14.8 11.8 12 11.3 13.9 12.8 11.1 12.3 9.6 12.7 11.2 14 12 13.5 12.3 12.8 10 10.9 11.2 13.4 10.9 9.9 12.9 14.6 13.2 13 12.4

1.34 1.26 1.14 1.1 1.15 1.17 0.97 1.08 1.07 1.02 1.13 0.86 1.04 0.93 0.85 1.19 1.01 1.13 1.02 1.11 1.13 1.14 0.96

1.13 0.76 1.03 0.76 1.1

0.18 0.12 0.35 −0.37 0.5 −0.13 −0.10 0.11 −0.43 0.02 −0.41 −0.48 −0.24 −1.10 −0.10 −0.12 −0.38 −0.48 −0.35 0.05 0.06 −0.21 −0.11 0.07 −0.17 0.26 −0.16 0.32

0.88

1.23 0.68 0.66 0.91 0.94 1.08 0.97 0.74 1.12 1.01 0.91 1.04 0.95 1 0.89 0.9 0.86 0.96 0.87 1.1 1.11 1.17 0.93 1.04 0.93 0.92 1.13 1.22

0.51

0.18 −0.27 −0.38 0.38 0 −0.62 0.04 −0.72 −0.07 −0.30 0.28 −0.14 0.11 −0.18 −0.10 −0.68 −0.54 −0.23 0.3 −0.24 −0.72 0.09 0.41 0.05 0.21 0.17

Mid Depth (cm)

Age (cal. kyr B.P.)

δ18Oc (‰ VPDB)

Mg/Ca (mmol/ mol)

Mg/Caderived SST (°C)

δ18OSW (‰ VPDB)

42.5 43.5 44.5 45.5 46.5 48.5 48.8 50.5 51.5 52.5 53.5 54.5 55.5 56.5 57.5 58.5 59.5 60.5 61.5 62.5 66.5 67.5 68.5 69.5 70.5 71.5 72.5 73.5 74.5 75.5 76.5 77.5 78.5 79.5 80.5 81.5 82.5 83.5 84.5 85.5 86.5 87.5 88.5 89.5 90.5 91.5 92.5 93.5 94 94.5 95.5 96 96.5 97.5 98.5 99.5 101.5 103.5 105 106.5 107.5 108.5 110.5 113.5 116 119.5 122 123.5 124 126 128 129.5 131.5

3.86 3.87 3.88 3.9 3.91 3.94 3.96 4.05 4.1 4.16 4.21 4.26 4.32 4.37 4.43 4.48 4.53 4.59 4.64 4.7 4.83 4.86 4.88 4.91 4.93 4.96 4.99 5.01 5.04 5.07 5.09 5.12 5.14 5.17 5.2 5.22 5.25 5.28 5.3 5.33 5.36 5.38 5.41 5.43 5.46 5.49 5.51 5.54 5.55 5.57 5.59 5.61 5.62 5.64 5.67 5.7 5.75 5.78 5.8 5.81 5.83 5.84 5.87 5.91 5.94 5.98 6.02 6.03 6.04 6.07 6.09 6.11 6.14

1.34 1.24 0.88 1.18 1.08 0.86

0.67 0.75 0.81 0.73 0.82

11 12.6 13.7 12.3 13.9

−0.04 0.25 0.13 0.09 0.38

0.73 0.84 0.71 0.73 0.75 0.76 0.66 0.66 0.64

12.3 14.3 11.8 12.1 12.5 12.7 10.7 10.8 10.3

0.29 −0.17 0.01 0.57 0.22 −0.37 −0.38 −0.59

0.75 0.68 0.77 0.83 0.83 0.74 0.69 0.77 0.83 0.74 0.75 0.74 0.69 0.77 0.7 0.79 0.76 0.78 0.86 0.7 0.66 0.79 0.78 0.72 0.77 0.86 0.76 0.77 0.72 0.74 0.68 0.68

12.6 11.2 13 14.1 14 12.3 11.4 12.9 14 12.4 12.6 12.3 11.4 12.9 11.6 13.3 12.7 13.2 14.5 11.5 10.8 13.4 13.1 11.9 12.9 14.5 12.8 12.9 12 12.5 11.1 11.1

0.85 0.88

14.4 14.9

0.77 0.83 0.68 0.76 0.72

13 14 11.3 12.8 12

0.2 −0.36 0.35 −0.28

0.62 0.76 0.74

9.8 12.9 12.4

−0.52 0.48 0.17

0.72 0.69

12 11.3

−0.03 −0.46

0.82 0.88

13.9 14.8

−0.71 0.44

0.9 1.02 1.13 1.6 1.2 1.1 1.07 0.98 1.13 1.51 1.04 0.96 1.11 0.97 1.34 0.87 1.02 0.98 1.12 1.09 0.99 1.04 1.29 1.27 0.99 1.11 1.07 1.15 1.08 0.99 1.05 0.95 1.11 1.04 0.91 1 1.06 0.93 1.43 1.34

0.5 −0.30 0.05 0.45 0.3 0.27 −0.43 0.1 0.3 0.06 0.09 −0.08 −0.26 0.36 0.02 0.15 0.12 0.21 0.59 −0.19 −0.45 0.23 0.07 −0.05 0.11 0.35 0.05 0.12 −0.21 0.39 −0.02

0.75

0.63 0.88 0.96 1.31 0.86 1.1 1.11 1.16 1.43 1.21 1.16 0.84 1.12 0.86 0.77 0.92 1.07 1.04 1.06 1.19

(continued on next page) 7

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

spatial difference in the apparent calcification depths at the northern and southern areas is also documented from the plankton-tow study conducted in the southern Japan Sea in early June, in which the habitat depth of N. incompta ranged from 0 to 200 m, with the maximum at 40–60 m in the northeastern areas (St. 6 and St. C in Kuroyanagi and Kawahata (2004)) and a maximum at 120–160 m, or a secondary distribution peak at 120–200 m, in the southwestern areas (St. D and St. 7, respectively, in Kuroyanagi and Kawahata (2004)). The integrated evaluation of the δ18Oc-based apparent calcification depth for N. incompta, the habitat of N. incompta, and oceanographic conditions in the southern Japan Sea suggest that the dominant habitat season for N. incompta might be spring, and the northern sites are marked by shallower apparent calcification depth, while the southwestern sites are deeper. Based on these considerations, at each core site, statistical spring temperatures at the estimated apparent calcification depths were extracted as the apparent calcification temperature (Tc) (Table 1).

Table 3 (continued) Mid Depth (cm)

Age (cal. kyr B.P.)

δ Oc (‰ VPDB)

134 137.5 138.5 139.5 141 145.5 147.5 148.5 149.5 150.5 151.5 152.5 153.5 155 156.5 157.5 160.5 163.5 164.5 165.5 167.5 168.5 169.5

6.17 6.22 6.23 6.24 6.26 6.33 6.37 6.39 6.41 6.43 6.44 6.46 6.48 6.51 6.54 6.55 6.61 6.66 6.68 6.7 6.74 6.75 6.77

0.91 1.01 1.01 1.21 1.05 1.32 1.01 0.92 0.84

18

1.04 0.98 0.98 0.81 0.98 0.94 1.22 0.89 0.63 0.86 0.91 1.14 0.79

Mg/Ca (mmol/ mol)

Mg/Caderived SST (°C)

δ OSW (‰ VPDB)

0.82

13.9

0.52

0.66

10.7

−0.14

0.74 0.75 0.84 0.86 0.77

12.3 12.5 14.3 14.5 12.9

−0.15 −0.19

0.84

14.2

0.35

18

0.49 0.05

5.2. N. incompta Mg/Ca paleothermometry

0.78

13.1

5.2.1. Mg/Ca-temperature calibration equation for N. incompta In general, when we plot the planktonic foraminiferal Mg/Ca ratio and calcification temperature, Mg/Ca ratio increases with exponentially with calcification temperature, which can be expressed by.

0.25

Mg / Ca = b × exp (a × T ), where exponential constant a is a temperature-sensitive component, and y-axis intercept b (pre-exponential constant) varies with species, due to the species-specific differences in Mg2+ incorporation. Most of the previous studies show that the temperature-sensitive component ranges from 0.07 to 0.11 (Anand et al., 2003; Cléroux et al., 2008; Mashiotta et al., 1999). Given that both the measured Mg/Ca and the estimate of the calcification temperature have uncertainty, a geometric mean regression should be used to construct the temperature calibration. Using a geometric mean regression, we derived the following temperature calibration for N. incompta in the southern Japan Sea (Fig. 7):

expected δ18Oc value of foraminifera formed in equilibrium with seawater (hereafter, δ18Oequilibrium). The δ18Oequilibrium profiles of foraminifera were calculated by the δ18Oc-temperature equation (Eq. (1)) (Shackleton, 1974) and the δ18O seawater (δ18Osw)-salinity relationship (Eq. (2)), the latter of which was constructed by the surface water (0–100 m water depth) in the southern Japan Sea (Kodaira et al., 2016):

T = 16.9 − 4.38[δ18Oc − δ18Osw ] + 0.1[δ18Oc − δ18Osw ]2

(1)

δ18Osw = −9.1 + 0.27 × salinity

(2)

We used statistical seasonal salinity and temperature (JODC, Japan Oceanographic Data Center; http://www.jodc.go.jp/) from the station closest to each core site. Furthermore, δ18Osw on the V-SMOW scale was corrected to the PDB scale by subtracting 0.27‰. We calculated the δ18Oequilibrium values in the water column from the surface to 120 m for spring, summer, autumn, and winter seasons at all core sites (Fig. 5). We assumed that N. incompta in the southern Japan Sea calcifies in isotopic equilibrium with seawater, which is supported by the North Atlantic observations (Keigwin and Pilskaln, 2015) in which the δ18Octemperature equation of Shackleton (1974) was used. In addition to the Shackleton (1974) equation, we also assessed two other commonly used δ18Oc-temperature equations for inorganic calcite (Kim and O'Neil, 1997) and N. incompta via culturing experiments (von Langen, 2001) (Fig. 5a). However, these equations can produce deeper calcification depths (> 100 m) at more than half of the sites, which seems to conflict with the habitat depth of shallow-dwelling N. incompta (< 100 m) documented in previous studies (Iwasaki et al., 2017; Kuroyanagi and Kawahata, 2004). Thus, this study applied the Shackleton (1974) equation. According to sediment trap studies in the North Pacific, N. incompta blooms twice a year during spring and late autumn–early winter (Kuroyanagi et al., 2002; Sagawa et al., 2013). The chlorophyll a concentration reaches the highest value at the top 40 m of the water column in May in the southern Japan Sea (Fig. 6). The measured foraminifera δ18Oc values matched the δ18Oequilibrium at shallower depths (20–50 m) in spring (April–June) and deeper depths (> 90 m) in summer (July–September) and winter (October–December) for the northeastern sites (Fig. 5b, c, f, g). In contrast, the apparent calcification depths at the southwestern sites (118, 132, 47, 308, and Oki-2) were estimated to be deeper (> 90 m) in all seasons (Fig. 5d, e). The

Mg / Ca = 0.311 × exp (0.07 × Tc ) (r = 0.80)

(3)

The pre-exponential and exponential constants have uncertainties (1 SE) of b ± 0.04 and a ± 0.012, respectively, and the standard error for the temperature estimate in this regression is 0.6 °C. The temperature-sensitive component in our calibration is the within the range (0.07 to 0.11) of most literature estimates. However, our temperature calibration represented lower pre-exponential and exponential constant values, compared with the recently constructed N. incompta Mg/Ca-temperature calibration that consists of the North Atlantic data and culturing experiment data (Mg/Ca = 0.40 × exp (0.09 × Tc)) (Morley et al., 2017) (Fig. 7). Although there is a significant difference between the Japan Sea and the compiled calibration from culturing and the North Atlantic data, the fact that our Mg/Ca ratios were well correlated with calcification temperatures suggests that the uptake of Mg into the calcite lattice of foraminifera tests should be primarily influenced by thermal environmental controls. We reason that the lower Mg/Ca ratios of N. incompta do not affect SST reconstruction in the southern Japan Sea, however in the following Section 5.2.2, we considered potential causes for the reduced Mg/Ca values in the southern Japan Sea. 5.2.2. Potential causes for lower Mg/Ca ratios of N. incompta in the Japan Sea We considered the following four potential factors that can cause the distinctly lower Mg/Ca ratios in the southern Japan Sea: cleaning method, dissolution effect, salinity effect, and encrustation. First, a cleaning protocol for the foraminifera Mg/Ca measurement includes a multistep process, which includes treatments with hot reducing (hydrazine/ammonium citrate) and then oxidizing (hydrogen 8

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

Fig. 4. Temporal changes in (a) δ18Oc, (b) δ18Osw, and (c) Mg/Ca ratios of N. incompta from pilot and piston cores at Site YK10-7-PC09. The 250-year running mean of both records is also represented as thick lines. The δ18Oc record at Site L3 (Oba et al., 1995) is also shown in the top panel as circles. (d) The red horizontal bars represent the periods in which the warm molluscan assemblages increased off Hokkaido at the northern end of the TWC (Matsushima, 2010). (e) Mg/Caderived SST from core YK10-7-PC09, diatom- and alkenonederived SST records from C-GC-8 (Koizumi, 2008), and MR0604-PC03B (Bae et al., 2014), respectively. The thick line in Mg/Ca-derived SST indicates the 250-year running mean. (f) Spring (May) daily insolation at 35°N for the last 8000 years (Laskar et al., 2004). Age control points ( ± 1σ) for core YK10–7-PC09 are also shown at the top of the panel. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

calcite, which was located at depths of 1500–1700 m in the preindustrial era and shoaled up to ~1000 m in 1999 due to the ongoing accumulation of anthropogenic CO2 in the Japan Sea (Park et al., 2006). Thus, our foraminifera samples, obtained from water depths of 220 m to 1500 m, need to be evaluated for the dissolution impact on Mg/Ca ratios (i.e. dissolution causes reduced Mg/Ca ratios). To identify the dissolution effect on Mg/Ca ratios in the southern Japan Sea, we calculated the water column calcite saturation state Δ[CO32−] (Δ[CO32−] = [CO32−]in situ – [CO32−]saturation). The carbonate ion concentration [CO32−] at saturation is calculated by Jansen et al. (2002). The in situ [CO32−] in the water column was computed by using the program CO2Sys.xls (Pierrot et al., 2006), with K1 and K2 refitted by Dickson and Millero (1987) and KHSO4 after Dickson (1990). For the Δ[CO32−] calculation, we used total alkalinity, TCO2, and hydrographic water column data from the southern Japan Sea, obtained by the survey in 2011 (Japan Meteorological Agency, http:// www.jma.go.jp/jma/indexe.html). Although Δ[CO32−] in 2011 may

peroxide buffered by sodium hydroxide) solutions to remove contaminants associated with FeeMn oxides on the shells and organic matters, respectively. A cleaning method called as “Mg cleaning” omits the reduction step. When Mg/Ca is the main interest, the simplified “Mg cleaning” method is often used because Mg is not much included in the FeeMn oxide (Barker et al., 2003). Importantly, the cleaning method with the reduction step causes etching of foraminifera calcite, thereby resulting in lower Mg/Ca values by up to 15% compared with those of the “Mg cleaning” method (Barker et al., 2003; Johnstone et al., 2016). Thus, there is a potential offset for Mg/Ca ratios if different cleaning methods were used. In this study, we derived our Mg/Ca data from the reductive and oxidative cleaning steps. Like our data, most of the Mg/ Ca data in the calibration equation of Morley et al. (2017) were also conducted by the reductive and oxidative cleaning steps. Therefore, the lower Mg/Ca values documented in southern Japan are not related to the cleaning methodology. Second, the Japan Sea is marked by a shallow saturation horizon of 9

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

Fig. 5. (a) Differences in the δ18Oc-temperature relationships of Shackleton (1974), Kim and O'Neil (1997), and von Langen (2001). This study used the equation of Shackleton (1974) to calculate δ18Oequilibrium (δ18Oe). (b–g) Comparison of the measured N. incompta δ18Oc values with calculated δ18Oe values (spring, summer, autumn, and winter) at some representative sites. Measured core-top δ18Oc values are presented by gray dotted lines. The δ18Oe was calculated from the statistically averaged temperature and salinity data, integrated for 1906 to 2003 in a 1° × 1° grid (latitude × longitude) (JODC). See more details in Sec. 5.1.

Third, previous studies have suggested that salinity might influence the foraminifera Mg/Ca ratios (Hönisch et al., 2013; Kısakürek et al., 2008; Martinez-Boti et al., 2011). Indeed, Martinez-Boti et al. (2011) investigated the plankton tow samples collected from the north and southeast Atlantic, the northeast Pacific, and the Norwegian Sea, and found that N. incompta Mg/Ca ratios are positively correlated with salinity changes (~16%/salinity unit in the range of 33.5–35.5 psu), even in open ocean settings. In our case, the calcification salinity inferred from the habitat depths of N. incompta is estimated to range from 33.5 to 34.5. This salinity range was same as the salinity range for previously published Mg/Ca ratios of N. incompta in the Southern Ocean, Atlantic Ocean, and northeast Pacific. Therefore, we interpreted that the distinctly lower Mg/Ca ratios documented only in the southern Japan Sea are not attributed to salinity in the southern Japan Sea. Fourth, several planktonic foraminifera deposit a veneer of calcite, called crust or encrust, on the surface of their shell at the end of the life cycle. Recent evidence suggests that calcite crusts are compositionally different in both δ18O and trace elements (i.e. higher δ18Oc and lower Mg/Ca) relative to the inner calcite (Jonkers et al., 2012). Globigerinoides sacculifer and Orbulina universa makes up 20–30% of the calcite crust layer, suggesting these layers are very important for the wholeshell isotopic and trace element compositions. Calcite crusts are considered to be precipitated in deeper water than the depth where species

not be the best representative for the evaluation of a dissolution effect on the Mg/Ca ratios of the core-top samples, as the saturation horizon of calcite was shoaled in the past ~200 years, we expected to see a potential relation among Δ[CO32−], depth, and Mg/Ca ratios in the southern Japan Sea. Regenberg et al. (2014) found that calcite dissolution occurs in a water column below a Δ[CO32−] value of 21.3 ± 6.6 μmol·kg−1, causing the Mg/Ca ratios of foraminiferal tests to decrease by 0.054 ± 0.019 mmol·mol−1 per μmol·kg−1 below the depth. Fig. 8 shows the vertical profile of Δ[CO32−] and the relationship between the bottom water Δ[CO32−] and the measured Mg/Ca ratios at each site. Except for Site 132 (223 m water depth, Δ[CO32−] = 48.9 μmol·kg−1), all core sites represented lower Δ[CO32−] bottom waters less than the critical threshold value of 21.3 μmol·kg−1. The lowest Δ[CO32−] of −10.6 μmol·kg−1 was observed at Site H-1 (1515 m water depth) (Fig. 8). Furthermore, we found that the shallowest and deepest sites presented almost identical Mg/Ca values (0.66 mmol·mol−1 and 0.70 mmol·mol−1, respectively) although these sites are bathed by water masses with distinctly different bottom water Δ[CO32−] values. Importantly, we could not find a significant indication that the depths or bottom water Δ[CO32−] has altered Mg/Ca ratios in the range of 220–1500 m water depths. These data suggest that the lower Mg/Ca ratio for N. incompta is the pristine signature in the southern Japan Sea. 10

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

Fig. 8. The upper panel shows the vertical profiles of the calcite saturation state Δ[CO32−] in the southern Japan Sea (37° 43′ N, 134° 44′ E). The lower panel shows the relation between Δ[CO32−] and the N. incompta Mg/Ca ratio.

Fig. 6. The upper and lower panel shows seasonal changes in temperature and chlorophyll a concentration in the upper 200 m water depths off northern Noto Peninsula (38.6°N, 137.3°E) in 2005 to 2006, obtained by the JMA (http:// www.jma.go.jp/jma/indexe.html). White lines present temperature contour, and white dots present observational months and depths. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

test are needed to address the primary cause for the difference between the Japan Sea and the compiled calibrations fully. 5.3. Millennial-scale fluctuations in water volume transported by the Tsushima Warm Current Using the basin- and species-specific Mg/Ca-temperature calibration equation constructed for core-top N. incompta in the southern Japan Sea, we reconstructed, for the first time, the SST evolution during the past 6800 years in the southern Japan Sea (Fig. 4e). The estimation of apparent calcification depth shows that the Mg/Ca-derived temperature reflects an average temperature at water depths of 20–50 m in spring (April–June) at Site PC09 (Fig. 5c). Indeed, the long-term trend for Mg/ Ca-derived SST from Site PC09 in the southern Japan Sea follows the solar insolation change for 35°N at the spring equinox (May) (Fig. 4f), confirming that N. incompta Mg/Ca reflects spring SSTs in the southern Japan Sea. The Mg/Ca-derived SSTs reconstructed at Site PC09 ranged from 9 °C to 15 °C over the past 6800 years, which were within the preferred water temperature range (9–15 °C) of N. incompta (Kuroyanagi and Kawahata, 2004). The 250-year running mean of the SST record clearly exhibited a millennial-scale variability, with an amplitude of 2–3 °C, and represented five pronounced warm periods interbedded with four cold intervals (Figs. 4e, 9d). Warmer conditions occurred at 6200–6000, 4900–4500, 4200–3800, 2600–2100, and 900–400 cal. year BP. We also found that the temporal changes in Mg/Ca-derived SSTs exhibited an almost identical trend as diatom-derived SST records (i.e. ratios of warm- and cold-water diatom species) at nearby Site CGC-8 (Koizumi, 2008), although the age for this core is not well determined compared to that of PC09 (Figs. 1a, 4e). Since the diatomderived SST is considered to reflect the annual mean SST, the temperature offset observed between Mg/Ca- and diatom-derived SST could be attributed to the SST differences between the annual mean and spring. The consistency of the millennial-scale SST evolution, reconstructed from both SST proxies, strongly confirms that the SSTs in the southern Japan Sea should have fluctuated on millennial timescales. To obtain more detailed information on the water mass property, we calculated the δ18Osw from Mg/Ca-derived SST and δ18Oc using the δ18Oc-temperature equation (Eq. (1)) (Fig. 4b). The calculated δ18Osw changed in phase with Mg/Ca-derived SST evolution, that is, during periods of higher SST, there were relatively saline water masses (Fig. 4b, e). This means that Site PC09 has experienced millennial-scale oceanographic changes between warm/saline water and cold/fresh

Fig. 7. Relationship between N. incompta Mg/Ca ratios and δ18Oc-based calcification temperature for the surface sediment samples (squares). An N. incompta Mg/Ca-temperature calibration based on North Atlantic and culturing experiment data is also shown (dotted line) (Morley et al., 2017).

typically dwell, possibly as a result of low temperatures acting to initiate formation. N. incompta also produces calcite crust on the shell surface (Bolton and Marr, 2013; Domitsu and Oda, 2006). However, N. incompta retrieved from shallow plankton tow also have the apparent formation of calcite crust layer, suggesting that crustal formation may not always be restricted to deeper water (Bolton and Marr, 2013). Indeed, N. incompta in the southern Japan Sea has encrust, but δ18Oc, reported from the southern Japan Sea, generally exhibited a value of ~1‰ and does not exhibit extremely heavier values as precipitated in deeper water. It is likely that N. incompta δ18Oc is not significantly influenced by encrustation. However, at this point, we could not determine whether or not encrustation on N. incompta shell reduce Mg/Ca values in the southern Japan Sea. Detailed studies on trace element compositions of encrustation and its contribution to the entire calcite 11

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

Fig. 9. Comparison of climate proxy records with external climate forcings for the last 8000 years. (a) total solar irradiance (Steinhilber et al., 2009), (b) volcanic forcing (Kobashi et al., 2017), (c) Mt. Logan ice core δ18O (Fisher et al., 2008), (d) Mg/Ca-derived SST record from the Japan Sea (PC09, this study), (e) alkenone-derived SST records from the western North Pacific (MD01–2421) (Isono et al., 2009), (f) stalagmite δ18O records from Baeg-nyong Cave (BN-1) in the eastern Korean Peninsula (Jo et al., 2017), (g) blue dotted line representing the dry period in Jeju Island off the southern Korean Peninsula (Mulyoungari) (Park et al., 2016), (h) Pulleniatina obliquiloculata δ18O records from the East China Sea (ECS, B-3GC) (Jian et al., 2000), and (i) δ18O variance of individual G. ruber from core V21–30 in the Eastern Equatorial Pacific (EEP), indicating ENSO variance was severely damped ~5000 cal. year BP and increased towards the late Holocene (4200 cal. year BP) (Koutavas and Joanides, 2012). The bold lines indicate the 250-year running mean. The blue bars depict the periods marked by predominant El Niño-like states, while light brown bars denote the periods characterized by increased TWC volume transport, which coincide with the periods of the lower δ18O, as per the Mt. Logan ice core data.

12

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

(< 1 °C) and was superimposed onto a long-term SST decrease (Isono et al., 2009) (Figs. 1b, 9d, e). Interestingly, these pronounced warmer SST periods (4200–3800, 2600–2100, and 900–400 cal. year BP) around Japan coincided with the lower δ18O of Mt. Logan ice core, from the Yukon Territory (Fisher et al., 2008) (Fig. 9c). Lower δ18O values of the Mt. Logan ice core indicate warmer/wetter conditions near the coast of the Gulf of Alaska. Lower δ18O values have been interpreted as representing enhanced moisture transport from the tropical Pacific during strong El Niño events (Fisher et al., 2008). The interval of 4200–4000 cal. year BP was the most pronounced, and has been observed in many Pacific and Asian proxy records as a period with a weak Asian summer monsoons (Wang et al., 2005), suggesting that the Mt. Logan δ18O record can be regarded as a representative proxy for North Pacific climate variability. However, the view that multi-centennialscale lower δ18O values from the Mt. Logan ice core reflect strong El Niño events is debatable because the marine sediment record off Peruvian coast, which is used as lithic proxy of El Niño flood events in Peru, does not indicate stronger El Niño events for these periods (Rein et al., 2004). Sagawa et al. (2014) also reported on the strong coupling between the δ18O records in the northwestern North Pacific and the Mt. Logan δ18O record. Higher solar irradiance could drive a positive AO-like spatial pattern (Ineson et al., 2011). This could explain why the western and eastern North Pacific regions have been affected by AO-like climate patterns on multi-centennial to millennial timescales, with warmer in the western North Pacific and more meridional moisture transport in the eastern North Pacific (Sagawa et al., 2014). Since stronger El Niñolike events, as reconstructed from the Peru flood events record, took place during periods of lower solar irradiance, solar variability could have played an important role in generating multi-centennial- to millennial-scale climate variability in the tropical to extratropical Pacific. However, in the mid to high latitudes of the North Pacific, solar forcing would have provoked AO-like spatial patterns rather than those of modern El Niño events. The covariation between solar insolation and SSTs in the Japan Sea suggests that the higher (lower) solar insolation would have increased (reduced) the TWC volume transport into the Japan Sea (Fig. 9a, d). A coupled climate model shows that during the positive phase of AO, the AO-associated surface atmospheric circulation affected the surface heat flux and ocean surface currents, resulting in PDO-like SST anomalies (a negative phase of PDO) (Cui et al., 2013). A study investigating the baroclinic transport of the TWC through the Tsushima Strait in the 1990s (positive PDO) and the 1970s (negative PDO) found large differences from June to October between the 1990s and the 1970s, with higher TWC volume transport occurring in the 1970s (negative PDO) (Senjyu et al., 2010). This implies that AO and PDO could be a potential bridge between solar forcing and changes in the TWC volume transport on multi-centennial to millennial time scales. Volcanic forcing is also considered to have influenced Holocene climate variability. Volcanic forcing has been reconstructed from the GISP2 sulfate record, which reflects both tropical and NH volcanic eruptions (Kobashi et al., 2017). The comparison of volcanic forcing with climate proxy records reveals that multiple strong eruptions, which occurred around ~200 cal. year BP, ~700 cal. year BP, and ~3600 cal. year BP, might have driven the weakening of the EASM, as clearly shown by the lowered δ18O of the Baeg-nyong Cave stalagmite (Fig. 9f). This result is supported by recent modelling studies, which show that large volcanic eruptions have weakened the EASM precipitation (Liu et al., 2016). Unlike the Baeg-nyong Cave stalagmite record, the Japan Sea SST records has less temporal resolution, and the age model is not adequately constrained, making it difficult to elucidate the impact of volcanic forcing on the SST-to-TWC volume transport change in the Japan Sea. However, given that both records are not synchronized at the multi-centennial to millennial timescales, we conclude that the longterm SST changes in the Japan Sea were not driven by volcanic forcing.

water. Interestingly, off Hokkaido at the northern end of the TWC the warm molluscan assemblages increased during 7200–5000, 4200–3200, 2500–2300, and 1000–900 cal. year BP (Matsushima, 2010), corresponding to the warmer SST periods reconstructed by foraminifera Mg/Ca ratio at Site PC09 and diatoms at Site C-GC-8 (Fig. 4d, e). Oscillation between warm/saline water and cold/fresh water, and the coherent appearance of the warm molluscan assemblages at millennial timescales, suggest changes to the volume transported in the TWC during at least the past ~7000 cal. year BP. When the TWC flow volume was higher throughout the year, it extended to off Hokkaido, and the period (spring to fall) for which southern Japan Sea surface water originated from the TWC became longer, leading to warmer SST in spring and also warmer annual mean SSTs, as shown in Fig. 2. Alkenone-SST data from MR0604-PC03B off Hokkaido reflect the summer season, and do not show coherent millennial-scale variability with those at Sites PC09 and C-GC-8 (Bae et al., 2014) (Fig. 4e). The different SST patterns between PC09 and MR0604PC03B can probably be attributed to (1) insensitivity of Site MR0604PC03B to such volume transport fluctuations of TWC due to the location of the site in the subpolar region or (2) insensitivity of summer SST to changes in the volume transport of the TWC (Fig. 2). In addition to TWC volume transport changes, the change in the habitat depth of N. incompta might also be a potential factor affecting SST evolution at Site PC09. We can expect that N. incompta calcified at the deeper depths if the mixed layer was deepened in response to an enhanced winter monsoon, or if N. incompta migrated during shell growth (Iwasaki et al., 2017). In these cases, N. incompta tests will record lower temperatures and higher δ18Osw (Fig. 1c). However, this expectation is opposite to the observed, millennial-scale variability marked by water mass properties of warm/saline and cold/fresh waters. Thus, N. incompta depth habitat change may not be a principal factor for millennial-scale SST variability at Site PC09. Seawater neodymium isotope data in the ECS for August 2015 indicated that water entering the Japan Sea consisted of approximately 10% from the CDW, 28% from the Yellow Sea Water, and 62% from the Kuroshio Water (Che and Zhang, 2018) —with the latter delivering warmer and saline waters to the Japan Sea. Therefore, TWC volume transport should be strongly related to the behavior of the Kuroshio Current, which could explain changes between warm/saline and cold/ fresh water mass properties in the southern Japan Sea. 5.4. Mechanisms of millennial-scale changes to TWC volume transport In the Pacific, the ENSO phenomenon represents the most important mode of natural climate variability. The mean state of the Pacific shifted from a La Niña-like state during the mid Holocene to a predominant El Niño-like ENSO state during the late Holocene (4200 cal. year BP) due to orbital insolation changes (Clement et al., 2000; Koutavas and Joanides, 2012) (Fig. 9i). The long-term shift in the mean state of the Pacific is also clearly documented from the Baeg-nyong Cave stalagmite (BN-1) δ18O from the Korean Peninsula, near the Japan Sea, around ~4500 cal. year BP (Jo et al., 2017) (Figs. 1b, 9f), suggesting that the EASM was weakened in response to the shift in the mean state of the Pacific (Wang et al., 2005). Furthermore, during the same period of 4600–2700 cal. year BP, the weakening of the Kuroshio Current is inferred from the heavier δ18O and the decreased abundance of Pulleniatina obliquiloculata, the Kuroshio Current indicator, in the ECS (Jian et al., 2000) (Fig. 9h). A weakening of the Walker and Hadley circulations is inferred from the pronounced dry/cold climate that occurred from 4400 to 1900 cal. year BP in Jeju Island in the northern ECS (Park et al., 2016) (Fig. 9g). Unlike these records, our SST records in the Japan Sea (PC09) do not show such obvious shift from the mid to the late Holocene. As a different feature, the SST records in the Japan Sea have varied synchronously with the SST at Site MD01-2421, at the northern end of the Kuroshio Current, although the SST variability was somewhat smaller 13

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

References

The larger eruptions appear to impact short-duration SST decreases in the Japan Sea, as seen, for example, around ~700 cal. year BP, ~2000 cal. year BP, ~5900 cal. year BP, and ~6400 cal. year BP (Fig. 9b, d). In conclusion, the comparison of the Japan Sea SST records with climate forcings and natural modes of climate variability reveals that the decrease in TWC volume transport, at the multi-centennial to millennial timescale, could result from solar insolation changes manifested through AO-PDO variability. Given that multiple large volcanic eruptions occurred in the mid Holocene rather than in the late Holocene, volcanic forcing on the TWC volume transport change would have been more significant in the mid Holocene, as seen in the highly variable SST record in the mid Holocene, and in the distinct SST decreases around ~5900 cal. Year BP and ~6400 cal. year BP.

Anand, P., Elderfield, H., Conte, M.H., 2003. Calibration of Mg/Ca thermometry in planktonic foraminifera from a sediment trap time series. Paleoceanography 18, 1050. https://doi.org/10.1029/2002kpa000846. Bae, S.W., Lee, K.E., Park, Y., Kimoto, K., Ikehara, K., Harada, N., 2014. Sea surface temperature and salinity changes near the Soya Strait during the last 19 ka. Quat. Int. 344, 200–210. https://doi.org/10.1016/j.quaint.2014.06.014. Barker, S., Greaves, M., Elderfield, H., 2003. A study of cleaning procedures used for foraminiferal Mg/Ca paleothermometry. Geochem. Geophys. Geosyst. 4, 8407. https://doi.org/10.1029/2003gc000559. Bolton, A., Marr, J.P., 2013. Trace element variability in crust-bearing and non crustbearing Neogloboquadrina incompta, P–D intergrade and Globoconella inflata from the Southwest Pacific Ocean: potential paleoceanographic implications. Mar. Micropaleontol. 100, 21–33. https://doi.org/10.1016/j.marmicro.2013.03.008. Boyle, E.A., Keigwin, L.D., 1985. Comparison of Atlantic and Pacific paleochemical records for the last 215,000 years: changes in deep ocean circulation and chemical inventories. Earth Planet. Sci. Lett. 76, 135–150. Che, H., Zhang, J., 2018. Water mass analysis and end-member mixing contribution using coupled radiogenic Nd isotopes and Nd concentrations: Interaction between marginal seas and the northwestern Pacific. Geophys. Res. Lett. https://doi.org/10.1002/ 2017gl076978. Clement, A.C., Seager, R., Cane, M.A., 2000. Suppression of El Niño during the MidHolocene by changes in the Earth's orbit. Paleoceanography 15, 731–737. https:// doi.org/10.1029/1999pa000466. Cléroux, C., Cortijo, E., Anand, P., Labeyrie, L., Bassinot, F., Caillon, N., Duplessy, J.-C., 2008. Mg/Ca and Sr/Ca ratios in planktonic foraminifera: Proxies for upper water column temperature reconstruction. Paleoceanography 23, PA3214. https://doi.org/ 10.1029/2007pa001505. Cui, X.-D., Gao, Y.-Q., Gong, D.-Y., Guo, D., Tore, F., 2013. Teleconnection between Winter Arctic Oscillation and Southeast Asian Summer Monsoon in the Pre-Industry simulation of a coupled climate model. Atmos. Ocean. Sci. Lett. 6, 349–354. https:// doi.org/10.3878/j.issn.1674-2834.12.0114. Darling, K.F., Kucera, M., Kroon, D., Wade, C.M., 2006. A resolution for the coiling direction paradox in Neogloboquadrina pachyderma. Paleoceanography 21. https://doi. org/10.1029/2005pa001189. de Villiers, S., Greaves, M., Elderfield, H., 2002. An intensity ratio calibration method for the accurate determination of Mg/Ca and Sr/Ca of marine carbonates by ICP-AES. Geochem. Geophys. Geosyst. 3. https://doi.org/10.1029/2001gc000169. Dickson, A.G., 1990. Standard potential of the reaction: AgCl(s) + 12H2(g) = Ag(s) + HCl(aq), and and the standard acidity constant of the ion HSO4− in synthetic sea water from 273.15 to 318.15 K. J. Chem. Thermodyn. 22, 113–127. https://doi.org/ 10.1016/0021-9614(90)90074-Z. Dickson, A.G., Millero, F.J., 1987. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res. Pt I 34, 1733–1743. https://doi.org/10.1016/0198-0149(87)90021-5. Domitsu, H., Oda, M., 2005. Japan Sea planktic foraminifera in surface sediments: geographical distribution and relationships to surface water mass. Paleontol. Res. 9, 255–270. Domitsu, H., Oda, M., 2006. Linkages between surface and deep circulations in the southern Japan Sea during the last 27,000 years: evidence from planktic foraminiferal assemblages and stable isotope records. Mar. Micropaleontol. 61, 155–170. Domitsu, H., Oda, M., 2008. Holocene influx of the Tsushima Current into the Japan Sea signalled by spatial and temporal changes in Neogloboquadrina incompta distribution. Holocene 18, 345–352. https://doi.org/10.1177/0959683607086772. Field, D.B., 2004. Variability in vertical distributions of planktonic foraminifera in the California Current: Relationships to vertical ocean structure. Paleoceanography 19. https://doi.org/10.1029/2003pa000970. Fisher, D., Osterberg, E., Dyke, A., Dahl-Jensen, D., Demuth, M., Zdanowicz, C., Bourgeois, J., Koerner, R.M., Mayewski, P., Wake, C., Kreutz, K., Steig, E., Zheng, J., Yalcin, K., Goto-Azuma, K., Luckman, B., Rupper, S., 2008. The Mt Logan Holocenelate Wisconsinan isotope record: Tropical Pacific-Yukon connections. Holocene 18, 667–677. https://doi.org/10.1177/0959683608092236. Friedrich, O., Schiebel, R., Wilson, P.A., Weldeab, S., Beer, C.J., Cooper, M.J., Fiebig, J., 2012. Influence of test size, water depth, and ecology on Mg/Ca, Sr/Ca, δ18O and δ13C in nine modern species of planktic foraminifers. Earth Planet. Sci. Lett. 319-320, 133–145. https://doi.org/10.1016/j.epsl.2011.12.002. Gray, L.J., Beer, J., Geller, M., Haigh, J.D., Lockwood, M., Matthes, K., Cubasch, U., Fleitmann, D., Harrison, G., Hood, L., Luterbacher, J., Meehl, G.A., Shindell, D., van Geel, B., White, W., 2010. Solar Influences on climate. Rev. Geophys. 48. https://doi. org/10.1029/2009rg000282. Greaves, M., Caillon, N., Rebaubier, H., Bartoli, G., Bohaty, S., Cacho, I., Clarke, L., Cooper, M., Daunt, C., Delaney, M., deMenocal, P., Dutton, A., Eggins, S., Elderfield, H., Garbe-Schoenberg, D., Goddard, E., Green, D., Groeneveld, J., Hastings, D., Hathorne, E., Kimoto, K., Klinkhammer, G., Labeyrie, L., Lea, D.W., Marchitto, T., Martinez-Boti, M.A., Mortyn, P.G., Ni, Y., Nuernberg, D., Paradis, G., Pena, L., Quinn, T., Rosenthal, Y., Russell, A., Sagawa, T., Sosdian, S., Stott, L., Tachikawa, K., Tappa, E., Thunell, R., Wilson, P.A., 2008. Interlaboratory comparison study of calibration standards for foraminiferal Mg/Ca thermometry. Geochem. Geophys. Geosyst. 9, Q08010. https://doi.org/10.1029/2008gc001974. Hase, H., Yoon, J.-H., Koterayama, W., 1999. The current structure of the Tsushima Warm Current along the Japanese coast. J. Oceanogr. 55, 217–235. https://doi.org/10. 1023/a:1007894030095. Hönisch, B., Allen, K.A., Lea, D.W., Spero, H.J., Eggins, S.M., Arbuszewski, J., deMenocal,

6. Conclusion We have presented the first N. incompta Mg/Ca and δ18Oc data set from 13 surface sediments and a downcore Mg/Ca record for the past 6800 cal. year BP in the southern Japan Sea. The δ18Oc-based apparent calcification depth for N. incompta represented shallower depths at the northern sites and deeper depths at the southwestern sites, and the habitat season was estimated to be spring. A newly constructed Mg/Ca calibration equation for N. incompta was presented as Mg/ Ca = 0.311 × exp (0.07 × T). Applying this species-specific Mg/Ca-temperature calibration, we, for the first time, reconstructed the SST evolution during the past 6800 years at Site YK10–7-PC09 off the central Japan. Mg/Ca data highlighted that warmer conditions occurred at 6200–6000, 4900–4500, 4200–3800, 2600–2100, and 900–400 cal. year BP. These periods corresponded to the periods in which warm molluscan assemblages increased at the northern end of the TWC, suggesting that the higher SST periods corresponded to the periods in which the volume transport of the TWC increased. Given that higher solar irradiance provoked positive AO-like spatial patterns and negative phase of the PDO, it is suggested that increased (reduced) TWC volume transport on multi-centennial to millennial time scales was caused by high (low) solar insolation through the potential bridge of AO and PDO. Larger and more frequent volcanic eruptions occurred in the mid Holocene rather than the late Holocene, and thus volcanic forcing on the TWC volume transport would have been more significant in the former, as seen in the highly variable SST during that time period and distinct SST drops around ~5900 cal. year BP and ~6400 cal. year BP. The millennial-scale fluctuations seen in the volume transport of the TWC and SST in the southern Japan Sea would have had a large impact on the evolution of vegetation and human adaptation in the northern Japanese islands, adjacent to the Japan Sea, over the last 6800 years. Declarations of Competing Interest None. Acknowledgements We acknowledge the great support of shipboard scientists, captain, and crews of R/V Yokosuka YK10-07 (JAMSTEC) and the T/V Nagasaki-Maru (Nagasaki University). This work was performed under the cooperative research program of the Center for Advanced Marine Core Research (CMCR), Kochi University (#11B034, 12A009, 12B037, 13A016, and 13B050), and supported by Sea of Japanology Promotion Organization. This work was partly supported by JSPS KAKENHI Grant Number JP17H01853. We would like to thank Editage (www.editage. jp) for English language editing. This manuscript was further improved by constructive comments from two anonymous reviewers and Dr. Zhengtang Guo. 14

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

10.1038/srep24331. Lyu, S.J., Kim, K., 2005. Subinertial to interannual transport variations in the Korea Strait and their possible mechanisms. J. Geophys. Res. 110. https://doi.org/10.1029/ 2004jc002651. Mann, M.E., Cane, M.A., Zebiak, S.E., Clement, A., 2005. Volcanic and solar forcing of the tropical Pacific over the past 1000 years. J. Clim. 18, 447–456. https://doi.org/10. 1175/Jcli-3276.1. Martin, S., Kawase, M., 1998. The southern flux of sea ice in the Tatarskiy Strait, Japan Sea and the generation of the Liman Current. J. Mar. Res. 56, 141–155. https://doi. org/10.1357/002224098321836145. Martinez-Boti, M.A., Mortyn, P.G., Schmidt, D.N., Vance, D., Field, D.B., 2011. Mg/Ca in foraminifera from plankton tows: Evaluation of proxy controls and comparison with core tops. Earth Planet. Sci. Lett. 307, 113–125. Mashiotta, T.A., Lea, D.W., Spero, H.J., 1999. Glacial–interglacial changes in Subantarctic sea surface temperature and δ18O-water using foraminiferal Mg. Earth Planet. Sci. Lett. 170, 417–432. https://doi.org/10.1016/S0012-821X(99)00116-8. Matsushima, Y., 2010. Warmings of the Tsushima current during the Holocene as deduced from the distribution of warm molluscan assemblages. Quat. Res. (Daiyonki-kenkyu) 49, 1–10. Mayewski, P.A., Rohling, E.E., Curt Stager, J., Karlén, W., Maasch, K.A., Meeker, L.D., Meyerson, E.A., Gasse, F., van Kreveld, S., Holmgren, K., Lee-Thorp, J., Rosqvist, G., Rack, F., Staubwasser, M., Schneider, R.R., Steig, E.J., 2004. Holocene climate variability. Quat. Res. 62, 243–255. https://doi.org/10.1016/j.yqres.2004.07.001. Mooers, C.N.K., Bang, I., Sandoval, F.J., 2005. Comparisons between observations and numerical simulations of Japan (East) Sea flow and mass fields in 1999 through 2001. Deep-Sea. Res. Pt. II. 52, 1639–1661. https://doi.org/10.1016/j.dsr2.2004.10.003. Morley, A., Babila, T.L., Wright, J., Ninnemann, U., Kleiven, K., Irvali, N., Rosenthal, Y., 2017. Environmental controls on Mg/Ca in Neogloboquadrina incompta: a core-top study from the subpolar North Atlantic. Geochem. Geophys. Geosyst. https://doi.org/ 10.1002/2017gc007111. Na, H., Isoda, Y., Kim, K., Kim, Y.H., Lyu, S.J., 2009. Recent observations in the straits of the East/Japan Sea: a review of hydrography, currents and volume transports. J. Mar. Syst. 78, 200–205. https://doi.org/10.1016/j.jmarsys.2009.02.018. Na, H., Kim, K.-Y., Chang, K.-I., Park, J.J., Kim, K., Minobe, S., 2012. Decadal variability of the upper ocean heat content in the East/Japan Sea and its possible relationship to northwestern Pacific variability. J. Geophys. Res. 117, C02017. https://doi.org/10. 1029/2011jc007369. Nagashima, K., Tada, R., Toyoda, S., 2013. Westerly jet-East Asian summer monsoon connection during the Holocene. Geochem. Geophys. Geosyst. https://doi.org/10. 1002/2013GC004931. Oba, T., Murayama, M., Matsumoto, E., Nakamura, T., 1995. AMS-14C ages of Japan Sea cores from the Oki Ridge. Quat. Res. (Daiyonki-kenkyu) 34, 289–296. Oda, M., Yamasaki, M., 2005. Sediment trap results from the Japan trench in the Kuroshio domain: Seasonal variations in the planktic foraminiferal flux. J. Foramin. Res. 35, 315–326. https://doi.org/10.2113/35.4.315. Park, G.-H., Lee, K., Tishchenko, P., Min, D.-H., Warner, M.J., Talley, L.D., Kang, D.-J., Kim, K.-R., 2006. Large accumulation of anthropogenic CO2 in the East (Japan) Sea and its significant impact on carbonate chemistry. Global. Biogeochem. Cy. 20, GB4013. https://doi.org/10.1029/2005GB002676. Park, J., Shin, Y.H., Byrne, R., 2016. Late-Holocene vegetation and climate change in Jeju Island, Korea and its implications for ENSO influences. Quat. Sci. Rev. 153, 40–50. https://doi.org/10.1016/j.quascirev.2016.10.011. Pierrot, D., Lewis, E., Wallace, D.W.R., 2006. MS Excel Program Developed for CO2 System Calculations, ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennessee. Regenberg, M., Steph, S., Nürnberg, D., Tiedemann, R., Garbe-Schönberg, D., 2009. Calibrating Mg/Ca ratios of multiple planktonic foraminiferal species with δ18Ocalcification temperatures: Paleothermometry for the upper water column. Earth Planet. Sci. Lett. 278, 324–336. https://doi.org/10.1016/j.epsl.2008.12.019. Regenberg, M., Regenberg, A., Garbe-Schönberg, D., Lea, D.W., 2014. Global dissolution effects on planktonic foraminiferal Mg/Ca ratios controlled by the calcite-saturation state of bottom waters. Paleoceanography 29, 127–142. https://doi.org/10.1002/ 2013PA002492. Reimer, P.J., Bard, E., Bayliss, A., Beck, J.W., Blackwell, P.G., Ramsey, C.B., Buck, C.E., Cheng, H., Edwards, R.W., Friedrich, M., Grootes, P.M., Guilderson, T.P., Haflidason, H., Hajdas, I., Hatté, C., Heaton, T.J., Hoffmann, D.L., Hogg, A.G., Hughen, K.A., Kaiser, K.F., Kromer, R., Manning, S.W., Niu, M., Reimer, R.W., Richards, D.A., Scott, E.M., Southon, J.R., Staff, R.A, Turney, C.S.M., van der Plicht, J., 2013. IntCal13 and marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55. https://doi.org/10.2458/azu_js_rc.55.16947. Rein, B., Lückge, A., Sirocko, F., 2004. A major Holocene ENSO anomaly during the medieval period. Geophys. Res. Lett. 31, L17211. https://doi.org/10.1029/ 2004gl020161. Robock, A., 2015. Chapter 53 - Climatic Impacts of Volcanic Eruptions. In: Sigurdsson, H. (Ed.), The Encyclopedia of Volcanoes. Academic Press, Amsterdam, pp. 935–942. Rosenthal, Y., Boyle, E.A., Labeyrie, L., 1997. Last glacial maximum paleochemistry and Deepwater circulation in the Southern Ocean: evidence from foraminiferal cadmium. Paleoceanography 12, 787–796. https://doi.org/10.1029/97pa02508. Sagawa, T., Kuroyanagi, A., Irino, T., Kuwae, M., Kawahata, H., 2013. Seasonal variations in planktonic foraminiferal flux and oxygen isotopic composition in the western North Pacific: Implications for paleoceanographic reconstruction. Mar. Micropaleontol. 100, 11–20. https://doi.org/10.1016/j.marmicro.2013.03.013. Sagawa, T., Kuwae, M., Tsuruoka, K., Nakamura, Y., Ikehara, M., Murayama, M., 2014. Solar forcing of centennial-scale East Asian winter monsoon variability in the mid- to late Holocene. Earth Planet. Sci. Lett. 395, 124–135. https://doi.org/10.1016/j.epsl.

P., Rosenthal, Y., Russell, A.D., Elderfield, H., 2013. The influence of salinity on Mg/ Ca in planktic foraminifers – evidence from cultures, core-top sediments and complementary δ18O. Geochim. Cosmochim. Acta 121, 196–213. https://doi.org/10. 1016/j.gca.2013.07.028. Horikawa, K., Kodaira, T., Zhang, J., Murayama, M., 2015. δ18Osw estimate for Globigerinoides ruber from core-top sediments in the East China Sea. Prog. Earth Planet. Sci. 2. https://doi.org/10.1186/s40645-015-0048-3. Ineson, S., Scaife, A.A., Knight, J.R., Manners, J.C., Dunstone, N.J., Gray, L.J., Haigh, J.D., 2011. Solar forcing of winter climate variability in the Northern Hemisphere. Nat. Geosci. 4, 753–757. https://doi.org/10.1038/ngeo1282. Isono, D., Yamamoto, M., Irino, T., Oba, T., Murayama, M., Nakamura, T., Kawahata, H., 2009. The 1500-year climate oscillation in the midlatitude North Pacific during the Holocene. Geology 37, 591–594. https://doi.org/10.1130/g25667a.1. Iwasaki, S., Kimoto, K., Kuroyanagi, A., Kawahata, H., 2017. Horizontal and vertical distributions of planktic foraminifera in the subarctic Pacific. Mar. Micropaleontol. 130, 1–14. https://doi.org/10.1016/j.marmicro.2016.12.001. Jansen, H., Zeebe, R.E., Wolf-Gladrow, D.A., 2002. Modeling the dissolution of settling CaCO3 in the ocean. Global. Biogeochem. Cy. 16. https://doi.org/10.1029/ 2000gb001279. Jian, Z., Wang, P., Saito, Y., Wang, J., Pflaumann, U., Oba, T., Cheng, X., 2000. Holocene variability of the Kuroshio Current in the Okinawa Trough, northwestern Pacific Ocean. Earth Planet. Sci. Lett. 184, 305–319. https://doi.org/10.1016/S0012-821X (00)00321-6. Jo, K.N., Yi, S., Lee, J.Y., Woo, K.S., Cheng, H., Edwards, L.R., Kim, S.T., 2017. 1000-Year Quasi-Periodicity of Weak Monsoon Events in Temperate Northeast Asia since the Mid-Holocene. Sci. Rep. 7, 15196. https://doi.org/10.1038/s41598-017-15566-4. Johnstone, H.J.H., Lee, W., Schulz, M., 2016. Effect of preservation state of planktonic foraminifera tests on the decrease in Mg/Ca due to reductive cleaning and on sample loss during cleaning. Chem. Geol. 420, 23–36. https://doi.org/10.1016/j.chemgeo. 2015.10.045. Jonkers, L., de Nooijer, L.J., Reichart, G.J., Zahn, R., Brummer, G.J.A., 2012. Encrustation and trace element composition of Neogloboquadrina dutertrei assessed from single chamber analyses –implications for paleotemperature estimates. Biogeosciences 9, 4851–4860. https://doi.org/10.5194/bg-9-4851-2012. Kawabe, M., 1982. Branching of the Tsushima current in the Japan Sea. J. Oceanogr. Soc. Jpn 38, 95–107. https://doi.org/10.1007/BF02110295. Keigwin, L.D., Pilskaln, C.H., 2015. Sediment flux and recent paleoclimate in JordanBasin, Gulf of Maine. Cont. Shelf Res. 96, 45–55. https://doi.org/10.1016/j. csr.2015.01.008. Kida, S., Qiu, B., Yang, J., Lin, X., 2016. The annual cycle of the Japan Sea throughflow. J. Phys. Oceanogr. 46, 23–39. https://doi.org/10.1175/jpo-d-15-0075.1. Kim, S.-T., O'Neil, J.R., 1997. Equilibrium and nonequilibrium oxygen isotope effects in synthetic carbonates. Geochim. Cosmochim. Acta 61, 3461–3475. https://doi.org/ 10.1016/S0016-7037(97)00169-5. Kim, J.-M., Kennett, J.P., Park, B.-K., Kim, D.C., Kim, G.Y., Roark, E.B., 2000. Paleoceanographic change during the last deglaciation, East Sea of Korea. Paleoceanography 15, 254–266. https://doi.org/10.1029/1999pa000393. Kısakürek, B., Eisenhauer, A., Böhm, F., Garbe-Schönberg, D., Erez, J., 2008. Controls on shell Mg/Ca and Sr/Ca in cultured planktonic foraminiferan, Globigerinoides ruber (white). Earth Planet. Sci. Lett. 273, 260–269. https://doi.org/10.1016/j.epsl.2008. 06.026. Kobashi, T., Menviel, L., Jeltsch-Thommes, A., Vinther, B.M., Box, J.E., Muscheler, R., Nakaegawa, T., Pfister, P.L., Doring, M., Leuenberger, M., Wanner, H., Ohmura, A., 2017. Volcanic influence on centennial to millennial Holocene Greenland temperature change. Sci. Rep. 7, 1441. https://doi.org/10.1038/s41598-017-01451-7. Kodaira, T., Horikawa, K., Zhang, J., Senjyu, T., 2016. Relationship between seawater oxygen isotope ratio and salinity in the Tsushima Current, the Sea of Japan. Chikyukagaku (Geochemistry) 50, 263–277. https://doi.org/10.14934/ chikyukagaku.50.26. Koizumi, I., 1989. Holocene pulses of diatom growths in the warm Tsushima Current in the Japan Sea. Diatom. Res. 4, 55–68. https://doi.org/10.1080/0269249X.1989. 9705052. Koizumi, I., 2008. Diatom-derived SSTs (Td’ ratio) indicate warm seas off Japan during the middle Holocene (8.2–3.3 kyr BP). Mar. Micropaleontol. 69, 263–281. https:// doi.org/10.1016/j.marmicro.2008.08.004. Koutavas, A., Joanides, S., 2012. El Niño–Southern Oscillation extrema in the Holocene and last glacial maximum. Paleoceanography 27, PA4208. https://doi.org/10.1029/ 2012PA002378. Kuroyanagi, A., Kawahata, H., 2004. Vertical distribution of living planktonic foraminifera in the seas around Japan. Mar. Micropaleontol. 53, 173–196. https://doi. org/10.1016/j.marmicro.2004.06.001. Kuroyanagi, A., Kawahata, H., Nishi, H., Honda, M.C., 2002. Seasonal changes in planktonic foraminifera in the northwestern North Pacific Ocean: sediment trap experiments from subarctic and subtropical gyres. Deep-Sea. Res. Pt. II. 49, 5627–5645. https://doi.org/10.1016/S0967-0645(02)00202-3. Kuzmin, Y.V., Burr, G.S., Jull, A.J.T., 2001. Radiocarbon reservoir correction ages in the Peter the Great Gulf, Sea of Japan, and eastern coast of the Kunashir, southern Kuriles (northwestern Pacific). Radiocarbon 43, 477–481. von Langen, P., 2001. Non-spinose Planktonic Foraminifera (Neogloboquadrina pachyderma) Cultured for Geochemical and Paleoceanographic Applications. Univ. of Calif, Santa Barbara. Laskar, J., Robutel, P., Joutel, F., Gastineau, M., Correia, A.C.M., Levrard, B., 2004. A long-term numerical solution for the insolation quantities of the Earth. Astron. Astrophys. 428, 261–285. https://doi.org/10.1051/0004-6361:20041335. Liu, F., Chai, J., Wang, B., Liu, J., Zhang, X., Wang, Z., 2016. Global monsoon precipitation responses to large volcanic eruptions. Sci. Rep. 6, 24331. https://doi.org/

15

Global and Planetary Change 183 (2019) 103028

K. Horikawa, et al.

Takikawa, T., Watanabe, T., Senjyu, T., Morimoto, A., 2017. Wind-driven intensification of the Tsushima Warm Current along the Japanese coast detected by sea level difference in the summer monsoon of 2013. Cont. Shelf Res. 143, 271–277. https://doi. org/10.1016/j.csr.2016.06.004. Wang, Y., Cheng, H., Edwards, R.L., He, Y., Kong, X., An, Z., Wu, J., Kelly, M.J., Dykoski, C.A., Li, X., 2005. The Holocene Asian Monsoon: links to solar changes and North Atlantic climate. Science 308, 854–857. https://doi.org/10.1126/science.1106296. Wanner, H., Beer, J., Butikofer, J., Crowley, T.J., Cubasch, U., Fluckiger, J., Goosse, H., Grosjean, M., Joos, F., Kaplan, J.O., Kuttel, M., Muller, S.A., Prentice, I.C., Solomina, O., Stocker, T.F., Tarasov, P., Wagner, M., Widmann, M., 2008. Mid- to Late Holocene climate change: an overview. Quat. Sci. Rev. 27, 1791–1828. https://doi.org/10. 1016/j.quascirev.2008.06.013. Wanner, H., Solomina, O., Grosjean, M., Ritz, S.P., Jetel, M., 2011. Structure and origin of Holocene cold events. Quat. Sci. Rev. 30, 3109–3123. https://doi.org/10.1016/j. quascirev.2011.07.010. Yokoyama, Y., Kido, Y., Tada, R., Minami, I., Finkel, R.C., Matsuzaki, H., 2007. Japan Sea oxygen isotope stratigraphy and global sea-level changes for the last 50,000 years recorded in sediment cores from the Oki Ridge. Palaeogeogr. Palaeoclimatol. Palaeoecol. 247, 5–17. https://doi.org/10.1016/j.palaeo.2006.11.018. Yoneda, M., Uno, H., Shibata, Y., Suzuki, R., Kumamoto, Y., Yoshida, K., Sasaki, T., Suzuki, A., Kawahata, H., 2007. Radiocarbon marine reservoir ages in the western Pacific estimated by pre-bomb molluscan shells. Nucl. Instrum. Methods Phys. Res., Sect. B 259, 432–437.

2014.03.043. Schiebel, R., Waniek, J., Bork, M., Hemleben, C., 2001. Planktic foraminiferal production stimulated by chlorophyll redistribution and entrainment of nutrients. Deep-Sea. Res. Pt. I. 48, 721–740. https://doi.org/10.1016/S0967-0637(00)00065-0. Senjyu, T., Han, I.-S., Matsui, S., 2010. Interdecadal variations of temperature and salinity structures in the Tsushima Strait. Pac. Oceanogr. 5, 44–55. Shackleton, N., 1974. Attainment of isotopic equilibrium between ocean water and the benthonic foraminifera genus Uvigerina: isotopic changes in the ocean during the last glacial. Colloq. Int. Du. C.N.R.S 203–209. Sigl, M., Winstrup, M., McConnell, J.R., Welten, K.C., Plunkett, G., Ludlow, F., Buntgen, U., Caffee, M., Chellman, N., Dahl-Jensen, D., Fischer, H., Kipfstuhl, S., Kostick, C., Maselli, O.J., Mekhaldi, F., Mulvaney, R., Muscheler, R., Pasteris, D.R., Pilcher, J.R., Salzer, M., Schupbach, S., Steffensen, J.P., Vinther, B.M., Woodruff, T.E., 2015. Timing and climate forcing of volcanic eruptions for the past 2,500 years. Nature 523, 543–549. https://doi.org/10.1038/nature14565. Steinhilber, F., Beer, J., Fröhlich, C., 2009. Total solar irradiance during the Holocene. Geophys. Res. Lett. 36. https://doi.org/10.1029/2009gl040142. Stuiver, M., Reimer, P.J., Reimer, R.W., 2017. CALIB 7.1 [WWW program]. Takei, T., Minoura, K., Tsukawaki, S., Nakamura, T., 2002. Intrusion of a branch of the Oyashio current into the Japan Sea during the Holocene. Paleoceanography 17. https://doi.org/10.1029/2001PA000666. Takikawa, T., Yoon, J.H., Cho, K.D., 2005. The Tsushima warm current through Tsushima Straits estimated from ferryboat ADCP data. J. Phys. Oceanogr. 35, 1154–1168. https://doi.org/10.1175/Jpo2742.1.

16