Millennial-scale changes in sea-surface temperature and productivity along the Kuroshio– Oyashio boundary during MIS-19 based on the radiolarian record from the Chiba composite section, central Japan

A high-resolution radiolarian record from 800 to 750 ka was examined from the Chiba composite section (CbCS) of the Kokumoto Formation, including the GSSP (Global Boundary Stratotype Section and Point) for the Lower–Middle Pleistocene boundary, on the Boso Peninsula, Pacic side of central Japan. Total radiolarian abundance was closely related to biological productivity in the sea-surface layer and was observed to increase and repeatedly decrease in the millennial-scale period. Summer SST (sea-surface temperature), which was estimated based on the radiolarian assemblage, was 19°C at the end of MIS-20 (790-793 ka) and uctuated between 21 and 26°C during MIS-19, with the warm periods tending to be synchronous with high productivity. Recent observations have revealed that productivity increases with a northward shift of the Kuroshio along the Kuroshio-Oyashio boundary zone. Therefore, high productivity in the warmer and stratied conditions during MIS-19 can be interpreted as being closely related to millennial-scale oscillations of the Kuroshio Extension. Such millennial-scale climatic changes were also recognized in southern Europe and are likely related to shifts in climate systems such as AO (Arctic Oscillations).


Introduction
Because Marine Isotope Stage (MIS)-19 is an interglacial period with an orbital composition of the Milankovitch cycle similar to that of the current interglacial (MIS-1), it is important to build a detailed understanding of the climatic features of this period for use in making future predictions (Tzedakis et al., 2012;Giaccio et al., 2015;Sánchez Goñi et al., 2016). High-resolution paleoclimatic records during  have been documented from the North Atlantic (Kleiven et al., 2011;Ferretti et al., 2015;Sánchez Goñi et al., 2016), Indian Ocean (Valet et al., 2014), southern Europe Simon et al., 2017;Nomade et al., 2019;Regattieri et al., 2019), Japan Suganuma et al., 2018;Haneda et al., 2020), Lake El'gygytgyn (Wennrich et al., 2014), Lake Baikal (Prokopenko et al., 2006), and Antarctica (Jouzel et al., 2007). The amplitudes and timing of millennial-scale variations of these paleoclimatic records tend to be synchronized among areas suggesting a global climatic teleconnection (Tzedakis et al., 2012;Nomade et al., 2019). In order to clarify the mechanism of such teleconnection, it is important to perform high-resolution reconstruction of the paleoenvironment in various areas of the world.
The Kazusa Group composed of Pleistocene deep-sea deposition is continuously distributed on the Boso Peninsula on the Paci c side of central Japan (e.g., Kazaoka et al., 2015). Furthermore, the Chiba composite section (CbCS) of the Kokumoto Formation in this group is a well-exposed and continuous marine sedimentary record across MIS-19 ( Fig. 1), which has been investigated in great detail from various aspects (GSSP Proposal Group, 2019;Suganuma et al., 2015;Nishida et al., 2015;Okada et al., 2017;Simon et al., 2019;Haneda et al., 2020;Haneda et al., submitted;Izumi et al., submitted;Kameo et al., submitted). Therefore, the CbCS was rati ed as a GSSP (Global Boundary Stratotype Section and Point) for the Lower-Middle Pleistocene boundary.
At present, the offshore area near the Boso Peninsula is in uenced by both the Kuroshio warm and Oyashio cold currents and, therefore, it is expected to be sensitive to the glacial-interglacial cycle and even small climatic changes in East Asia. Suganuma et al. (2018) discussed the close relationship between climatic changes in this area and climatic dynamics in East Asia based on the results of various proxies from the CbCS. Recently, more detailed millennial-scale studies from this section have been conducted for oxygen isotopes of foraminifera (Haneda et al., 2020), the geochemical record (Izumi et al., submitted) and calcareous nanofossils (Kameo et al., submitted).
Radiolarians, a marine plankton group with opaline skeletons, are preserved in deep-sea sediments as microfossils and are widely used as a paleoceanographic proxy. Examination of this microfossil group is well suited for detecting changes in the Kuroshio-Oyashio front that are closely related to past climatic changes around the Boso Peninsula (e.g., Chinzei et al., 1987;Yasudomi et al., 2014). In total, 36 radiolarian species and species groups have been reported from the CbCS (Motoyama et al., 2017), and radiolarian assemblages related to climatic changes were reported in Suganuma et al. (2018) but with low-resolution, preliminary results, owing to the inclusion of few species.
In this study, we conducted high resolution analysis of radiolarian fossils during MIS-19 from the CbCS.
Because radiolarians are secondary producers in the ecosystem, total abundance of the fossil serves as a proxy for biological productivity. In addition, sea-surface temperature (SST) in the past can be extrapolated from the faunal assemblage. In this paper, millennial-scale changes of paleoceanographic conditions during MIS-19 are discussed based on the results of this study and other proxies.

Methods
A total of 236 samples, including 195 new samples and 41 samples that were used for preliminary analysis in Suganuma et al. (2018), were processed for radiolarian analysis in this study (Supplementary   Tables 1 and 2). Sampling locations, stratigraphic framework and age models are based on Suganuma et al. (2018) and Haneda et al. (2020) (Supplementary Fig. 1).
Freeze-dried samples were weighed and wet sieved using 45 µm meshes, and then two types of slides were prepared for quantifying the abundance (Q-slide) and for faunal analysis (F-slide) based on the standard technique described in Itaki et al. (2018). Preservation level of the radiolarian fossil was checked as good (majority of specimens complete, with no or minor dissolution, recrystallization, and/or breakage), moderate (minor, but common dissolution, with a small amount of breakage of specimens) and poor (strong dissolution, recrystallization, or breakage, many specimens unidenti able).
The total number (abundance) of radiolarians in 1 g of dry sediment was estimated using the following equation: Total radiolarian abundance (individuals/g) = total number of individuals on Q-slide x 200 / sample weight (g) For the 153 of 195 samples newly collected in this study, the relative abundance (% of total assemblage) of the species was estimated by counting and identifying more than 300 individuals on the F-slide; however, when radiolarian individuals were scarce, as many as could be identi ed were counted (Supplementary Table 1). Radiolarians were observed under an optical microscope at x40 to x200 magni cation. Identi cations were made using a taxonomic framework adapted from Itaki (2009) and Matsuzaki and Itaki (2017).
In this study, we have estimated paleo SST using 2 different transfer equations based on modern dataset from surface sediments in the northwestern Paci c reported by Matsuzaki and Itaki (2017).
The transfer function method based on Q-mode factor analysis and multi-regression analysis established by Imbri and Kipp (1971) have been widely used for reconstruction of the paleo SST based on microfossil assemblages (IKM: Imbri and Kipp method). Matsuzaki and Itaki (2017) proposed a radiolarian-based transfer function equation for the estimation of summer SST from surface sediments in the northwestern Paci c. Totally 153 data from the CbCS newly reported in this study, which were counted for 30 species/species groups as much as possible to identify, were applied to the transfer function equation derived from dataset of Matsuzaki and Itaki (2017) using a statistical software package PAST (Harmer et al., 2001). In the CbCS, 9 species/species groups were recognized in which 30 species/species groups that Matsuzaki and Itaki (2017) regarded as surface dwellers, while other 21 species were absent or very rare. A transfer function to the summer SST based on 3 factors showing cumulative contribution of 96% indicates that correlation coe cient is 0.95 and error is ±1.27°C (Supplementary Table 3).
Another method for the SST reconstruction is the Tr value, which is a radiolarian-based climate index originally proposed by Nigrini (1970) that has the following simple equation using only limited indicator species: where Xw, Xt and Xc are the number of warm-, temperate-and cold-water radiolarian species and species groups, respectively. Suganuma et al. (2018) applied the Tr value to preliminary results from 41 samples of the CbCS, and data used to estimate Tr values in this study are listed in Supplementary Table 2. Furthermore, looking at the radiolarian data of Matsuzaki and Itaki (2017), which was compiled using the same radiolarian analysis method as in this study, we can see a correlation between Tr values and summer SST with r = 0.96 (Fig. 2). The following binomial equation derived from this relationship was applied to the CbCS results to estimate the paleo SST. Estimated error is ±1.57°C.

Results And Discussion
Total radiolarian abundance Radiolarian fossils were collected from all analyzed samples. Preservation level was moderate to good, and no in uence on assemblage and abundance is expected. Total radiolarian abundance ranged between 80 to 1,300 individuals/g with higher values during the peak of MIS-19c as reported in Suganuma et al. (2018). Further, periodic uctuations with about 2,000 to 3,000-year intervals were observed during the study period.
Generally, changes in the number of radiolarians that are secondary producers are closely related to primary production at the near sea-surface and can therefore be used as an indicator of relative productivity. In actual, the high number of radiolarians in surface sediments is recognized in the subarctic Paci c Ocean, Southern Ocean and equatorial upwelling zone, where biological productivity is high (Boltovskoy et al., 2010). According to total radiolarian ux changes from a time-series sediment trap deployed at Station N40 (40°N, 165°E) near the Kuroshio-Oyashio boundary in the northwestern Paci c show positive correlation (r=0.68) with total mass ux closely related to diatom ux (Okazaki et al., 2005). In Figure 3, TOC (total organic carbon) and Ca/Ti (calcium/titanium ratio), which are indicators of productivity obtained from the CbCS (Izumi et al., submitted), show a general tendency to increase with radiolarians in MIS-19. In addition, some of the short-cycle uctuations observed in radiolarians also show synchronized changes, but there are also periods of non-synchronization. Ca/Ti shows a peak value at 771 to 787 ka, and short-period uctuations observed in radiolarians are not con rmed. Ca/Ti is associated with an increase or decrease in shells of foraminifera and coccolith with carbonate skeletons, while radiolarians of secondary producers re ect overall biological production, including other producers. Therefore, short-period uctuations not recorded in carbonate would have been recorded in radiolarians. TOC, like radiolarian, re ects overall biological production. In fact, many short cycle variations appear to be synchronous with those of radiolarians. However, TOC maxima at 760 and 764 ka did not coincide with radiolarian peaks. According to Izumi et al. (submitted), these uctuations are interpreted as being due to oxygen-depleted bottom-water conditions. That is, oxygen consumed due to stagnation of the water mass improved the preservation of organic matter near the bottom.

Radiolarian assemblages
In this high-resolution analysis, a total of 30 species and species groups were counted (Supplementary  Matsuzaki and Itaki (2017), and these accounted for 5% to 45% of the radiolarian assemblage in the CbCS. At present, higher abundances of these groups occur in the Kuroshio Current where sea-surface temperatures range between 20 and 29°C (Matsuzaki and Itaki, 2017). On the other hand, S. resurgens, L. setosa and S. venustum characterize the cold-water mass of the Oyashio region, accounting for 7%-37% of radiolarians in the CbCS. These groups are associated with cold waters ranging from 12 to 18°C (Matsuzaki and Itaki, 2017). While warm-water species increased during MIS-19, cold-water species tended to increase in MIS-20 and MIS-18. The temperate species L. buetschlii shows variation similar to the cold-water assemblage. Larcopyle minor and Cycladophora davisiana are both deep dwellers adapted to middle and high latitudes in the North Paci c, respectively (Matsuzaki and Itaki, 2017).

SST reconstruction
Both reconstructions of paleo-SST based on IKM and Tr show good consistency each other (Supplementary Figure 2). Because IKM cannot to be applied for preliminary dataset of 41 samples reported by Suganuma et al (2018) due to limitation of counting categories (only 10 species/species groups), Tr based SST applied to all examined 194 data is used for discussion in this paper.
The Tr value was estimated using the indicator species shown in Supplementary Table 2 and Supplementary Figure 3, which were found in common in this study and in Suganuma et al. (2018). The Tr value uctuated considerably between 0.2 and 0.8 throughout the examined period, and the multiple maxima and minima likely re ect oscillations of the Kuroshio Current. Figure 3 shows summer SST variations in the CbCS converted from the Tr value. The water temperature varied from 16 to 27° C, and the lowest SST was observed at the end of MIS-20 (790-794 ka). This pattern is generally consistent with results from the oxygen isotope ratio of planktonic foraminifera Globigerina bulloides d'Orbigny (δ 18 O Gb ), except for during . Minor inconsistencies between summer SST and δ 18 O Gb during MIS-19c might be due to differences in the season in which these data were recorded; radiolarian-based SST is estimated as summer values, while it is expected that δ 18 O Gb is largely determined in spring based on the modern production season of G. bulloides reported from sediment trap experiments in the northwestern Paci c Ocean (Kuroyanagi et al., 2002).
Distinct millennial-scale uctuations ranging between 20 and 27°C were observed during MIS-19. The current summer SST near the Boso Peninsula is around 26°C, which almost corresponds to the highest value of the reconstructed temperature. On the other hand, the temperature was 20 to 24°C in cold periods of MIS-19, which corresponds to the current Fukushima-Sendai offshore. That is, most of MIS-19 was 2 to 6°C cooler than the present, suggesting the strong in uence of the Oyashio Current. Tanaka et al. (2017) reported that the annual SST ranged between 16 and 23°C during MIS-19 based on diatom fossil assemblages from core TB2, which was drilled near the CbCS. They noted that the SST shifted from the Oyashio phase to the Kuroshio phase at 770 ka; however, such a trend in the climatic shift was not observed in our record.
Millennial-scale Kuroshio uctuations during the interglacial state have also been reported from other interglacial periods. Holocene 1500-year cycles of the SST uctuations have been reported based on UK 37 (Isono et al., 2009) and diatom fossil assemblages (Koizumi, 2008) from a marine sedimentary core (MD01-2421), which were collected from the western Paci c at 36°N near the Boso Peninsula. In their studies, the amplitude of water temperature uctuation was estimated to be about 1°C. Yasudomi et al. (2014), who examined in detail the radiolarians of the last interglacial period (MIS-5e) using the same core, showed that the Tr value uctuated with a 500-year cycle. The Tr value (0.6-0.9) in their study corresponded to a range of 26 to 28°C according to the summer SST derived from the equation in this study. Thus, the water temperature in the Holocene and MIS-5e was higher and had a smaller uctuation than in MIS-19.

Relationship between productivity and SST
The millennium-scale productivity maxima inferred from the total radiolarian abundance tends to be during the warmer and cooler intervals that appeared after and before 785 ka, respectively (Fig. 3). The high productivity observed during cooler intervals observed at the end of MIS-20 and the earliest part of MIS-19 is likely affected by the high nutrient supply from the Oyashio water with a southward shift of the polar front (Fig. 4c), which is probably a response to the southward shift of the westerly jet with intensi cation of the winter Aleutian Low, as discussed by Suganuma et al. (2018) and Haneda et al. (2020). On the other hand, high productivity during warmer intervals during MIS-19 can be explained by decadal observations of modern oceanic conditions. Nishibe et al. (2015) proposed that high productivity is caused by development of favorable photosynthesis conditions with a layered structure, in which the high temperature Kuroshio water overlays the low temperature Oyashio water. In addition, the areal extent of the Kuroshio-Oyashio layered structure varies from year-to-year, and this interannual variability affects primary productivity, making it possible to relate these variations to inter-decadal climate regime shifts in the North Paci c (Nishikawa et al., 2016). Therefore, increases in productivity during warmer phases are periodically recognized during MIS-19 in the CbCS and are likely the result of the expansion and retreat of layered structures (Fig.4a, b).
The millennial-scale climatic changes during MIS-19 can also be recognized in records from the northern Atlantic Ocean (Kleiven et al., 2011) and central Europe Sánchez Goñi et al., 2016;Regattieri et al., 2019). Figure 5 shows the probable correlations between climate records for the Sulmona Basin in Italy Regattieri et al., 2019) and the CbCS in Japan (this study). Synchronous trends in each region suggest the strength of a large-scale teleconnection over the northern hemisphere of the Arctic Oscillation (AO) associated with winter Aleutian Low intensity (Tompson and Wallace, 1998) during MIS-19. The wet conditions in southern Europe were caused by the southern shift of westerly storm tracks during the negative phase of the AO. On the other hand, the Kuroshio transport increased with the intensi cation of the Aleutian Low during the negative AO (Deser et al., 1999). As shown in Figure 5, a consistent relationship is seen between paleo-records of humidity in southern Italy and the Kuroshio expansion in the CbCS during MIS-19.

Conclusions
High resolution radiolarian analysis for the MIS-19 period was performed on the Chiba composite section, including the Lower-Middle Pleistocene GSSP, and paleoceanographic changes were compared with geochemical proxies reported from the same section.
The total radiolarian abundance showed millennial-scale variations with a tendency for synchronized TOC and Ca/Ti, which is an effective proxy of productivity.
Surface water temperature records reconstructed from the assemblages varied between 19 and 26°C and tended to be synchronized with planktonic oxygen isotope records. The Younger Dryas-like event at the end of MIS-20 showed the lowest value, and millennia-scale uctuations ranging between 21 and 26°C were observed during MIS-19. SST during MIS-19 seems to have been slightly colder than during other interglacial periods such as the Holocene and MIS-5e.
High productivity with millennial-scale periodicity during MIS-19 tended to increase with the development of the layered Kuroshio-Oyashio structure during warm periods. This is likely related to expansion of favorable conditions for photosynthesis, such as the light environment, with the overlay of the warm Kuroshio water on the cold Oyashio water.
Millennial-scale uctuations in the surface water temperature during MIS-19 can be correlated with European climate changes Sánchez Goñi et al., 2016;Regattieri et al., 2019), and these are thought to have emerged as a result of atmospheric circulation teleconnection over a wide area. However, there are limited reports of high-resolution analysis in MIS-19, and it is expected that detailed teleconnection mechanisms will be elucidated by comparing analysis results over wide geographic areas. Authors' information TI is a senior researcher of Geological Survey of Japan (GSJ), AIST, Japan; SU is a master's course student at Chiba University and an AIST research assistant, Japan; YH is a post-doc fellow at Geological Survey of Japan (GSJ), AIST, Japan; KI is an assistant professor at Chiba University, Japan; YK is a researcher at the National Museum of Nature and Science, Japan; YS is an associate professor at NIPR, Japan; MO is a professor at Ibaraki University, Japan Maps showing (a) major ocean currents around Japan, (b) summer sea-surface temperature with location of Boso Peninsula, and (c) simpli ed geological map . Red stars in (c) indicate locations of the Urajiro, Yanagawa, Yoro River, Yoro-Tabuchi, and Kokusabata sections that comprise the Chiba composite section (CbCS).  Comparisons among paleoceanographic the following proxies: (on the left y-axis) Oxygen isotope record of planktonic foraminifera Globigerina bulloides from the Yoro River and Yoro-Tabuchi sections (thick line) and Kokusabata, Yanagawa and Urajiro sections of Haneda et al. (2020) (heavy orange line indicates moving average over 5 points), total radiolarian abundance (heavy black line indicates moving average over 5 points) and Ca/Ti ratio (heavy magenta line) and (on the right y-axis) Tr-based summer SST (dots with thin line for original data and heavy red line indicating moving average for 3 points) and total organic carbon (TOC) (heavy green line). Oxygen isotope records are from Haneda et al. (2020). TOC and Ca/Ti are from Izumi et al. (submitted). Pale yellow and green bands indicate intervals of radiolarian abundance maxima during warmer and colder periods, respectively.

Figure 4
Schematics of oceanographic conditions indicating (a) Oyashio phase likely present in late MIS-20 characterized by high productivity and low temperature, and (b) cooler phase in MIS-19 when the Kuroshio-Oyashio layered structure was contracted and (c) same conditions but with warmer phase with expanded layer structure. Figure 5