Balota et al. Progress in Earth and Planetary Science
https://doi.org/10.1186/s40645-021-00438-3(2021) 8:48

RESEARCH ARTICLE

Progress in Earth andPlanetary Science

Open Access

Paleoceanography and dinoflagellate cyst
stratigraphy across the Lower–Middle
Pleistocene Subseries (Calabrian–ChibanianStage) boundary at the Chiba composite
section, Japan
Eseroghene J. Balota1, Martin J. Head1* , Makoto Okada2, Yusuke Suganuma3,4 and Yuki Haneda5

Abstract
A dinoflagellate cyst record from the highly resolved Chiba composite section in Japan has been used to reconstructsea-surface paleoceanographic changes across the Lower–Middle Pleistocene Subseries (Calabrian–Chibanian Stage)boundary at the global stratotype, constituting the first detailed study of this microfossil group from the Pleistocene of
the Japanese Pacific margin. Cold, subarctic water masses from 794.2 ka gave way to warming and rapid retreat of the
Subpolar Front at 789.3 ka, ~ 2000 years before the end of Marine Isotope Stage (MIS) 20. Throughout the fullyinterglacial conditions of MIS 19c, assemblages are consistent with warm sea surface temperatures but also reveal
instability and latitudinal shifts in the Kuroshio Extension system. The abrupt dominance of Protoceratium reticulatum
cysts between 772.9 and 770.4 ka (MIS 19b) registers the influence of cooler, mixed, nutrient-rich waters of theKuroshio–Oyashio Interfrontal Zone resulting from a southward shift of the Kuroshio Extension. Its onset at 772.9 ka
serves as a local ecostratigraphic marker for the Chibanian Stage Global Boundary Stratotype Section and Point (GSSP)
which occurs just 1.15 m (= 1300 years) below it. An interval from 770.1 ka to the top of the examined succession at
765.8 ka (MIS 19a) represents warm, presumably stratified but still nutrient-elevated surface waters, indicating anorthward shift of the Kuroshio Extension ~ 5 kyrs after the termination of full interglacial conditions on land.
Keywords: Dinoflagellate cysts, Paleontology, Palynology, Paleoceanography, MIS 19, GSSP, Pleistocene, Chiba,
Chibanian, Japan

1 Introduction
The Chiba section, located in the central Boso Peninsula,
Chiba Prefecture, east-central Japan, serves as the Global
Boundary Stratotype Section and Point (GSSP) for the
Chibanian Stage and Middle Pleistocene Subseries (Head2019, 2021; Suganuma et al., in press). It is one of five sections comprising the Chiba composite section, an expanded and continuous silty marine sedimentary* Correspondence: mjhead@brocku.ca
1
Department of Earth Sciences, Brock University, St. Catharines, ON L2S 3A1,
CanadaFull list of author information is available at the end of the article

succession that bears excellent records of paleoceanographic and paleoclimatic change across the Early–Middle
Pleistocene boundary. The Chiba section (35° 17′ 39.6′′
N, 140° 08′ 47.6′′ E to 35° 17′ 36.9′′ N, 140° 08′ 47.2′′ E)
is a segment of the Yoro River exposure and is located 70
m west the Yoro-Tabuchi section (35° 17′ 48.1′′ N, 140°09′ 02.1′′ E to 35° 17′ 41.1′′ N, 140° 08′ 49.7′′ E) which
extends the composite section upwards (Fig. 1). The
Matuyama–Brunhes paleomagnetic reversal, whichfalls within Marine Isotope Stage (MIS) 19, represents
the primary guide to the Early–Middle Pleistocene
boundary (Head et al. 2008). The Chiba and Yoro-© The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License,
which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give
appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate ifchanges were made. The images or other third party material in this article are included in the article's Creative Commonslicence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commonslicence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain
permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 2 of 38

Fig. 1 Location of the Chiba and Yoro-Tabuchi sections examined in the present study. a Location of the Chiba section in the central Boso
Peninsula. Selected cities and the two nearby international airports of Haneda (Tokyo International Airport) and Narita (New Tokyo International
Airport) are shown. b Topography of the Yoro River in the vicinity of the Chiba and Yoro-Tabuchi sections. The Chiba section forms part of the
Yoro River section, and is continuous with the Yoro-Tabuchi section. All are part of the Chiba composite section. The Global Boundary Stratotype
Section and Point (GSSP) is located on the east bank of the Yoro River near where the power lines cross overhead (from fig. 8c of Suganuma
et al., in press). c Google Earth image of the square shown in (b). d Chiba section showing the position of the GSSP (red star) which defines theboundary between the Calabrian and Chibanian stages and Lower and Middle Pleistocene subseries (from fig. 10a of Suganuma et al., in press)

Tabuchi sections together yield one of the most detailed records available through MIS 19 and the
Matuyama–Brunhes paleomagnetic reversal (Head2021).
The Chiba composite section has been the subject ofnumerous micropaleontological studies, mostly involving
benthic and planktonic foraminifera, radiolarians,

calcareous nannofossils, and pollen (Kazaoka et al. 2015;
Suganuma et al. 2018; Kameo et al. 2020). Dinoflagellate
cysts have not previously been published from the Chiba
composite section or indeed at high temporal resolution
from any Pleistocene locality along the Pacific margin ofJapan. Dinoflagellates are protists and include phototrophic, heterotrophic, and mixotrophic species (Schnepf

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

and Elbrächter 1992). It is likely that most, if not all,phototrophic (chloroplast-bearing) dinoflagellates arealso capable of ingesting prey and are hence mixotrophic(Jeong et al. 2010). Dinoflagellates represent a significant
component of the modern plankton in the world’s
oceans. The resting stage, known as a cyst, is usually the
only part of the life cycle that is geologically preservable.
For species that produce organic-walled cysts, the outerwall withstands acid treatments and is studied in palynological preparations. Only ~ 13–16% of the ~ 2000 dinoflagellate species living today produce organic-walledcysts (Head 1996a; Penaud et al. 2018), but the modern
distributions of these cysts on the ocean floor demonstrate their sensitivity to a variety of sea-surface parameters including temperature, salinity, and nutrient levels.
They are therefore used widely to reconstruct pastoceanographic conditions (de Vernal et al. 2020).
Phototrophic dinoflagellates are confined to the photic
zone, and the heterotrophic dinoflagellates will also presumably be concentrated here where their prey is plentiful. The record of dinoflagellate cysts in sedimentaryarchives is therefore generally taken to represent seasurface conditions. Interpreting seasonal signals fromthe dinoflagellate cyst record is, however, more uncertain. Cyst-producing dinoflagellates in high northern latitudes bloom from spring through fall during a shortbiological summer, and are dormant as resting cysts during the winter months (Matthiessen et al. 2005). Nonetheless, sediment trap studies undertaken in lower
latitudes have shown that cyst production can occur atvarious time of the year, with different species producing
cysts at different times. A sediment trap study from theCariaco Basin off Venezuela linked cyst production totimes of seasonal, wind-driven upwelling, with both heterotrophs and phototrophs having greatest fluxes during
February through April and also to a lesser extent in July
(Bringué et al. 2019). A study from southwest Taiwan
waters in the South China Sea, which is influenced byboth the winter (March–April) and summer (July–
August) East Asian monsoons, showed increases in thefluxes of almost all taxa in July–August, reflecting increased river and nutrient input during the summer
monsoon (Li et al. 2018). In two embayments along thesouthern coast of South Korea, phototrophic cyst production was also found to be mostly restricted to thewarmest months (July–September) and the fall (Shinet al. 2012, 2018). Within the water column, motile cells
of Gonyaulax spinifera, which produce cysts assignable
to the cyst-defined genus Spiniferites, were found to belargely restricted to the months of March–August basedon a 5-year survey in the Yellow Sea of China (Liu et al.
2017). At Omura Bay, southwestern Japan, cyst fluxes ofheterotrophic species were found to be greatest in fall
and winter, correlating with the production of diatoms

Page 3 of 38

upon which they feed, whereas autotrophs occurred moregenerally through the year (Fujii and Matsuoka 2006) but
with Spiniferites species having greatest fluxes in the latespring and fall (Pospelova et al. 2018). Pospelova et al.
(2018) compiled the results of eight globally distributed
sediment trap studies, focusing on fluxes of the diverse
and widespread phototrophic genus Spiniferites. Theseauthors found that although the cyst fluxes of all species
responded in similar ways, they were not driven by auniform seasonal pattern. Local changes in hydrography
instead appeared to be the main triggers, with elevatedcyst production corresponding to conditions reflecting
minimal turbidity, availability of nutrients, some watercolumn stratification or stability, and an absence of
sea-ice (Pospelova et al. 2018). Significantly for the present
study, motile cells of Protoceratium reticulatum, anotherimportant cyst-producing species, were found to bepresent only during the summer months in the surface
waters off northeastern Japan (Koike et al. 2006, and see
below). It therefore appears that the Chiba dinoflagellate
cyst record reflects spring–fall sea-surface conditions atleast for some species, including the cysts of Protoceratium
reticulatum. It is possible or even likely, however, that theheterotrophs represent cooler-season conditions. Morestudies of the monthly production of motile cells and cysts
in the surface waters off eastern Japan are needed to gain
clearer insights into the seasonal signal carried by the
Chiba dinoflagellate cyst record.
Two dominant surface current systems meet today off
the Boso Peninsula: the warm and nutrient-depleted
Kuroshio Current flowing from the south, and the cold
nutrient-rich subarctic Oyashio Current flowing fromthe north. The Subarctic Front forms where the cold
Oyashio Current meets and descends beneath the Kuroshio Current. These currents mix to form a significant
latitudinal sea-surface temperature (SST) gradient that ismost pronounced off the Boso Peninsula (Fig. 2). These
two currents have been interacting since at least the
Pleistocene (Okazaki et al. 2010; Gallagher et al. 2015)
and their respective strengths and positions reflect
broader changes in the ocean–atmosphere system.
The present study aims to document the organicwalled dinoflagellate cyst record of the Chiba composite
section, and using modern species distributions reconstruct its paleoceanographic evolution from late MIS 20
to mid-MIS 19a. This study revises and expands uponan earlier unpublished study of the dinoflagellate cysts
from the Chiba composite section (Balota 2018). MIS
19c serves as an analogue for the present pre-industrial
interglacial, both having similar orbital configurations(e.g., Tzedakis et al. 2012; Yin and Berger 2012; Giaccio
et al. 2015; Vavrus et al. 2018; Nomade et al. 2019). The
Chiba composite section is therefore optimally positioned to capture the same interplay between theBalota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 4 of 38

Fig. 2 Present oceanography of the northwestern Pacific Ocean, showing annual sea-surface temperature and salinity from the World Ocean Atlas
2013 (Locarnini et al. 2013) drawn using Ocean Data View software (Schlitzer 2015). Major oceanographic features are included. TWC = Tsugaru Warm
Current. FOI = first Oyashio intrusion. SF = Subarctic Front formed by the Subarctic Current, an eastward extension of the Oyashio Current. KEF =Kuroshio Extension Front. KOIZ = Kuroshio–Oyashio Interfrontal Zone, a zone of mixing between the SF and KEF. TS = Tokara Strait. Adapted fromfig. 1 of Suganuma et al. (2018)

Kuroshio and Oyashio currents that is now observed off
the Boso Peninsula (Suganuma et al. 2018).
1.1 Chiba composite section

The Chiba composite section has been studied intensively and yields one of the most highly resolved marine
records of the Matuyama–Brunhes paleomagnetic reversal available (Suganuma et al. 2015; Okada et al. 2017;
Simon et al. 2019; Haneda et al. 2020a); this boundary
having already been chosen as the primary guide to the
GSSP (Head et al. 2008). The succession is astronomically dated both by high-resolution foraminiferal δ18O
stratigraphy (Okada et al. 2017; Suganuma et al. 2018;
Haneda et al. 2020b) and a zircon U-Pb age of 772.7 ±7.2 ka (Suganuma et al. 2015) obtained from the ~ 2cm-thick Ontake-Byakubi-E (Byk-E) tephra bed (Takeshita et al. 2016) which provides a local and regional
marker for the GSSP. The GSSP is dated astronomicallyat 774.1 ka and occurs just below the top of Marine Isotope Substage (MIS) 19c (Suganuma et al. 2018; Suganuma et al., in press). The directional midpoint of the
Matuyama–Brunhes boundary occurs 1.1 m above the
GSSP and has an astronomical age of 772.9 ka (Suganuma et al. 2018; Haneda et al. 2020a).
The Chiba composite section occurs within in theupper part of the Kokumoto Formation, Kazusa Group,and represents continuous and generally stable deposition on the continental slope of the eastern (Pacific)
margin of Japan. Trace fossil evidence suggests water
depths exceeding 800 to 1000 m (Nishida et al. 2016).
Along with high sedimentation rates of 89 cm/kyr at

the boundary, with no evidence of abrupt deposition,
this open-ocean setting allows the integration of bothmarine and terrestrial paleoenvironmental proxies(Suganuma et al. 2018). High-resolution benthic andplanktonic foraminifera δ18O and pollen records extend
from 801 ka in MIS 20 to 748 ka (752 ka for the pollen)
in MIS 18. All three substages of MIS 19 are recognizedin the benthic foraminiferal δ18O record (Haneda et al.
2020b). Following the substage characterization of
Nomade et al. (2019), MIS 19c corresponds to theonset (Termination IX) and warmest part of the stage(the MIS 19 plateau), MIS 19b to the first climatic
cooling, and MIS 19a to the most unstable part ofStage 19. The current Chiba composite section age
model is based on Suganuma et al. (2018) but uses
the full benthic foraminiferal δ18O benthic dataset ofHaneda et al. (2020b) to identify the positions ofstage and substage boundaries as follows: 787.5 ka(MIS 20–19c), 773.9 ka (MIS 19c–19b), 770.1 ka(MIS 19b–19a), and 756.9 ka (MIS 19a–18) with achronological uncertainty of ~5 kyr (Haneda et al.
2020b; Suganuma et al., in press). In addition, a significant sea surface and subsurface temperature drop
just prior to the onset of MIS 19 seems to represent
a Younger Dryas-type cooling event (Suganuma et al.
2018). The terrestrial climate as reflected in thepollen record largely mirrors these changes, with fullinterglacial conditions extending from 785.0 to 775.1± 5.0 ka with a duration of 9.9 kyr and so mostly coinciding with MIS 19c (Suganuma et al. 2018, inpress; Kameo et al. 2020; Kubota et al. 2021).

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Additional marine paleoenvironmental proxies obtained from the Chiba composite section, although at
lower stratigraphic resolution, include calcareous nannofossils, planktonic and benthic foraminifera, radiolaria,
and Mg/Ca subsurface (> 100 m) winter–spring
paleotemperature records from the planktonic foraminifera Globorotalia inflata (Suganuma et al. 2018).
1.2 Modern oceanographic setting

The waters off the Boso Peninsula are presently under
the influence of the subtropical Kuroshio Current, thesubarctic Oyashio Current, and the Tsugaru Warm
Current. The Oyashio Current descends beneath the
Kuroshio Current to form the Subarctic Front in thenorthwestern Pacific Ocean. A pronounced latitudinalsea-surface temperature (SST) gradient which is greatest
off the Boso Peninsula is created by the mixing of thesetwo currents (Fig. 2).
The Kuroshio Current is a western boundary current
that forms part of the wind-driven North Pacific Subtropical Gyre. It transports heat and salt from the IndoPacific Warm Pool into the higher latitudes of the North
Pacific. From its inception east of the Philippines, itflows northeast past Taiwan, into the East China Sea
where it follows the Okinawa Trough, through theTokara Strait, and then eastwards along the south coastof Japan where it follows a straight or meandering path(interannual bimodality) depending on the magnitude of
upstream transport (Qiu 2019). Off the Boso Peninsula
at around 35° N, the current diverts eastwards awayfrom the coast of Japan and forms the Kuroshio Extension system. Between 140° E and 160° E, the mean axisof the Kuroshio Extension is displaced interannually between 33.5° N and 35.5° N (Qiu 2019). The Kuroshio
Current off central Japan today has an annual mean sea
surface temperature (SST) and salinity (SSS) of 19–21 °C
and 34 psu, respectively (Locarnini et al. 2013; Zweng
et al. 2013). Southward latitudinal SST and SSS gradients
across the Kuroshio Extension are + 0.7 ± 0.2 (in August) to + 1.8 ± 0.7 (in December) °C/100 km and − 0.10
(in March) to − 0.19 (in September) psu/100 km, respectively (Kida et al. 2015). The surface waters of theKuroshio Current for most of the year are oligotrophic(kuro and shio in Japanese mean “dark current” with reference to the clear dark-blue waters lacking phytoplankton and detritus), although some nutrient mixing occurs
toward the end of winter for a few months. A nutrient
stream flows below the surface euphotic zone and is separated from it by a strong pycnocline. Nonetheless, sometransfer of nutrients to the euphotic zone occurs, particularly downstream (Komatsu and Hiroe 2019; Nagai
et al. 2019), and partly explains the rich pelagic fishstock occurring in the Kuroshio Current (Saito 2019).
This nutrient stream contributes significantly to the

Page 5 of 38

Kuroshio–Oyashio Interfrontal Zone (KOIZ) (Komatsu
and Hiroe 2019), where the Kuroshio Current mixes
with nutrient-rich waters of the Oyashio Current in theregion off central Japan today to create the strongest
latitudinal sea-surface temperature (SST) gradient in thenorthwestern Pacific Ocean.
The Oyashio Current is also a western boundary current
although within the wind-driven North Pacific Subpolar
Gyre (Qiu 2019). Its source area, the subarctic North Pacific, is dominated by upwelling and excessive precipitation over evaporation, making this a cold, low-salinity,
nutrient rich current. It is an extension of the East Kamchatka Current but receives input from the Sea of
Okhotsk which changes its properties so that elevateddissolved-oxygen values occur throughout its upper 700
m depth (Qiu 2019). Its name, Oya and shio in Japanesemeaning “parent current,” refers to the high biologicalproductivity it sustains. The Oyashio Current flows along
the east coast of Hokkaido and then bifurcates, with one
branch deflecting east-northeastwards as the Subarctic
Current. The southern margin of this current meets warm
saline waters from the south to generate the Subarctic
Front which has temperature and salinity values of 5°C
and 33.8 psu at a depth of 100 m. The other branch flows
southward along the east coast of Honshu as the first Oyashio intrusion and can be defined by the 5 °C isotherm at
100 m depth. Its southward penetration is influenced by
the seasonally-fluctuating Aleutian Low pressure systemand presently varies between 38.5° N in April and 41.5° N
in December, but also varies on interannual and longer
timescales (Qiu 2019). The first Oyashio intrusion potentially has a direct impact on the continental shelf andslope off the Boso Peninsula. Today off northern Japan at
42.5–43.5° N, the Oyashio Current has a modern annual
mean SST and SSS of 6–8 °C and 33.0 psu, respectively(Locarnini et al. 2013; Zweng et al. 2013). Southward latitudinal SST and SSS gradients across the Subarctic
Current are from + 2.0 ± 1.5 (in October) to + 3.3 ± 0.4(in April) °C/100 km, and − 0.35 (in April and December)to − 0.54 (in September) psu/100 km, respectively (Kidaet al. 2015).
In addition to the Kuroshio and Oyashio currents, theTsugaru Warm Current influences the waters off the
Boso Peninsula. The Tsugaru Warm Current is an extension of the Tsushima Current, itself a branch of theKuroshio Current, and flows from the Sea of Japanthrough the Tsugaru Strait. It then flows southward
along the eastern coast of Honshu, and landward of thefirst Oyashio intrusion. It contrasts with Oyashio watersin having warmer temperatures (greater than ~ 6 °C)
and relatively high salinities (33.7–34.2) (Hanawa and
Mitsudera 1986).
The latitudinal displacement of oceanic fronts in themodern North Pacific, including the subpolar front,

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

derives from changes in the position and intensity ofprevailing westerly winds. These changes appear to belinked to the decadal variability of the Aleutian Low, alow-pressure atmospheric system that develops aroundthe Aleutian Island in the North Pacific during winter.
When the Aleutian Low intensifies (weakens), it causes asouthward (northward) shift in the subpolar front (Taguchi et al. 2012). This relationship has been used to explain variations in winter SST reconstructions throughthe Chiba composite section (Suganuma et al. 2018;
Haneda et al. 2020b; Kubota et al. 2021).
1.3 Previous mid-Pleistocene dinoflagellate cyst studies
along the Pacific margin of JapanNo previous stratigraphically detailed dinoflagellate cyst
studies of the mid-Pleistocene from the Pacific marginof the Japanese islands are known. However, Harada(1984) presented a relatively low-resolution record of six
cores taken from Osaka Bay, about 470 km west of the
Chiba locality. The deposits belong to the Osaka Groupand include the Azuki tephra bed which has been correlated with MIS 21 (Kazaoka et al. 2015). These deposits
should include the interval represented by the Chiba
composite section. Osaka Bay today is more fully under
the influence of the Kuroshio Current than the Chiba locality. The dinoflagellate cyst assemblages reflect fluctuating nearshore restricted marine paleoenvironments, as
might be expected. Some assemblages are dominated by
Polysphaeridium zoharyi which today thrives in warm,
hypersaline nearshore paleoenvironments (Zonneveld
et al. 2013). Harada (1984) reported Lingulodinium
machaerophorum, the Spiniferites group, the cysts ofProtoceratium reticulatum (as Operculodinium centrocarpum), and protoperidiniacean cysts as varying usually
between subordinate and co-dominant in abundance,with Tuberculodinium vancampoae rare to common inmost samples but occasionally dominant. Hystrichokolpoma sp. was reported outside of the published counts(Harada 1984). In general, this dinoflagellate cyst record
does not compare closely with that of the Chiba composite section.
1.4 Modern North Pacific dinoflagellate cyst distributions

Dinoflagellate cyst distributions in modern sediments of
the North Pacific and its adjoining seas are well documented as follows: west coast of Mexico, 15–25° N (Kielt
2006; Vásquez-Bedoya et al. 2008; Limoges et al. 2010);
northeastern Pacific margin, 25–43° N (Pospelova et al.
2008) and 40–60° N (Radi and de Vernal 2004); eastern
Bering and Chukchi seas (Radi et al. 2001); North Pacific, 64–37° N, including the Gulf of Alaska, Bering Sea,
western subarctic gyre, Okhotsk Sea, and central North
Pacific both north and south of the Subarctic Front(Bonnet et al. 2012); and the South China Sea, 22–4° N

Page 6 of 38(Kawamura 2002, 2004; Li et al. 2020). These large datasets are mostly concentrated around the continental
margins and adjoining seas. They are based on standardized laboratory processing and taxonomic methodologies(de Vernal et al. 2020) that allow their basin-wide integration. In addition, the Yellow Sea and East China Sea,
36–29° N, have also been documented (Cho and Matsuoka 2001), and smaller-scale and coastal studies along
the western margin of the North Pacific (e.g., Matsuoka
1976 and references therein, 1985, 1987, 1992 and references therein; Pospelova and Kim 2010 and references
therein) also provide valuable although more localized
information. For example, the small-scale study of surface samples off Hachinohe, northeastern coast of Honshu by Matsuoka (1976) provides useful information on
dinoflagellate cyst assemblages influenced by the Tsugaru Warm Current and Oyashio Current. A small-scale
study of Akkeshi Bay and Lake Saroma in Hokkaido,
northern Japan, similarly provides important informationon the influence of the Oyashio Current in this area
(Matsuoka 1987).
Although a gap in these large datasets includes muchof offshore eastern Japan today, the database along thenorthern and western margins of the Pacific is sufficient
to allow the characterization of assemblages associatedwith the warm nutrient-depleted Kuroshio Current andthe cold, nutrient-rich low-salinty Oyashio Current.
These two currents will have provided the main ecological controls on dinoflagellate cyst assemblages in the
Chiba composite section across the Early–Middle Pleistocene boundary, and their influence should therefore be
detectable in the Chiba record.

2 Materials and methods
2.1 Samples

In total, 107 samples from late MIS 20 to mid-MIS 19a
were processed for marine palynology from the Chiba
and Yoro-Tabuchi sections of the Chiba composite section (Fig. 3). Sample numbers are prefixed TB (Chiba
section, formerly known as the Tabuchi section) or TB2(Yoro–Tabuchi section). Samples were collected under
the direction of MO and are subsamples of those used
for foraminiferal isotope and pollen analysis (Okada
et al. 2017; Suganuma et al. 2018; Haneda et al. 2020b).
Seventy samples are from the Chiba section: samples
TB145 to TB2 taken from − 14.5 to − 0.15 m (− 12.25 to− 0.15 m excluding sand [turbidite] layers) below the
Byk-E tephra bed and representing 794.21–774.31 ka.
Thirty-seven samples are from the Yoro-Tabuchi section: samples TB2-34 to TB2-00 and TB2-39 to TB2-109
taken from 0.15 to 7.40 m above the Byk-E tephra bed
representing 773.97–765.80 ka. The samples therefore
span a total stratigraphic thickness of 19.65 m (excluding
turbidite layers) and are dated from 794.21 to 765.80 ka

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Fig. 3 Samples used in the present study. The lithology is from fig. 4of Suganuma et al. (2018) and paleomagnetic polarity record from
Okada et al. (2017) and Haneda et al. (2020a). The vertical scale (inm) represents stratigraphic distance from the Byk-E tephra bed. The
GSSP is located at the base of the Byk-E tephra in the Chiba section
which is part of the Yoro River section (Fig. 1). The Yoro-Tabuchi
section is located about 70 m northeast (Fig. 1) and correlated bytephra beds

with a duration of 28,400 years using the age model of
Suganuma et al. (2018).
Most samples in the present study were taken at 20
cm intervals representing ~ 324 years on average. Somesamples within Termination IX, the interval from − 8.5
to − 5.9 m below the Byk-E bed and ranging in age from
791 to 785 ka, are spaced at ~ 10 cm intervals to improve resolution across this important climatictransition.
2.2 Sample processing

Samples were processed at Brock University following
standard protocols, as follows. Each sample was dried
and weighed. A total of 10 g of sediment was treatedwith room temperature 7.5% HCl for several hours, androom temperature 38% HF for ~ 2 days with thrice-daily
swirling, and neutralization steps using distilled water.

Page 7 of 38

No acetolysis, alkali, oxidation, ultrasound, or othertreatments were used. One tablet of Lycopodium clavatum spores (batch number 1031 containing on average
20,848 spores per tablet; Department of Geology, Lund
University, Sweden) was added to the organic residue,
which was vigorously mixed and then sieved through a
10-μm nylon mesh. Tablets containing Lycopodium clavatum spores are introduced to residues for the purposeof estimating palynomorph concentrations (see below).
The spores are darkened by acetolysis during the manufacturing process, and this appears also to increase theirpropensity to take up stain. These introduced sporescannot then be confused with any in-situ Lycopodium
clavatum spores that may occur naturally in thesamples.
Sieved residues were stained with safranin-o andmounted on microscope slides using glycerine jelly following an adaptation of the method described by Evitt(1984). No oxidation, alkali or ultrasound treatments
were applied. At least two slides were made from the >10 μm sieved residue of each sample for counting underthe microscope. The residues from selected samples
were also sieved at 20 μm and microscope slides madefor morphologic/taxonomic analyses. In addition, surplus residues from samples TB2-22, TB2-00, TB2-97
were heated to ~ 80 °C in a 3% wt. solution of sodium
hexametaphosphate for 1 h, ultrasonicated for 1 min,and sieved at 10 μm and 20 μm. This treatment, whichremoved some of the amorphous organic material andconcentrated the cysts, did not noticeably affect the cyst
morphology. These samples were used primarily formorphological studies, and the resulting microscopeslides bear the suffix MJH. All surplus residues werestored in vials containing glycerine to which one drop ofliquefied phenol had been added to prevent microbial
growth.
2.3 Microscopy

Microscope slides were examined under a Leica DM
2500 transmitted light microscope by EB, with routine
counting performed on the 10-μm slides using a dry 40×
objective lens. A 100× oil immersion objective lens wasused for detailed morphological analysis and critical
identification of small palynomorphs. Dinoflagellate cysts
and acritarchs were counted to the highest taxonomic
level possible (see below). Benthic microforaminiferal
linings were counted only when containing at least six
chambers to avoid over-representation owing to fragmentation (Traverse and Ginsburg 1966). Most samples
were counted until at least 300 in-situ dinoflagellate
cysts had been enumerated. For 16 samples with low
dinoflagellate cyst concentrations, at least 200 specimens
were counted; and nine samples yielded fewer than 200
counts, even after scanning up to three slides for each.

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 8 of 38

Most samples yielded counts of at least 100 Lycopodium
clavatum spores.
A 10-μm slide for each sample was also examined
under a 40× objective lens by MJH to estimate qualitatively the relative abundance of terrestrial (mostly woody
and cuticular plant tissues) versus marine (amorphousorganic matter: AOM) components of the organic residue (Fig. 14g, h). These two broad categories were labeled as dominant, abundant, common, moderate, rare,or trace, to provide a first-order approximation of thepalynofacies. The dominant component of each sample
is shown in Figs. 16, 18c, and 19h. AOM is a common
constituent of marine sediment. Its relatively structureless appearance owes to the unicellular algae that dominate marine biomass and for which resistant structural
tissues are often unnecessary (Tyson 1995). AOM canalso result from the degradation of terrestrial plant matter, although typically in such circumstances some original structure remains and particles would be present
showing a transition between weakly and strongly degraded plant matter. In the Chiba section, the AOM iswell preserved and “fluffy” in texture with abundant minute inclusions (Batten 1996), and no features suggestinga terrestrial source were observed. Marine dinoflagellate
cysts were sometimes enclosed in this AOM (e.g., Fig. 8d,e, g–i) and it was also occasionally found within the central bodies of the cysts themselves (e.g., Fig. 4j–l); thisintimate association supporting the interpretation of amarine origin for the AOM.
Specimens were photographed under bright field illumination by MJH using a Leica DMR microscope
equipped with a Leica DFC550 digital camera, and are illustrated in Figs. 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, and 14.

belong overwhelmingly to the genus Brigantedinium but
because of folding, an archeopyle was seldom clearly observed and we cannot exclude the possibility that diplopsalid species bearing theropylic archeopyles (e.g., see
Mertens et al. 2020) are also represented. On rare occasion where the archeopyle could be seen clearly, Brigantedinium simplex and Brigantedinium cariacoense(Fig. 9g) were both identified. Specimens of Spiniferites
mirabilis (Fig. 5g–i) were identified as such regardless ofwhether the characteristic antapical flange was seen or
not, as this feature is not always visible in polar orientations. Spiniferites pachydermus sensu Mertens et al.
(2015) described from modern sediments of İzmir Bay,
Turkey has a distinctive central body surface layer that isdensely perforated, identical with that seen in the Chiba
specimens (Fig. 6a–i, Fig. 7a–c). Spiniferites pachydermus described by Rossignol (1964) from the Pleistocene
or Holocene of the Ashdod borehole, coastal plain,
Israel, was described as having a thick central body wall
(Rossignol 1964) but details of its structure and surface
are not known, as discussed in Mertens et al. (2018).
The Chiba specimens are considered not to belong toSpiniferites pachydermus sensu stricto. Spiniferites spp.
group A refers to several species with a thin central bodywall and a smooth or weakly ornamented surface, andinclude Spiniferites cf. belerius (Fig. 5d–f) and Spiniferites bulloides. Owing to crumpling and unfavorable
orientation, these specimens were grouped during
counting as Spiniferites spp. group A. All other Achomosphaera and Spiniferites species are grouped as Achomosphaera + Spiniferites spp. indeterminate.
The taxonomy of the marine acritarch Nanobarbophora walldalei (Fig. 14a–c) follows Head (1996b, 2003).

2.4 Taxonomy

2.5 Statistical analyses

The present study largely follows the taxonomy of Van
Nieuwenhove et al. (2020), Mertens et al. (2020), and Limoges et al. (2020) for the dinoflagellate cysts, exceptthat the cosmopolitan cyst morphotype (Fig. 8j–l,
Fig. 9a–c) known in the Quaternary literature as Operculodinium centrocarpum sensu Wall and Dale (1966) isgiven its non-fossil name Protoceratium reticulatum following Paez-Reyes and Head (2013). It should not be
confused with the larger and more robust Operculodinium centrocarpum sensu stricto (Fig. 8d, e), originallydescribed from the Miocene of Australia (Deflandre andCookson 1955). Selenopemphix undulata (Fig. 11f–i)
was not always easy to separate from Selenopemphix
nephroides (Fig. 11d, e) owing to the weakly expressed
undulations on the cingular crests of some specimens.
They were grouped as Selenopemphix nephroides +undulata in the counts. Owing to variable preservation,
all smooth-walled round brown acavate cysts were labeled as “round brown cysts.” They are assumed to

The concentrations (specimens per gram dry weight) of
palynomorphs (Fig. 16) were estimated using the methodof Stockmarr (1971), and the taxonomic richness andevenness of samples were also calculated (Fig. 16).
The taxonomic richness of a sample is the total number of taxa recorded in that sample. In the present study,
this represents the number of dinoflagellate cyst taxa recorded in the count (usually ~ 300 specimens) for eachsample.
Taxonomic evenness quantifies how equal taxa are ina sample, and greatest evenness is where all taxa in asample share the same abundance. This study uses the
Simpson D index which is not sensitive to taxonomic
richness and is one of the most meaningful and robust
diversity measures available (Magurran 2004). It is usually expressed as 1/D and ranges from 0 to 1 where
higher values indicate greater evenness. To calculate
taxonomic evenness, it is necessary first to derive Simpson’s D = ∑ pi2 where pi is the proportion of each taxon

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 9 of 38

Fig. 4 Dinoflagellate cysts from the Chiba composite section. Max. dia. = maximum diameter. EF = England Finder reference. a Tuberculodinium
vancampoae, polar view at upper focus; cyst max. dia. 122 μm; sample TB 16, slide 1 (20 μm), EF E25/4. b Polysphaeridium zoharyi, apical view of
hypocyst at upper focus; central body max. dia. 52 μm; sample TB 98, slide 1 (10 μm), EF E20/1. c, d Lingulodinium machaerophorum, dorsal viewat upper and mid-foci; central body max. dia. 58 μm; sample TB2 99, slide 1, EF E36/0. e, f Impagidinium aculeatum, uncertain view at upper- andmid-foci; central body max. dia. 35 μm; sample TB2 26, slide 1, EF E20/3. g–i Impagidinium paradoxum, antapico-dorsal view at upper, mid-, andlower foci; central body length 26 μm; sample TB2 30, slide 2, EF K26/3. j–l Impagidinium patulum, dorsal view at upper, mid-, and lower foci;central body max. length 63 μm; sample TB 92, slide 1, EF Q34/4

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 10 of 38

Fig. 5 Dinoflagellate cysts from the Chiba composite section. Max. dia. = maximum diameter. EF = England Finder reference. a–c Nematosphaeropsis
labyrinthus, equatorial view at upper, mid-, and lower foci showing nearly smooth central body surface; ectophragm max. dia. 52 μm, central bodymax. dia. 27 μm; sample TB2 97, slide 2 (10 μm) MJH, EF J17/2. d–f Spiniferites cf. belerius, dorsal view at upper, mid-, and slightly lower foci; central
body length 31 μm; sample TB2 97, slide 3 (20 μm) MJH, EF T21/3. g–i Spiniferites mirabilis, equatorial view at upper, mid-, and lower foci; central bodylength 62 μm; sample TB 16, slide 1 (10 μm), EF V17/4

in a sample. Then, Simpson’s measure of evenness (E1/D)
is calculated by dividing the reciprocal form of D by the
number of taxa in the sample:
E1/D = (1/D) / S
where S = total number of taxa present in the sample(Magurran 2004).

3 Results
All 107 samples were found to contain dinoflagellate
cysts. A total of 29 in-situ dinoflagellate cyst taxa werecounted along with the acritarch Nannobarbophora
walldalei. The full names of all taxa reported and theirsystematic classification are listed in Table 1. Taxa are

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 11 of 38

Fig 6 Dinoflagellate cysts from the Chiba composite section. Max. dia. = maximum diameter. EF = England Finder reference. a–i Spiniferites
pachydermus sensu Mertens et al. (2015) showing distinctive irregularly perforate surface ornament; a–d left lateral view at upper to lower foci;central body length 49 μm; sample TB2 00, slide 1 (10 μm), EF D11/2; e–i right lateral view at upper through lower foci; note irregular surface
perforations in i; central body length 57 μm; dark ovoidal body in lower center is 5.8 μm long; sample TB 16, slide 1 (20 μm), EF E26/1. Scale bar
on g = 2 μm

illustrated in Figs. 4, 5, 6, 7, 8, 9, 10, 11, 12, 13, 14. The
relative abundances of all counted taxa are plotted inFig. 15. Dinoflagellate cyst concentrations per gram dryweight, taxonomic richness and evenness of dinoflagellate cyst assemblages, and the concentrations per gramdry weight of benthic microforaminiferal linings are all

given in Fig. 16. All raw counts and calculated values are
given in Additional file 1.
The preservation of dinoflagellate cysts varies from goodto moderate, with specimens often affected by some folding/compression and breakage, and the heterotrophs sometimes showing partial corrosion. Some specimens haveBalota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 12 of 38

Fig. 7 Dinoflagellate cysts from the Chiba composite section. Max. dia. = maximum diameter. EF = England Finder reference. a–c Spiniferites pachydermus
sensu Mertens et al. (2015), dorsal view at upper (operculum in place), slightly lower and mid-focus; note apical protuberance and preserved endospore (arrow);
central body length 43 μm, central body width 38 μm; sample TB2 00, slide 1 (10 μm) MJH, EF V16/4. d, e Spiniferites ramosus sensu Rochon et al. (1999),
ventral-left-lateral view at upper and lower foci; central body length 33 μm; sample TB2 97, slide 3 (20 μm) MJH, EF M32/4. f, g Spiniferites sp. (a representative of
Spiniferites spp. group A), apical view at upper and mid-foci, note preserved endospore (arrow); central body max. dia. 30 μm; sample TB2 97, slide 2 (10 μm)
MJH, EF F13/0. h, i Spiniferites sp. B, view uncertain at upper and mid-foci; thin wall with distinctly granular periphragm surface; some processes tips petaloid;
central body length 56 μm; sample TB2 97, slide 3 (20 μm) MJH, EF D34/0

preserved endosperms (Fig. 7b, g). Cyst concentrations varyfrom 907 to 317,932 cysts per gram dry weight. Opaquemineral inclusions, presumably diagenetic pyrite, were
found in all samples. The palynofacies are characterizedthroughout by common to dominant terrestrial components, mostly woody and cuticular tissues but also sporesand pollen (Fig. 14g). Marine AOM (Fig. 14h) dominates or

co-dominates much of the interval from sample TB 63(786.60 ka) to TB2 24 (772.85 ka). Dinoflagellate cysts are a
relatively minor component of the palynofacies, and counting them is hence very time consuming for most samples.
Few reworked dinoflagellate cysts were recognized; themost distinctive being specimens of the genus Cleistosphaeridium (Fig. 14d–f) which occur as isolated

Balota et al. Progress in Earth and Planetary ScienceFig. 8 (See legend on next page.)(2021) 8:48

Page 13 of 38

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 14 of 38(See figure on previous page.)
Fig. 8 Dinoflagellate cysts from the Chiba composite section. Max. dia. = maximum diameter. EF = England Finder reference. a–c Pyxidinopsis
reticulata, unknown view at upper through mid-foci; max. dia. (excluding ornament) 35 μm, max. crest height ~ 1.0 μm; sample TB 16, slide 1 (10μm), EF S21/1. d, e Operculodinium centrocarpum sensu stricto, view uncertain, upper and mid-focus; processes have expanded fibrous bases andaculeate tips; central body wall ~ 1.0 μm thick with thick spongy-fibrous periphragm; central body length 59 μm; sample TB 78, slide 2 (10 μm),
EF H20/1. f–i Operculodinium israelianum, apical? view; upper through mid-foci; note solid fibrous processes that may be acuminate or minutely
expanded distally; central body max. dia. 45 μm; sample TB 88, slide 2 (10 μm), EF W37/4. j–l cyst of Protoceratium reticulatum, dorsal view at
upper, slightly lower, and mid-foci; central body max. dia. 37 μm; sample TB2 61, slide 1 (10 μm), EF O18/3

Fig. 9 (See legend on next page.)

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 15 of 38(See figure on previous page.)
Fig. 9 Dinoflagellate cysts from the Chiba composite section. Max. dia. = maximum diameter. EF = England Finder reference. a–c cyst of Protoceratium
reticulatum, ventral view at upper, slightly lower, and mid-foci; b showing characteristic rounded adapical margin of detached operculum, also in ventral view,
within cyst; central body max. dia. 40 μm; sample TB2 00, slide 3 (10 μm) MJH, EF Q9/4. d–f Operculodinium? longispinigerum, view uncertain; note finely
granulate central body surface, solid tapering processes, somewhat flexuous with finely granulate surfaces distally and with circular bases; central body max. dia.
33 μm; sample TB 58, slide 1 (10 μm), EF J10/1. g Brigantedinium cariacoense, ventral view at mid-focus on archeopyle; cyst max. dia. 38 μm; sample TB 34, slide
1 (10 μm), EF H40/0. h, i Brigantedinium sp., dorsal view at mid- and lower focus; cyst max. dia. 36 μm; sample TB 72, slide 1 (10 μm), EF K38/1

Fig. 10 Dinoflagellate cysts from the Chiba composite section. Max. dia. = maximum diameter. EF = England Finder reference. a–c Lejeunecysta
sp. A, dorsal view at upper, mid-, and lower foci; cyst length 67 μm; sample TB 50, slide 2 (10 μm), EF O40/3. d–f Lejeunecysta sp. B, ventral viewat upper, mid-, and lower foci; cyst length 78 μm; sample TB2 59, slide 2 (10 μm), EF R37/1. g–i Quinquecuspis concreta, ventral view at upper
through lower foci; cyst length 75 μm; sample TB 16, slide 2 (10 μm), EF N37/0

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 16 of 38

Fig. 11 Dinoflagellate cysts from the Chiba composite section. Max. dia. = maximum diameter. EF = England Finder reference. a–c Selenopemphix
quanta, antapical view at upper, mid-, and lower foci; central body width 75 μm, height 76 μm; sample TB2 97, slide 3 (20 μm) MJH, EF N13/3. d,e Selenopemphix nephroides, polar view at mid- and lower foci; cyst max. dia. 58 μm; sample TB 66, slide 2 (10 μm), EF G36/3. f–i Selenopemphix
undulata; f, g antapical view at upper and lower foci showing weak cingular crest undulations; cyst width 49 μm; sample TB 12, slide 1 (20 μm),
EF L29/3; h, i antapical view at upper and lower foci showing pronounced cingular crest undulations; cyst max. dia. 56 μm; sample TB 114, slide 1(10 μm), EF O33/1

specimens (Additional file 1). These specimens have
similar preservation to the in-situ cysts, and are considered reworked primarily because Cleistosphaeridium is a
predominantly Eocene–Miocene genus (Eaton et al.
2001).
All assemblages are dominated by neritic taxa, withspecimens of the oceanic genus Impagidinium (Fig. 4e–l) and oceanic Nematosphaeropsis labyrinthus (Fig. 5a–c) occurring sporadically and usually rarely. Based on aqualitative assessment of the in-situ dinoflagellate cyst

assemblages, cyst concentrations, and abundance of theacritarch Nanobarbophora walldalei, eight informal assemblage biozones (Fig. 11) are described in ascending
stratigraphic order, as given below, with sample depths
expressed as meters below or above the Byk-E tephra
bed and astronomical ages based on Suganuma et al.
(2018, in press). Qualitative observations on the palynofacies are given for each (sub)biozone, and the dominant
palynofacies component for each sample is shown on
Figs. 16, 18c, and 19h.

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 17 of 38

Fig. 12 Dinoflagellate cysts from the Chiba composite section. Max. dia. = maximum diameter. EF = England Finder reference. a–d
Trinovantedinium applanatum; a, b dorsal view at upper and lower foci; central body max. length 71 μm, width 72 μm; sample TB2 97, slide 2 (10μm) MJH, EF L28/0; c, d dorsal view at upper and mid-foci; central body max. length 72 μm, width 67 μm; sample TB2 97, slide 2 (10 μm) MJH, EF
Q24/2. e–i Trinovantedinium cf. harpagonium showing flattened bifurcate process terminations with strongly recurved tips; e, f ventral view at
mid- and slightly lower focus; central body length 57 μm, width 50 μm; sample TB2 97, slide 4 (20 μm) MJH, EF G15/0; g–i ventral view at upper
through lower foci; central body length 49 μm; sample TB 92, slide 1 (10 μm), EF W43/1

3.1 Dinoflagellate cyst assemblage biozone 1 (Df1)

Samples: TB 145–92; depth − 14.5 to − 9.18 m (− 12.25
to − 9.18 m without sand [turbidite] layers); age 794.21–
791.72 ka; upper MIS 20.
Description: Heterotrophs in general, and roundbrown cysts (76–93%) in particular, dominate assemblages and have their highest sustained abundance (upto 95%) in this biozone. The heterotroph Selenopemphix

quanta (1.3–9.7%) is the second most abundant species,
followed by Selenopemphix nephroides + undulata (0–3.1%). Phototrophic species are rare throughout, and include Spiniferites spp. group A (1.3–7.4%). Cyst concentrations fluctuate from 907 to 2464 cysts/g. All samples
are dominated by plant tissues and terrestrial sporomorphs, with marine AOM occurring in trace to rare
quantities in nearly all samples.

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 18 of 38

Fig. 13 Dinoflagellate cysts from the Chiba composite section. Max. dia. = maximum diameter. EF = England Finder reference. a, b Xandarodinium
xanthum, uncertain view at upper and lower foci; central body max. dia. 52 μm; sample TB 18, slide 1 (10 μm), EF F22/2. c–f Echinidinium aculeatum; c,d uncertain view at upper and lower foci; central body max. dia. 27 μm; sample TB 42 slide 1 (10 μm), EF N29/2; e, f uncertain view at upper and lower
foci; central body max. dia. 23 μm; sample TB 16, slide 2 (10 μm), EF E42/0. g–i Cyst of Scrippsiella trifida, lateral view at upper, mid-, and lower foci;central body length 29 μm; sample TB 56, slide 2 (10 μm), EF R39/3

3.2 Dinoflagellate cyst assemblage biozone 2 (Df2)

3.3 Sub-biozone Df2a

Samples: TB 90–59; depth − 8.98 to − 5.85 m; age
791.55–785.47 ka; upper MIS 20–lower MIS 19c.
Description: This biozone spans Termination IX and ismainly characterized by a progressive decline in the relative
abundance of round brown cysts from 92 to 29% and an
overall rise in Selenopemphix quanta from 1.7 to 18%. Biozone 2 is subdivided into sub-biozones Df2a, Df2b, and Df2c.

Samples: TB 90–80; depth − 8.98 to − 8.00 m; age
791.55–790.32 ka; upper MIS 20.
Description: This subzone begins with a sharp drop
and then rise in round brown cysts (48–61%) and acorresponding rise and then drop in Spiniferites spp.
group A (12–22%). There is a slight increase also in
Spiniferites mirabilis (2.1–7.3%), the cysts ofBalota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 19 of 38

Fig. 14 An acritarch (a–c), a presumed reworked dinoflagellate cyst (d–f), and palynofacies (g, h) from the Chiba composite section. Max. dia. =maximum diameter. EF = England Finder reference. a–c Nannobarbophora walldalei, uncertain view at upper, mid-, and lower foci; central bodymax. dia. 29 μm; sample TB2 30, slide 2 (10 μm), EF E15/3. d–f Cleistosphaeridium placacanthum (presumed reworked), apical view at upper, midand lower foci showing granulate central body surface with well-developed penitabular ridges; central body max. dia. 53 μm; sample TB 114,
slide 1 (10 μm), EF P16/4. g, h Organic residue sieved at 10 μm showing (g) terrestrially dominated (sample TB2 105, slide 1, EF D21/4) and (h)AOM-dominated (sample TB 14, slide 1, EF D22/0) palynofacies; cyst = dinoflagellate cyst, AOM = amorphous organic matter, PT = plant tissues(woody tissues and cuticle); scale bar = 20 μm

Protoceratium reticulatum (3.1–7.3%), and Operculodinium israelianum (0–3.5%). Nematosphaeropsis labyrinthus rises to 7.3% near the base of this subzone. Insitu cyst concentrations fluctuate from 1024 to 1825

cysts/g. All samples are dominated by plant tissues
and terrestrial sporomorphs, with marine AOM occurring in rare to moderate quantities in most
samples.

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 20 of 38

Table 1 Dinoflagellate cyst and acritarch taxa recorded in the present study, and their classification and authorial attributions. All
taxa are considered in situ with the exception of the genus Cleistosphaeridium which is presumed reworked
Subclass PERIDINIPHYCIDAE Fensome et al., 1993
Order GONYAULACALES Taylor, 1980
Suborder GONIODOMINEAE Fensome et al., 1993
Family PYROPHACACEAE Lindemann, 1928
Subfamily HELGOLANDINIOIDEAE Fensome et al., 1993
Genus Tuberculodinium Wall, 1967
Tuberculodinium vancampoae (Rossignol, 1962) Wall, 1967. Fig. 4a.
Subfamily PYRODINIOIDEAE Fensome et al., 1993
Genus Polysphaeridium Davey and Williams, 1966 emend. Bujak et al., 1980
Polysphaeridium zoharyi (Rossignol, 1962) Bujak et al., 1980. Fig. 4b.
Suborder GONYAULACINEAE (Autonym)
Family GONYAULACACEAE Lindemann, 1928
Subfamily GONYAULACOIDEAE (Autonym)
Genus Achomosphaera Evitt, 1963
Achomosphera spp. indet. Grouped with Achomosphera+Spiniferites spp. indet. in the counts.
Genus Impagidinium Stover and Evitt, 1978
Impagidinium aculeatum (Wall, 1967) Lentin and Williams, 1981. Fig. 4e, f.
Impagidinium paradoxum (Wall, 1967) Stover and Evitt, 1978. Fig. 4g–i.
Impagidinium patulum (Wall, 1967) Stover and Evitt, 1978. Fig. 4j–l.
Genus Nematosphaeropsis Deflandre and Cookson 1955 emend. Wrenn, 1988
Nematosphaeropsis labyrinthus (Ostenfeld, 1903) Reid, 1974. Fig. 5a–c.
Genus Spiniferites Mantell, 1850 emend. Sarjeant, 1970
Spiniferites sp. cf. S. belerius Reid, 1974. Fig. 5d–f. Grouped with Spiniferites spp. group A in the counts.
Spiniferites mirabilis (Rossignol 1964) Sarjeant, 1970 emend. Limoges et al., 2018. Fig. 5g–i.
Spiniferites pachydermus sensu Mertens et al. (2015). Non Spiniferites pachydermus (Rossignol 1964) Reid, 1974. Figs. 6a–i, 7a–c.
Spiniferites ramosus (Ehrenberg, 1837) Mantell, 1854 sensu Rochon et al. 1999. Fig. 7d, e. Grouped with Spiniferites spp. group A in the counts.
Spiniferites sp. Fig. 7f, g. Grouped with Spiniferites spp. group A in the counts.
Spiniferites spp. group A.
Spiniferites sp. B. Fig. 7h, i. Not recorded in the counts.
Spiniferites spp. indet. Grouped with Achomosphera+Spiniferites spp. indet. in the counts.
Family LINGULODINIACEAE Sarjeant and Downie, 1974 emend. Gu et al. in Zhang et al., 2020
Genus Lingulodinium Wall, 1967 emend. Dodge, 1989
Lingulodinium machaerophorum (Deflandre and Cookson 1955) Wall, 1967. Fig. 4c, d.
Genus Pyxidinopsis Habib, 1976
Pyxidinopsis reticulata McMinn and Sun, 1994 emend. Marret and de Vernal, 1997. Fig. 8a–c.
Family PROTOCERATIACEAE Lindemann 1928 emend. Gu and Mertens, 2020
Genus Operculodinium Wall, 1967 emend. Matsuoka et al., 1997
Operculodinium centrocarpum (Deflandre and Cookson 1955) Wall, 1967 sensu stricto. Fig. 8d, e.
Operculodinium israelianum (Rossignol, 1962) Wall, 1967. Fig. 8f–i.
Operculodinium? longispinigerum Matsuoka, 1983. Fig. 9d–f.
Genus Protoceratium Bergh, 1881 emend. Gu and Mertens, 2020
Protoceratium reticulatum (Claparède and Lachmann, 1859) Bütschli, 1885. Figs. 8j–l, 9a–c.
Protoceratium reticulatum – short processes. This morphotype occurs only rarely and was grouped with Protoceratium reticulatum in the counts.
Family UNCERTAIN
Genus Cleistosphaeridium Davey et al., 1966 emend. Eaton et al. 2001
Cleistosphaeridium placacanthum (Deflandre and Cookson 1955) Eaton et al. 2001. Fig. 14d–f. Presumed reworked. Grouped with Cleistosphaeridium
spp. in the counts.
Cleistosphaeridium spp. Presumed reworked.
Order PERIDINIALES Haeckel, 1894
Suborder PERIDINIINEAE (Autonym)
Family PROTOPERIDINIACEAE Balech, 1988
Subfamily PROTOPERIDINIOIDEAE Balech, 1988
Genus Brigantedinium Reid, 1977 ex Lentin and Williams, 1993. Grouped with round brown cysts in the counts.
Brigantedinium cariacoense (Wall, 1967) Lentin and Williams, 1993. Fig. 9g. Grouped with round brown cysts in the counts.
Brigantedinium simplex Wall, 1965 ex Lentin and Williams, 1993. Grouped with round brown cysts in the counts.
Brigantedinium sp. Fig. 9h, i. Grouped with round brown cysts in the counts.
Genus Lejeunecysta Artzner and Dörhöfer, 1978, emend. Lentin and Williams, 1976

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 21 of 38

Table 1 Dinoflagellate cyst and acritarch taxa recorded in the present study, and their classification and authorial attributions. All
taxa are considered in situ with the exception of the genus Cleistosphaeridium which is presumed reworked (Continued)
Lejeunecysta sp. A. Fig. 10a–c. Grouped with Lejeunecysta spp. total in the counts.
Lejeunecysta sp. B. Fig. 10d–f. Grouped with Lejeunecysta spp. total in the counts.
Genus Quinquecuspis Harland, 1977
Quinquecuspis concreta (Reid, 1977) Harland, 1977. Fig. 10g–i.
Genus Selenopemphix Benedek, 1972 emend. Head, 1993, nom. cons.
Selenopemphix quanta (Bradford, 1975) Matsuoka 1985. Fig. 11a–c.
Selenopemphix nephroides Benedek, 1972 emend. Bujak in Bujak et al., 1980. Fig. 11d, e. Grouped with Selenopemphix nephroides + undulata in the
counts.
Selenopemphix undulata Verleye et al., 2011. Fig. 11f–i. Grouped with Selenopemphix nephroides + undulata in the counts.
Genus Trinovantedinium Reid, 1977, emend. de Verteuil and Norris, 1992
Trinovantedinium applanatum (Bradford, 1977) Bujak and Davies, 1983. Fig. 12a–d. Not seen during counting.
Trinovantedinium sp. cf. T. harpagonium de Verteuil and Norris, 1992. Fig. 12e–i.
Genus Xandarodinium Reid, 1977
Xandarodinium xanthum Reid, 1977. Fig. 13a, b.
Subfamily UNCERTAIN
Genus Echinidinium Zonneveld, 1997 ex Head et al., 2001
Echinidinium aculeatum Zonneveld, 1997 ex Mertens et al. 2020. Fig. 13c–f.
Family THORACOSPHAERACEAE Schiller, 1930 emend. Tangen in Tangen et al., 1982
Genus Pentapharsodinium Indelicato and Loeblich III, 1986 emend. Montresor et al., 1993
Pentapharsodinium dalei Indelicato and Loeblich III, 1986
Genus Scrippsiella Balech, 1959 ex Loeblich III, 1965
Scrippsiella trifida Lewis, 1991 ex Head, 1996. Fig. 13g–i.
Group ACRITARCHA Evitt, 1963
Genus Nannobarbophora Habib and Knapp, 1982
Nannobarbophora walldalei Head, 1996. Fig. 14a–c.

3.4 Sub-biozone Df2b

Sample: TB 78; depth − 7.75 m; age 789.76 ka; upper MIS 20.
Description: This subzone is represented by a single
sample showing a distinct rise in round brown cysts(92%) and corresponding drop in all other taxa. The cyst
concentration is 3670 cysts/g. The sample is dominatedby plant tissues and terrestrial sporomorphs, with raremarine AOM.
3.5 Sub-biozone Df2c

Samples: TB 76–59; depth − 7.55 to − 5.85 m; age
789.31–785.47 ka; upper MIS 20–lower MIS 19c.
Description: This subzone records declining abundances of round brown cysts from 61 to 29%, and increasing abundances of Selenopemphix quanta to 18%.
Selenopemphix nephroides + undulata has its highest
abundance (12%) in this biozone. Among the phototrophs, Spiniferites spp. group A increases from 7.6 to25%, and Spiniferites mirabilis increases to 16% at thebase of the subzone but declines to 4.6% toward the top.
Cysts of Protoceratium reticulatum resume low abundances of 1.6–10%. Cyst concentrations fluctuate from1125 to 3682 cysts/g. Samples from the base of the subzone to sample TB 70 (787.96 ka) are dominated byplant tissues and terrestrial sporomorphs, with marine
AOM occurring mostly in rare to moderate quantities.

From sample TB 66 (787.30 ka) to the top of the subzone, marine AOM becomes more common, and ismostly abundant to dominant from sample TB 63(786.60 ka) to the top of the subzone.
3.6 Dinoflagellate cyst assemblage biozone 3 (Df3)

Samples: TB 58–40; depth − 5.75 to − 3.95 m; age
785.20–781.20 ka; MIS 19c.
Description: Declining abundances of heterotrophs,
including round brown cysts from 42 to 12% andSelenopemphix nephroides + undulata from 4.7 to 0.2%,
elevated abundances of the heterotroph Echinidinium
aculeatum (0.3–10%), and high abundances of the phototroph Spiniferites spp. group A (20–37%), characterize thiszone. Occurring throughout the zone are Selenopemphix
quanta (6.3–17%), Spiniferites pachydermus sensu Mertens et al. (2015) (1.6–15%), Operculodinium israelianum(0–3.0%), and cysts of Scripsiella trifida (0–1.3%).
Xandarodinium xanthum reaches 1.3% at the top of thezone. Cyst concentrations fluctuate from 916 to 4128
cysts/g. Plant tissues and terrestrial sporomorphs in general co-dominate with marine AOM throughout this zone.
3.7 Dinoflagellate cyst assemblage biozone 4 (Df4)Samples: TB 38–22; depth − 3.75 to − 2.15 m; age
780.74–777.13 ka; MIS 19c.

Balota et al. Progress in Earth and Planetary ScienceFig. 15 (See legend on next page.)(2021) 8:48

Page 22 of 38

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 23 of 38(See figure on previous page.)
Fig. 15 Relative abundance of dinoflagellate cysts and an acritarch from the Chiba and Yoro-Tabuchi sections plotted against the age model of
Suganuma et al. (2018, in press). MIS and substage boundary positions are from Haneda et al. (2020b). All taxa are considered to be in situ. The
position of Byk-E tephra bed is shown. The local dinoflagellate cyst biozonation (biozones Df1–8) is from the present study. All abundances are
expressed as percentages of the total in-situ dinoflagellate cyst counts (or dinoflagellate cyst + N. walldalei counts for the abundances of N.
walldalei). See also Fig. 16

Description: The most notable feature of this zone is
the sustained acme of Lingulodinium machaerophorum(17–39%) which is accompanied by a drop in the abundance of both Spiniferites spp. group A (to 8.3%) andround brown cysts (to 8.0%). The heterotroph Echinidinium aculeatum has sustained significant abundances(7.0–10%). The phototrophs Spiniferites mirabilis (2.9–16%), Achomosphaera + Spiniferites spp. indet. (3.4–
10%), and Operculodinium israelianum (0.8–3.3%) all attain relatively high values in this zone, with the heterotroph Selenopemphix quanta showing a slight decline (to4.6%). Cyst concentrations fluctuate from 1631 to 3233
cysts/g. Marine AOM dominates most samples throughthis zone, although plant tissues and terrestrial sporomorphs occur commonly in most samples.

3.8 Dinoflagellate cyst assemblage biozone 5 (Df5)

Samples: TB 20–12; depth − 1.95 to − 1.15 m; age
776.68–775.44 ka; MIS 19c.
Description: This zone is characterized by an increase in
Spiniferites mirabilis to peak values (21%) and a sharp decline in Lingulodinium machaerophorum (to 5.2%). Spiniferites spp. group A drops to 4.7%. Spiniferites
pachydermus sensu Mertens et al. (2015) has values of
1.1–10%. Species of the oceanic genus Impagidinium in
total rise to 1.8%, and Tuberculodinium vancampoae increases to between 0.7 and 2.3%. A rise in round browncysts to 33% is also recorded, and Echinidinium aculeatum maintains abundances of 4.7–12%. Cyst concentrations fluctuate from 1838 to 2585 cysts/g. Marine AOM
dominates all samples through this zone, with plantFig. 16 Marine palynology and palynofacies of the Chiba and Yoro-Tabuchi sections plotted against the age model of Suganuma et al. (2018, inpress). MIS and substage boundary positions are from Haneda et al. (2020b). The position of Byk-E tephra bed is shown. The biozonation(biozones Df1–8) is from the present study, with total heterotrophs (brown) versus total phototrophs expressing the overall dinoflagellate cyst
assemblage compositions. Dominant palynofacies component (brown line = terrestrial represented mostly by woody and cuticular plant tissues,
blue line = marine represented by amorphous organic matter [AOM]) is given for each sample based on qualitative visual estimate. In a few
samples, marine and terrestrial components co-dominate. Concentrations of dinoflagellate cysts (× 10,000) and benthic microforaminiferal linings(× 100) are per gram dry weight of sediment

810

800

790

780

Byk-E

770

760

Ku2

750
Ku1

740

P

ol

a

GSSP

s
rix inu
La P

Deciduous Evergreen
o
an

ps

is
ed

ed

)
us

n

io
ct

0

100%

s

Df1

c
Df2
b
a

Df3

Df4

Df5

Df6

Df7

Achomosphaera/Spiniferites spp. indet.

Protoceratium reticulatum
Operculodinium israelianum
Spiniferites mirabilis

Selenopemphix nephroides +S. undulata
Echinidinium aculeatum

Other species

Spiniferites spp. group A

Lingulodinium machaerophorum

0 -40

Sea level equivalent(m relative to modern)

120 80 40

35°N
65°N

June insolation Benthic stack(W m-2)
δ18O (‰ VPDB)

810

800

790

780

770

760

750

Age
(ka)
470 490 510 530 5.0 4.5 4.0 3.5
740

Df8

100%

Spiniferites pachydermus sensu
Mertens et al. (2015)

neSelenopemphix quanta

Key to dinoflagellate cyst taxa

50

50

zo

Other heterotrophic species

100 0

0

)
ub

Round brown cysts

50

1a

1b

2a

2b

3a

3b

3c

l
v
n
(s
a
ru
av
ba
ea
ry
Pi
st
S
le
dl
l.
C
n. s
ca tryaona yclo
ad
c
a
h
e
o
c
v
o
x
e
o
r
C
re
bg nu lko . C
br(ee ia ia ea Pte Os
br
n
s
s
AP
c
/
le
Su ala Ze enty ea uo r
us
AT
en
ol
ou
pi iac eq ome ssa ns / usroMp
us dob s / bg rs s
re
s
u
o
s
s
n
e
l
c
e
g
s
e
t
i
d
d
u
d
i
if
er
ia xo eta yp pr gla rp lnu gu uer pi mu . S the inu AP por
Tann (˚C)
ca
ec
on
N S
Ev
D
Lo
Sc Ta M Cr Cu Ju Ca A Fa Q Le Ul QCO P
05 10 15

Coniferous+ < 0.5%

ea bies ug
A
Ts

10%

c
Pi

Main tephra beds

IS
M

y

Full interglacial conditions

itarDinoflagellate cyst
asemblages

Age
(ka)

18

19a

19b

19c

20

Dinoflagellate cyst
biozones

Fig. 17 (See legend on next page.)
Full interglacial conditions

Balota et al. Progress in Earth and Planetary Science(2021) 8:48
Page 24 of 38

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 25 of 38(See figure on previous page.)
Fig. 17 Dinoflagellate cyst synthetic diagram showing the most abundant taxa and local assemblage biozonation (this study) plotted alongside
the major pollen taxa and quantified variations in the mean annual temperature (Tann) based on pollen and using the modern analogue
technique (from fig. 7 of Suganuma et al. 2018). The age model is based on Suganuma et al. (2018) and MIS and substage boundary positions arefrom Haneda et al. (2020b). Included for comparison are the LR04 benthic stack (Lisiecki and Raymo 2005), the eustatic curve of Elderfield et al.
(2012), and the 65°N and 35°N June insolation curves (from Laskar et al. 2004)

tissues and terrestrial sporomorphs occurring commonly
in most samples.
3.9 Dinoflagellate cyst assemblage biozone 6 (Df6)

Samples: TB 10–2, TB2 34–26; depth − 0.95–0.95 m;
age 775.21–773.07 ka; MIS 19c–b.
Description: An increase in Spiniferites spp. group
A to 45%, representing its acme in this succession,
characterizes this zone, together with increased abundances of Achomosphera + Spiniferites spp. indet. to
22% in its lower part and Lingulodinium machaerophorum rising to 31% in the upper part of the zone.
Tuberculodinium vancampoae has its highest values
in this zone, reaching 4.4%. Spiniferites mirabilis
maintains moderately high but fluctuating values of
4.1–20%. Spiniferites pachydermus sensu Mertens
et al. (2015) rises to 17% near the top of this zone.
Among the heterotrophs, round brown cysts decrease
to 0.3% through this zone, whereas Echinidinium aculeatum has moderate values (2.6–8.4%) but is absent
or rare above this zone. Both Selenopemphix quanta(up to 21%) and Xandarodinium xanthum (up to2.3%) have their acmes in this zone, as does the acritarch Nanobarbophora walldalei (up to 5.0% of thetotal in-situ dinoflagellate cysts). Cyst concentrations
fluctuate from 1969 to 4839 cysts/g. From the base
up to sample TB2-32 (773.75 ka), marine AOM dominates with plant tissues and terrestrial sporomorphs
being common to abundant. Above this, plant tissues
and terrestrial sporomorphs dominate to the top of
the zone, with marine AOM common to abundant.

quanta (0–2.0%). This biozone records by far thehighest cyst concentrations, at 21,639–317,932
cysts/gram. The lowest sample (TB2-24) is dominated by marine AOM, with plant tissues and terrestrial sporomorphs being abundant. Fromsample TB2-22 (772.62 ka) to the top of the zone,
samples are dominated by plant tissues and terrestrial sporomorphs, with marine AOM becoming rare from sample TB2-14 (771.72 ka)
upwards.
3.11 Dinoflagellate cyst assemblage biozone 8 (Df8)

Samples: TB2 00, TB2 39–109; depth 3.55–7.40 m; age
770.14–765.80 ka; uppermost MIS 19b, MIS 19a.
Description: A steep decline in the cysts of Protoceratium reticulatum from 93% top of biozone 7 to 47% at
the base of biozone 8, and declining to a minimum of
2.0% in this biozone, and the rapid rise to dominance of
Spiniferites pachydermus sensu Mertens et al. (2015)(38–69%) throughout this zone, are defining features.
Other species with a notable presence are Spiniferites
spp. group A (2.3–9.9%), Lingulodinium machaerophorum (1.0–22%), Nematosphaeropsis labyrinthus (0–2.6%), and the heterotrophic taxa, round brown cysts(2.3–38%), Selenopemphix quanta (0.3–13%), and Selenopemphix nephroides + undulata (up to 2.9%). Cyst
concentrations fluctuate from 2459 to 19,205 cysts/g,
representing a significant drop from concentrations insubjacent biozone Df7. Samples are dominated by planttissues and terrestrial sporomorphs, with marine AOM
occurring in rare to trace amounts.

3.10 Dinoflagellate cyst assemblage biozone 7 (Df7)

Samples: TB2 24–02; depth 1.15–3.35 m; age 772.85–
770.37 ka; MIS 19b.
Description: The sustained dominance of Protoceratium reticulatum cysts (73–93%) characterizes
this zone. These cysts rise abruptly at the base of
the biozone having not previously attained abundances higher than 17% (in the highest sample ofthe subjacent zone), and fall abruptly at the topof the biozone. The only other relatively persistent species in this zone are Spiniferites spp. group
A (0.3–4%), Lingulodinium machaerophorum (0.3–
4.7%), and Spiniferites pachydermus sensu Mertens et al. (2015) (3.7–18%), and the heterotrophs,
round brown cysts (0.3–1.0%) and Selenopemphix

4 Discussion
All assemblages are dominated by neritic dinoflagellate
cysts, with species of the oceanic genus Impagidinium
and predominantly oceanic Nematosphaeropsis labyrinthus usually occurring rarely at most. The abundanceof terrestrial material, mostly woody and cuticular tissues but also spores and pollen, indicates important
downslope transport from the shelf. This taphonomic
process likely accounts also for some of the neritic dinoflagellate cysts, but a strong primary paleoecological signal is clearly preserved. Marine AOM, which dominates
or co-dominates the palynofacies for much of the interval from 786.60 ka to 772.85 ka, closely follows the totalorganic carbon/total nitrogen (C/N) and δ13Corg records

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 26 of 38

Fig. 18 Dinoflagellate cyst synthetic diagram (this study) compared with the foraminiferal δ18O records of the Chiba composite section. a Insolation at
65°N in June, and precession and obliquity parameters (Laskar et al. 2004). b Planktonic (G. bulloides) and benthic foraminiferal δ18O records of the
Chiba composite section (Haneda et al. 2020b) based on the age model of Suganuma et al. (2018). c Dominant palynofacies component (brown line,
terrestrial; blue line, marine amorphous organic matter [AOM]) from Fig. 16. d Dinoflagellate cyst synthetic diagram showing the most abundant taxa
and local assemblage biozonation (this study). Substage classification of MIS 19 with stadials (MIS 19-s1–s4) and interstadials (MIS 19-i1–i4) follows
Haneda et al. (2020b) but with modified labeling and MIS 19a benthic isotope oscillations (MIS 19a-o1 to MIS 19a-o4) following Head (2021). Bluearrow marks the suggested position of a Younger Dryas-type cooling event according to Suganuma et al. (2018)

Balota et al. Progress in Earth and Planetary ScienceFig. 19 (See legend on next page.)(2021) 8:48

Page 27 of 38

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 28 of 38(See figure on previous page.)
Fig. 19 Dinoflagellate cyst record (this study) compared with paleoclimatic and paleoceanographic records through MIS 20 to MIS 18 from the
Chiba composite section (CbCS) (from Suganuma et al. 2018, in press). a Organic carbon stable isotope (δ13Corg) and b C/N ratio (= total organiccarbon [TOC]/total nitrogen [TN]) for bulk samples (Izumi et al. 2021). c Relative abundance of nannofossil F. profunda (Kameo et al. 2020). d Blueshaded area: Radiolarian concentrations (proxy for biological production); red line: Tr values (sea-surface temperature index based on warm- andcold-water radiolarian species). e Relative abundance of planktonic foraminifera and results of factor analysis. f Δδ18OG. bulloides–G. inflata (bul-inf),
corresponding to the temperature gradient (hence stratification) between surface and subsurface waters. g Mg/Ca paleotemperature for G. inflata(Tinf) considered to represent the subsurface (> 100 m) winter temperature (Kubota et al. 2021). h Dominant palynofacies component (brown line,
terrestrial; blue line, marine amorphous organic matter [AOM]) from Fig. 16. i Dinoflagellate cyst synthetic diagram showing most abundant taxa
and local assemblage biozonation (this study). Blue arrow marks the suggested position of a Younger Dryas-type cooling event according to
Suganuma et al. (2018)

and radiolarian concentrations (Fig. 19) and therefore
seems to reflect elevated organic production.
The presence of opaque mineral inclusions, presumably diagenetic pyrite, in all samples reflects oxygendepleted conditions below the water/sediment interface,perhaps facilitated by the rapid sedimentation rates, although the presence of benthic microforaminiferal linings in all but one sample (Fig. 16) and intense
bioturbation throughout (Nishida et al. 2016) attest to
oxygenated bottom waters and near-surface sediment.
The pyrite presumably formed below the interval of intense bioturbation.
Numerous proxies have been used to reconstruct the
paleoenvironmental history of the Chiba composite section, including foraminiferal isotopes, pollen, and organic geochemistry at very high temporal resolution as
discussed in detail in Suganuma et al. (2018, in press).
These highly resolved records are integrated and compared with the marine palynological data (Figs. 17, 18,
and 19) below.
4.1 Dinoflagellate cyst assemblage biozone Df1(794.21–791.72 ka), upper MIS 20

This biozone reflects cold and relatively nutrient-rich
subarctic water masses based on the overwhelming
dominance of round brown cysts (76–93%). The Subarctic Front would therefore have been south of the
Chiba section. There are no close modern analoguesof this cyst association, although high abundances ofround brown cysts up to ~ 60% are found in thenorthernmost North Pacific today (Bonnet et al.
2012). Differences with these modern assemblages include the lower abundances of Nematosphaerposis
labyrinthus and Pyxidinopsis reticulata, perhaps
implying lower salinities than at present in the northernmost North Pacific, and apparent absence of Spiniferites elongatus which may suggest somewhat warmer
conditions for the Chiba composite section. Today,
the dominance of round brown cysts is generally associated with high biological productivity (Zonneveld
et al. 2013), but cyst concentrations are not elevatedin biozone Df1. High sedimentation rates of 1.23 m/

kyr (Suganuma et al., in press) will have had a diluting effect during biozone Df1, but productivity does
not seem to be have been especially elevated unlessround brown cysts are underrepresented significantly
through preservational loss.
During this time, insolation for June was increasing(Fig. 17). Other marine proxies in general reflect coolwater masses, although Mg/Ca values for Globorotalia
inflata indicate rather high winter–spring temperatures of ~ 15.5 °C at > 100 m depth (Fig. 19). The
pollen record shows ameliorating climatic conditions
on land with an increase in broadleaved deciduous
species already by 796 ka. Biozone Df1 coincides withthe lower third of pollen subzone 1b of Suganuma
et al. (2018) which represents subarctic coniferous
and deciduous broadleaved mixed forest (Fig. 17).
The dominance of terrestrially derived organic mattercan be explained by transport from a partially
exposed shelf owing to the lowered global sea level,
but also apparently by relatively low marine productivity as discussed above and inferred from other marine indicators including low radiolarian concentrations
and more negative δ13Corg and higher Ca/Ti ratios(Suganuma et al., in press; Izumi et al. 2021; Fig. 19).
In general, the progressive decrease in roundbrown cysts from biozone Df1 through Df3, which
represents the transition from glacial MIS 20 tointerglacial MIS 19, signals the decreasing influenceof cold subarctic surface waters. This trend closely
matches that of increasing temperate tree pollen(Quercus subgenus Lepidobalanus pollen and of total
deciduous broadleaved plants; Fig. 17) which signals
increasingly warm conditions on land. It also
matches the foraminiferal δ18O stratigraphy whichshows a general trend of decreasing values throughthis interval (Fig. 18b).

4.2 Dinoflagellate cyst assemblage biozone Df2(791.55–785.47 ka), upper MIS 20–lower MIS 19c

This biozone encompasses Termination IX and is divided into three sub-biozones.

(2021) 8:48

Page 29 of 38

4.3 Sub-biozone Df2a (791.55–790.32 ka), upper MIS 20

north of the Chiba composite section during the beginning of sub-biozone Df2c at ~ 789.31 ka.
The interpreted rapid warming at the start of subbiozone Df2c (789.31 ka) is consistent with most marine
proxies including the benthic and planktonic foraminiferal δ18O records (Figs. 18 and 19), and also with increasing pollen of deciduous broad-leaved trees throughthis subzone (Fig. 17). The northward shift of the Subarctic Front at ~ 789.31 ka predates the end of MIS 20
and also the peak in June insolation by about 2000 years(Fig. 17). Changes in palynofacies, with marine AOM becoming more common from ~ 787.28 ka and thenmostly abundant to dominant from 786.60 ka, precisely
follow increases in δ13Corg and decreases in C/N values(Suganuma et al., in press; Izumi et al. 2021; Fig. 19).
These changes occur just after the start of MIS 19c andalso coincide precisely with a sharp reduction in valuesof G. bulloides δ18O at 787 ka. They signify a lower input of terrestrial material and/or higher biogenic productivity at a time of rapid sea-surface warming, with the
combination of sea-level rise and warmer waters in theearliest part of MIS 19c driving this change. Increasing
marine AOM from 787.28 ka seems to reflect mostly arise in biogenic productivity which is indicated by a risein radiolarian concentrations in the upper part of thiszone (Suganuma et al. 2018, in press).

Balota et al. Progress in Earth and Planetary Science

An abrupt decline in round brown cysts (85–52%) andrise in Spiniferites spp. group A at the beginning of thiszone suggests a reduction in the influence of subarctic
water masses and therefore a rise in SSTs. A small increase in Operculodinium israelianum, a mostly tropical–subtropical species (Zonneveld et al. 2013), to ~ 3%
is consistent with this suggested rise in SST.
Within the pollen record, however, a discrete warming
event is not recognized, and within the Globigerina bulloides δ18O record sub-biozone Df2a is represented byhigher values that have been tentatively attributed to a
Younger-Dryas-like cooling event (Suganuma et al. 2018;
Figs. 18 and 19). One possible explanation for this discrepancy is that because round brown cysts are particularly susceptible to oxidation on the sea floor (Hopkins
and McCarthy 2002), a Younger-Dryas-like cooling
event might have invigorated bottom-water oxygenationand caused the selective loss of some round brown cysts.
Nonetheless, Mg/Ca values for Globorotalia inflata indicate rather stable winter–spring subsurface (> 100 m)
temperatures at around 15.5 °C, at odds with the nearsurface (< 50 m) Globigerina bulloides δ18O record.
4.4 Sub-biozone Df2b (789.76 ka), upper MIS 20

A single sample containing abundant round brown cysts(92%) might reflect a brief southward return of the Subarctic Front and hence represent a cooling event.
Brief cooling is consistent with single δ18O and Mg/Ca
data points for Globorotalia inflata, and this interval isclose to single-point deflections in the total organic carbon/total nitrogen (C/N) and δ13Corg record for bulk
samples (Figs. 18 and 19). Higher resolution multi-proxysampling is needed to substantiate this possible event.
4.5 Sub-biozone Df2c (789.31–785.47 ka), upper MIS 20–
lower MIS 19c

At the base of this sub-biozone, a sharp drop in theabundance of round brown cysts and a rise in Spiniferites mirabilis to 16% indicates a significant rise in seasurface temperatures. This temperate to tropical species
has its distributional limits today approximately following the subtropical fronts on both hemispheres (Zonneveld et al. 2013; de Vernal et al. 2020). Abundances
greater than 15% occur typically where summer SSTs
are 15 °C or more, and summer SSS exceed ~ 32 psu. It
occurs in coastal and open ocean environments and cantolerate reduced salinities and both oligotrophic andnutrient-elevated conditions (Zonneveld et al. 2013). In
the northern North Pacific today, Spiniferites mirabilis isassociated only with more southerly sites under the influence of the Kuroshio Extension (Bonnet et al. 2012).
This implies that the Subarctic Front moved rapidly

4.6 Dinoflagellate cyst assemblage biozone Df3 (785.20–
781.20 ka), MIS 19c

This biozone Df3 is marked by generally sustained abundances (1.6–15%) of Spiniferites pachydermus sensu
Mertens et al. (2015), a species occurring in modern sediments of İzmir Bay, eastern Aegean Sea, Mediterranean
where the waters are eutrophic, summer SSTs are ~ 25–
27 °C, and summer SSSs are ~ 33–39 psu for the innerbay (Mertens et al. 2015; Sayın et al. 2006). Although
there are uncertainties regarding the identity of this distinctive undescribed species, it has likely been recorded
at least in part from modern sediments under the name
Spiniferites pachydermus, a coastal to open marine species considered to have a temperate to tropical distribution, with abundances greater than 5% when summer
SSTs exceed ~ 18 °C and summer SSSs exceed ~ 33 psu(Zonneveld et al. 2013). It is restricted to fully marine
environments where mesotrophic to eutrophic conditions occur including upwelling areas (Zonneveld et al.
2013). Spiniferites pachydermus sensu Mertens et al.
(2015) has possibly been reported from Holocene
shallow-marine sediments of the Tsushima Islands, west
Japan (Matsuoka 1994, as Spiniferites cf. bentorii), which
are under the influence of the Kuroshio/Tsushima
Warm currents. Spiniferites spp. group A is an abundant(20–37%) constituent of biozone Df3, and as with mostother members of this genus, represents a neritic

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Page 30 of 38

component. Elevated abundances of the heterotroph
Echinidinium aculeatum (0.3–10%) in this biozone arealso significant. This species has a mesotrophic/ eutrophic temperate to tropical modern global distribution,
being confined to regions with unstratified upper waters(Zonneveld et al. 2013).
The tentative estimate of summer SST exceeding ~ 18
°C based on Spiniferites pachydermus (possibly in thesense of Mertens et al. 2015) is broadly consistent with
subsurface (> 100 m) winter temperatures of 15–18 °C
based on Globorotalia inflata Mg/Ca data for biozone
Df3. The start of biozone Df3 coincides with the onset
of full interglacial conditions on land, as registered byhigh abundances of deciduous tree pollen including
Quercus subgenus Lepidobalanus and the sustained
presence of evergreen tree pollen (Fig. 17). All marine
proxies are consistent with sea-surface temperatures thatare among the warmest for the Chiba composite section.
The general co-dominance or alternating dominance ofmarine AOM with terrestrial organic matter throughout
this zone is reflected also in the δ13Corg and C/N values(Suganuma et al., in press; Izumi et al. 2021; Fig. 19a, b)
and presumably relates to high biological productivity
judging from the radiolarian concentrations (Fig. 19d).

signal does not appear to be reflected in the other marine proxies. Relatively high abundances of the coccolith
Florisphaera profunda (Fig. 19c) indeed suggests moderate water column stratification, although not necessarily
at the time of year when Lingulodinium machaerophorum would have been blooming. Relatively highabundances of Echinidinium aculeatum (6.8–10%)
throughout this zone suggest weak stratification, as
noted above (Zonneveld et al. 2013). Relatively weakstratification is also reflected in the difference between
benthic and surface dwelling (G. bulloides) foraminiferal
δ18O values at this time (fig. 3d of Haneda et al. 2020b).
Slightly higher benthic and planktonic foraminiferal
δ18O values (Fig. 18b) in the middle of this zone where
Lingulodinium machaerophorum reaches highest abundances (39%) corroborate the interpretation that theKuroshio Extension may have shifted southwards, resulting in diffuse upwelling. The dominance of marine
AOM through this biozone is consistent with relatively
high marine organic productivity, as suggested by continued high δ13Corg values and radiolarian concentrations (Fig. 19a, d).

4.7 Dinoflagellate cyst assemblage biozone Df4 (780.74–
777.13 ka), MIS 19c

This biozone records a sharp decline in Lingulodinium
machaerophorum (to 5.2%) and a rise in Spiniferites
mirabilis to its highest abundances (21%) in the Chiba
composite section. Spiniferites mirabilis has abundances
greater than 20% today mostly where summer SSTs are 16°C or more, and summer SSS exceed ~ 32 psu (Zonneveld
et al. 2013). Spiniferites pachydermus sensu Mertens et al.
(2015) has values of 1.1–10%, and species of the oceanic
genus Impagidinium become somewhat more abundant,rising to 1.8%. The equatorial to temperate Echinidinium
aculeatum has a peak abundance of 12% in this zone, implying continued weak surface water stratification. Tuberculodinium vancampoae, which rises to 2.3%, is atemperate to tropical species found in coastal embayments
around Japan today. It mostly occurs in central and southern areas of Japan (Zonneveld et al. 2013) but extends tonortheastern Honshu (Matsuoka 1976). It has been reported from the mid-Pleistocene of Osaka Bay to occasionally dominate or co-dominate assemblages (Harada
1984). It presumably represents transport from the shelf.
The assemblage composition in general therefore indicates
warm, weakly stratified surface waters, which accords withbenthic foraminiferal δ18O values that are at their lowest,
and planktonic δ18O values that become increasingly low
through this biozone (Fig. 18b). The pollen record reflects
full interglacial conditions on land, and most marine proxies point to continuing warm SSTs. A northward shift of
the Kuroshio Extension best explains this combination ofobservations. The continued dominance of marine AOM

Lingulodinium machaerophorum (17–39%) characterizes
this biozone. This is a temperate to tropical euryhaline
species particularly abundant today in (1) estuarine environments with increased nutrients and lowered salinities(e.g., Wall et al. 1977; Morzadec-Kerfourn 1977; Daleet al. 1999), (2) bays that have experienced eutrophication (Dale and Fjellså 1994; Dale et al. 1999; Matsuoka
1999; Shin et al. 2010), (3) below river discharge plumes(Zonneveld et al. 2013), and (4) areas affected by elevated nutrient levels arising from diffuse upwelling (Dale
1996; Zonneveld et al. 2013). The thermophilic Spiniferites mirabilis remains at significant levels (2.9–16%). Spiniferites mirabilis today is mostly distributed within thesubtropical fronts of both hemispheres. It is considereda temperate to tropical species, and can be associatedwith eutrophic environments (Zonneveld et al. 2013).
The tropical–subtropical Operculodinium israelianum
although not common (≤ 3.3%) has its highest occurrence in this zone. This biozone therefore signals an increase in nutrient input to the surface waters, with apossible lowering of salinity. It might be related to asouthward shift in the position of the Kuroshio Extension or an increase in its intensity that would induce a
diffuse upwelling of nutrient-elevated waters.
Full interglacial conditions on land and warm seasurface conditions continue through biozone Df4 asreflected in all proxies. However, a strong upwelling

4.8 Dinoflagellate cyst assemblage biozone Df5 (776.68–
775.44 ka), MIS 19c

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

is again consistent with relatively high marine organic
productivity based on high δ13Corg values and radiolarianconcentrations (Fig. 19a, d).
4.9 Dinoflagellate cyst assemblage biozone Df6 (775.21–
773.07 ka), MIS 19c–b

This biozone represents a brief increase in Lingulodinium
machaerophorum, reaching 31% in its upper part, implying the return of diffuse nutrient input to the surface waters, as inferred for biozone Df4. The presence of
Echinidinium aculeatum (2.6–8.4%) is consistent withweak surface water stratification. Significant values of Spiniferites mirabilis (4.1–20%) and of Spiniferites pachydermus sensu Mertens et al. (2015) rising to 17% near the topof this zone indicate continued warm SSTs, as does
Tuberculodinium vancampoae which reaches its maximum of 4.4% in this zone. The abundance peak of the extinct acritarch Nanobarbophora walldalei (up to 5.0% of
the total in-situ dinoflagellate cysts) is consistent with thisinterpretation, as this species is associated with tropical towarm/mild-temperate paleoenvironments (Head in Headand Westphal 1999; Head 2003) and is associated withwarmer MISs in the Mediterranean (as Acritarch sp. B in
Versteegh 1994, 1995; Versteegh and Zonneveld 1994).
Selenopemphix quanta reaches its highest abundance(21%) in this zone. This species has a broad temperature
tolerance and occurs from tropical to subpolar regions
today but is most abundant in upwelling regions and at
oceanic fronts where nutrient levels are elevated (Zonneveld et al. 2013). On balance, biozone Df6 particularly in
its latter half suggests a slight southward shift of the Kuroshio Extension, bringing mixed waters of the KOIZ overthe site of deposition, and hence somewhat elevated nutrient levels. It may represent a transitional state between
biozones Df5 and Df7.
This interpretation would imply somewhat cooler waters for this biozone, particularly during the latter half.
Biozone Df6 spans the MIS 19c–b boundary which ismarked by progressively higher benthic foraminiferal
δ18O values. The base of this biozone corresponds to thetermination of full interglacial conditions as determinedby pollen analysis, and a decline in deciduous tree pollen
in the lower part of biozone Df6 reflects cooling on land,
which is followed by a warming in the upper part of thebiozone based on the MAT reconstruction (Fig. 17).
Planktonic foraminiferal δ18O values in contrast are very
low except at the top of this biozone where they becomemarkedly higher (Fig. 18b).
In general, marine proxies reflect transitional conditions
through this biozone. SSTs nonetheless remained warm as
corroborated by values exceeding ~ 15 °C based on Mg/
Ca data for Globorotalia inflata (Fig. 19g), but likely
dropped near the top of this biozone judging from theradiolarian Tr ratio. Low percentages of the calcareousPage 31 of 38

nannofossil F. profunda in the latter part of this zone
would seem to confirm reduced ocean stratification at thistime. A significant shift from marine AOM-dominatedpalynofacies in the lower part of the biozone to a mostly
terrestrially dominated palynofacies from 773.52 ka near
the top of the biozone is mirrored by declining δ13Corg
and increasing C/N values (Fig. 19a, b). It appears to represent a sharp decline in biological productivity based on
the reduced concentration of radiolarians (Fig. 19d). It also
corresponds to a sharp drop in SST as inferred fromhigher planktonic foraminiferal δ18O values, this signaling
the onset of stadial 1 (MIS 19-s1) within the earlier part of
MIS 19b (Fig. 18).
4.10 Dinoflagellate cyst assemblage biozone Df7 (772.85–
770.37 ka), MIS 19b

This biozone represents the most abrupt change inthe examined interval of the Chiba composite section,with cysts of Protoceratium reticulatum (73–93%) rising rapidly in abundance at the base of the zone,
dominating throughout, and falling abruptly at theend of this biozone. The only other relatively common species is the thermophilic Spiniferites pachydermus sensu Mertens et al. (2015) (3.7–18%).
Protoceratium reticulatum is a potentially yessotoxinproducing (Liu et al. 2017; Wang et al. 2019), bloomforming opportunistic dinoflagellate found in Japanesewaters today (e.g., Koike et al. 2006). It is a cosmopolitan species whose cysts, known in the literature
also as Operculodinium centrocarpum sensu Wall andDale (1966), can dominate today at high latitudes including the Okhotsk Sea (Bonnet et al. 2012) and off
Hachinohe, northeastern Japan, which is under the influence of the Tsugaru Warm Current (Matsuoka1976) and Oyashio Current. It also dominates the
autotrophic component of modern cyst assemblages
from Akkeshi Bay, eastern Hokkaido, which is alsostrongly influenced by the Oyashio Current (Matsuoka
1987). Its global modern distribution shows an affinity
for mesotrophic to eutrophic and cold to temperateenvironments (Bonnet et al. 2012), and it appears well
adapted to unstable conditions where oceanic andneritic waters mix (Dale 1996). This is seen in the
North Atlantic where it serves as an indicator for the
North Atlantic Current both in modern assemblages(Harland 1983; Rochon et al. 1999; Zonneveld et al.
2013) and in Plio-Pleistocene records (e.g., De Schepper et al. 2009, 2013; Hennissen et al. 2014, 2017).
Unusually, it can be abundant in both neritic andoceanic settings, and this may be attributable to its
unusual life cycle (Salgado et al. 2017) that can sustain productivity in oceanic waters where sufficientnutrients exist. This species appears to represent
summer sea-surface conditions, given that within theBalota et al. Progress in Earth and Planetary Science(2021) 8:48

surface waters of Okkirai Bay, northeastern Japan,
motile cells of Protoceratium reticulatum were observed only from mid-June to late August, with peakabundances recorded from late June to late July. The
highest density of cells was observed in the surface
layer (0–5 m), and maximum abundance appeared tobe correlated to periods of lowered surface water salinity due to rainfall (Koike et al. 2006). Similarly, inthe northern Yellow Sea of China, motile cells of Protoceratium reticulatum were found to be largely restricted to the months of April, May, and June, andthe cysts most common in the sediment from March
to August (Liu et al. 2017). The cysts of this species
form when nutrient levels decline, and the cysts
themselves have an obligatory dormancy period of ~ 4months. The cysts are clearly important to the ecology of this species, and appear to represent an overwintering strategy when conditions are unfavorable
for population growth (Salgado et al. 2017). The dominance of Protoceratium reticulatum cysts in biozone
Df7 is therefore interpreted to reflect cooler, nutrientelevated and unstable spring–summer surface waters
under the influence of the KOIZ, brought about by asouthward shift of the Kuroshio Extension. It may be
noted that this species has been reported from themid-Pleistocene of Osaka Bay, but while abundant insome samples (Harada 1984), it does not attain the
exceptional abundances that characterize biozone Df7.
Biozone Df7 spans the upper two-thirds of MIS 19b, thissubstage representing the glacial inception that terminates
the interglacial conditions of MIS 19c. This biozone includes much of stadial 1 and the lower half of interstadial
1 (Fig. 18; Head 2021). Its onset is marked by an abrupt
shift to higher planktonic foraminiferal δ18O values(Fig. 18b), implying cooler surface waters, and occurs
within a trend of increasing benthic foraminiferal δ18O
values through MIS 19b and specifically at a minor increase. However, other marine proxies do not record pronounced cooling, although factor analysis of planktonic
foraminiferal assemblages shows a slight increase in transitional (cooler) waters during biozone Df7 and a slightdecrease in the influence of the Kuroshio Current(Fig. 19e). Radiolarian Tr values also indicate somewhat
cooler waters. Lower abundances of the coccolith Florisphaera profunda (Fig. 19c) indicate reduced water column stratification consistent with the interpretation of
unstable conditions. The pollen record similarly does notshow pronounced changes with the exception of an increased abundance of the temperate conifer Cryptomeria
during biozones Df6 and 7 which possibly indicates gradual cooling (Suganuma et al. 2018).
The highest cyst concentrations (21,639–317,932
cysts/gram) are recorded in biozone Df7, implying enhanced biological productivity consistent with thePage 32 of 38

influence of the nutrient-rich KOIZ. In contrast, however, δ13Corg and C/N values continue their declining/
increasing trends respectively through this biozone,
and marine AOM is subordinate to plant tissues andterrestrial sporomorphs in all but the lowest sampleof this biozone. In addition, radiolarian concentrations
as a measure of biogenic production show much
lower values than for MIS 19c. It is possible, therefore, that high dinoflagellate cyst concentrations reflect productivity limited to the spring–summer
months and are not representative of annual biological production.
The abrupt rise in Protoceratium reticulatum cysts at
the inception of biozone Df7 occurs approximately
across two samples separated by 20 cm (TB2-26 at 0.95
m and TB2-24 at 1.15 m above the Byk-E bed) and suggests a change to cooler summer SSTs within ~ 300
years. This pronounced paleoceanographic shift occurs
within the directional transition zone (0.25–1.95 m) of
the Matuyama–Brunhes paleomagnetic reversal, and isindeed close to its midpoint which is astronomically
dated at 772.9 ka. A connection between a collapse in
the Earth’s magnetic field intensity, as occurs during areversal, and increased atmospheric penetration of galactic cosmic rays leading to more extensive cloud coverand ultimately global cooling, has been proposed frequently in the literature (Kitaba et al. 2017 and references therein) but remains open to debate. The timingof the onset of biozone Df7 does not however coincidewith the start of field intensity decline, as indicated by
the 10Be and paleointensity records, which is progressive
and begins earlier than the directional transition zone
(Okada et al. 2017; Simon et al. 2019; Haneda et al.
2020a). Moreover, Protoceratium reticulatum cyst abundance at the end of this biozone drops almost as rapidly
as it begins without any obvious change in the field intensity, which remains low until ~ 760 ka (Simon et al.
2019; Haneda et al. 2020a).

4.11 Dinoflagellate cyst assemblage biozone Df8 (770.14–
765.80 ka), MIS 19a

A steep decline in Protoceratium reticulatum cysts
from 93% at the top of biozone Df7 to 47% at thebase of biozone Df8 and then to a minimum of 2%,
and corresponding rise to dominance of Spiniferites
pachydermus sensu Mertens et al. (2015) with abundances of 38–69%, represents the abrupt transition toa unique association within the Chiba record. The latter species is a known thermophile and, as noted
above, probably well adapted to fully marine environments when mesotrophic to eutrophic conditions prevail. Moderate surface-water nutrient levels are also
reflected by a relative increase in heterotrophic

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

dinoflagellate cysts, including round brown cysts (2.3–
38%) and Selenopemphix quanta (0.3–13%).
Cyst concentrations (2459 to 19,205 cysts/g), although
representing a significant decline from peak values during biozone Df7, remain higher than before that time. In
contrast, marine AOM is rare, and consistently low
δ13Corg values, high C/N ratios, and low concentrationsof radiolarians (Fig. 19) all reflect low overall biologicalproductivity for this biozone.
The apparent contradiction between moderatesurface-water nutrient levels and low biological productivity may be linked to water-column stratification.
Elevated abundances of the coccolith Florisphaera profunda indicate pronounced water column stratification(Fig. 19c), and the near absence of the extant Echinidinium aculeatum which today is confined to regions with
unstratified upper waters (Zonneveld et al. 2013) is consistent with stratification throughout this biozone.
An abrupt shift to lower values in both the planktonic
and especially benthic foraminiferal δ18O values signifies
warming at the onset of biozone Df8 and defines thebase of MIS 19a. While the onset of biozone Df8 aligns
precisely with that of MIS 19a-o1, it occurs midway
through the interstadial MIS 19-i1 as characterized by
the planktonic foraminiferal δ18O record (Fig. 18). This
discrepancy is perhaps related to seasonal differences in
the proxies examined: the foraminifera registering winter–spring conditions and at least some dinoflagellates
recording the spring–fall. There are no substantialchanges in assemblage composition through biozone
Df8. However, both planktonic and benthic foraminiferal
δ18O values are higher in its upper half, from ~ 768 ka
onwards, corresponding to the cooler conditions ofstadial 2 within MIS 19a (Fig. 18), and this is perhaps
reflected in the lower cyst concentrations recorded in
the second half of the biozone.
The increase in June insolation at this time (Figs. 17
and 18a) may have contributed to surface water stratification. The abundance of Spiniferites pachydermus sensu
Mertens et al. (2015) therefore possibly relates to summer water-column stratification.
Hence, biozone Df8 is interpreted to mark the establishment of warm, stratified, nutrient-elevated, surface
water conditions that persisted to the top of the examined interval. The Kuroshio Extension Front is interpreted to have shifted northwards at the beginning of
this zone, causing the intrusion of the southern marginof the KOIZ.
This interpretation is corroborated by varimax factor
loadings and reconstructed SSTs of planktonic foraminiferal assemblages which show at ~ 770 ka an abrupt
rise in the influence of the warm Kuroshio Current, anda concomitant decline in (cool) transitional waters. The
pollen record for biozone Df8 is at low stratigraphic

Page 33 of 38

resolution, but increasing values of the temperate conifers Tsuga and Picea (Fig. 17) indicate a cooler climate
on land than for biozone Df7.
Suganuma et al. (2018) had previously proposed anorthward shift of the Kuroshio Extension at this time,
postdating the termination of full interglacial conditions
on land by ~ 5 kyrs. These authors proposed that relatively high winter insolation at 50° N at this time might
have contributed to a weakening of the Siberian High, awinter phenomenon, and hence weakening of the East
Asian Winter Monsoon (EAWM). This will have allowed
the westerly jet, which influences the position of theKuroshio Current, to take a more northerly path in winter. Suganuma et al. (2018) provided two lines of evidence for this. Firstly, grain-size variations in loesspaleosol successions on the Chinese Loess Plateau indicate a weak EAWM for up to 20,000 years after the endof fully interglacial conditions (Sun et al. 2006; Hao et al.
2012). Secondly, from the Chiba composite section itself,
a slight increase in the differential between the δ18O of
the surface-dwelling foraminifera G. bulloides and subsurface G. inflata indicates an increase in water column
stratification during the cold seasons because these two
species are abundant at different depths off the Japanesearchipelago today in winter (Suganuma et al. 2018).
Therefore, increased water column stratification during
winter, representing decreased wind mixing, is consistent with a weaker EAWM. Sea-surface conditions were
warm as indicated by the thermophilic Spiniferites
pachydermus sensu Mertens et al. (2015), but the season(s) of maximum growth and cyst production are notknown for this species. A summer northward shift of theKuroshio Extension Front might, however, be needed to
explain the abundance of this species. Evidence from the
Chinese Loess Plateau provides a pattern of weakening
summer monsoons during this time (Sun et al. 2006)
which would have reduced wind stress over the ocean.
This together with the peak in June insolation at thistime (Figs. 17 and 18) may therefore provide a mechanism for water-column stratification and elevated seasurface temperatures during the spring–summer
months. This raises the possibility that the westerly jet,which influences the latitude of the Kuroshio Extension,
took a more northerly path in summer, as well as inwinter, relative to summer conditions during biozone
Df7. More information is needed on the seasonality of
Spiniferites pachydermus sensu Mertens et al. (2015) toclarify this possibility.

5 Conclusions
This is the first detailed dinoflagellate cyst study of the
Pleistocene from the Pacific margin of the Japaneseislands. Using closely spaced (10 or 20 cm) samples fromthe highly constrained adjacent Chiba and Yoro-Tabuchi

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

sections of the Chiba composite section, it establishes adetailed paleoceanographic reconstruction (794.21 to765.80 ka; late MIS 20 to mid-MIS 19a) across the
Early–Middle Pleistocene Subseries (Calabrian–Chibanian Stage) boundary at the type locality. The location ispresently close to the confluence of the warm Kuroshio
and cold Oyashio currents and is therefore well positioned to explore their relative influences over time, especially during MIS 19 when conditions were similar tothe present interglacial. The dinoflagellate cyst record
reveals previously undocumented detail regarding
surface-water instability through MIS 19, including the
response of dinoflagellates to Termination IX, to fullinterglacial conditions during MIS 19c, the arrival ofcooler conditions during MIS 19b, and a return towarmer conditions at the beginning of MIS 19a during
interstadial MIS 19-i1. The dinoflagellate cyst assemblages are overwhelmingly dominated by neritic taxa,
and preservation varies from good to moderate. The
palynofacies is characterized by common to dominantterrestrial material, and it is therefore assumed thatdinoflagellate cyst assemblages reflect changes across thecontinental shelf and not simply oceanic waters above
the continental slope on which the sediments were deposited. The dominance of marine AOM particularly between 786.60 and 772.85 ka, representing most of MIS
19c and the earliest part of MIS 19b, closely follows thehigh-resolution records for δ13Corg and C/N (Suganuma
et al., in press; Izumi et al. 2021; Fig. 19) and corroborates the interpretation based on elevated concentrationsof radiolarians (Fig. 19) that biological production wasenhanced through this interval. The dinoflagellate cyst
record is subdivided into eight assemblage biozones.
Dinoflagellate cyst assemblage biozone Df1 (794.21–
791.72 ka, upper MIS 20) is dominated by heterotrophic
round brown cysts and reflects cold and relatively
nutrient-rich subarctic waters, although presumably not
fully glacial conditions.
Sub-biozone Df2a (791.55–790.32 ka, upper MIS 20) is
characterized by a reduction in round brown cysts thatsuggests a reduced influence of subarctic water masses
and therefore a rise in SSTs. However, preservational
factors cannot be excluded as some marine proxies suggest a Younger-Dryas-like cooling event during thisinterval.
Sub-biozone Df2b (789.76 ka, upper MIS 20) is represented by a single sample dominated by round browncysts and which might represent a brief southward return of the Subarctic Front, although further samplingthrough this interval is needed to confirm a possible
cooling event.
Sub-biozone Df2c (789.31–785.47 ka, upper MIS 20–
lower MIS 19c) is marked by a sharp drop in the abundance of round brown cysts and a rise in Spiniferites

Page 34 of 38

mirabilis indicating a significant rise in sea-surface temperatures and rapid retreat of the Subarctic Front at ~789.31 ka, predating the end of MIS 20 and also thepeak in June insolation by ~ 2000 years. A relative increase in marine AOM from ~ 787 ka is consistent witha rise in biogenic productivity.
Dinoflagellate cyst assemblage biozone Df3 (785.20–
781.20 ka, MIS 19c) includes a sustained presence of thethermophilic Spiniferites pachydermus sensu Mertens
et al. (2015) and represents warm and relatively unstratified surface waters with elevated nutrient levels. Its inception coincides with the onset of full interglacialconditions on land. Other marine proxies give seasurface temperatures that are among the warmest for
the Chiba composite section.
Dinoflagellate cyst assemblage biozone Df4 (780.74–
777.13 ka, MIS 19c), characterized by relatively highvalues of Echinidinium aculeatum and abundant Lingulodinium machaerophorum, signals elevated nutrient
levels and perhaps a lowering of salinity, and appears to
represent diffuse upwelling possibly related to a southward shift in the position of the Kuroshio Extension or
an increase in its intensity. The dominance of marine
AOM through this zone is consistent with relatively highmarine organic productivity as reflected by otherproxies.
Dinoflagellate cyst assemblage biozone Df5 (776.68–
775.44 ka, MIS 19c) is marked by a steep decline in Lingulodinium machaerophorum and rise in the abundanceof the thermophilic Spiniferites mirabilis and Echinidinium aculeatum to their highest values implying continued warm, weakly stratified surface waters with reduced
nutrient levels, and suggesting a northward shift of theKuroshio Extension.
Dinoflagellate cyst assemblage biozone Df6 (775.21–
773.07 ka, MIS 19c–b) marks a brief return to an increased abundance of Lingulodinium machaerophorum
and suggests, particularly during its latter half, a slightsouthward shift of the Kuroshio Extension. It may represent a transitional state between biozones Df5 and Df7.
Although the base of this biozone corresponds to the termination of full interglacial conditions as determined bypollen analysis, and the termination of MIS 19c falls withthe middle of this biozone, significant cooling is not registered in the dinoflagellate cyst record. A shift from marine
AOM-dominated to a mostly terrestrially dominated palynofacies at 773.52 ka appears to reflect a sharp decline inbiological productivity and signals the onset of MIS 19-s1(stadial 1) within the earlier part of MIS 19b.
Dinoflagellate cyst assemblage biozone Df7 (772.85–
770.37 ka, MIS 19b) represents an abrupt (within ~ 300
years) and sustained dominance of Protoceratium reticulatum cysts accompanied by a one- or two-order magnitude increase in cyst concentrations, signaling the rapid

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

onset of unstable, cooler, and biologically productive
surface waters during the spring–summer months. This
is interpreted to mark the influence of the Kuroshio–
Oyashio Interfrontal Zone resulting from a southward
shift in the Kuroshio Extension. This biozone corresponds to the upper two thirds of MIS 19b and its onset
broadly coincides with the glacial inception terminating
the interglacial conditions of MIS 19c. The abrupt risein Protoceratium reticulatum cysts defining the base of
biozone Df7 also serves as an unambiguous local ecostratigraphic marker for the Chibanian Stage GSSP which
occurs just 1.15 m (= 1300 years) below it. This rise also
coincides with the directional midpoint of the
Matuyama–Brunhes boundary in the Chiba section(Haneda et al. 2020a).
Dinoflagellate cyst assemblage biozone Df8(770.14–765.80 ka, MIS 19a) represents an abrupt
replacement of Protoceratium reticulatum cysts withthe thermophilic Spiniferites pachydermus sensu
Mertens et al. (2015), marking the intrusion of
warmer although still nutrient enriched surface waters. This is interpreted to represent a northward
shift of the Kuroshio Extension Front and exposure
to the southern margin of the Kuroshio–Oyashio
Interfrontal Zone. Pronounced water column stratification seems best to explain the composition of assemblages in this biozone including the near absenceof Echinidinium aculeatum. Ecological informationon the season(s) of maximum growth and cyst production is not available for Spiniferites pachydermus
sensu Mertens et al. (2015), but if its abundance
represents a summer signal then this coincides witha peak in June insolation. These conditions imply anorthward shift of the westerly jet in summer which
would permit the Kuroshio Current to reach higher
latitudes than previously. A simultaneous weakeningof the East Asian Summer Monsoon would also explain water-column stratification at this time.
Abbreviations
AOM: Amorphous organic matter; Byk-E: Ontake-Byakubi-E tephra bed;
EASM: East Asian Summer Monsoon; EAWM: East Asian Winter Monsoon;
KOIZ: Kuroshio–Oyashio Interfrontal Zone; GSSP: Global Boundary Section
and Point; MIS: Marine Isotope Stage; SSS: Sea-surface salinity; SST: Seasurface temperature

6 Supplementary Information
The online version contains supplementary material available at https://doi.
org/10.1186/s40645-021-00438-3.
Additional file 1. Raw data including counts of all dinoflagellate cysts
and other palynomorphs.

Acknowledgements
We are indebted to Kenneth N. Mertens and an anonymous colleague for
their exceptionally constructive and insightful reviews of the manuscript.

Page 35 of 38

Authors’ contributions
MJH proposed the research in discussion with MO and YS. Samples werecollected under the direction of MO who supplied them for analysis. EJB
processed the samples and analyzed them for marine palynology under the
direction of MJH who photographed the specimens, prepared the plates,
and undertook preliminary palynofacies analysis. The MS was written by MJH
and EB with input from YS, MO and YH. All authors read and approved thefinal manuscript.
Authors’ information
EJB is a former MSc student of MJH at Brock University where the initialresearch was undertaken. MJH is a professor at Brock University, Canada,with an interest in Cenozoic dinoflagellate cysts and acritarchs, stratigraphic
classification, and the formal subdivision of the Quaternary System. He has a
Ph.D. from the University of Aberdeen. MO is a professor of Earth Sciences,and presently Vice-Dean of the College of Science, at Ibaraki University,
Japan. He received his Ph.D. from the University of Tokyo. His research interests include magnetostratigraphy and oxygen isotope stratigraphy and theirapplications in paleoceanography and tectonic events during the Cenozoic
in Japan and surrounding areas. YS is an associate professor at the National
Institute of Polar Research, Japan. He received his Ph.D. from the Universityof Tokyo. His research interests focus on cosmogenic radionuclides and theirapplication in Earth sciences, including the precise dating of geomagnetic reversals and the timing of the growth and decay of the Antarctic ice sheets.
YH is a postdoctoral researcher at the Geological Survey of Japan, AIST. He
has a Ph.D. from Ibaraki University. His research includes the magnetostratigraphy and oxygen isotope stratigraphy of the Upper Pliocene and Lower
Pleistocene of central Japan and their utilization for paleoceanographic reconstructions in the northwestern marginal region of the Pacific Ocean during and after the intensification of Northern Hemisphere glaciation.
Funding
This work was supported by a Natural Sciences and Engineering ResearchCouncil of Canada Discovery Grant to MJH, and JSPS KAKENHI grants(16H04068 and 19H00710) awarded to MO.
Availability of data and materials
Data supporting the results reported in this article are provided in Additional
file 1.

Declarations
Competing interests
The authors declare that they have no competing interests.
Author details
1
Department of Earth Sciences, Brock University, St. Catharines, ON L2S 3A1,
Canada. 2Department of Earth Sciences, Ibaraki University, 2-2-1 Bunkyo, Mito,
Ibaraki 310-8512, Japan. 3National Institute of Polar Research, 10-3 Midori-cho,Tachikawa, Tokyo 190-8518, Japan. 4Department of Polar Science, School ofMultidisciplinary Sciences, The Graduate University for Advanced Studies(SOKENDAI), Hayama, Japan. 5Geological Survey of Japan, AIST, Higashi 1-1-1
Central 7, Tsukuba, Ibaraki 305-8567, Japan.
Received: 8 May 2020 Accepted: 28 June 2021

References
Balota EJ (2018) Western Pacific paleoceanography across the Early–Middle
Pleistocene boundary (~773 ka, Marine Isotope Stage 19): dinoflagellate cystsof the Chiba composite section, Japan. MSc dissertation, Brock University
Batten DJ (1996) Palynofacies and palaeoenvironmental interpretation. In:
Jansonius J, McGregor DC (eds) Palynology: principles and applications, vol 3.
American Association of Stratigraphic Palynologists Foundation, Dallas, pp1011–1064
Bonnet S, de Vernal A, Gersonde R, Lembke-Jene L (2012) Modern distribution of
dinocysts from the North Pacific Ocean (37–64°N, 144°E–148°W) in relation tohydrographic conditions, sea-ice and productivity. Mar Micropaleontol 84–85:
87–113

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

Bringué M, Pospelova V, Tappa EJ, Thunell RC (2019) Dinoflagellate cyst
production in the Cariaco Basin: A 12.5 year-long sediment trap study.
Progress Oceanogr 171:175–211. https://doi.org/10.1016/j.pocean.2018.12.007
Cho H-J, Matsuoka K (2001) Distribution of dinoflagellate cysts in surface
sediments from the Yellow Sea and East China Sea. Mar Micropaleontol 42:
103–123
Dale B (1996) Chapter 31. Dinoflagellate cyst ecology: modeling and geologicalapplications; vol. 3. In: Jansonius J, McGregor DC (eds) Palynology: Principles
and applications. American Association of Stratigraphic Palynologists
Foundation, Dallas, pp 1249–1275
Dale B, Fjellså A (1994) Dinoflagellate cysts as paleoproductivity indicators: stateof the art, potential, and limits. In: Zahn R et al. (eds), Carbon Cycling in the
Glacial Ocean: Constraints on the Ocean’s Role in Global Change. NATO ASI
Series, vol. I, 17:521–537
Dale B, Thorsen TA, Fjellså A (1999) Dinoflagellate cysts as indicators of cultural
eutrophication in the Oslofjord, Norway. Estuar Coast Shelf Sci 48(3):371–382.
https://doi.org/10.1006/ecss.1999.0427
De Schepper S, Groeneveld J, Naafs BDA, Van Renterghem C, Hennissen J, Head
MJ, Louwye S, Fabian K (2013) Northern Hemisphere glaciation during the
globally warm early Late Pliocene. Plos One 8(12):e81508. https://doi.org/1
0.1371/journal.pone.0081508
De Schepper S, Head MJ, Groeneveld J (2009) North Atlantic Current variability
through marine isotope stage M2 (circa 3.3 Ma) during the mid-Pliocene.
Paleoceanogr 24(4):24. https://doi.org/10.1029/2008PA001725
de Vernal A, Radi T, Zaragosi S, Van Nieuwenhove N, Rochon A, Allan E, De
Schepper S, Eynaud F, Head MJ, Limoges A, Londeix L, Marret F, Matthiessen
J, Penaud A, Pospelova V, Price A, Richerol T (2020) Distribution of common
modern dinoflagellate cyst taxa in surface sediments of the Northern
Hemisphere in relation to environmental parameters: the new n=1968
database. Mar Micropaleontol 159:101796. https://doi.org/10.1016/j.marmicro.2019.101796
Deflandre G, Cookson IC (1955) Fossil microplankton from Australian late
Mesozoic and Tertiary sediments. Austral J Mar Freshw Res 6(2):242–313
Eaton GL, Fensome RA, Riding JB, Williams GL (2001) Re-evaluation of the statusof the dinoflagellate cyst genus Cleistosphaeridium. Neues Jahrbuch für
Geologie und Paläontologie Abhandlungen 219(1–2):171–205. https://doi.
org/10.1127/njgpa/219/2001/171
Elderfield H, Ferretti P, Greaves M, Crowhurst S, McCave IN, Hodell D, Piotrowski
AM (2012) Evolution of ocean temperature and ice volume through the midPleistocene climate transition. Science 337(6095):704–709. https://doi.org/1
0.1126/science.1221294
Evitt WR (1984) Some techniques for preparing, manipulating and mounting
dinoflagellates. J Micropalaeontol 3(2):11–18. https://doi.org/10.1144/jm.3.2.11
Fujii R, Matsuoka K (2006) Seasonal change of dinoflagellates cyst flux collected
in a sediment trap in Omura Bay, West Japan. J Plankton Res 28(2):131–147.
https://doi.org/10.1093/plankt/fbi106
Gallagher SJ, Kitamura A, Iryu Y, Itaki T, Koizumi I, Hoiles PW (2015) The Pliocene torecent history of the Kuroshio and Tsushima Currents: a multi-proxy approach.
Prog Earth Planet Sci 2(1):17. https://doi.org/10.1186/s40645-015-0045-6
Giaccio B, Regattieri E, Zanchetta G, Nomade S, Renne PR, Sprain CJ, Drysdale RN,
Tzedakis PC, Messina P, Scardia G, Sposato A, Bassinot F (2015) Duration anddynamics of the best orbital analogue to the present interglacial. Geology
2015209(7):603–606. https://doi.org/10.1130/G36677.1
Hanawa K, Mitsudera H (1986) Variation of water system distribution in the
Sanriku coastal area. J Oceanogr Soc Japan 42(6):435–446. https://doi.org/1
0.1007/BF02110194
Haneda Y, Okada M, Kubota Y, Suganuma Y (2020b) Millennial-scale hydrographic
changes in the northwestern Pacific during marine isotope stage 19:
teleconnections with ice melt in the North Atlantic. Earth Planet Sci Let 531:
115936. https://doi.org/10.1016/j.epsl.2019.115936
Haneda Y, Okada M, Suganuma Y, Kitamura T (2020a) A full sequence of the Matuyama–
Brunhes geomagnetic reversal in the Chiba composite section, Central Japan. Prog
Earth Planet Sci 7(1):44. https://doi.org/10.1186/s40645-020-00354-y
Hao Q, Wang L, Oldfield F, Peng S, Qin L, Song Y, Xu B, Qiao Y, Bloemendal J,
Guo Z (2012) Delayed build-up of Arctic ice sheets during 400,000-year
minima in insolation variability. Nature 490(7420):393–396. https://doi.org/1
0.1038/nature11493
Harada K (1984) Study of dinoflagellates from the submarine strata at the KansaiInternational Airport in Osaka Bay off Senshu, Central Japan. In: Nakaseko K(ed) Geological survey of the submarine strata at the Kansai International
Airport in Osaka Bay, Central Japan. Rept. Calamity Sci. Inst, Osaka, pp 77–90

Page 36 of 38

Harland R (1983) Distribution maps of recent dinoflagellate cysts in bottom
sediments from the North Atlantic Ocean and adjacent seas. Palaeontol 26:
321–387
Head MJ (1996a) Modern dinoflagellate cysts and their biological affinities. In:
Jansonius J, DC MG (eds) Palynology: principles and applications, vol 3.
American Association of Stratigraphic Palynologists Foundation, Dallas, pp1197–1248
Head MJ (1996b) Late Cenozoic dinoflagellates from the Royal Society borehole
at Ludham, Norfolk, eastern England. J Paleontol 70(4):543–570. https://doi.
org/10.1017/S0022336000023532
Head MJ (2003) Neogene occurrences of the marine acritarch genus
Nannobarbophora Habib and Knapp, 1982 emend., and the new species N.
gedlii. J Paleontol 77(2):382–385. https://doi.org/10.1017/S0022336000043717
Head MJ (2019) Formal subdivision of the Quaternary System/Period: present
status and future directions. Quat Int 500:32–51. https://doi.org/10.1016/j.qua
int.2019.05.018
Head MJ (2021) Review of the Early–Middle Pleistocene boundary and Marine
Isotope Stage 19. Prog Earth Planet Sci (this issue)
Head MJ, Pillans B, Farquhar SA (2008) The Early–Middle Pleistocene transition:
characterization and proposed guide for the defining boundary. Episodes
31(2):255–259. https://doi.org/10.18814/epiiugs/2008/v31i2/014
Head MJ, Westphal H (1999) Palynology and paleoenvironments of a Pliocene
carbonate platform: the Clino Core, Bahamas. J Paleontol 73(1):1–25. https://doi.org/10.1017/S0022336000027505
Hennissen JAI, Head MJ, De Schepper S, Groeneveld J (2014) Palynologicalevidence for a southward shift of the North Atlantic Current at ~2.6 Ma
during the intensification of late Cenozoic Northern Hemisphere glaciation.
Paleoceanogr 28. https://doi.org/10.1002/2013PA002543
Hennissen JAI, Head MJ, De Schepper S, Groeneveld J (2017) Dinoflagellate cyst
paleoecology during the Pliocene–Pleistocene climatic transition in the
North Atlantic. Palaeogeog Palaeoclimatol Palaeoecol 470:81–108. https://doi.
org/10.1016/j.palaeo.2016.12.023
Hopkins JA, McCarthy FMG (2002) Post-depositional palynomorph degradation in
Quaternary shelf sediments: a laboratory experiment studying the effects ofprogressive oxidation. Palynology 26:167–184
Izumi K, Haneda Y, Suganuma Y, Okada M, Kubota Y, Nishida N, Kawamata M,
Matsuzaki T (2021) Multiproxy sedimentological and geochemical analyses
across the Lower–Middle Pleistocene boundary: chemostratigraphy andpaleoenvironment of the Chiba composite section, central Japan. Prog Earth
Planet Sci 8(10):1–19
Jeong HJ, Du Yoo Y, Kim JS, Seong KA, Kang NS, Kim TH (2010) Growth, feedingand ecological roles of the mixotrophic and heterotrophic dinoflagellates inmarine planktonic food webs. Ocean Sci J 45(2):65–91. https://doi.org/10.1
007/s12601-010-0007-2
Kameo K, Kubota Y, Haneda Y, Suganuma Y, Okada M (2020) Calcareous
nannofossil biostratigraphy of the Lower–Middle Pleistocene boundary of
the GSSP, Chiba composite section in the Kokumoto Formation, Kazusa
Group, and implications for sea-surface environmental changes. Prog Earth
Planet Sci 7(1):36. https://doi.org/10.1186/s40645-020-00355-x
Kawamura H (2002) Marine palynological records in the southern South China Sea
over the last 44 kyr. Doctoral dissertation, Christian-Albrechts-Universität zu Kiel
Kawamura H (2004) Dinoflagellate cyst distribution along a shelf to slope transectof an oligotrophic tropical sea (Sunda Shelf, South China Sea). Phycol Res
52(4):355–375. https://doi.org/10.1111/j.1440-1835.2004.tb00345.x
Kazaoka O, Suganuma Y, Okada M, Kameo K, Head MJ, Yoshida T, Sugaya M,
Kameyama S, Ogitsu I, Nirei H, Aida N, Kumai H (2015) Stratigraphy of the
Kazusa Group, Boso Peninsula: an expanded and highly-resolved marine
sedimentary record from the Lower and Middle Pleistocene of central Japan.
Quat Int 383:116–135. https://doi.org/10.1016/j.quaint.2015.02.065
Kida S, Mitsudera H, Aoki S, Guo X, Ito S, Kobashi F, Komori N, Kubokawa A,
Miyama T, Morie R, Nakamura H, Nakamura T, Nakano H, Nishigaki H, Nonaka
M, Sasaki H, Sasaki YN, Suga T, Sugimoto S, Taguchi B, Takaya K, Tozuka T,
Tsujino H, Usui N (2015) Oceanic fronts and jets around Japan: a review. J
Oceanogr 71:469–497
Kielt J-F (2006) Distribution des assemblages palynologiques et microfaunistiques lelong des côtes Ouest mexicaines. Dissertation, Université du Québec à Montréal
Kitaba I, Hyodo M, Nakagawa T, Katoh S, Dettman DL, Sato H (2017) Geologicalsupport for the Umbrella Effect as a link between geomagnetic field andclimate. Sci Rep 7(1):40682. https://doi.org/10.1038/srep40682
Koike K, Horie Y, Suzuki T, Kobiyama A, Kurihara K, Takagi K, Kaga S-N, Oshima Y(2006) Protoceratium reticulatum in northern Japan: environmental factors

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

associated with seasonal occurrence and related contamination of
yessotoxin in scallops. J Plankton Res 28(1):103–112. https://doi.org/10.1093/
plankt/fbi103
Komatsu K, Hiroe Y (2019) Structure and impact of the Kuroshio nutrient stream. In:
Nagai T, Saito H, Suzuki K, Takahashi M. (eds) Kuroshio Current: physical,
biogeochemical, and ecosystem dynamics. Geophysical Monograph 243:85–104
Kubota Y, Haneda Y, Kameo K, Itaki T, Hayashi H, Shikoku K, Izumi K, Head MJ,
Suganuma Y, Okada M (2021) Paleoceanography of the northwestern Pacificacross the Early–Middle Pleistocene boundary (Marine Isotope Stages 20–18).
Prog Earth Planet Sci 8(29):1–24. https://doi.org/10.1186/s40645-020-00395-3
Laskar J, Robutel P, Joutel F, Gastineau M, Correia ACM, Levrard B (2004) A longterm numerical solution for the insolation quantities of the Earth. AstronAstrophys 428(1):261–285. https://doi.org/10.1051/0004-6361:20041335
Li Z, Pospelova V, Kawamura H, Luo C, Mertens KN, Hernández-Almeida I, Ying K,
Wuh Y, Wui H, Xiang R (2020) Dinoflagellate cyst distribution in surface
sediments from the South China Sea in relation to hydrographic conditions
and primary productivity. Mar Micropaleontol 159:101815. https://doi.org/10.1
016/j.marmicro.2019.101815
Li Z, Pospelova V, Lin H-L, Liu L, Song B, Gong W (2018) Seasonal dinoflagellate
cyst production and terrestrial palynomorph deposition in the East Asian
Monsoon influenced South China Sea: a sediment trap study from theSouthwest Taiwan waters. Rev Palaeobot Palynol 257:117–139. https://doi.
org/10.1016/j.revpalbo.2018.07.007
Limoges A, Kielt JF, Radi T, Ruiz-Fernandez AC, de Vernal A (2010) Dinoflagellate
cyst distribution in surface sediments along the south-western Mexican coast(14.76°N to 24.75°N). Mar Micropaleontol 76(3–4):104–123. https://doi.org/1
0.1016/j.marmicro.2010.06.003
Limoges A, Van Nieuwenhove N, Head MJ, Mertens KN, Pospelova V, Rochon A(2020) A review of rare and less well known extant marine organic-walled
dinoflagellate cyst taxa of the orders Gonyaulacales and Suessiales from theNorthern Hemisphere. Mar Micropaleontol 159:101801. https://doi.org/10.101
6/j.marmicro.2019.101801
Lisiecki LE, Raymo ME (2005) A Pliocene-Pleistocene stack of 57 globally
distributed benthic δ18O records. Paleoceanography 20. https://doi.org/10.1
029/2004PA001071 PA1003
Liu L, Wei N, Gou Y, Li D, Liang Y, Xu D, Liu R, Sui S, Jiang T (2017) Seasonalvariability of Protoceratium reticulatum and yessotoxins in Japanese scallop
Patinopecten yessoensis in northern Yellow Sea of China. Toxicon 139:31–40.
https://doi.org/10.1016/j.toxicon.2017.09.015
Locarnini RA, Mishonov AV, Antonov JI, Boyer TP, Garcia HE, Baranova OK, Zweng
MM, Paver CR, Reagan JR, Johnson DR, Hamilton M, Seidov D (2013) World
Ocean Atlas 2013, Volume 1: Temperature. Levitus S (ed), Mishonov A(technical ed) NOAA Atlas NESDIS 73, 40 pp
Magurran AE (2004) Measuring biological diversity. Blackwell Science Ltd, Oxford,
pp i–vii + 1–i–vii 256
Matsuoka K (1976) Recent thecate and fossilized dinoflagellates off Hachinohe
coast, northeastern Japan. Publ Seto Mar Biol Lab 23 (3/5):351–369, pl. I–IV
Matsuoka K (1985) Organic-walled dinoflagellate cysts from surface sediments ofNagasaki Bay and Senzaki Bay, West Japan. Bull Fac Liberal Arts Nagasaki
Univ (Nat Sci) 25:1–17
Matsuoka K (1987) Organic-walled dinoflagellate cysts from surface sediments of
Akkeshi Bay and Lake Saroma, North Japan. Bull Fac Liberal Arts Nagasaki
Univ (Nat Sci) 28:35–123
Matsuoka K (1992) Species diversity of modern dinoflagellate cysts in surface
sediments around the Japanese Islands. In: Head MJ, Wrenn JH (eds)
Neogene and Quaternary Dinoflagellate Cysts and Acritarchs. American
Association of Stratigraphic Palynologists Foundation, Dallas, pp 33–53
Matsuoka K (1994) Holocene dinoflagellate cyst assemblages in shallow water
sediments of the Tsushima Islands, west Japan. Rev Palaeobot Palynol 84(12):155–168. https://doi.org/10.1016/0034-6667(94)90048-5
Matsuoka K (1999) Eutrophication process recorded in dinoflagellate cyst
assemblages—a case of Yokohama Port, Tokyo Bay, Japan. Sci Total Environ
231(1):17–35. https://doi.org/10.1016/S0048-9697(99)00087-X
Matthiessen J, de Vernal A, Head M, Okolodkov Y, Zonneveld K, Harland R (2005)
Modern organic-walled dinoflagellate cysts in Arctic marine environments
and their (paleo-) environmental significance. Paläontol Zeitschrift 79(1):3–51.
https://doi.org/10.1007/BF03021752
Mertens KN, Aydin H, Uzar S, Takano Y, Yamaguchi A, Matsuoka K (2015)
Relationship between the dinoflagellate cyst Spiniferites pachydermus and
Gonyaulax ellegaardiae sp. nov. from Izmir Bay, Turkey, and molecularcharacterization. J Phycol 51(3):560–573. https://doi.org/10.1111/jpy.12304

Page 37 of 38

Mertens KN, Gu H, Gurdebeke PR, Takano Y, Clarke D, Aydin H, Li Z, Pospelova V,
Shin HH, Li Z, Matsuoka K, Head MJ (2020) A review of rare, poorly known,
and morphologically problematic extant marine organic-walled dinoflagellate
cyst taxa of the orders Gymnodiniales and Peridiniales from the Northern
Hemisphere. Mar Micropaleontol 159:101773. https://doi.org/10.1016/j.marmicro.2019.101773
Mertens KN, Van Nieuwenhove N, Gurdebeke PR, Aydin H, Bogus K, Bringué M,
Dale B. De Schepper S, de Vernal A, Ellegaard M, Grothe A, Gu Haifeng, Head
MJ, Heikkilä M, Limoges A, Londeix L, Louwye S, Marret F, Masure E,
Matsuoka K, Mudie PJ, Penaud A, Pospelova V, Price AM, Ribeiro S, Rochon A,
Sangiorgi F, Schreck M, Torres V, Uzar S, Versteegh GJM, Warny S, Zonneveld
K (2018) The dinoflagellate cyst genera Achomosphaera Evitt 1963 andSpiniferites Mantell 1850 in Pliocene to modern sediments: a summary ofround table discussions. Palynology 42: supplement 1:10–44
Morzadec-Kerfourn M-T (1977) Les Kystes de dinoflagellés dans les sédiments
Récents le long des côtes Bretonnes. Revue de Micropaléntologie 20:157–166
Nagai T, Clayton S, Uchiyama Y (2019) Multiscale routes to supply nutrients
through the Kuroshio nutrient stream. In: Nagai T, Saito H, Suzuki K,
Takahashi M. (eds) Kuroshio Current: physical, biogeochemical, andecosystem dynamics. Geophysical Monograph 243:105–125
Nishida N, Kazaoka O, Izumi K, Suganuma Y, Okada M, Yoshida T, Ogitsu I, Nakazato
H, Kameyama S, Kagawa A, Morisaki M, Nirei H (2016) Sedimentary processes
and depositional environments of a continuous marine succession across theLower–Middle Pleistocene boundary: Kokumoto Formation, Kazusa Group,
central Japan. Quat Int 397:3–15. https://doi.org/10.1016/j.quaint.2015.06.045
Nomade S, Bassinot F, Marino M, Simon Q, Dewilde F, Maiorano P, Isguder G,
Blamart D, Girone A, Scao V, Pereira A, Toti F, Bertini A, Combourieu-Nebout
N, Peral M, Bourles DL, Petrosino P, Gallicchio S, Ciaranfi N (2019) Highresolution foraminifer stable isotope record of MIS 19 at Montalbano Jonico,
southern Italy: a window into Mediterranean climatic variability during a loweccentricity interglacial. Quat Sci Rev 205:106–125. https://doi.org/10.1016/j.
quascirev.2018.12.008
Okada M, Suganuma Y, Haneda Y, Kazaoka O (2017) Paleomagnetic direction andpaleointensity variations during the Matuyama-Brunhes polarity transition
from a marine succession in the Chiba composite section of the Boso
Peninsula, central Japan. Earth Planets Space 69(1):45. https://doi.org/10.11
86/s40623-017-0627-1
Okazaki Y, Timmermann A, Menviel L, Harada N, Abe-Ouchi A, Chikamoto MO,
Mouchet A, Asahi H (2010) Deepwater formation in the North Pacific during
the Last Glacial Termination. Science 329(5988):200–204. https://doi.org/1
0.1126/science.1190612
Paez-Reyes M, Head MJ (2013) The Cenozoic gonyaulacacean dinoflagellate genera
Operculodinium Wall, 1967 and Protoceratium Bergh, 1881 and their phylogenetic
relationships. J Paleontol 87(5):786–803. https://doi.org/10.1666/12-103
Penaud A, Hardy W, Lambert C, Marret F, Masure E, Servais T, Siano R, Wary M,
Mertens KN (2018) Dinoflagellate fossils: Geological and biologicalapplications. Rev micropaléontol 61(3-4):235–254. https://doi.org/10.1016/j.
revmic.2018.09.003
Pospelova V, de Vernal A, Pedersen TF (2008) Distribution of dinoflagellate cysts
in surface sediments from the northeastern Pacific (43–25°N) in relation tosea-surface conditions and upwelling. Mar Micropaleontol 68(1-2):21–48.
https://doi.org/10.1016/j.marmicro.2008.01.008
Pospelova V, Kim S-J (2010) Dinoflagellate cysts in recent estuarine sedimentsfrom aquaculture sites of southern South Korea. Mar Micropaleontol 76(1-2):
37–51. https://doi.org/10.1016/j.marmicro.2010.04.003
Pospelova V, Zonneveld KAF, Heikkilä M, Bringué M, Price AM, Esenkulova S,
Matsuoka K (2018) Seasonality in Spiniferites cyst production: a review of
sediment trap studies. Palynology 42(sup1):162–181. https://doi.org/10.1080/
01916122.2018.1465738
Qiu B (2019) Kuroshio and Oyashio currents. In: Cochran SJK, Bokuniewicz HJ,
Yager PL (eds) Encyclopedia of Ocean Sciences, 3rd edn. Academic, London,
pp 384–394. https://doi.org/10.1016/B978-0-12-409548-9.11295-3
Radi T, de Vernal A (2004) Dinocyst distribution in surface sediments from thenortheastern Pacific margin (40–60°N) in relation to hydrographic conditions,productivity and upwelling. Rev Palaeobot Palynol 128(1-2):169–193. https://doi.org/10.1016/S0034-6667(03)00118-0
Radi T, de Vernal A, Peyron O (2001) Relationships between dinocyst
assemblages in surface sediments and hydrographic conditions in the Beringand Chukchi seas. J Quat Sci 16(7):667–680. https://doi.org/10.1002/jqs.652
Rochon A, de Vernal A, Turon J-L, Matthiessen J, Head MJ (1999) Distribution ofrecent dinoflagellate cysts in surface sediments from the North Atlantic Ocean

Balota et al. Progress in Earth and Planetary Science(2021) 8:48

and adjacent seas in relation to sea-surface parameters. American Association ofStratigraphic Palynologists, Contributions Series, No. 35, pp 1–152
Rossignol M (1964) Hystrichosphères du Quaternaire en Méditerranée orientale,dans les sédiments Pléistocènes et les boues marines actuelles. Rev
micropaléontol 7:83–99
Saito H (2019) The Kuroshio: its recognition, scientific activities and emerging
issues. In: Nagai T, Saito H, Suzuki K, Takahashi M (eds) Kuroshio Current:
physical, biogeochemical, and ecosystem dynamics. Geophysical Monograph
243, 3–11, doi: https://doi.org/10.1002/9781119428428.ch1
Salgado P, Figueroa RI, Ramilo I, Bravo I (2017) The life history of the toxic marine
dinoflagellate Protoceratium reticulatum (Gonyaulacales) in culture. Harmful
Algae 68:67–81. https://doi.org/10.1016/j.hal.2017.07.008
Sayın E, Pazı I, Eronat C (2006) Investigation of water masses in İzmir Bay, western
Turkey. Turkish J Earth Sci 15:343–372
Schlitzer R (2015) Ocean Data View, http://odv.awi.de.
Schnepf E, Elbrächter M (1992) Nutritional strategies in dinoflagellates—a review
with emphasis on cell biological aspects. Europ J Protistol 28:3–24, 1, doi:
https://doi.org/10.1016/S0932-4739(11)80315-9
Shin HH, Lia Z, Lima D, Leeb K-W, Seoc MH, Lim WA (2018) Seasonal productionof dinoflagellate cysts in relation to environmental characteristics in JinhaeMasan Bay, Korea: One-year sediment trap observation. Estuar Coast Shelf Sci
215:83–93. https://doi.org/10.1016/j.ecss.2018.09.031
Shin HH, Mizushima K, Oh SJ, Park JS, Noh IH, Iwataki M, Matsuoka K, Yoon YH(2010) Reconstruction of historical nutrient levels in Korean and Japanese
coastal areas based on dinoflagellate cyst assemblages. Mar Poll Bull 60(8):1243–1258. https://doi.org/10.1016/j.marpolbul.2010.03.019
Shin HH, Park JS, Kim Y-O, Baek SH, Lim D, Yoon YH (2012) Dinoflagellate cyst
production and flux in Gamak Bay, Korea: a sediment trap study. Mar
Micropaleontol 94–95:72–79
Simon Q, Suganuma Y, Okada M, Haneda Y, Team ASTER (2019) High-resolution
10
Be and paleomagnetic recording of the last polarity reversal in the Chiba
composite section: Age and dynamics of the Matuyama–Brunhes transition.
Earth Planet Sci Let 519:92–100. https://doi.org/10.1016/j.epsl.2019.05.004
Stockmarr J (1971) Tablets with spores used in absolute pollen analysis. Pollen
Spores 13:615–621
Suganuma Y, Haneda Y, Kameo K, Kubota Y, Hayashi H, Itaki T, Okuda M, Head MJ,
Sugaya M, Nakazato H, Igarashi A, Shikoku K, Hongo M, Watanabe M, Satoguchi
Y, Takeshita Y, Nishida N, Izumi K, Kawamura K, Kawamata M, Okuno J, Yoshida
T, Ogitsu I, Yabusaki H, Okada M (2018) Paleoclimatic and paleoceanographic
records of Marine Isotope Stage 19 at the Chiba composite section, central
Japan: a reference for the Early–Middle Pleistocene boundary. Quat Sci Rev 191:
406–430. https://doi.org/10.1016/j.quascirev.2018.04.022
Suganuma Y, Okada M, Head MJ, Kameo K, Haneda Y, Hayashi H, Irizuki T, Itaki T,
Izumi K, Kubota Y, Nakazato H, Nishida N, Okuda M, Satoguchi Y, Simon Q,
Takeshita Y (in press) Formal ratification of the Global Boundary Stratotype
Section and Point (GSSP) for the Chibanian Stage and Middle Pleistocene
Subseries of the Quaternary System: the Chiba Section, Japan. Episodes,
https://doi.org/10.18814/epiiugs/2020/020080
Suganuma Y, Okada M, Horie K, Kaiden H, Takehara M, Senda R, Kimura J, Haneda
Y, Kawamura K, Kazaoka O, Head MJ (2015) Age of Matuyama–Brunhes
boundary constrained by U-Pb zircon dating of a widespread tephra.
Geology 43(6):491–494. https://doi.org/10.1130/G36625.1
Sun YB, Clemens SC, An ZS, Yu ZW (2006) Astronomical timescale andpalaeoclimatic implication of stacked 3.6-Myr monsoon records from the
Chinese Loess Plateau. Quat Sci Rev 25(1-2):33–48. https://doi.org/10.1016/j.
quascirev.2005.07.005
Taguchi B, Nakamura H, Nonaka M, Komori N, Kuwano-Yoshida A, Takaya K, Goto
A (2012) Seasonal evolutions of atmospheric response to decadal SST
anomalies in the North Pacific subarctic frontal zone: observations and acoupled model simulation. J Climate 25(1):111–139. https://doi.org/10.1175/
JCLI-D-11-00046.1
Takeshita Y, Matsushima N, Teradaira H, Uchiyama T, Kumai H (2016) A marker
tephra bed close to the Middle Pleistocene boundary: distribution of the
Ontake-Byakubi tephra in central Japan. Quat Int 397:27–38. https://doi.org/1
0.1016/j.quaint.2015.03.054
Traverse A, Ginsburg RN (1966) Palynology of the surface sediments of Great
Bahama Bank, as related to water movement and sedimentation. Mar Geol
4(6):417–459. https://doi.org/10.1016/0025-3227(66)90010-7
Tyson RV (1995) Sedimentary organic matter. Organic facies and palynofacies.
Chapman and Hall, London, pp i–xvii+1–i–xvi615

Page 38 of 38

Tzedakis PC, Channell JET, Hodell DA, Kleiven HF, Skinner LC (2012) Determining
the natural length of the current interglacial. Nat Geosci 5(2):138–141.
https://doi.org/10.1038/ngeo1358
Van Nieuwenhove N, Head MJ, Limoges A, Pospelova V, Mertens KN, Matthiessen
J, De Schepper S, de Vernal A, Eynaud F, Londeix L, Marret F, Peynaud A,
Radi T, Rochon A (2020) An overview and brief description of common
marine organic-walled dinoflagellate cyst taxa occurring in surface sedimentsof the Northern Hemisphere. Mar Micropaleontol 159:101814. https://doi.
org/10.1016/j.marmicro.2019.101814
Vásquez-Bedoya LF, Radi T, Ruiz-Fernández AC, de Vernal A, Machain-Castillo ML,
Kielt JF, Hillaire-Marcel C (2008) Organic-walled dinoflagellate cysts andbenthic foraminifera in coastal sediments of the last century from the Gulf ofTehuantepec, South Pacific Coast of Mexico. Mar Micropaleontol 68(1-2):49–
65. https://doi.org/10.1016/j.marmicro.2008.03.002
Vavrus SJ, He F, Kutzbach JE, Ruddiman WF, Tzedakis PC (2018) Glacial inceptionin Marine Isotope Stage 19: an orbital analog for a natural Holocene climate.
Sci Rep 8(1):10213. https://doi.org/10.1038/s41598-018-28419-5
Versteegh GJM (1994) Recognition of cyclic and non-cyclic environmental
changes in the Mediterranean Pliocene: a palynological approach. Mar
Micropaleontol 23(2):147–183. https://doi.org/10.1016/0377-8398(94)90005-1
Versteegh GJM (1995) Palaeoenvironmental changes in the Mediterranean andNorth Atlantic in relation to the onset of northern hemisphere glaciations (2.
5 Ma B.P.)—a palynological approach. Published doctoral dissertation: CIP
Gegevens Koninklijke Bibliotheek, Den Haag, 134 p
Versteegh GJM, Zonneveld KAF (1994) Determination of (palaeo-)ecologicalpreferences of dinoflagellates by applying detrended and canonicalcorrespondence analysis to Late Pliocene dinoflagellate cyst assemblages ofthe south Italian Singa section. Rev Palaeobot Palynol 84(1-2):181–199.
https://doi.org/10.1016/0034-6667(94)90050-7
Wall D, Dale B (1966) Living fossils in western Atlantic plankton. Nature 211(5053):
1025–1026. https://doi.org/10.1038/2111025a0
Wall D, Dale B, Lohman GP, Smith WK (1977) The environmental and climatic
distribution of dinoflagellate cysts in modern marine sediments from regionsin the North and South Atlantic oceans and adjacent areas. Mar
Micropaleontol 2:121–200. https://doi.org/10.1016/0377-8398(77)90008-1
Wang N, Mertens KN, Krock B, Luo Z, Derrien A, Pospelova V, Liang Y, Bilien G,
Smith KF, De Schepper S, Wietkamp S, Tillmann U, Gu H (2019) Cryptic
speciation in Protoceratium reticulatum (Dinophyceae): Evidence frommorphological, molecular and ecophysiological data. Harmful Algae 88(101610):1–15, 101610, doi: https://doi.org/10.1016/j.hal.2019.05.003
Yin QZ, Berger A (2012) Individual contribution of insolation and CO2 to theinterglacial climates of the past 800,000 years. Climate Dynamics 38(3-4):709–
724. https://doi.org/10.1007/s00382-011-1013-5
Zonneveld KAF, Marret F, Versteegh GJM, Bogus K, Bonnet S, Bouimetarhan I,
Crouch E, de Vernal A, Elshanawany R, Edwards L, Esper O, Forke S, Grøsfjeld
K, Henry M, Holzwarth U, Kielt J-F, Kim S-Y, Ladouceur S, Ledu D, Chen L,
Limoges A, Londeix L, Lu SH, Mahmoud MS, Marino G, Matsouka K [sic],
Matthiessen J, Mildenhal DC [sic], Mudie P, Neil HL, Pospelova V, Qi Y, Radi T,
Richerol T, Rochon A, Sangiorgi F, Solignac S, Turon J-L, Verleye T, Wang Y,
Wang Z, Young M (2013) Atlas of modern dinoflagellate cyst distribution
based on 2405 data points. Rev Palaeobot Palynol 191:1–197, doi: https://doi.
org/10.1016/j.revpalbo.2012.08.003
Zweng MM, Reagan JR, Antonov JI, Locarnini RA, Mishonov AV, Boyer TP, Garcia
HE, Baranova OK, Johnson DR, Seidov D, Biddle MM (2013) World Ocean
Atlas 2013, vol. 2: Salinity. In: Levitus S (ed), Mishonov A (technical ed) NOAA
Atlas NESDIS, vol. 74, 39 pp

Publisher’s NoteSpringer Nature remains neutral with regard to jurisdictional claims inpublished maps and institutional affiliations.