J Oceanogr (2017) 73:309–320
DOI 10.1007/s10872-016-0404-y

ORIGINAL ARTICLE

Temporal variations in phytoplankton biomass over the
past 150 years in the western Seto Inland Sea, Japan
Narumi K. Tsugeki1,4 · Michinobu Kuwae1 · Yukinori Tani2 · Xinyu Guo1 ·Koji Omori1 · Hidetaka Takeoka3

Received: 2 March 2016 / Revised: 27 August 2016 / Accepted: 16 November 2016 / Published online: 7 December 2016
© The Oceanographic Society of Japan and Springer Japan 2016

Abstract We examined fossil pigments in a 210Pb-dated
sediment core to document the temporal variations in
phytoplankton biomass over the past 150 years in a semienclosed bay, Beppu Bay, in the western Seto Inland Sea,
Japan. The flux of fossil pigments was used as an index
of phytoplankton biomass, which we reconstructed after
removing the effect of post-burial degradation on the concentrations of fossil pigments. The flux doubled from the
1960s to the early 1970s, decreased or remained stable in
the early 1980s, and increased again from the late 1980s
to the early 1990s. The first increase in phytoplankton biomass during the 1960s was likely caused by eutrophication
due to an increase in terrestrial nutrient fluxes from watersheds. The decreasing phytoplankton biomass in the early
1980s was likely related to the establishment of a sewage
treatment system that reduced the terrestrial nutrient fluxes
to the sea. However, the terrestrial nutrient fluxes could
not explain the second increase from the late 1980s to theearly 1990s. Intensification of the influx of nutrients fromthe shelf slope to the sea was likely the cause of the second increase in phytoplankton biomass. This is supportedby the inverse relationship between phytoplankton biomass* Narumi K. Tsugeki
ntsugeki@cc.matsuyama‑u.ac.jp
1

Center for Marine Environmental Studies, Ehime University,
2‑5 Bunkyo‑Cho, Matsuyama 790‑8577, Japan2

Department of Environmental and Life Sciences, Schoolof Food and Nutritional Sciences, University of Shizuoka,
Shizuoka 422‑8526, Japan

3

South Ehime Fisheries Research Center, Ehime University,
1289‑1 Funakoshi, Ainan, Minami‑Uwa 798‑4292, Japan

4

Present Address: Faculty of Law, Matsuyama University, 4‑2
Bunkyo‑Cho, Matsuyama 790‑8578, Japanand sea level at the shelf slope, the latter being an index
of the intensity of the influx of oceanic nutrients from theshelf slope to the sea. The supply of oceanic nutrients may
be therefore a critical factor in the determination of primary
production in the western Seto Inland Sea.
Keywords Primary production · Pigments ·Eutrophication · Kuroshio current · Palaeoceanography ·Seto Inland Sea

1 Introduction
In recent decades, inland sea ecosystems have been severely
impacted by nutrient inputs associated with anthropogenic
activities in their watersheds (Carpenter et al. 1998; Cloern 2001; Yamamoto 2003). Excessive nutrient inputs fromwatersheds have led to eutrophic conditions in coastal seas
and induced the frequent occurrence of red tides, whichhave become a widespread social problem (Cloern 2001).
For example, in the Seto Inland Sea, red tide blooms havebeen apparent since the 1960s, their occurrence being contemporaneous with increased inputs of terrestrial nutrients
due to industrialization and urbanization in the watershed(Honjo 1993; Takeoka 2002; Yamamoto 2003).
The input of oceanic nutrients from shelf slope waters,
however, can also be an important determinant of primary production in the coastal ocean (Prezelin et al. 2004;
Nakano et al. 2005). Field observations have demonstrated
that primary production in shelf waters along the Japanese Pacific coast is greatly stimulated by nutrients fromthe shelf slope (Ozaki et al. 2004; Nakano et al. 2005). It
has also been demonstrated that the intrusion of oceanic
water dramatically changes nutrient concentrations andthe biomass of the dominant phytoplankton in shelf waters

13

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60

50

Seto Inland Sea
10
20

30

Beppu Bay 40
60
70

40

30
20
10

Bu

ng

oC
ha

nn

Ono Riv.

Oita meteorologicalobservatory(a)33 20'Nel50

Otozu Riv.

13

33 30'N
10 km

0Oita Riv.

(Kaneda et al. 2002a; Hayami et al. 2004; Kuroda et al.
2010; Nakano et al. 2005). Nutrient concentrations within
the inland sea, in addition to those in shelf waters, also
show remarkable year-to-year variability that is concordant
with variations in nutrient inputs from the shelf slope (Sugimatsu and Isobe 2010). Many studies have drawn attention
to the importance of nutrients supplied to the Seto Inland
Sea from the ocean (e.g., Fujiwara et al. 1997; Takeoka
2002; Hayami et al. 2004). Those studies have demonstrated that, along with the input of nutrients from land
runoff, the supply of nutrients from the offshore ocean may
intensify primary production in the inland sea. However, allof these studies have been limited to a timeframe shorter
than several years. Therefore, we actually do not know how
variations in oceanic and terrestrial nutrient supplies overa timeframe longer than a few decades affect primary production in a coastal or inland sea (Ozaki et al. 2004; Yamamoto 2003). Understanding how such long-term variations
affect lower tropic level ecosystems is useful for developing good strategies for the management and rehabilitationof coastal and inland aquatic ecosystems (Boesch 2002).
Long-term monitoring data are necessary to elucidate
how inland-sea ecosystems respond to nutrients supplied
from the land and ocean. However, inland-sea monitoring
programs were not started until the 1970s, when eutrophication was already recognized as a problem (Yamamoto2003). Consequently, those monitoring programs cannot
provide the data needed to assess environmental conditions
before the occurrence of eutrophication.
A paleoceanographic approach using appropriate proxies in sediment cores can potentially enable the productivity in oceans to be reconstructed (Cooper 1995; Chmura
et al. 2004; Rabalais et al. 2007). Fossil pigment of chlorophyll derivatives derived from phytoplankton and preserved in coastal sediments is used to reconstruct the phytoplankton biomass that existed in the past (Chmura et al.
2004; Rabalais et al. 2007). Some studies have successfully reconstructed past phytoplankton biomass in coastal
ecosystems and identified the main factors that controlled
historical changes in biomass, such as the effects of nutrient loads from urbanizing watersheds (Chmura et al. 2004;
Rabalais et al. 2007).
Beppu Bay is a suitable site for investigating the effects ofoceanic and terrestrial nutrient supplies on primary production in an inland sea because the bay enables us to obtain
undisturbed sediment cores that reflect high sediment accumulation rates (Kuwae et al. 2013) and because it is very
close to the Bungo Channel, a conduit to the Pacific Ocean
that is frequently stimulated by nutrient inputs from the shelfslope (Fig. 1b; Kaneda et al. 2002a). In this study, we applied
the paleoceanographic approach to the analysis of sedimentcollected from Beppu Bay in the western Seto Inland Sea
to examine long-term changes in phytoplankton biomass.

N. K. Tsugeki et al.

33 10'N

131 50'E

131 40'E

131 30'E

35

Set
Kyushu

la
o In

nd

Sea

Shikoku

Kii
ChannelBungo
ChannelHosojima

North Pacific
30

(b)
130

0

500 km135

Fig. 1  Bathymetric maps (contour intervals in m) showing a thelocation of the coring site (filled circle) and b the location of Beppu
Bay in the western Seto Inland Sea, Japan. Open and closed squares
in a show monitoring sites where measurements of nutrients (closed)and chlorophyll a concentrations (open) were made in the bay (seeSect. 3.3)

We analyzed fossil chlorophyll a pigments in the sedimentfrom Beppu Bay to (1) reveal the temporal variations of phytoplankton biomass in the western Seto Inland Sea over the
past 150 years, and (2) identify the causes of those changes.

2 Study site
Beppu Bay is a semi-enclosed bay in the western Seto InlandSea, Japan (Fig. 1). The basin of the bay has a maximum
depth of 72 m in its innermost region and a deep sill at its
mouth, where the water depth is ~50 m. These bathymetricfeatures result in highly stagnant bottom-water conditions(e.g., Kameda and Fujiwara 1995; Kuwae et al. 2007) andenable the bay to provide undisturbed sediment cores thatreflect high sediment accumulation rates (Kuwae et al. 2013).

Temporal variations in phytoplankton biomass over the past 150 years in the western Seto…

The main rivers that flow into the bay are the Oita andOno rivers (Fig. 1a). The combined discharge from theserivers allowed us to examine the effects of terrestrial nutrient inputs on primary production. On the other hand,
Beppu Bay is also a suitable site for investigating theeffects of oceanic nutrient supplies on primary production in the inland sea because the bay is very close to the
Bungo Channel, a conduit to the ocean that is frequently
stimulated by nutrient inputs from the shelf slope (Fig. 1b;
Kaneda et al. 2002a).

3 Materials and methods
3.1 Sampling and chronology
We used a gravity corer (model HRL, Rigo Co. Ltd.,
Saitama, Japan) to collect an undisturbed sediment core
(BG091010-1) from the innermost region of Beppu Bay
in September 2009 (water depth 71.5 m; 33°16.4958′N,
131°32.1845′E). The core sample was undisturbed during the coring process and carefully sliced at 1-cm intervals from the surface to the bottom. Aliquots of thesliced samples were sealed in shielding bags and storedat −20 °C for analysis of fossil pigments. Core chronology was determined by the constant initial concentration(CIC) method of 210Pb dating (Robbins and Edgington1975). The validity of the 210Pb dating was checked bycomparison with the peak in 137Cs activity, which is associated with the fallout maximum of 1964 in Japan (Hirose
et al. 2008a). The activities of 210Pb, 214Pb, and 137Cs
were determined by γ-spectrometric analysis of dried
sediment. Dried samples were sealed in standard holders
for two weeks to allow 222Rn and its short-lived daughter (214Pb) to equilibrate. Radioactivities were determinedwith a high-purity Ge detector (GXM25P, EG&G ORTEC,
Tokyo, Japan) equipped with a multichannel analyzer(MCA7700, Seiko EG&G, Tokyo, Japan). The activity of210
Pbsupported was estimated by measuring the activity of
214
Pb, whereas the activity of 210Pbexcess was determinedfrom the difference between the total
and supported

210 Pb 210 Pb
210 Pb
214 Pb .
excess =total −
3.2 Fossil pigments
Concentrations of fossil pigments were quantified by highperformance liquid chromatography (HPLC). The frozen sediments were placed in 10-mL glass vials. HPLCgrade acetone was added (3 mL), and the pigments wereextracted at 0 °C during agitation in an ultrasonic bath(Tani et al. 2009a, b). The extracts were collected after
centrifugation at 2000 rpm for 5 min. These procedures
were repeated at least three times for each sample until311

the supernatant was completely colorless. The combined
extract was evaporated to dryness under N2, dissolved in
3 mL diethyl ether, and washed with an aqueous solutionof NaCl (1 M). After evaporating the ether phase to dryness under N2, the residue was dissolved in 200–500 µL ofacetone together with an internal standard, mesoporphyrin
IX dimethyl ester (Sigma–Aldrich, St. Louis, MO, USA),and analyzed by HPLC (LC-10AD, Shimadzu, Kyoto,
Japan) using a photodiode array detector (SPD-M10AVP,
Shimadzu). A Wakopack Navi C30-5 reverse-phase column(4.6 mm diameter and 250 mm length; Wako Pure Chemical Industries, Ltd., Osaka, Japan) was used for separation.
Mobile-phase solvent A consisted of a mixture of acetonitrile and water (90:10 by volume); solvent B was 100%
ethyl acetate. A linear gradient from 100% A to 100% B
over 40 min was followed by an isocratic hold for 10 min
at 100% B. The flow rate was 1.0 mL min−1. Pigments analyzed in this study were chlorophyll a (a major photosynthetic pigment ubiquitous in all taxonomic algae) and its
derivatives. Pheophytin a and pyropheophytin a were identified based on their retention times, absorption spectra, andquantified using commercially available reference compounds and absorption coefficients, as shown in Tani et al.
(2002). More hydrophilic chlorophyll a derivatives withabsorption spectra similar to pheophorbide a (pheophytina) were eluted before intact chlorophyll a when analyzed
by the C30-5 reversed-phase HPLC. We did not identify
these derivatives because of a lack of commercially available reference compounds for them. In this study, we therefore grouped these derivatives together as “pheophorbidea” (Nara et al. 2005) and calculated the total concentrationof them under the assumption that they have the same specific absorption coefficient as pheophorbide a. The sum ofchlorophyll a and its derivatives (pheophytin a, pyropheophytin a, and “pheophorbide a”) is denoted here “Chl-a.”
3.3 Meteorological and in situ data
We used the meteorological, physical, chemical and biological monitoring data to examine the effects of nutrientsfrom the land and shelf slope on the reconstructed fluxes of
Chl-a into the sediments, and to test the reliability of thereconstructed Chl-a fluxes.
Meteorological data, including annual averages of air
temperature and wind speed, and the monthly sum of precipitation and sunshine duration were obtained from the
Oita Local Meteorological Observatory, which is locatedon the south coast of Beppu Bay (Fig. 1). At the Oita
Observatory, air temperature, precipitation, and daylight
hours have been recorded since the late nineteenth century,
whereas wind speed has been recorded since 1951. Because
the Japan Meteorological Agency changed the methods
used to measure daylight hours and wind speed in 1985 and

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1975, respectively, we used information on daylight hours
and wind speed only after 1985 and 1975, respectively.
There are two major rivers that flow into Beppu Bay: the
Oita and Ono rivers (Fig. 1a). The monthly flow volume
in each river (Oita and Ono; the Funai-Ohashi and Shirataki-Bashi observation sites, respectively) was obtained
from the database of the Water Information System (http://
www1.river.go.jp/) operated by the Japanese Ministry ofLand, Infrastructure, Transport and Tourism (Ministry ofLand, Infrastructure, Transport and Tourism 2008).
Concentrations of dissolved inorganic nitrogen (DIN)
and orthophosphate (PO4-P) in Beppu Bay from 1973 to2003 were obtained from a regular survey conducted by
the National Research Institute of Fisheries and Environment of the Inland Sea. Monthly measurements of DIN and
PO4-P concentrations have been made at 13 sites (closed
squares in Fig. 1a) in the bay since 1973. Concentrationsof chlorophyll a in Beppu Bay were obtained from theJapanese Ministry of the Environment. Measurements ofchlorophyll a concentrations have been made at four sites
in Beppu Bay (open squares in Fig. 1a) as a part of anarea-wide comprehensive water-quality survey since 1981.
Terrestrial nutrient inputs of total nitrogen (TN) and phosphorus (TP) into the Seto Inland Sea were obtained from
Sekine and Ukita (1997) and SECA (2001).
The sea level data at Station Hosojima on the Pacific
Ocean side of Kyushu Island (Fig. 1b) since 1894 wereobtained from the Japan Metrological Agency. The sea
level at Hosojima Station is associated with the strengthof intrusions of cold, nutrient-rich bottom water fromthe shelf slope onto the shelf and the thermal contractionof the water column along the coasts of western Kyushu
and southern Shikoku (Fujiwara et al. 2004). Because theintrusion of cold slope water occurs primarily in the summer (Kaneda et al. 2002a), we used the average sea-levelanomalies (i.e., the differences from the long-term monthly
means) in early summer to fall (May–October) as proxies for nutrient supply from the slope region offshore the
Bungo Channel. In addition, the bottom water temperaturesin early summer to fall at an offshore site near the samplingstation (double square in Fig. 1a) were used as a proxy forthe historical variation in the strength of bottom intrusionfrom the shelf slope. The bottom-water temperatures since
1979 were obtained from the monthly survey conducted by
the National Research Institute of Fisheries and Environment of the Inland Sea.
3.4 Data processing
Chl-a concentrations per unit of dry sediment mass wereconverted to fluxes (mg m−2 year−1) using mass accumulation rates obtained from 210Pb dating (see Sect. 4.1). To
check the reliability of the reconstructed Chl-a fluxes, we

13

N. K. Tsugeki et al.

investigated the relationship between the fluxes and themonitoring chlorophyll a concentrations in Beppu Bay
since 1981. The time resolution per sample of the sediment core after the 1980s was about 2–3 years dependingon the sediment depth. Thus, we averaged concentrationsof chlorophyll a for the years that correspond with the sediment samples that were used to estimate the fluxes. To elucidate the effects of nutrients supplied from the shelf slope
on temporal variations in phytoplankton biomass in Beppu
Bay, we compared sea level anomalies from early summer to fall at Station Hosojima and the reconstructed Chla anomalies (i.e., differences from the long-term mean)
through the sediment core. Prior to analysis, the fluxes ofreconstructed Chl-a were log(x)-transformed to stabilize
the variance, where x is the flux of reconstructed Chl-a.

4 Results
4.1 Lithology, 137Cs and 210Pbexcess radioactivity,
and age–depth model
Our sediment core was almost constant in terms of grain
size except for the turbidite layers (as described below), andthe lithology was characterized by finely laminated blackand olive-gray silty clay above a depth of about 20 cm, but
below that it was characterized by massive olive-black orgrayish olive silty clay (for a detailed account of the lithology in the Beppu Bay sediments, see Kuwae et al. 2013).
Many turbidite layers were recognized in the Beppu Bay
sediment and thought to be formed as a result of earthquakes, tsunamis, and flooding in the region surrounding
the bay (Kuwae et al. 2013). These layers were characterized by high density associated with high magnetic susceptibility (Kuwae et al. 2013). In our sediment core, there
were also high-density, high-magnetic-susceptibility layers at depths of 19–21, 37–39, 42–44, and 84–90 cm. We
removed these layers for dating purposes due to the rapidityof the sedimentation event (Kuwae et al. 2013) and thereafter expressed the sediment depth as the corrected depth forsubsequent analysis.
The fact that the vertical profile of 210Pbexcess in thesediment core decreased exponentially with mass depth(Fig. 2a) suggests that the sedimentation rate was constantand that there had been no vertical disturbance. Under
such conditions, the CIC model (Robbins and Edgington1975) is the most appropriate for determining sediment age(Andersen 2006). The 210Pbexcess activities plotted against
the corrected depth of sediment decreased systematicallyfrom 0.24 Bq g−1 in the surface layer to 0.016 Bq g−1 at acore depth of 31 cm. Based on the CIC age model (Robbins
and Edgington 1975), the average mass accumulation rateof the sediment was estimated to be 0.0713 g cm−2 year−1,

313

Temporal variations in phytoplankton biomass over the past 150 years in the western Seto…
210Pb

137Cs

excess-1(Bq g-1)(Bq g )
0.001

0.01

(a)

0.1

1

0.0001

0.001

0.01
0
3

(b)

1

7
11
15

-2

Mass depth (g cm )

2
3

20
4

23

5

27

Corrected sediment depth (cm)Fig. 2  Vertical profiles of a210
Pbexcess and b 137Cs activity(Bq dry g−1) for the sedimentcore in Beppu Bay. c Age–depth
model based on the constantinitial concentration model ofRobbins and Edgington (1975)

6
31
7

Calendar year (A.D.)

2010
1990

(c)

137Cs fallout maxima

1970
1950
1930
1910
1890
1870
1850

0

5

and the calendar year ranged from 1896 at a core depthof 36.5 cm to 2009 at the surface. Because the 137Cs fallout maximum in Japan occurred in 1963 (Hirose et al.
2008a), the peak in 137Cs activity at a depth of about 20 cm(Fig. 2b) is considered to have occurred in the early 1960s.
This timing agrees well with the age estimated by 210Pb
dating (1963 AD, Fig. 2c). As described before, lamination was visible in the uppermost 20 cm above the horizon
at the peak of 137Cs activity. In the corresponding layersof the cores collected near the site of the core employedin this study, the thicknesses of laminae were almost constant (Kuwae et al. 2013), probably due to constant formation of annual varves. The lithological evidence implies
that the sedimentation rate and dilution effect were almost
unchanged after the 1960s, which is consistent with the linear trend in 210Pbexcess.

10
15
20
25
30
Corrected sediment depth (cm)35

40

4.2 Fossil pigments and temporal variations
in phytoplankton biomass
In the Beppu Bay sediment, pheophytin a, pyropheophytin a, and “pheophorbide a” were detected as chlorophylla derivatives (Fig. 3a). Pheophytin a and pyropheophytin acomprised around 60% or more of the total Chl-a (chlorophyll a and its derivatives) throughout the core, and “pheophorbide a” comprised the remainder (9–44%). The concentration of Chl-a in our core was low prior to the 1950s(Fig. 3b), but there was a small amount of temporal variation prior to the 1950s, although the magnitude of the variation was small compared to the variations after the 1960s.
The Chl-a concentration in the 1960s reached levels 2.3fold higher than those prior to the 1950s. In the 1970s, theChl-a concentrations decreased but remained higher than

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''Pheophorbide-a''

Chlorophyll-a

60
40

Chl-a concentration(µg g-1)

20

Fluxes of reconstructed Chl-a(mg m-2 year)

Pyropheophytin-a

Pheophytin-a

(a)

50
40
30
20
10

(b)

0
50

4.0

40

3.0

30
2.0

20

1.0

10

(c)

0

Average of Chlorophyll aconcentration (mg L-1)

Relative(%)

80

Chl-a / Pheo-a ratio

Fig. 3  Age profiles of a therelative abundance of theconcentration of the biological proxy common to all algal
taxa (chlorophyll a and its
derivatives: “pheophorbide a”,
pyropheophytin a, and pheophytin a), b the concentrationof Chl-a (chlorophyll a and its
derivatives), and c the fluxes ofreconstructed Chl-a [Chl-a wascorrected by removing the effectof post-burial degradation;dashed and solid lines represent
the fluxes calculated using
the first and second methods,
respectively; see Sect. 4.2], andd the ratio of chlorophyll a topheophytin a. The thick solidline with closed squares in cshows the average of the chlorophyll a concentrations during
four seasons in the surface
water of Beppu Bay based on
the regular monitoring data

N. K. Tsugeki et al.

0.3
0.2
0.1
1840

(d)
1860

1880

1900

1920

1940

1960

1980

2000

Year (AD)the concentrations during the 1950s. In the early 1990s, theChl-a concentrations again increased greatly.
The temporal variations in the concentrations of Chl-a
indicate that phytoplankton production rates in Beppu Bay
were considerably lower before the 1960s. However, toreach a robust conclusion, we needed to consider biotic andabiotic degradation of Chl-a in sediments that may havecaused the concentrations to decrease over time (Leavitt
and Carpenter 1990; Ming-Yi et al. 1993) and consequently
may have led to the apparently low Chl-a concentrations
before the 1950s. In order to eliminate the effects of degradation on the temporal variations in the Chl-a concentration, we calculated a degradation rate based on the assumption that pigment degradation follows first-order kinetics(e.g., Ishiwatari et al. 2009):

13(Chl − a)t = (Chl − a)0 × exp[−kt],
where (Chl-a)t is the normalized concentration of Chl-a attime t; t is the number of years after sedimentation of the
Chl-a (=0 at the sediment surface); and k is a first-order
rate constant (year−1). We estimated the first-order rate
constant using two calculation methods. First, we used theall data from the late 1840s to 2009 (the surface), as shownin Fig. 3b, yielding the following least squares equation:(Chl − a)t = 32.0 × exp[−0.011t] (r 2 = 0.81).

(1)Second, we used the data before the 1950s because therapid increase in Chl-a concentration that occurred after the
1960s was probably caused by an intensification of phytoplankton production associated with anthropogenic nutrient

315

We then reconstructed the Chl-a concentration prior topost-burial degradation (Fig. 3c) using the Chl-a concentration at the sediment surface obtained from Eqs. 1 and 2([Chl-a]0) and the ratio of the measured Chl-a concentration in a sample to the normalized Chl-a concentration attime t, respectively:(Reconstructed Chl − a)sample= (Chl − a)0 × (Chl − a)sample /(Chl − a)t
Flux of reconstructed Chl − a= Reconstructed Chl − a × AR,

(3)

(4)

where AR
is
the
mass
accumulation
rate(0.0713 g cm−2 year−1) obtained from the 210Pb-based CIC
model (Robbins and Edgington 1975). The temporal variations in the fluxes of reconstructed Chl-a calculated using
the two methods described above showed obvious increases
during the 1960s and around 1990, though only smallamplitude changes occurred before the 1950s (Figs. 3c,8a). The ratio of chlorophyll a to pheophytin a, which isindicative of the degree of preservation of labile pigments(Leavitt and Hodgson 2001; Reuss et al. 2010), gradually
increased until the late 1940s and then decreased, but again
increased towards the 1960s, although the value was lower
than 0.23, which was the maximum value before the late
1940s (Fig. 3d). Afterwards, it varied among years by lessthan 0.23 except during the early 1970s and after the late
1990s. It should be noted that the ratio greatly decreasedaround 1990. These results suggest that the marked increasein the fluxes of reconstructed Chl-a during the 1960s andaround 1990 compared to those before the 1940s cannot be
fully explained by the degradation effect, but rather can be
explained by increased productivity.
4.3 Meteorological, environmental, and oceanographic
conditions
Air temperatures in Beppu Bay area have been gradually
increasing, especially since (roughly) 1980 (Fig. 4a). The
monthly sum of precipitation has varied from year to year
but does not exhibit a temporal trend (Fig. 4b). Daylight
hours has varied among years, but they decreased slightly
from the 1980s to the early 1990s (Fig. 4c). The wind speed
decreased and then increased around 1980 but has changed
little since that time (Fig. 4d).

Air temperature (

18
17

(a)

16
15
2800

Precipitation
(mm)

(2)

Duration of sunlight(hours)(Chl − a)t = 16.9 × exp[−0.0062t] (r 2 = 0.53).

Wind speed (m s -1 )loading—an intensification also seen in other bays of the
Seto Inland Sea (Hirose et al. 2008b; Yoshioka et al. 2012).
Therefore, including data obtained after the 1960s may
bias the estimated effects of degradation. Consequently, we
obtained the following least squares equation:)

Temporal variations in phytoplankton biomass over the past 150 years in the western Seto…

(b)

2300
1800
1300
2500

(c)

2000
1500
2.9
2.5

(d)

2.1
1.7
1880

1900

1920

1940

1960

1980

2000

Year (AD)Fig. 4  Long-term changes in a the annual average air temperature,b the monthly sum of precipitation, c the duration of sunlight, and dthe annual average wind speed at Oita, the site of the meteorologicalobservatory nearest to Beppu Bay, are shown by thin lines. In eachpanel, the 3-year moving average is indicated by a bold line

Monthly flow volumes in the Oita and Ono rivers around
Beppu Bay are shown in Fig. 5. The volumes of both rivers
increased in the early 1980s and around 1993, though theyfluctuated slightly in the 1970s, but were about the same
before and after the early 1990s.
The DIN concentrations in Beppu Bay were relatively
high until the late 1970s, but subsequently decreased. They
increased temporarily in the mid-1980s and again increased
greatly in the early 1990s (Fig. 6a). The concentrations of
PO4-P (Fig. 6b) varied in a similar manner. According to
the monitoring data, the annual mean chlorophyll a concentration in Beppu Bay was high from the late 1980s to theearly 1990s and then decreased abruptly (thick solid linewith closed squares in Fig. 3c).
The riverine nutrient inputs to the Seto Inland Sea, suchas TN and TP, dramatically increased from the late 1950s
to the early 1970s, and then decreased towards the early
1980s (Fig. 7). Since then, the terrestrial nutrient input of
TN has barely changed, although it has gradually decreased
since the 1990s (Fig. 7a), whereas that of TP has also gradual decreased (Fig. 7b).

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N. K. Tsugeki et al.

4000

Oita riverMonthly flow volume (m 3 s -1)

3000
2000
1000
0
14,00012,000

Ono river

10,000
8000
6000
4000
2000
1970

1975

1980

1985

1990

1995

2000

Year (AD)1000

TN (ton day-1)

(a)

(b)

Year (AD)Fig. 6  Long-term changes in the monthly average a DIN and b
PO4-P concentrations in the surface layer (thin lines) measured at 13
sites in Beppu Bay from 1973 to 2003. The thick line in each panel
shows the 12-month moving average

(a)

800
600
400
200
0
90

TP (ton day -1 )PO4-P (µmol L-1)

DIN (µmol L-1)

Fig. 5  Monthly flow volumes in the Oita and Ono rivers (upper and lower panels, the Funai-Ohashi and Shirataki-Bashi sites, respectively)around Beppu Bay from 1970 to 2000. The bold line in each panel shows the 12-month moving average

(b)

70
50
30
10

1950

1960

1970

1980

1990

2000

2010

Year (AD)Fig. 7  Historical variations in the terrestrial nutrient inputs of total
nitrogen (TN) and phosphorus (TP) to the Seto Inland Sea

The bottom-water temperature from early summer
to fall in Beppu Bay showed a decreasing trend fromthe 1980s to the early 1990s (Fig. 8b). Since then, it has
greatly increased, although it has varied among years. The
sea level at Hosojima Station changed greatly from 1894
to 2005 (Fig. 8c), but was (similar to the bottom-water13

temperature) relatively low during the period from the
1980s to the early 1990s. In addition to that period, the sea
level was low around the late 1910s, in the 1930s, and in
the 1960s, whereas values were high around 1900, in the317

Temporal variations in phytoplankton biomass over the past 150 years in the western Seto…

1.0

(a)

0.5
0.0
-0.5
-1.0
1840

1860

1880

1900
18

Bottom WT ()

Fluxes of Chl-a anomaly
Ln (mg m-2 year-1)

Fig. 8  Anomalies in the afluxes of reconstructed Chl-a(corrected by removing theeffect of post-burial degradation; dashed and solid lines
indicate the flux anomaly
calculated using the first andsecond methods, respectively;
see Sect. 4.2), b bottom-watertemperatures in early summer tofall at an offshore site near the
sampling station, and c sea levelat Hosojima Station, averaged
from early summer to fall (Mayto October)

1940

1960

1980

2000

(b)

17
16
15

1900
15
Sea level anomaly (cm)

1920

10

1920

1940

1960

1980

2000

(c)

5
0
-5
-10

-15
1900

period from the 1940s to the 1950s, and in the early 1970s.
The recent period of low sea level is known to be consistent
with thermal effects given that the water temperature in the
Bungo Channel has also been low recently due to the intensified intrusion of bottom water from the shelf slope into
the channel (Fujiwara et al. 2004).

5 Discussion
5.1 Reconstructed primary productivities and thefactors that caused changes
The Seto Inland Sea is a major fishing ground in Japan(Imai et al. 2006), and its watershed is one of the mostindustrialized areas. Many industrial facilities were built
in the coastal zone of the sea after 1963, when the New

1920

1940
1960
Year (AD)

1980

2000

Industrial City Law was enacted (Takeoka 2002). Industrialization and urbanization since the 1960s have greatly
increased terrestrial nutrient inputs to the Seto Inland
Sea (Fig. 7; Sekine and Ukita 1997; SECA 2001). This
increase in nutrient loading was responsible for a sevenfold
increase in the number of red tide blooms between 1965
and 1976 (Okaichi 1997). In accordance with previous
reports (Honjo 1993; Okaichi 1997; Yamamoto 2003), theprimary productivity in Beppu Bay, as reconstructed fromour sedimentary records, was relatively low until roughly
1960 and then increased greatly until the early 1970s. In
the Seto Inland Sea, an environmental conservation law
was enacted in the late 1970s to reduce nutrient loadingfrom the watershed. Since then, terrestrial nutrient input
has reduced (Fig. 7; see also Yamamoto 2003). Indeed,
our sedimentary records showed that primary productivity
in the bay decreased from the 1970s to the early 1980s, a

13

318

time during which nutrient concentrations in the bay also
declined (Fig. 6). Honjo (1993) and Yamamoto (2003) havealso reported that the frequency of red tide blooms in the
Seto Inland Sea decreased after the 1970s, and attributed
this decrease to the reduction in nutrient loading from thewatershed. The density of flagellate cysts in the sedimentsof the eastern Seto Inland Sea (Harima-Nada) peakedaround 1970 and decreased thereafter (Ichimi et al. 2005).
All these results suggest that the degree of eutrophicationin the Seto Inland Sea has decreased since the late 1970s.
Interestingly, our results also demonstrated a large
increase in Chl-a fluxes from the late 1980s to the early
1990s. This temporal pattern of phytoplankton biomass
after the late 1980s in Beppu Bay is consistent with monitoring data for chlorophyll a obtained by the Japanese Ministry of the Environment (Fig. 3c; r = 0.774 and 0.699,
p = 0.014 and 0.036; dashed and solid lines showing thefluxes calculated using the first and second methods,
respectively). Because the limiting factor for phytoplankton growth in this bay is probably nutrients (Horiguchi andTerasawa 2000), and because there was an increase in the
nutrient concentrations around the early 1990s in the bay(Fig. 6), it is reasonable that the temporal increase in nutrient concentrations during this period was responsible forthe increase in phytoplankton biomass at the same time.
The next question is why the nutrient concentrations
increased in the early 1990s. One might suspect that nutrient supply from the watershed increased during this time.
However, as mentioned above, an efficient nutrient control
program for the Seto Inland Sea had been in place since
the late 1970s (Yamamoto 2003), and accordingly, the terrestrial nutrient inputs such as TP and TN clearly started
to decrease in the early 1970s, and they were almost constant or tended to decrease before and after the early 1990s(Fig. 7; Sekine and Ukita 1997; SECA 2001). The amountof precipitation and the volume of discharge from rivers
into Beppu Bay did not almost change around the early
1990s (Figs. 4, 5). It is thus difficult to attribute the increasein nutrient concentration after the early 1990s to increased
nutrient loading from the watershed.
Alternatively, an enhanced supply of nutrients from theshelf slope may have led to the increase in nutrient concentrations around the early 1990s in Beppu Bay. Coldand nutrient-rich water from the shelf slope intermittently
intrudes into the bottom waters of the Bungo Channel(Kaneda et al. 2002a), which connects Beppu Bay to the
Pacific Ocean. This phenomenon is called bottom intrusion (Kaneda et al. 2002a). When bottom intrusion occurs,
nutrient concentrations and phytoplankton biomass change
dramatically in the Bungo Channel (Koizumi 1999; Kaneda
et al. 2002a; Nakano et al. 2005; Kuroda et al. 2010). For
instance, Nakano et al. (2005) demonstrated that phytoplankton biomass in the Bungo Channel increased abruptly

13

N. K. Tsugeki et al.

in response to nutrients supplied from the ocean via bottom
intrusion, and phytoplankton biomass was higher in a yearof frequent occurrence of bottom intrusions than in a yearof infrequent occurrence of such intrusions. In Beppu Bay,bottom-water temperatures decreased towards the 1980s
and were very low during the early 1990s (Fig. 8b), which
was likely due to intensified bottom intrusion from theshelf slope into the bay. Thus, it is likely that the temporary
enhancement of nutrient supplies from the shelf slope inthe early 1990s raised the nutrient concentrations in Beppu
Bay, and consequently stimulated the primary productivity in the bay. Supporting this inference, it is recognizedthat diatom productivity in not only Beppu Bay (Kuwae,
in preparation) but also the Bungo Channel (Kuwae et al.
2006), as estimated from diatom valves in the sediments,
increased at around that time. Also, some studies haveshown that nutrient concentrations in the eastern parts of
the Seto Inland Sea (Osaka Bay; Sugimatsu and Isobe,2010) and those in the Kii Channel (Ozaki et al. 2004),
which connects the Seto Inland Sea and the Pacific Ocean,
increased around the same period because of the intensified
bottom intrusion from the shelf slope.
5.2 Effects of variability of the Kuroshio axis
on primary productivity
Kaneda et al. (2002b) and Kuroda et al. (2010) have proposed that the intensity of bottom intrusions into the Bungo
Channel is related to the position of the Kuroshio axis. Bottom intrusion waters originate from the upwelled wateron the slope (Kaneda et al. 2002a), and the upwelling iscontrolled by Ekman dynamics near the bottom beneath
the Kuroshio Current (Ichikawa and Kaneda 2000). When
the Kuroshio flows near Kyushu, bottom intrusion into the
Bungo Channel frequently occurs (Kaneda et al. 2002a). In
contrast, when the Kuroshio moves further offshore from
Kyushu, bottom intrusions occur infrequently. Therefore,
the extent of nutrient stimulation from shelf slope water
via bottom intrusions depends on the path of the Kuroshio(Sugimatsu and Isobe 2010).
The coastal sea level reflects the intensity of bottom
intrusion because the temperature change associated withcold upwelled water can cause the sea level to vary (Fujiwara et al. 2004; Kuroda et al. 2010). When our data werecompared with the sea-level data at Hosojima Station(Fig. 1b), significant negative correlations between the sea
level and the fluxes of reconstructed Chl-a were detected(Fig. 8a, c; r = –0.588 and –0.507, p = 0.010 and 0.004;
the r values are the correlation coefficients for the flux ofreconstructed Chl-a calculated using the first and second
methods, respectively). The inverse relationship between
phytoplankton biomass and sea level implies that theintensity of nutrient inputs from the shelf slope caused byTemporal variations in phytoplankton biomass over the past 150 years in the western Seto…

variations in the position of the Kuroshio axis is an important influence on primary productivity in Beppu Bay. In
concordance with our results, Kuwae et al. (2006) has previously reported similar patterns between the sea level at
Hosojima and sedimentary records of diatom productivity
in Bungo Channel.

6 Conclusions
Sedimentary records showed that phytoplankton biomass
in Beppu Bay within the Seto Inland Sea increased greatly
from the 1960s to the 1970s and decreased or remained stable in the early 1980s as a result of the establishment of asewage treatment system that reduced the influx of terrestrial nutrients to the sea. However, phytoplankton biomass
increased again from the late 1980s to the early 1990s. This
increase was probably caused by an influx of nutrients fromthe shelf slope as a result of intensified frequency of bottom intrusion. This inference is supported by the inverse
relationship between the reconstructed phytoplankton
biomass and the sea level at Hosojima, which is a proxy
for the intensification of bottom intrusion (Fujiwara et al.
2004). Because the sea level on the southeast coast of Japanvaries on a decadal timescale that is related to oceanic currents such as the Kuroshio (Senjyu et al. 1999), the resultspresented here imply that primary productivity in the Seto
Inland Sea has been greatly affected by variations in oceanic nutrient inputs on a decadal timescale.
In the Seto Inland Sea, the reduction in phytoplankton
productivity induced by the regulation of terrestrial nutrient inputs is thought to have been the primary reason for
the reduction in fishery production after the 1980s (Yamamoto 2003). Our results, however, imply that the remarkable increase in phytoplankton biomass in Beppu Bay after
the 1980s was due to an influx of nutrients from the ocean.
This conclusion raises another question, namely whether
enhanced phytoplankton biomass affects fishery productionin the bay. Further studies are therefore necessary to clarify whether and how the bottom-up effects of variations inprimary productivity due to changes in the supply of nutrients associated with variations of the Kuroshio axis have
impacted fishery production in the Seto Inland Sea.
Acknowledgements We thank Drs. Naoki Yoshie, Tomohiro
Komorita, Mitsuyo Saito, Naoki Fujii, and Kazuyoshi Moriya as wellas the captain of R/V Isana from the Center for Marine Environmental Studies (CMES) of Ehime University for their field sampling,technical support, and helpful discussions. This study was financially
supported by the 2007 Special Funds for Education and Research of
the Ministry of Education Culture, Sports, Science and Technology,
Japan, and was also partly supported by Grants-in-Aid for Scientific
Research (22340155 and 21244073) from the Japan Society for the
Promotion of Science, as well as by research grants (to MY and NT)

319

from the Mitsui & Co., Ltd. Environment Fund (no. R09-B022) andthe Kurita Water and Environment Foundation (grant no. 17210),
respectively.

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