ORIGINAL PAPER

Biotic response of benthic foraminifera in Aso-kai lagoon,central Japan, to changes in terrestrial climate and oceanconditions (~AD 700–1600)

Hiroyuki Takata • Satoshi Tanaka • Koji Seto •

Saburo Sakai • Katsumi Takayasu •

Boo-Keun Khim

Received: 12 November 2012 / Accepted: 1 January 2014 / Published online: 16 January 2014

� Springer Science+Business Media Dordrecht 2014

Abstract We investigated responses of shallow-

water benthic foraminifera to changes in climate and

ocean conditions, using sediment core ASC2 from

Aso-kai lagoon, central Japan. Six AMS 14C dates

reveal that the studied interval corresponds to sedi-

ments deposited from *AD 700 to 1600. Sulfur

content of the bulk sediment and multi-dimensional

scaling (MDS) axis 1 of fossil benthic foraminifera

indicate that the composition of the benthic forami-

nifera community was closely related to dissolved

oxygen (DO) concentration in the hypolimnion. The

sulfur content and MDS axis 1 also revealed two shifts

over the 900-year interval. In the first phase (*AD

700–1250), the Shannon–Wiener Index (H0), E (S200),

evenness and rank abundance curve (RAC) kurtosis

indicate a gradual deterioration in structure of the

benthic foraminifera community. In that period, there

are statistically significant correlations between the

faunal composition (MDS axis 1) and faunal structure

[Shannon–Wiener (H0), E (S200), evenness and RAC

kurtosis]. In the second phase (*AD 1250–1600),

however, faunal composition and structure show no

marked correspondence. Instead, abundance of ben-

thic foraminifera fluctuated on a scale of *200 years.

Thus, a shift in the biotic response of benthic

foraminifera in Aso-kai lagoon occurred in ca. AD

1250. Gradual deterioration of benthic foraminifera,

with taxonomic losses, is consistent with declining DO

in the first phase, possibly associated with the

increasing influence of the Tsushima Warm Current.

Electronic supplementary material The online version ofthis article (doi:10.1007/s10933-014-9764-8) contains supple-mentary material, which is available to authorized users.

H. Takata � K. Seto

Research Center for Coastal Lagoon Environments,

Shimane University, Matsue 690-8504, Japan

H. Takata

Marine Research Institute, Pusan National University,

Busan 609-735, Korea

S. Tanaka

Faculty of Education, Kyoto University of Education,

Kyoto 612-8522, Japan

S. Sakai

Institute of Biogeosciences, Japan Agency for Marine-

Earth Science and Technology, Yokosuka 237-0061,

Japan

K. Takayasu

Shimane University, Matsue 690-8504, Japan

B.-K. Khim (&)

Department of Oceanography, Pusan National University,

Busan 609-735, Korea

e-mail: bkkhim@pusan.ac.kr

123

J Paleolimnol (2014) 51:421–435

DOI 10.1007/s10933-014-9764-8

The possibility that closure of Aso-kai lagoon and

development of the sand bar affected benthic foram-

inifera cannot, however, be ruled out. No correspond-

ing response was observed in the second phase, during

which there was no distinct taxonomic loss. Large

variations in abundance, however, were a consequence

of strength of the East Asian summer and winter

monsoons. The shift in the biotic response of benthic

foraminifera in Aso-kai lagoon during the period AD

700–1600 was apparently a result of changes in

climate and ocean conditions on the East Asian

continental margin.

Keywords Benthic foraminifera � Biotic

response � Tsushima Warm Current � East Asian

monsoon � Aso-kai lagoon

Introduction

Centennial- to millennial-scale climate and environ-

mental changes in East Asia are influenced by activity

of the East Asian monsoon (Yamada et al. 2010). The

behavior of the East Asian monsoon has been inferred

from proxy climate records and historical archives in

China and Japan, such as stable oxygen isotopes in

stalagmites (Wang et al. 2005; Zhang et al. 2008), tree-

rings (Kitagawa and Matsumoto 1995) and lake

sediment records (Nakagawa et al. 2006; Chu et al.

2009; Liu et al. 2009; Yamada et al. 2010). These

studies revealed that the activity of the East Asian

monsoon is linked to variation in summer insolation

and solar activity (Wang et al. 2005; Nakagawa et al.

2006).

Surface-water properties in the Northwestern

Pacific and Sea of Japan (East Sea) influence centen-

nial- to millennial-scale climate and environmental

conditions in East Asia, especially along the conti-

nental margins. For example, pulses in the Td’ ratio

(warm-water to cold-water diatoms) from fossil

records of hemipelagic diatoms in the Northwestern

Pacific region are related to fluctuations of the

Kuroshio and Tsushima Warm Current (Kanaya and

Koizumi 1966; Koizumi 1989; Koizumi and Sakam-

oto 2010). The Td’ ratio is considered an indicator of

the Tsushima Warm Current in the Sea of Japan (East

Sea) (Koizumi 1989, 2008; Khim et al. 2005). In

particular, the Td’ ratio shows cyclicities on the order

of 6,000, 2,400, 1,600 and 300–400 years. Among

them, the 1,600-year cycle might be related to Bond

events (*1,500-year cycle). In core MD01-2401 from

the Northwestern Pacific, Isono et al. (2009) reported

that variations in alkenone-derived sea surface tem-

perature (SST) were consistent with Bond events

(*1,500-year fluctuations). Because surface currents

transport heat to the East Asian continental margin,

their fluctuations are important for understanding

climate and environmental variations in that region.

Coastal environments along the East Asian conti-

nental margin have been affected by both terrestrial

climate (East Asian monsoon) and ocean conditions

(Tsushima Warm Current). Recent paleontological

studies postulated that benthic foraminifera (Rhizaria)

responded sensitively to decade-order sea-level

changes in brackish-water lagoons, as a consequence

of seawater inflow prior to the 1980s (Lake Nakaumi:

Nomura 2003; Lake Obuchi-numa: Nomura et al.

2006; Kumihama Bay: Nomura et al. 2008; Lake

Kugushi: Nomura and Kawano 2010). Nomura (2003)

stated that centimeter-scale sea-level changes were

observed in the twentieth century along the coasts of

the Japanese Islands, with high sea levels in the 1940s–

1950s and low levels in the 1960s–1970s. Nomura

et al. (2008) later suggested that such sea-level

fluctuations were generally related to Pacific Decadal

Oscillations (Mantua and Hare 2002) and that benthic

foraminifera responded to the climate-driven changes

of seawater inflow to the lagoons. Thus, shallow-water

biota provides a useful proxy for climate and ocean-

ographic conditions in coastal regions. We assume that

similar biotic responses in coastal environments,

related to fluctuations in terrestrial and oceanic

climate, occurred prior to the twentieth century, but

there are few studies on the response of shallow-water

biota in coastal regions of the East Asian continental

margin.

Aso-kai lagoon is located on the coast of central

Japan (Fig. 1). Presently, the hypolimnion of the

lagoon is nearly anoxic throughout most of the year

(Nakanishi et al. 1979; Takata et al. 2005a). Takata

et al. (2006a) investigated fossil benthic foraminifera

in Aso-kai lagoon to understand environmental

changes that occurred over the past 1,200 years. They

concluded that relative to present, prior to about AD

1600, the lagoon received a greater quantity of

seawater, which entered through a wide channel in

the barrier sand bar. They also concluded that there

were several cycles in the absolute and relative

422 J Paleolimnol (2014) 51:421–435

123

abundances of benthic foraminifera. They did not,

however, address changes in the benthic foraminifera

prior to 400 years ago because of poor age constraint

on their record.

Sedimentation rate in the lagoon is generally higher

(several mm/year) than that in hemipelagic sediments.

This rapid deposition enables investigation of centen-

nial-scale variations in proxy environmental records

from the lagoon sediments. Additionally, benthic

foraminifera respond to multiple variables in the

aquatic environment, including salinity, DO and

trophic state. Thus, analyses of both fossil benthic

foraminifera and sediment geochemistry in Aso-kai

lagoon allowed us to address the biotic response of the

coastal ecosystem to influences of both climate and

ocean conditions on the East Asian continental

margin. We studied fossil benthic foraminifera and

sediment geochemistry in well-dated core ASC2 from

Aso-kai lagoon to: (1) describe the biotic response of

benthic foraminifera during the period *AD

700–1600 and (2) clarify how the coastal ecosystem

responded to changes in climate and ocean conditions

on a centennial timescale.

Materials and methods

Study area

Aso-kai lagoon is a brackish lagoon on the coast of the

Sea of Japan (East Sea). It has an area of approxi-

mately 4.9 km2 and a maximum water depth of 13 m

(Fig. 1). The lagoon is connected to Miyazu Bay, one

of the small embayments of Wakasa Bay. It is largely

separated from Miyazu Bay by sand bars (‘‘Amano-

hashidate’’ and ‘‘Sho-tenkyo’’), and only connected by

a narrow channel, called ‘‘Kiredo’’ (*4 m deep),

which branches into two small parts in its southern

area (Fig. 1). Epilimnetic water temperature, salinity

and DO show strong seasonal variability, whereas the

hypolimnion varies little (Takata et al. 2005a). Salinity

of hypolimnetic water ([30 %) is nearly equal to

seawater. Because of density stratification of the

lagoon water, vertical mixing to the hypolimnion is

limited, and below 10 m water depth, the water is

nearly anoxic for C 8 months of the year. Inflow of

oxygen-rich seawater to the lagoon hypolimnion

occurs only during winter (Nakanishi et al. 1979;

Takata et al. 2005a). Renewal and oxygenation of deep

water in winter, however, is restricted to locations

adjacent to the sand bar, and the hypolimnion of the

interior lagoon remains nearly anoxic throughout most

of the year (Takata et al. 2005a). Modern benthic

foraminifera indicate oxygen-poor hypolimnetic

waters. The foraminiferal fauna of the near-anoxic

hypolimnion in the central to inner parts of the lagoon

is characterized by dominance of Virgulinella fragilis,

whereas Trochammina cf. japonica is common in the

seasonally oxygen-poor area adjacent to the sand bar

(Takata et al. 2005a).

In the past, Aso-kai lagoon was a small inlet of

Miyazu Bay (Hirai 1995). According to Hirai (1995),

referring to a study of historical archives by S. Odani,

the main sand bar (Amano-hashidate) developed

slowly southwestward after ca. 6–5 ka BP. In contrast,

historical archives and paintings of the lagoon indicate

the Sho-tenkyo sand bar developed rapidly, during the

Edo era (AD 1603–1868), with reclamation of the

southeastern corner of the lagoon, close to the channel,

for rice agriculture. It is believed that during the period

Fig. 1 Location and bathymetry of Aso-kai lagoon. Solid circle

represents the coring site of core ASC2. TWC Tsushima Warm

Current

J Paleolimnol (2014) 51:421–435 423

123

covered by our study (*AD 700–1600), Aso-kai

lagoon was connected to Miyazu Bay through a wider

channel, without the Sho-tenkyo sand bar. This is

supported by several paintings of the lagoon during the

Muromachi era (AD 1336–1573) (Hirai 1995). These

paleogeographic inferences are largely consistent with

the paleoenvironmental interpretation of Takata et al.

(2006a), in terms of the timing of establishment *AD

1600, of nearly year-round hypoxia in Aso-kai lagoon.

Sediment core ASC2

In this study we re-analyzed a sediment core (ASC2)

that had been investigated previously by Takata et al.

(2005b, 2006a). On 25 July 2002, core ASC2 was

collected from the central part of Aso-kai lagoon

(35�33.7850N, 135�10.5570E), in 11.4 m of water,

using a Mackereth-type piston corer (Fig. 1). Core

ASC2 is 399 cm long. The lithology of core ASC2

consists of black to dark gray mud that possesses

distinct or faint laminations, or is bioturbated. Lami-

nations were observed in the following intervals: 75–0,

125–90, 160–130, 290–260 and 314–302 cm (Fig. 2).

The 160–130 and 290–260 cm laminated intervals are

correlated with intervals of high sulfur content in other

sediment cores from this lagoon (Tanaka unpublished

data; Takata et al. 2006a). No obvious erosional

surface was identified. Lithological features such as

lamination frequency were used to divide the core into

a lower and upper section at 144 cm depth.

Five AMS 14C dates were obtained on a plant

sample and four mollusc shells from core ASC2, at the

University of Arizona Radiocarbon Laboratory

(Table 1). In a previous investigation (Takata et al.

2006a), a 14C age was determined on a mollusc shell at

327 cm. That radiocarbon age was converted to a

calendar age using CALIB 6.0.0 (Stuiver et al. 2005).

New dates were calibrated using IntCal09 for plant

debris and Marine09 for mollusc shells (Reimer et al.

2009). No DR value has been reported for reservoir

effects on marine-organism carbonate in the southern

Sea of Japan (East Sea). We calculated two calendar

ages for each sample, one assuming a DR value of 0, i.e.

the average value of the global reservoir in the ocean

without the influence of deep water, and one with

44 ± 24, the average value for the northern Sea of

Japan (East Sea) (Kuzmin et al. 2001) (Table 1). The

two approaches to age calibration yielded differences

of \50 year. Quantification of the reservoir effect is

complicated by mixing of freshwater runoff and

marine water in the lagoon (Yamaguchi et al. 2004).

Ultimately, we adopted DR = 0 to obtain calendar

ages. Average sedimentation rates (mm year-1)

between dated samples in the core were 1.3

(368–327 cm), 7.6 (327–292 cm), 1.7 (292–250 cm),

3.5 (250–199 cm) and 4.5 (199–135 cm) (Fig. 3). Core

ASC2 records the past 1,300 years of paleoenviron-

mental changes and our study interval encompasses the

time from the late part of the Dark Age Cold Period,

through the Medieval Warm Period in Europe, to the

early part of the Little Ice Age.

0

100

200

300

400

Dep

th (

cm)

895(+48 / -52)

307(+9 / -22, +99 / +114)

595(+35 / -36)

Upp

er p

art

Low

er p

art

Mud with distinct lamination

Mud with obscure lamination

Massive mud

Molluscan fossil

Wood fossil

Echinoid fossil

1212(+42 / -39)

450(+36 / -28)

849(+50 / -39)

Fig. 2 Columnar sections of core ASC2 (modified from Takata

et al. 2006a). Ticks in the lower part of the core indicate horizons

used for sediment geochemical and foraminiferal analyses.

Calendar ages (cal year BP) are shown at the right

424 J Paleolimnol (2014) 51:421–435

123

Analytical methods

Core sediments were sampled for foraminifera and

other variables at 1-cm intervals. Samples were split

into two parts for sedimentological and foraminifera

analyses. Subsamples were weighed immediately after

separation. Water content of each subsample for

sedimentological analysis was determined by weight

loss after drying at 70 �C. Dry weights of subsamples

for foraminifera analysis were estimated from the wet

weight of the foraminifera subsample and the water

content of the subsample for sedimentological ana-

lysis from the same depth.

Prior to foraminifera analysis, subsamples were

washed on a 74-lm-mesh sieve (Oda 1978), after

which residues were dried at 70 �C. Benthic foram-

inifera specimens were picked from 41 samples in this

study and were combined with the 12 published data of

Takata et al. (2005b), resulting in 53 samples taken

4 cm apart. Between 200 and 300 specimens were

collected from split aliquots. Specimens were identi-

fied and counted using a binocular stereomicroscope.

Taxonomic assignments followed Matoba (1970) and

Nomura and Seto (2002). Generic classification refers

to Loeblich and Tappan (1987).

To evaluate the faunal composition statistically,

non-metric multi-dimensional scaling (MDS) was

applied on Bray-Curtis distances. A square-root

transformed data matrix of relative abundance, con-

sisting of 40 taxa (those with at least three counts in at

least one sample) and 53 samples (more than 70

specimens) was analyzed with the statistical program-

ming environment R (R Development Core Team

2010), using the vegan community ecology package

(Oksanen et al. 2010). We determined the correlation

between stratigraphic changes of the score of each

MDS axis and relative abundance of each taxon.

Additionally, to evaluate the stratigraphic change in

faunal structure, the Shannon–Wiener diversity index

(H0) and rarefaction (E (S200)) were calculated for each

sample. The evenness measure of Buzas and Gibson

(1969) and RAC (rank abundance curve) kurtosis were

also calculated for each sample. Calculations of the

Shannon–Wiener index (H0) and evenness were per-

formed in Microsoft Excel. Rarefaction (E (S200)) was

calculated using the statistical programming environ-

ment R with the vegan community ecology package.

Dep

th (

cm)

Age (cal BP)

0

50

100

150

200

250

300

350

4000 200 400 600 800 1000 1200 1400

Stu

dy in

terv

al

1.3 mm yr

-1

7.6 mm yr

-1

1.7 mm yr

-1

3.5 mm yr

-1

4.5 mm yr

-1

Fig. 3 Age-depth plot for core ASC2 with 1-r uncertainty for

age estimation. The shaded area shows the interval studied in

this investigation

Table 1 Radiocarbon ages in six horizons of core ASC2

Depth

(cm)

Material d13C Conventional14C age (1r)

Calender age 1 (1r)* Calender age 2

(1r)**

Laboratory

code

Remarks

135 Plant -28.1 263 (±29) 307 (?9/-22, ?99/?114) AA93078 IntCal09

199 Theora sp. -1.5 807 (±35) 450 (?36/-28) 406 (?53/-45) AA99018 Marine09

250 Fulvia hungerfordi -0.5 1,018 (±35) 595 (?35/-36) 569 (?39/-40) AA93077 Marine09

292 Theora sp. -0.6 1,306 (±35) 849 (?50/-39) 808 (?56/-48) AA99017 Marine09

327*** Theora sp. -1.9 1,350 (±40) 895 (?48/-52) 847 (?55/-53) Beta-202280 Marine09

368 Paphia undulata -0.8 1,647 (±36) 1212 (?42/-39) 1169 (?56/-45) AA96078 Marine09

* Calibration program: CALIB 6.0; DR = 0 (average value of global reservoir in ocean)

** Calibration program: CALIB 6.0; DR = 44 ± 24 (Kuzmin et al. 2001)

*** Takata et al. (2006a)

J Paleolimnol (2014) 51:421–435 425

123

Following Webb et al. (2009) and Webb and Leighton

(2011), we calculated RAC using the relative abun-

dance of each taxon and calculated RAC kurtosis for

each sample in the Statistical programming environ-

ment R.

Dry sediment subsamples for X-ray fluorescence

(XRF) elemental analysis were partly ground using an

agate mortar. The powdered sample was dried at

50 �C, and was then compressed to make an XRF

briquette. Each XRF briquette was analyzed using an

energy dispersive X-ray Fluorescence Element Ana-

lyzer, MESA-500 W, Horiba Co., Ltd. The analysis

was performed under vacuum conditions, using an Rh

X-ray tube target with 15 and 50 kV X-ray tube

voltages, for light and heavy elements, respectively.

Analysis time was 250 s for each X-ray tube voltage

(total 500 s). Weight percent of 11 elements (SiO2,

Na2O, MgO, Al2O3, P2O5, S, K2O, CaO, TiO2, MnO

and Fe2O3) was quantified by the standard regression

method, using the computer software MESA-500 W

of Horiba Co., Ltd. The calibration line for each

element was based on a linear equation, using 12

standards provided by Dr. H. Fukusawa. In this study,

we focused only on the sulfur content of the bulk

sediment, which reflects anoxia in the hypolimnetic

water of the lagoon.

Statistical correlation between indices of benthic

foraminifera and sulfur content in the bulk sediment

was examined using Spearman’s rank coefficient, to

consider the relationship between MDS axis and each

taxon. We consider that MDS axis 1 represents a

primary signal of variations in faunal composition

(Yasuhara et al. 2012) and compared it to other proxy

data.

Results

Sulfur content of the bulk sediments of core ASC2 is

relatively greater in the 310–240 and 160–150 cm

intervals (Fig. 4). The Benthic Foraminiferal Number

(BFN) shows considerable variation over the length of

the section. The BFN displays three depth intervals

with high values: *320–290, *260–220 and

*180–160 cm. In the 277–264 cm interval, with

distinct laminations, benthic foraminifera were rare.

Forty-three genera and 94 species of benthic foram-

inifera were identified in the study interval. Preserva-

tion of benthic foraminifera was generally good,

without serious dissolution or fragmentation. Trocham-

mina cf. japonica, Eggerelloides advena, Elphidium

somaense, Virgulinella fragilis, Quinqueloculina sp. A,

and Ammonia sp. A were common constituents in the

study interval. T. cf. japonica and E. somaense alternate

in relative abundance twice in the sequence (Fig. 4). In

addition, V. fragilis was only common at depths in the

upper half of the study interval. Two MDS axes were

recognized. The MDS axis 1 score generally increased

in the *380–280 cm interval, declined to about

240 cm, and increased again up to 150 cm. MDS axis

2 was less variable and displayed the lowest value in the

uppermost sample (Fig. 4).

The Shannon–Wiener index (H0) and E (S200)

decreased upward in the *380–280 cm interval, but

were quite low in the 280 to 260 cm interval, just

below the interval with sparse benthic foraminifera

(Fig. 4). There was, however, no marked stratigraphic

change for the Shannon–Wiener index (H0) and E

(S200) in the *260–150 cm interval. Similarly, even-

ness and RAC kurtosis decreased and increased

upward in the *380–280 cm interval, respectively,

whereas there was no marked stratigraphic change in

the *260–150 cm interval. Increasing RAC kurtosis

was more evident than decreasing evenness at

*280 cm. Thus, the relative abundances of benthic

foraminifera changed dramatically above and below

the depths in which benthic foraminifera were rare

(277–265 cm). We subdivided the study interval into

two subintervals (*380–280 cm and *260–150 cm,

respectively) and these two subintervals were desig-

nated as the first and second phases.

There are some significant statistical correlations

between indices in the core (Table 2). Additionally,

we examined the correlation in the first phase (*AD

700–1250) and second phase (*AD 1250–1600)

separately. There were several strong correlations

among the indices in the first phase, but fewer and

generally weaker correlations in the second phase

(Table 2).

Discussion

Composition and structure of the benthic

foraminiferal community in Aso-kai lagoon

The composition of fossil benthic foraminifera in Aso-

kai lagoon was evaluated using Multi-dimensional

426 J Paleolimnol (2014) 51:421–435

123

scaling (MDS). Characteristics of the two MDS axes

were considered, in light of ecological information on

modern benthic foraminifera in Aso-kai lagoon (Tak-

ata et al. 2005a), and other brackish systems (Matsu-

shima Bay: Matoba 1970; Lake Hamana: Matsushita

and Kitazato 1990; Tokyo Bay: Kosugi et al. 1991;

Osaka Bay: Tsujimoto et al. 2006b). Relative abun-

dances of Trochammina cf. japonica and Elphidium

somaense have positive and negative relations with

MDS axis 1, respectively (Table 3). Trochammina

hadai, morphologically equivalent to our T. cf.

japonica (Matsushita and Kitazato 1990), is a charac-

teristic species of MDS axis 1, based on Plate 2, 1a–c

of Matsushita and Kitazato 1990), and is known to be

tolerant of seasonally oxygen-poor conditions (\2 ml/l)

in Lake Hamana, central Japan (Matsushita and

Kitazato 1990). In Aso-kai lagoon, T. cf. japonica

was found near the sand bar, where there is commonly

an inflow of oxygenated water in winter (Takata et al.

2005a). Nomura and Seto (1992) suggested that T.

hadai is tolerant of salinity to *25 % in Lake

Nakaumi, southwest Japan. E. somaense is a common

species in the middle-to-outer bay environments of the

Japanese coasts (Matoba 1970; Kosugi et al. 1991).

According to Nomura and Seto (1992), this species has

a preference for high salinity ([28 %) in the Sakai

Channel, between Lake Nakaumi and the Sea of Japan

(East Sea). Additionally, there is a statistically positive

correlation between MDS axis 1 and sulfur content of

bulk sediments (Table 2). High sulfur content usually

indicates oxygen-poor conditions in brackish water, as

a consequence of active sulfur reduction. Hence, MDS

axis 1 indicates alternation between a seasonally

oxygen-poor condition (more positive score) and the

bay environment (more negative score).

Quinqueloculina sp. A, Q. sp. B and Virgulinella

fragilis show negative correlations with MDS axis 2,

whereas Eggerelloides advena has a positive relation

with MDS axis 2 (Table 3). Quinqueloculina spp. are

common constituents in shallow-water neritic envi-

ronments (Matoba 1970; Nomura and Seto 2002) and

Virgulinella fragilis can live in persistently anoxic

conditions (Bernhard 2003; Takata et al. 2005a).

Eggerelloides advena is commonly reported from bay

environments of the Japanese Islands (Matoba 1970;

Takata et al. 2006b; Tsujimoto et al. 2006b), espe-

cially from polluted, organic-rich substrates (Tsujim-

oto et al. 2006b). Although it is difficult to specify

Fig. 4 Stratigraphic changes in a sulfur content (wt %) of the

bulk sediment, b number of benthic foraminifera (BFN benthic

foraminiferal number), c Shannon–Wiener (H0) and E (S200),

d RAC kurtosis and evenness, e relative abundance of each

major taxon, f MDS axis 1 and g MDS axis 2 of core ASC2

J Paleolimnol (2014) 51:421–435 427

123

characteristics of MDS axis 2, negative scores of this

axis probably represent nearly year-round oxygen

deficiency in the restricted lagoon. MDS results

therefore suggest that fossil benthic foraminifera in

the study period were controlled mainly by DO

content in the hypolimnetic water.

An increase in MDS axis 1 from *AD 700 to 1250

suggests a DO decrease in the hypolimnetic water of

Aso-kai lagoon, a trend that is reversed between *AD

1250 and 1600 (Fig. 5). Sulfur content in bulk

sediments is high in deposits with more positive

scores for MDS axis 1 (Fig. 5). Hence, we infer severe

deterioration in hypolimnetic conditions for benthic

foraminifera in Aso-kai lagoon ca. AD 1250–1600.

More negative scores of MDS axis 2 support severe

deterioration of hypolimnetic conditions (i.e. low DO)

in the latter part of the second phase, as discussed

previously by Takata et al. (2006a). Timing of the

Table 2 Results of Spearman rank correlation of the indices in (a) whole studied interval (380–150 cm), (b) first phase

(380–280 cm) and (c) second phase (260–150 cm)

Sulfur (%) Shannon–Wiener (H0) E (S200) Evenness RAC kurtosis

(a) whole interval

MDS axis 1 q = 0.77

P < 0.01

q = -0.66

P < 0.01

q = -0.63

P < 0.01

q = -0.35

P < 0.05

q = 0.60

P < 0.01

Shannon–Wiener (H0) q = -0.74

P < 0.01

E (S200) q = -0.78

P < 0.01

q = 0.91

P < 0.01

Evenness q = -0.34

P < 0.05

q = 0.69

P < 0.01

q = 0.48

P < 0.01

RAC kurtosis q = 0.70

P < 0.01

q = -0.88

P < 0.01

q = -0.77

P < 0.01

q = -0.72

P < 0.01

(b) first phase

MDS axis 1 q = 0.94

P < 0.01

q = -0.84

P < 0.01

q = -0.85

P < 0.01

q = -0.60

P < 0.01

q = 0.86

P < 0.01

Shannon–Wiener (H0) q = -0.83

P < 0.01

E (S200) q = -0.87

P < 0.01

q = 0.94

P < 0.01

Evenness q = -0.57

P < 0.01

q = 0.79

P < 0.01

q = 0.61

P < 0.01

RAC kurtosis q = 0.81

P < 0.01

q = -0.92

P < 0.01

q = -0.81

P < 0.01

q = -0.81

P < 0.01

(c) second phase

MDS axis 1 q = 0.39

P < 0.05

q = 0.09

NS

q = 0.17

NS

q = -0.41

P < 0.05

q = -0.26

NS

Shannon–Wiener (H0) q = -0.36

NS

E (S200) q = -0.30

NS

q = 0.74

P < 0.01

Evenness q = 0.34

NS

q = 0.32

NS

q = -0.20

NS

RAC kurtosis q = 0.26

NS

q = -0.61

P < 0.01

q = -0.39

P < 0.05

q = -0.41

P < 0.05

428 J Paleolimnol (2014) 51:421–435

123

more negative MDS axis 2 is generally consistent with

enhanced closure of the lagoon by rapid development

of the Sho-tenkyo sand bar and bottom reclamation in

the southeastern corner of the lagoon during the Edo

era (AD 1603–1868) (Hirai 1995).

Structure of the fossil benthic foraminiferal com-

munity in Aso-kai lagoon was evaluated using the

Shannon–Wiener species diversity index (H0), E

(S200), the evenness measure of Buzas and Gibson

(1969) and RAC kurtosis. Webb et al. (2009) argued

for extinction and subsequent recovery of deep-sea

benthic foraminifera and ostracoda across the Paleo-

cene–Eocene Thermal Maximum, using species rich-

ness, evenness and RAC kurtosis. They postulated that

RAC kurtosis is a useful index to judge faunal

structure, whether the community is ‘‘stable’’ or

‘‘stressed’’ (low and high kurtosis, respectively), and

evaluate the predominance of a few taxa. There is

statistical correlation among all variables, i.e. sedi-

ment sulfur content, faunal composition (MDS axis 1)

and structure (Shannon–Wiener (H0), E (S200), even-

ness and RAC kurtosis) of benthic foraminifera in the

first phase (*AD 700–1250) (Table 2). In contrast,

there is a general lack of statistical correlation among

these indices in the second phase (*AD 1250–1600),

except for a weak positive correlation between sulfur

content and faunal composition (MDS axis 1)

(Table 2). This implies corresponding patterns of

gradual deterioration, not only in sediment geochem-

istry and faunal composition, but also in faunal

structure of fossil benthic foraminifera in the first

phase. There is, however, almost no corresponding

change in the faunal structure in the second phase, in

spite of similar patterns in both sediment geochemistry

and faunal composition of benthic foraminifera.

Additionally, there are considerable differences with

respect to taxonomic loss in the first and second

phases, based on species diversity.

Abundance of benthic foraminifera displayed large

fluctuations in the second phase, relative to the first

phase. Benthic foraminifera abundance displays

*200-year cycles, as opposed to 300–500-year cycles

for sediment geochemistry and benthic foraminifera

faunal composition (Fig. 5). The fluctuations in total

abundance are mainly driven by the abundance of

Eggerelloides advena (Fig. 4), as there is statistical

correlation between these two measures (whole study

Table 3 Correlations between each taxon and scores of multi-

dimensional scaling (MDS) axes 1 and 2

MDS

axis1

MDS

axis2

Textularia earlandi 0.40 0.09

Spiroplectamina sp. A 0.24 0.12

Eggerelloides advena -0.33 0.69

Trochammina cf. japonica 0.84 0.27

Trochammina pacifica 0.37 -0.04

Siphonaperta sp. -0.32 -0.18

Quinqueloculina elongata -0.20 -0.27

Quinqueloculina seminulum -0.28 -0.11

Quinqueloculina sp. A 0.41 -0.69

Quinqueloculina sp. B 0.32 -0.74

Miliolinella sidebottomi -0.35 -0.12

Miliolinella sp. A 0.18 0.12

Massilina secans -0.41 -0.17

Unilocular -0.46 -0.06

Bolivina sp. A -0.22 0.06

Brizalina seminuda -0.56 -0.15

Bulimina sp. A -0.54 -0.14

Buliminella elegantissima 0.30 -0.13

Uvigerinella glabra -0.61 0.04

Stainforthia sp. -0.10 0.12

Reussella pacifica -0.44 -0.20

Virgulinella fragilis 0.23 -0.63

Ammonia sp. A (compact type) -0.68 -0.11

Ammonia sp. A (inflate type) -0.69 -0.11

Ammonia sp. B -0.38 -0.12

Ammonia japonica -0.12 0.11

Buccella frigida -0.13 -0.12

Buccella tenerrima -0.24 -0.23

Valvulineria hamanakoensis -0.06 -0.24

Pseudoparrella naraensis -0.48 -0.23

Rosalina globularis -0.24 -0.14

Elphidium advenum -0.54 -0.09

Elphidium reticulosum -0.35 -0.05

Elphidium excavatum

forma excavata

-0.14 -0.51

Elphidium excavatum

forma selseyensis

0.08 -0.60

Elphidium somaense -0.82 -0.13

Elphidium subincertum -0.28 0.09

Elphidium sp. A 0.34 -0.40

Pseudononion japonicum -0.50 -0.20

Nonionella stella -0.43 -0.24

J Paleolimnol (2014) 51:421–435 429

123

interval: q = 0.60 and P \ 0.01; first phase: q = 0.64

and P \ 0.01; second phase: q = 0.70 and P \ 0.01).

This species is a common constituent of polluted

organic-rich substrates (Alve 1995; Tsujimoto et al.

2006b). Tsujimoto et al. (2006a) reported that this

species increased in Osaka Bay after the 1990s and

speculated that its increase was attributable to changes

in primary producers, from dinoflagellate to diatoms.

There is, however, no marked change in the fossil

diatom flora in Aso-kai lagoon during the study period

(Tanaka unpublished data). Eggerelloides advena is

also regarded as an opportunistic species in polluted

areas (Alve 1995). Additionally, Alve and Goldstein

(2010) reported that Eggerelloides scaber could

deliver propagules to deep-water sites (320 m) of the

Skaggerak Basin (North Sea), as it has a small body

size (\32 lm) and could have great dispersal

potential, with dormancy periods of as much as

several months to years. Hence, we suggest that E.

advena (Fig. 5) affects the abundance of benthic

foraminifera in core ASC2 and may overwhelm the

signal of faunal structure in the second phase (*AD

1250–1600) in spite of the similar variation in MDS

axis 1 (faunal composition) in the first phase (*AD

700–1250).

Biotic responses of benthic foraminifera

in the Aso-kai lagoon *AD 1250

Collapse of benthic foraminifera fauna at *AD 1250

Stratigraphic changes in sediment sulfur content,

faunal composition (MDS axis 1) and faunal structure

[Shannon–Wiener (H0)] in Aso-kai lagoon in the first

phase (*AD 700–1250) show a similar pattern to that

of the Td’ ratio in the Sea of Japan (East Sea)

(Koizumi 2008; Fig. 5). Td’ ratio is regarded as an

indicator of the Tsushima Warm Current in the Sea of

Japan (East Sea) (Koizumi 1989, 2008; Khim et al.

2005). Isono et al. (2009) reported a relatively low

SST at ca. 1.5 and *0.3 ka, but relatively warm SST

at *1.0 ka in the northwest Pacific. This timing is

roughly consistent with changes in the benthic foram-

inifera data from our study, i.e. the latter part of the

second phase (*AD 1250–1600), the early part of the

first phase (*AD 700–1250), and *AD 1250 severe

deterioration, respectively. Isono et al. (2009) also

suggested a correspondence between fluctuations of

the Kuroshio extension in the northwest Pacific and

Bond events in the North Atlantic. The Tsushima

Warm Current is a branch of the Kuroshio, which

Fig. 5 Downcore variations in a relative abundance of

hematite-stained grains in cores MC51 and VM29-191 from

the North Atlantic (Bond et al. 2001), b diatom Td’ ratio of core

DG-GC-6 in the Sea of Japan (East Sea) (Koizumi 2008),

c sulfur content (wt %) of the bulk sediment, d MDS axis 1,

e Shannon–Wiener (H0), f abundances of all benthic

foraminifera and Eggerelloides advena in core ASC2, g atmo-

spheric radiocarbon concentration (D14C) (Reimer et al. 2004)

and (h) stable oxygen isotope ratio of the stalagmite in

Wangxiang Cave (Zhang et al. 2008). LYWMP Late Yuan

Weak Monsoon Period; LMWMP Late Ming Weak Monsoon

Period

430 J Paleolimnol (2014) 51:421–435

123

flows into the Sea of Japan (East Sea), and its

fluctuations may also be related to climate changes

associated with Bond events. Cyclicity of the Tsushi-

ma Warm Current was suggested by Koizumi and

Sakamoto (2010). Bond et al. (2001) reported a

stratigraphic change in the relative abundance of

hematite-stained grains in cores MC52 and VM29-191

from the North Atlantic (Fig. 5). The decreasing trend

from *AD 600–1300 corresponds to Bond Events 0

and 1 and displays a pattern similar to that for faunal

composition and structure of benthic foraminifera in

Aso-kai Lagoon during the first phase.

There was a severe deterioration in the latter part of

the first phase (*AD 1250), which included a

subsequent interval when benthic foraminifera were

very rare. This suggests that primary productivity was

enhanced and/or ventilation of the hypolimnetic water

was limited in Aso-kai lagoon. Such a scenario is

explained by either density stratification in the lagoon

as a consequence of development of warm epilimnetic

water with low salinity, or by closure of the lagoon as a

consequence of sand bar development. Fossil diatom

data from core ASC1 in the Aso-kai lagoon (collected

*1 km east of core ACS2) (Tanaka unpublished

data), however, show predominantly abundant marine

to brackish-water diatoms (e.g. Thalassiosira lineata,

T. excentrica, Diplonites interrupta and Cyclotella

striata) at roughly the same time, based on litho-

stratigraphic correlation of the profiles. This implies

there was not a major decline in the influence of saline

water to the epilimnion of the lagoon compared to

earlier or subsequent times. This is consistent with the

previous interpretation, which suggested the lagoon

received a greater quantity of seawater than today,

which flowed in through a wide channel in the sand bar

(Hirai 1995; Takata et al. 2006a). In addition, accord-

ing to Fukusawa (1997), there was likely no marked

sea-level decline in the adjacent area of Lake Suigetsu,

along the coast of Wakasa Bay, central Japan. Thus, it

is not certain that deterioration of benthic foraminifera

fauna at *AD 1250 was related to the closure of the

lagoon by sandbar development, but it remains

possible that closure of Aso-kai lagoon by sandbar

development affected benthic foraminifera.

Heat transport by the Tsushima Warm Current into

the Sea of Japan (East Sea), as shown by the Td’ ratio,

might also promote stratification of the water within

the Aso-kai lagoon, and may extend the duration of an

oxygen-poor hypoliminion during the warm season.

Based on a sedimentological study, Yamada et al.

(2010) suggest that a warm and humid period occurred

during *AD 750–1200 in Lakes Ni-no-Megata and

San-no-Megata, in northern Japan. In addition, Fukus-

awa (1997) also suggests that precipitation increased

from the early ninth century to the middle of the

thirteenth century in the adjacent areas of Lake

Suigetsu. In particular, *AD 1150–1170, Trocham-

mina cf. japonica dominated the benthic foraminifera

([80 %) in core ASC2, whereas common shallow-

marine taxa, such as Elphidium spp. and Eggerelloides

advena, were rare (Fig. 4). Because it is thought that T.

hadai, probably morphologically equivalent to our T.

cf. japonica, is tolerant of slight salinity variations

(Nomura and Seto 1992), epilimnetic water with

slightly lower salinity might have occasionally

reached the bottom at the core site and affected

benthic foraminifera, as did oxygen deficiency. Rel-

atively high amounts of precipitation in the surround-

ing area of the Aso-kai lagoon, as mentioned by

Fukusawa (1997) for the adjacent area of Lake

Suigetsu, might account not only for stratification of

the waters, but also for high primary productivity as a

consequence of a riverine nutrient supply at the time of

the *AD 1250 deterioration. A warm climate and/or

enhanced precipitation might have caused conditions

that account for the gradual deterioration of both the

hypolimnion and the benthic foraminiferal fauna in the

first phase (*AD 700–1250) in Aso-kai lagoon. Thus,

it is notable that the small, but increasing influence of

the Tsushima Warm Current caused severe deteriora-

tion in the hypolimnion and the benthic ecosystem

*AD 1250. Therefore, the gradual deterioration of

benthic foraminifera, with taxonomic loss in the first

phase of Aso-kai lagoon, might be explained by the

increasing influence of the Tsushima Warm Current

(possibly associated with Bond events), although we

cannot dismiss the possibility that closure of Aso-kai

lagoon as a consequence of development of the sand

bar, influenced benthic foraminifera.

Variations in the abundance of benthic foraminifera

In the second phase (*AD 1250–1600), relations

between the indices of faunal structure and other

indices in the Aso-kai Lagoon and Td’ ratio of the

hemipelagic diatom record are not clear (Fig. 5).

Figure 5 also shows that high abundance of benthic

foraminifera in the second phase of the Aso-kai lagoon

J Paleolimnol (2014) 51:421–435 431

123

(*AD 1400 and 1600) seems to be correlated with

times of relatively high solar activity (Reimer et al.

2004) and a weak East Asian summer monsoon

(Zhang et al. 2008), i.e. the Late Yuan Weak Monsoon

Period (LYWMP: AD 1350–1380) and the Late Ming

Weak Monsoon Period (LMWMP: AD 1580–1640).

In addition, a sedimentological study in Lake Kusai on

the Qinghai-Tibetan Plateau in China provides evi-

dence for a relatively strong winter monsoon in AD

1325–1390 and AD 1450–1550 (Liu et al. 2009).

Other studies have also postulated that both proxies for

East Asian summer and winter monsoon variations

show similar trends, with see-saw patterns (Yamada

et al. 2010). The high abundance of the opportunistic

benthic foraminifera, E. advena, in Aso-kai lagoon is

roughly correlated with the relatively weak East Asian

summer monsoon and the relatively strong East Asian

winter monsoon. Such an environment may have

generated a specific condition, with low precipitation

in the summer and enhanced wind mixing of waters in

the study area during the winter season. In particular,

enhanced wind mixing of water in the area surround-

ing the lagoon might have caused the high abundance

of E. advena in Aso-kai lagoon, by dispersing

propagules. Although there is no information about

distribution of modern benthic foraminifera in Miyazu

Bay, Verneuilina propinqua, morphologically proba-

bly equivalent to our E. advena, has been reported in

Maizuru Bay (Morishima 1947, 1948), which is

located about 15 km southeast of the study area and

one of the inlets to Wakasa Bay as well as Miyazu Bay.

According to Morishima (1947), this species was

present with abundant Textularia spp. in the outer part

of Maizuru Bay. Occurrence of this species supports

the above scenario about dispersal of propagules from

the surrounding area (Wakasa Bay coast) into Aso-kai

lagoon during the study period. Hence, seasonal

differences between the East Asian summer and

winter monsoon might account for changes in the

abundance of (opportunistic) benthic foraminifera in

Aso-kai lagoon. Thus, the biotic response in the

second phase (*AD 1250–1600), which is character-

ized by no great taxonomic loss and frequent varia-

tions in abundance, is explained by short-term

fluctuations in the East Asian monsoon, but no

noticeable change in the Tsushima Warm Current.

We cannot, however, rule out the possibility that

closure of the Aso-kai lagoon by development of the

sand bar affected benthic foraminifera.

There is an abundance peak of benthic foraminifera

at *AD 1100, in the first phase. It appears to be

correlated with evidence for climatic deterioration in

the tenth century in Lakes Ni-no-Megata and San-no-

Megata (Yamada et al. 2010). In addition, it is also

correlated with an interval of higher d18O in a

stalagmite (i.e. weak East Asian summer monsoon),

at the time of transition between the Northern and

Southern Song Dynasties (Zhang et al. 2008) and a

relatively strong East Asian winter monsoon period

(AD 1000–1100) (Liu et al. 2009). Thus, the abun-

dance peak of benthic foraminifera in the first phase

appears to be related to activities of the East Asian

summer and winter monsoon. This timing, however,

corresponds to relatively low solar activity, i.e. the

Oort sunspot minimum (Reimer et al. 2004). Envi-

ronmental conditions that influence benthic forami-

nifera seem to change between the first and second

phases, especially their effect on taxonomic losses, but

abundance of benthic foraminifera in Aso-kai lagoon

during the study period seems to be best correlated

with climate proxies for the East Asian monsoon.

Responses of benthic foraminifera in Aso-kai

lagoon to climate and ocean environment changes

at *AD 1250

During the period *AD 700–1250, benthic forami-

nifera responded to DO levels in the hypolimnion,

perhaps driven by fluctuations of the Tsushima Warm

Current. It remains possible, however, that sand bar

formation and the closure of Aso-kai lagoon were also

influential. From *AD 1250 to 1600 there was no

marked response of benthic foraminifera to the DO

level in the hypolimnion, but there were changes in the

abundance of benthic foraminifera, perhaps in

response to the East Asian summer and winter

monsoons. The first and second phases in core ASC2

generally correspond to the late part of the Dark Age

Cold Period through the Medieval Warm Period, and

to the early part of the Little Ice Age in Europe,

respectively (Fig. 5). A transition from relatively

humid and warm, to dry and cool conditions between

*AD 1200 and AD 1300, has been inferred from tree-

ring and lake sediment records in Japan (Kitagawa and

Matsumoto 1995; Fukusawa 1997; Yamada et al.

2010). Abundance of benthic foraminifera in Aso-kai

lagoon is thought to be related to the activity of the

East Asian summer and winter monsoons, and similar

432 J Paleolimnol (2014) 51:421–435

123

changes were observed in tenth-century sediment

records from Lakes Ni-no-Megata and San-no-Megata

(Yamada et al. 2010). Yamada et al. (2010), however,

reported no comparable sedimentological change in

the early part of the Little Ice Age, i.e. the second

phase in Aso-kai lagoon. This lack of agreement

between northern and central Japan suggests a latitu-

dinal difference in the influence of the East Asian

monsoon on the East Asian continental margin. We

cannot, however, dismiss other possibilities, such as

differential responses of climate proxies in each lake

system to climate changes. Thus, it is notable that

fluctuations in the terrestrial and oceanic climate may

have caused a shift in the biotic response of the coastal

ecosystem, which might have been related to telecon-

nections in the Northern Hemisphere, based on the

previous studies in the East Asian margin (Koizumi

and Sakamoto 2010; Yamada et al. 2010).

Decadal-scale changes within coastal ecosystems

are often interpreted in the context of a ‘‘regime shift’’

in the coastal water system, together with recent human

impact (Katsuki et al. 2008). As Nomura (2003) pointed

out in paleoenvironmental studies of the twentieth

century, our results suggest that changes in climate and

oceanographic conditions can prompt a shift in the

biotic response of a coastal ecosystem, from gradual

deterioration with taxonomic loss, to no marked

taxonomic loss, but significant fluctuations in the

abundance of (opportunistic) species. In fact, Nomura

(2003), Nomura et al. (2008) and Nomura and Kawano

(2010) also noted in several lagoons of the Japanese

Islands, that the occurrence of benthic foraminifera

after the 1980s revealed a different mode of biotic

response, which was characterized by a deviation from

the correspondence between sea-level change and the

occurrence of benthic foraminifera. They suggested a

possible relationship between recent climate warming

and a different biotic response. Long-term changes in

the biotic response of shallow-water biota may provide

useful insights into the response of coastal ecosystems,

with respect to future climate warming.

Conclusions

We re-investigated benthic foraminifera and geochemis-

try in sediment core ASC2 from Aso-kai lagoon, covering

the period *AD 700–1600. We found 300–500-year-

scale alternations in sediment sulfur content and faunal

composition (MDS axis 1) of benthic foraminifera during

the 8th-16th centuries AD. In the first phase (*AD

700–1250), faunal structure (Shannon–Wiener (H0), E

(S200), evenness and RAC kurtosis) changed simulta-

neously with sediment sulfur content and faunal compo-

sition. In contrast, in the second phase (*AD

1250–1600), no such temporal correspondence was

observed. Instead, there were 200-year-scale fluctuations

in the abundance of benthic foraminifera in this latter

phase. Biotic response of benthic foraminifera in Aso-kai

lagoon shifted from a gradual deterioration with taxo-

nomic loss to no marked change without taxonomic loss,

but with abundance fluctuations of opportunistic species.

A shift in the biotic response of benthic foraminifera

occurred *AD 1250 in Aso-kai lagoon. The response of

benthic foraminifera was consistent with a decrease in

hypolimnetic DO from *AD 700 to 1250, perhaps a

consequence of increasing influence of the Tsushima

Warm Current or, alternatively, closure of Aso-kai lagoon

with development of the sand bar. From *AD 1250 to

1600, changes in the abundance of benthic foraminifera

were possibly associated with variations in the East Asian

summer and winter monsoons. Our results suggest that

biotic responses of benthic foraminifera in Aso-kai lagoon

over the last 1,000 years were caused by shifts in the

influence of climate (East Asian monsoon) and oceano-

graphic conditions (Tsushima Warm Current).

Acknowledgments We thank D. Dettman (University of

Arizona) for arranging radiocarbon dating. We are indebted to

K. Yamada (Waseda University) for suggestions about XRF

element analysis, to M. Yasuhara (University of Hong-Kong) for

suggestions about Multi-dimensional scaling, and to A. Webb

(Yale University) for suggestions about RAC kurtosis. We also

thank S. Murakami (Shimane University) for partial foraminifera

analysis of core ASC2 and A. Tujimoto (Shimane University) for

comments about foraminifera ecology. J. Naito (Miyazu Fishery

Cooperative) helped collect field samples. H. Asahi (Pusan

National University) helped draw a figure. We appreciate the

detailed reviews of two anonymous reviewers and constructive

comments of M. Brenner (Editor). This work was supported by

grants-in-aid (no. 12740282 to S. Tanaka and no. 15540436 to K.

Seto) for scientific research from the Ministry of Education,

Science and Culture (Japan), by the Center for Academic Sciences

and Earthquake Research (Grant No. CATER 2012-7040 to B.-K.

Khim), and partly by East Asian Seas Time series-I (to B.-K.

Khim) of the Ministry of Oceans and Fisheries (Korea).

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