Organic Geochemistry 103 (2017) 125–135

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Organic Geochemistry
journal homepage: www.elsevier.com/locate/orggeochem

Variations in lignin-derived phenols in sediments of Japanese lakes over

the last century and their relation to watershed vegetation
Fujio Hyodo a,⇑, Michinobu Kuwae b, Naoko Sasaki c, Ryoma Hayashi d, Wataru Makino e, Soichiro Kusaka f,
Narumi K. Tsugeki g, Seiji Ishida e, Hajime Ohtsuki e, Kohei Omoto h, Jotaro Urabe e
a
Research Core for Interdisciplinary Sciences, Okayama University, Okayama 700-8530, Japan
b
Center for Marine Environmental Studies, Ehime University, Matsuyama 790-8577, Japan
c
Graduate School of Life and Environmental Sciences, Kyoto Prefectural University, Kyoto 606-8522, Japan
d
Lake Biwa Museum, Kusatsu 525-0001, Japan
e
Graduate School of Life Sciences, Tohoku University, Sendai 980-8578, Japan
f
Museum of Natural and Environmental History, Shizuoka, Shizuoka 422-8017, Japan
g
Faculty of Law, Matsuyama University, Matsuyama 790-8578, Japan
h
Graduate School of Natural Science and Technology, Okayama University, Okayama 700-8530, Japan

a r t i c l e i n f o a b s t r a c t

Article history: Lignins have been used as a biomarker to explore changes in terrestrial organic matter input into lakes
Received 20 August 2016 and to investigate past watershed vegetation. Burial of organic carbon (OC) in lake sediments, an impor-
Received in revised form 30 October 2016 tant component of the global C cycle, is likely associated with the terrestrial OC input. However, few stud-
Accepted 4 November 2016
ies have explored changes in terrestrial C input into lakes in the last century. Furthermore, the
Available online 11 November 2016
relationship between lignin phenol compositions and watershed vegetation remains poorly examined.
In this study, we examined changes in OC concentrations, OC mass accumulation rates (MAR), and lignin
Keywords:
phenol compositions over the last century in sediments from six lakes in Japan that differ in watershed
CuO oxidation
Eutrophication
land-use and vegetation. The sediments were dated using 210Pb and 137Cs, and showed increased OC con-
GIS centrations and MARs in three lowland lakes over the last century. This pattern was not found in three
Lake sediment mountain lakes. In one of the lowland lakes, lignin phenol concentrations normalized to OC did not
Terrestrial organic matter change during the periods with high OC concentrations and MARs. This indicates that not only eutroph-
Watershed vegetation ication but also enhanced terrestrial OC input could lead to greater burial of OC. The lignin phenol com-
positions did not show clear trends over the last century in most of the lakes examined. The ratios of
syringyl to vanillyl phenols and the lignin phenol vegetation index had significant relationships with pro-
portions of angiosperms in watershed vegetation. These results demonstrate that lignin phenols are use-
ful in inferring recent as well as past changes in lake watershed environments.
Ó 2016 Elsevier Ltd. All rights reserved.

1. Introduction can indicate taxonomic groups of higher plants (gymnosperms

Lignins are polymers of phenols synthesized by higher
(vascular) plants to support their vascular systems (Weng and
Chapple, 2010; Novo-Uzal et al., 2012). The types of phenols
yielded by alkaline copper oxide (CuO) oxidation differ among
plant taxa and among tissue types. Vanillyl phenols are present
in all higher plant tissues, whereas syringyl phenols are synthe-
sized only by angiosperms, and cinnamyl phenols are only abun-
dant in non-woody tissues. Therefore, lignin phenol compositions
⇑ Corresponding author at: Research Core for Interdisciplinary Sciences, Okayama
University, 3-1-1, Tsushimanaka, Okayama 700-8530, Japan. Fax: +81 86 251 8705.
E-mail address: fhyodo@cc.okayama-u.ac.jp (F. Hyodo).
and angiosperms) and tissue types (woody tissue and non-woody
tissue) of land-derived organic matter (Hedges and Mann, 1979;
Jex et al., 2014). Most terrestrial plants produce lignins, which
are recalcitrant toward microbial degradation (Meyers, 1997). As
such, lignins found in sediments have often been used to explore
historical changes in terrestrial organic matter input in aquatic
ecosystems and terrestrial vegetation (Hedges et al., 1982;
Meyers and Ishiwatari, 1993; Jex et al., 2014).
Recent studies have shown that organic carbon (OC) accumula-
tion rates in inland freshwater sediments (e.g., lakes) are compara-
ble to, or much higher than, those in marine sediments and
terrestrial soils, indicating the importance of organic C burial in lake
ecosystems in the global C cycle (Cole et al., 2007; Tranvik et al.,

http://dx.doi.org/10.1016/j.orggeochem.2016.11.001
0146-6380/Ó 2016 Elsevier Ltd. All rights reserved.
126 F. Hyodo et al. / Organic Geochemistry 103 (2017) 125–135
2009; Hanson et al., 2014). The high burial efficiency of OC in lake
sediments is likely related to the preservation of terrestrially
derived organic C in sediments on a millennial timescale (Cole
et al., 2007; Sobek et al., 2009). The C accumulation rates are also
known to be higher in lakes exposed to greater anthropogenic influ-
ences, such as eutrophication (Schelske and Hodell, 1991; Meyers,
2006; Downing et al., 2008; Anderson et al., 2013), logging, urban-
ization (Moingt et al., 2014), and impoundment (Teisserenc et al.,
2014). Despite such recent changes in C input into lake ecosystems,
few studies have explored the relative contribution of terrestrial
organic matter to C deposits over the last century (Hyodo et al.,
2008; Moingt et al., 2014; Chmiel et al., 2015).
Earlier studies used lignin phenols in lake sediments to recon-
struct past vegetation types in watersheds, such as gymnosperms
versus angiosperms or woody versus herbaceous species, by refer-
ring to the phenol compositions of plant tissues of these taxonomic
groups (Hedges et al., 1982; Ishiwatari and Uzaki, 1987; Moingt
et al., 2014). Further, abiotic (e.g., photo-oxidation) and microbial
degradation prior to sedimentation can alter lignin phenol compo-
sitions (Hedges et al., 1988; Opsahl and Benner, 1995; Hernes and
Benner, 2003). Teisserenc et al. (2010) confirmed that lignin-
derived phenols reflect the vegetation in the watershed in a boreal
region. However, it is still unclear whether this relationship could
hold in temperate regions where angiosperms often dominate over
gymnosperms.
In this study, we explored historical changes in the OC concen-
trations, OC mass accumulation rates (MAR), and lignin phenol
compositions in the sediments of three lowland and three moun-
tain lakes in Japan. We dated the sediments using 210Pb and 137Cs
and focused on the last century, when the anthropogenic influ-
ence became globally significant. Watersheds of the lowland lakes
currently include both urban and agricultural lands, whereas
those of the mountain lakes appear to be unaffected by direct
human activity. Therefore, it was expected that eutrophication
and land-use change altered OC MARs and lignin phenol compo-
sitions in the lowland lakes over the last century. However, such
patterns were not expected to emerge in the mountain lakes. Fur-
ther, these lakes include watershed vegetation in a temperate
region that differ in proportions of angiosperms and gym-
nosperms as well as life forms such as trees and grasses. These
differences allowed us to assess the environmental factors that
affect lignin phenol compositions through a comparison of the
lakes. We investigated the relationship between lignin phenol
compositions and the watershed vegetation, which was estimated
using a geographic information system (GIS). For the analysis, we
added the results of a previous analysis of Lake Biwa, the largest
lake in Japan (Hyodo et al., 2008). Our results showed that the
patterns in OC inputs into lakes and the relative contribution of
terrestrial OC to them varied across the different lakes examined,
and that lignin phenols could certainly reflect the watershed
vegetation.
2. Materials and methods
2.1. Study sites
We sampled the lake sediments of six lakes: lakes Akan, Oshima-
Ohnuma, Kizaki, Rausu, Niseko-Ohnuma and Mikuri-ga-ike
(Fig. 1 and Table 1). Three of these lakes (Akan, Oshima-Ohnuma
and Kizaki) are situated on plains where the watersheds include
urban and agricultural areas. The other three lakes (Rausu, Niseko-
Ohnuma and Mikuri-ga-ike) are located in mountainous regions
with no urban or agricultural areas in the watershed (Fig. 1). We
used previously published data on Lake Biwa to compare lignin phe-
nol compositions across lake sediments (Hyodo et al., 2008).
2.2. Sediment sampling
Sediment samples of lakes Rausu and Niseko-Ohnuma and
those of lakes Mikuri-ga-ike and Kizaki were collected in July
2010 and August 2011, respectively. Sediments of Lake Akan were
collected in July 2010 and July 2012, because the sediment core
(Ak2) obtained by the first sampling in 2010 (30 cm) was not long
enough to represent the last century (see Results). The core col-
lected in 2012 (AKE) was used for OC and lignin phenol analyses.
Samples of lakes Rausu, Niseko-Ohnuma, Mikuri-ga-ike and Akan
(Ak2) were collected using a gravity corer fitted with an acrylic
tube (11 cm i.d. and a length of 50 cm; model HR, RIGO Co., Ltd.,
Saitama, Japan). Cores from Lake Oshima-Ohnuma were collected
in February 2011 using a 1 m long gravity corer (model HRL, RIGO
Co., Ltd.). The samples from lakes Kizaki and Akan (AKE) were col-
lected by professional divers using the acrylic tubes. Several undis-
turbed cores were collected from each lake. One core from each
lake was selected for this study and was sectioned at 1 cm intervals
immediately after collection. The only exception was that for Lake
Mikuri-ga-ike which was sectioned at 0.5 cm intervals. The sam-
ples were placed into plastic bags and were stored in freezers. They
were later freeze-dried and homogenized using a mortar and pes-
tle for the following analyses.
2.3. Determination of the age and accumulation rates of the core
sediments
The core chronology was determined by the constant rate of
supply (CRS) method of 210Pb dating (Appleby and Oldfield,
1978) and was checked by the 137Cs peak traced in 1962–1963
(Appleby, 2001). The age of a given sample mass depth was calcu-
lated using the 210Pbexcess inventory, which was obtained by the
numerical integration of the radioactivity of 210Pbexcess versus the
mass depth profile using the following equations (Appleby, 2001):
Z 1
A¼ CðmÞdm ð1Þ
m
and
Z 1
Að0Þ ¼ CðmÞdm; ð2Þ
0
where m denotes the depth of the sediment layer of age t, C(m) is
the radioactivity of 210Pbexcess at the depth m, and A and A(0) are
210
Pbexcess inventories below m and the total inventories, respec-
tively. From the values calculated above, the age t of sediments at
depth m were calculated by
t ¼ 1=k lnðAð0Þ=AÞ; ð3Þ
where k is the 210Pb radioactivity decay constant.
Accumulation rate (r) at a given sample mass depth m was
determined from the equation (Appleby, 2001)
r ¼ kA=CðmÞ; ð4Þ
where k is the 210Pb radioactivity decay constant, A is the total
inventory below the mass depth, and C(m) is the radioactivity of
210
Pbexcess at the depth m.
210
Pb, 214Pb, and 137Cs activities were determined by the
c-spectroscopy analysis of the dried sediment. The dried samples
were sealed in standard holders for one month to allow 222Rn
and its short-lived daughters to equilibrate. Radioactivities for
the cores Mk6 from Lake Mikuri-ga-ike and Ra1 from Lake Rausu
were determined with a Ge-detector (GWL–90-15–S, EG & G
ORTEC, USA) equipped with a multichannel analyzer (MCA7700,
 F. Hyodo et al. / Organic Geochemistry 103 (2017) 125–135 127

Akan Rausu
45°N R
A
N
145°E
O
40°N

130°E M K
35°N
B

140°E 0 2 km 0 0.5 km
135°E
Oshima- Niseko-
Ohnuma Ohnuma
Watershed

Conifer forest (gymnosperm)

Mixed forest
(gymnosperm/angiosperm)
Broadleaved forest (angiosperm)

Grassland (angiosperm)
No vegetation
(urban area/bare ground)
No vegetation (open water) 0 5 km 0 0.5 km

Biwa Kizaki Mikuri-ga-ike

0 10 km 0 1 km 0 0.2 km

Fig. 1. Locations of the lakes studied in Japan, and the watershed vegetation. Capital letters in the map on the upper left indicate the location of each lake. The vegetation of
Lake Biwa was used to compare lignin-derived phenol compositions among the Japanese lakes. Vegetation in each lake watershed was estimated using GIS. See Section 2.6 for
details.

SEIKO EG & G, Tokyo, Japan) at the Research Institute for Humanity
and Nature, Japan. Radioactivities for the other cores (Ak2 and AKE
from Lake Akan, Ni1 from Lake Niseko-Ohnuma, Os2 from Lake
Oshima-Ohnuma, and K2 from Lake Kizaki) were determined with
a Ge-detector (GXM25P, EG & G ORTEC, Tokyo, Japan) equipped
with a multichannel analyzer (MCA7700, SEIKO EG & G, Tokyo,
Japan) at the Center for Marine Environmental Studies, Ehime
University, Japan. The activity of 210Pbsupported was estimated by
measuring the activity of 214Pb, and the activity of 210Pbexcess was
determined from the difference between the total and the sup-
ported 210Pb (210Pbexcess = 210Pbtotal  214Pb).
Turbidite layers were found in the core-sampled sediments of
Lake Kizaki, at depths of 4–10 cm, 13–17 cm, 20–25 cm,
30–32 cm, 39–50 cm and 53–58 cm. They were characterized by
high values of dry bulk density and magnetic susceptibility
(data not shown). The turbidite layers were removed from the orig-
inal depths before the dates were calculated based on the CRS
model.
Although the CRS-based dating method requires a total inven-
tory of 210Pbexcess in the sediments, we could not retrieve samples
from depths which were close to the detection limit of 210Pbexcess,
for K2 (Lake Kizaki) and Ak2 (Lake Akan). For the core K2, we esti-
mated the inventory of the depths below the core bottom from an
exponential regression model of 210Pbexcess versus the mass depth
(g/cm2) derived from the 210Pbexcess data below 58 cm, whose
levels showed an exponential decrease in 210Pbexcess. For Ak2, we
128 F. Hyodo et al. / Organic Geochemistry 103 (2017) 125–135

Table 1
Characteristics of Japanese lakes examined in this study.

Lake Typea Altitude Latitude Longitude Maximuma Lake area Watershed area Angiosperm/vegetationb Grass/vegetationb
(m) depth (m) (km2)b (km2)b
Lowland lakes
Akan Eutrophic 418 43°270 N 144°060 E 39 12 98 0.41 0.03
Oshima-Ohnuma Mesotrophic? 128 41°590 N 140°410 E 13.6 10 160 0.67 0.26
Kizaki Mesotrophic 758 36°330 N 137°500 E 29.5 1.6 21 0.64 0.13
Biwac Mesotrophic 81 35°200 N 136°100 E 103.6 709 3072 0.63 0.36
Mountain lakes
Rausu Oligotrophic 732 44°010 N 145°040 E 2.1 0.4 5.5 0.78 0.08
Niseko-Ohnuma Oligotrophic 699 42°530 N 140°370 E 15 0.09 0.99 0.97 0.63
Mikuri-ga-ike Oligotrophic 2407 36°340 N 137°350 E 15 0.02 0.14 0.87 0.26
a
Lake types were based on biodiversity Center of Japan, Ministry of the Environment, http://www.biodic.go.jp/reports/2–4/4–7-1.html.
b
These lake characteristics were estimated on the basis of GIS data. See Section 2.6 for details.
c
The data on lignin-derived phenols of Lake Biwa derived from Hyodo et al. (2008) were used for comparison.

used three high-magnetic susceptibility events to estimate the lignin phenol vegetation index (LPVI) introduced by Tareq et al.
ages at sample depths based on stratigraphic correlations between (2004) based on the following equation
the cores Ak2 and AKE (9.5 cm for Ak2 and 10.5 cm for AKE;    
16.5 cm for Ak2 and 18.5 cm for AKE; and 25.5 cm for Ak2 and SðS þ 1Þ CðC þ 1Þ
LPVI ¼ þ1  þ1 ; ð5Þ
28.5 cm for AKE). Vþ1 Vþ1

where V, S, and C are expressed as a percentage of the total weight

2.4. Organic carbon concentration and mass accumulation rates
Organic carbon contents of the dried samples were measured
using an elemental analyzer (Flash 2000, Thermo Fisher Scientific).
To remove the inorganic carbon, the samples were treated with
0.5 N HCl. The OC MARs were estimated based on the accumulation
rates and the OC concentrations.
2.5. Lignin-derived phenol analysis
We used five to ten sections of the sediment core from each lake
for lignin-derived phenol analysis. These phenols were analyzed
based on CuO oxidation methods (Hedges and Ertel, 1982) as
described in a previously study (Hyodo et al., 2008). Briefly, sedi-
ments containing approximately 10 mg of OC were oxidized under
alkaline conditions with CuO in 10 ml Teflon containers with stain-
less steel jackets at 155 °C in a drying oven for 3 h. Once the con-
tainers were opened, known amounts of ethyl vanillin were
added to the solution as an internal standard. The alkaline solu-
tions were acidified to pH 1 by adding concentrated HCl, and the
organic phase was extracted with ethyl acetate. The ethyl acetate
was evaporated to dryness under a stream of N2 gas. The lignin
phenols were dissolved in pyridine and were derivatized with a
trimethylsilylation agent (99% BSTFA + 1% TMCS, Aldrich). The
derivatized CuO oxidation products were analyzed using a gas
chromatograph (GC-2014, Shimadzu) fitted with
30 m  0.25 mm i.d. DB-1 capillary column and a flame ionization
detector. The column temperature was raised from 100 °C to
270 °C at a rate of 4 °C/min. The lignin phenols were identified
by comparing the GC retention time to that of the commercial
standards.
The lignin phenol concentrations were estimated as the total
weight in milligrams of the sum of vanillyl phenols (V; vanillin, ace-
tovanillone, vanillic acid), syringyl phenols (S; syringaldehyde, ace-
tosyringone, syringic acid), and cinnamyl phenols (C; p-coumaric
acid, ferulic acid) normalized to 100 mg of OC (mg/100 mg-OC)
(Hedges and Mann, 1979). The S/V and C/V ratios could indicate
the taxonomic groups (gymnosperms and angiosperms) and tissue
types (woody tissue and non-woody tissue) of higher plants,
respectively (Jex et al., 2014). In addition, the ratio of vanillic acid
to vanillin, (Ad/Al)v, was used as an index of oxidative lignin
degradation (Opsahl and Benner, 1995). We also estimated the
of lignin per 100 mg OC. Different types of plant tissues produce
distinct values of LPVI: 1 for gymnosperms woods, 12–27 for non-
woody gymnosperm tissues, 67–181 for angiosperm woods and
378–1090 for non-woody angiosperm tissues. Analytical precision
for these lignin parameters was better than 10%.
2.6. GIS analysis on the vegetation cover in watersheds
Vegetation data were compiled based on a GIS-based vegetation
maps at scales of 1:25,000 or 1:50,000 using ArcGIS (ESRI, Inc.). The
vegetation data maps, which were created from aerial pho-
tographs, satellite images and field surveys, were provided by the
Biodiversity Center of Japan, Ministry of the Environment of Japan.
We used data from a 1999–2004 census that provided 1:25,000
scale maps of lakes Rausu, Akan and Biwa. For lakes
Oshima-Ohnuma, Kizaki, Niseko-Ohnuma, and Mikuri-ga-ike,
where 1:25,000 maps were not available, datasets from a
1994–1998 census at a scale of 1:50,000 were used.
We classified the watershed vegetation in the following four
classes and estimated their areas in the watersheds: (1) coniferous
forest (gymnosperm trees), (2) broad-leaved forest (angiosperm
trees), (3) herbaceous vegetation (grasses), and (4) non-
vegetation areas. When the vegetation consisted of two classes
(e.g., coniferous and broad-leaved mixed forest), we equally split
a the vegetation areas into the two classes.
2.7. Statistical analysis
We applied one-way analysis of variance (ANOVA) to examine
the differences in lignin phenol parameters (lignin phenol concen-
tration, S/V, C/V, LVPI, and (Ad/Al)v) across the seven lakes, includ-
ing Lake Biwa. In this analysis, the lignin phenol parameters of all
sediment layers were used. We used simple regression analysis to
examine whether the proportions of angiosperms (angiosperm
trees and grass) and of grasses in all the vegetation in each water-
shed affect the lignin phenol parameters (S/V, C/V and LVPI). For
this analysis, the mean values of these parameters in all sediment
layers were estimated for each lake and were then used in the
regression analyses. We also used only the surface layers of the
sediments corresponding to the 1990s to the present (the top
layer), during which period the watershed vegetation was
 F. Hyodo et al. / Organic Geochemistry 103 (2017) 125–135 129

Lake Akan Lake Rausu

210
Pb 210
Pb
214
Pb 214
Pb
137
Pb (Bq/g) Cs 137
Cs

Lake Oshima-Ohnuma Lake Niseko-Ohnuma

Radioactivity for 137Cs (Bq/g)

210 210
Pb Pb
214
214

214
Pb Pb
Pb and

137 137
Cs Cs
210
Radioactivity for

Lake Kizaki 210 Lake Mikuri-ga-Ike 210

Pb Pb
214 214
Pb Pb
137 137
Cs Cs

Depth (cm) Depth (cm)

Fig. 2. Radioactivity of 210Pb, 214

Pb, and 137
Cs of the lake sediments. Gray zones in the panel of Lake Kizaki indicates the turbidite layers. Error bars indicate standard
deviations of radioactivities.

accessed, to estimate the mean values. These statistical analyses
were performed using JMP (Macintosh ver.9.02, SAS Institute).
3. Results
3.1. Radioactivity of 210
Pb, 214
Pb, and
chronologies
The 210Pb radioactivity in all the lake sediments for our study
declined non-exponentially with depth (Fig. 2), implying that the
sediment accumulation rates were not constant and that the use
of the CRS model was the most appropriate for determining sedi-
ment age (Appleby and Oldfield, 1978). The 210Pb chronologies
(Supplementary Fig. S1) showed that the calendar year
corresponding to a core depth of 4.5 cm for Lake Rausu was
1929. The years were 1903 for the core depth of 44.5 cm for core
AKE of Lake Akan, 1870 for 14.5 cm for Lake Niseko-Ohnuma,
1882 for 34.5 cm for Lake Oshima-Ohnuma, 1861 for 10.75 cm
137
Cs and CRS-based for Lake Mikuri-ga-ike, and 1880 for 21.5 cm (a section removed
because of the turbidite layers) for Lake Kizaki. Although CRS age
models can extend to deeper levels, they have very large age
errors > 100 years. Calendar-age errors in the records of lakes
Niseko-Ohnuma, Oshima-Ohnuma, Mikuri-ga-ike, and Kizaki were
estimated to be < 4 years after the 1960s, < 11 years around 1930,
and < 25 years in the early 20th century. Age errors in Lake Akan
were < 5 years after the 1960s, < 17 years around 1930, and
130 F. Hyodo et al. / Organic Geochemistry 103 (2017) 125–135

< 39 years in the early 20th century. In the record of Lake Rausu,
errors were < 5 years after the 1970s, < 13 years during the
1950s, and < 30 years during the 1920s.
The maximum radioactivity of 137Cs (Fig. 2) was found at depths
of 26.5 cm for core AKE from Lake Akan, 14.5 cm for Lake Oshima-
Ohnuma, 28.5 cm (13.5 cm: depth in the core in which all the sec-
tions containing turbidite layers were removed) for Lake Kizaki,
8.5 cm for Lake Niseko-Ohnuma, and 6.75 cm for Lake Mikuri-ga-
ike. We assigned these depths to the fallout maxima around
1963 (Roberts, 1998), which agrees with the ages estimated by
210
Pb dating (Supplementary Fig. S1). We could not check the con-
currence for Lake Rausu because the 137Cs peak was unclear in the
depth profile, probably due to low sedimentation rates and physi-
cal or biological mixing of the sediments. Volcanic glasses of Ta-a
(from eruptions in AD 1739) and Ko-c2 (AD 1694) were abundant
at the depths of 7–9 cm and 9–10 cm, respectively, of the core from
Lake Rausu (data from Yugo Nakamura in Hokkaido University are
not shown). The accumulation rates, estimated from the tephra
horizon and the sediment ages, were 0.008–0.009 g/cm2/yr. These
rates were consistent with those of 0.010 ± 0.002 g/cm2/yr at a core
depth of 2.5 cm that was estimated from the CRS age model
(Supplementary Fig. S2).
Three high-magnetic susceptibility events at core depths of
10.5 cm, 18.5 cm, and 28.5 cm for AKE were dated at AD 1997,
1983, and 1968 respectively. We dated sample depths for core
Ak2 based on the linear interpolation between the event depths
and dates in AKE and Ak2. The bottom depth of the core Ak2 was
AD 1961. The age model for core Ak2 (Supplementary Fig. S1) is
consistent with the 137Cs peak in the core Ak2 (24.5–26.5 cm,
Supplementary Fig. S1).
3.2. Organic carbon concentration and mass accumulation rates
The OC concentrations in the sediments of the three lowland
lakes were approximately 4% at the bottom layers and showed
upward increasing trends in Lake Akan in 1950 and in lakes
Oshima-Ohnuma and Kizaki in 1960 (Fig. 3). Such increasing
trends were not observed in the mountain lakes. The OC concentra-
tion in Lake Rausu sediments was relatively constant at 5%. The OC
concentration in Lake Niseko-Ohnuma decreased in 1940 from 15%
to 10% and showed a constant trend thereafter. The OC concentra-
tion in Lake Mikuri-ga-ike sediments began to increase in 1960,
reached a peak (ca. 10%) in 1970, and returned to the previous level
(5%) in 1980.
The OC MAR in lowland lake sediments showed increasing
trends during the previous century. The sediment core of Lake
Akan showed that the OC MAR increase started in 1940, and fur-
ther increased in 1960, and maintained high values with occasional
fluctuations. The OC MAR of Lake Oshima-Ohnuma increased in
1970, further increased after 1990, and maintained this trend
(Fig. 3). The OC MAR of Lake Kizaki increased in 1960 and seemed
to have decreased once in 1990. The sediments of the mountain
lakes did not show increasing trends similar to those of the low-
land lakes. The sediments of Lake Rausu did not show a clear trend

OC MAR OC MAR
1 1
10
20 2
Age (Year)

Depth(cm)

30
Age (Year)

Depth(cm)
Akan

Rausu

3
40
4
44
5
48

1 1
5
5
10
Niseko-Ohnuma
Oshima-Ohnuma
Age (Year)

Age (Year)
Depth(cm)

Depth(cm)

15 10
20
25 13

29 15
30
16

2 1

12 3
Mikuri-ga-ike

5
Age (Year)

Depth(cm)

20
Age (Year)

Depth(cm)
Kizaki

28 7
36
9

40 10

(%) (mg/cm2/yr) (%) (mg/cm2/yr)

Fig. 3. Changes in organic carbon (OC) concentrations and mass accumulation rates (MAR) in the sediments of three lowland lakes (Lake Akan, Lake Oshima-Ohnuma, and
Lake Kizaki) and three mountain lakes (Lake Rausu, Lake Niseko and Lake Mikuri-ga-ike). Note that the scales of the x and y axes are different among the lakes.
 F. Hyodo et al. / Organic Geochemistry 103 (2017) 125–135 131

Lignin/OC S/V C/V (Ad/Al)v LPVI

2
8
10
16

Age (year)

Depth(cm)
22
Akan 26
30

40

52

2
5
7
Oshima-Ohnuma

10
Age (year)

Depth(cm)
15

22

30
45

2
4
12
18
Age (year)

Depth(cm)
20
Kizaki

32
36
37

39
62

(mg/100mg-OC)

Fig. 4. Changes in lignin phenol concentrations (Lignin/OC), S/V, C/V, (Ad/Al)v and LPVI in the sediments of the lowland lakes. Note that the scales of the x and y axes are
different among the lakes. Data for the sediments for which dates could not be determined due to low radioactivity are also shown with the sampling depth for comparison.

of OC MAR over the last century. Moreover, the OC MAR in Lake
Niseko-Ohnuma increased from 1940, and the trend continues to
the present day, whereas the OC concentration became lower. As
observed in the OC concentrations, the MAR in Lake Mikuri-ga-
ike peaked in 1970 with the highest value (15 mg/cm2/yr) out of
all the lakes examined.
3.3. Lignin-derived phenols
The lignin phenol concentration in Lake Akan sediments
decreased from 1.2 to 0.8 mg/100 mg-OC in 1960, and to
0.6 mg/100 mg-OC in 1980, after which time it remained constant
(Fig. 4). Lake Kizaki sediments also showed a lignin phenol concen-
tration that decreased from 1.0 to 0.8 mg/100 mg-OC in 1950 and
further decreased to 0.7 mg/100 mg-OC in 1970. Meanwhile, the
lignin phenol concentration in Lake Oshima-Ohnuma remained
relatively constant at 1.0 mg/100 mg-OC through the core. In the
mountain lakes, such decreasing trends were never observed
(Fig. 5). In particular, the lignin phenol concentrations in Lake
Mikuri-ga-ike did not show a clear trend despite large variations
in OC concentrations and MAR over the last century. The lignin
phenol concentrations of lakes Rausu and Niseko-Ohnuma were
relatively high at 2 mg/100 mg-OC.
Regarding the lignin phenol parameters, the S/V and C/V ratios
of the lowland and mountain lake sediments, except for Lake Akan,
showed no clear historical trend over the last century (Figs. 4 and
5). The S/V and C/V ratios of Lake Akan sediments have tended to
increase since 1970. The LPVI of Lake Akan sediments showed an
increasing trend, especially in 1970. In both the lowland and
mountain lakes, no clear change in (Ad/Al)v was noted over the last
century.
The S/V and C/V ratios differed significantly among the seven
lakes including Lake Biwa (F = 70.3, P < 0.0001 and F = 122.2,
P < 0.0001, for S/V and C/V respectively; Supplementary Fig. S3).
The LPVI also showed significant differences among the lake sedi-
ments (F = 115.3, P < 0.0001). The (Ad/Al)v of the lake sediments
differed significantly across the lakes (F = 96.6, P < 0.0001), and
was higher in Lake Mikuri-ga-ike than in the other lakes.
These lignin phenol compositions of the lake sediments showed
a good correspondence to the watershed vegetation estimated
using GIS. When the mean values of all sediment layers were used,
the S/V ratio had a significant relationship with the proportion of
grass in watershed vegetation (Fig. 6). LPVI also had significant
relationships with the proportions of angiosperm and of grass in
all watershed vegetation. These significant relationships of
S/V and LVPI were also observed when the means of the surface
sediment layers, corresponding to the years between 1990 and
the present, were used. However, the relation of LPVI to the
proportions of grass in all the vegetation became marginally
significant (r2 = 0.498, P = 0.0762) (data not shown).
132 F. Hyodo et al. / Organic Geochemistry 103 (2017) 125–135

Lignin/OC S/V C/V (Ad/Al)v LPVI

1
2

Age (year)

Depth(cm)
Rausu
3

3
5
6
Niseko-Ohnuma

9
Age (year)

Depth(cm)
10
11
12
13
14
17

2
3
Mikuri-ga-ike

4
Age (year)

Depth(cm)
5
6
7
8

10

(mg/100mg-OC)

Fig. 5. Changes in lignin phenol concentration, S/V, C/V, (Ad/Al)v and LPVI in the sediments of the mountain lakes. Note that the scales of the x and y axes are different among
the lakes. Data for the sediments with undeterminable dates, owing to low radioactivity, are also shown with the sampling depth for comparison.

4. Discussion monitoring began in 1973, possibly because of the increase of

4.1. OC concentrations and mass accumulation rates
The sediments dated by 210Pb and 137Cs showed that OC con-
centrations and MARs in the lowland lakes showed increasing
trends over the last century. The OC MAR indicates changes in
the delivery rates of organic matter to the sediments, although
the occurrence of post-burial degradation of organic matter in sur-
face sediments with oxic pore-water needs to be taken into
account (Meyers and Teranes, 2001). In Lake Akan, the increase
of OC MAR occurred after the 1930s, when tourism became popu-
lar; the area, including Lake Akan, became a designated National
Park (Kataoka, 1994). The further increase of OC MAR after 1960
is consistent with previous reports that transparency in the lake
water dropped from the 1930s (7–9 m) to the 1960s (4–7.5 m)
due to eutrophication caused by increased loads of sewage water
(Sakata and Hino, 1994). The transparency in the lake water
seemed to be rather constant (3–6 m) in the 1980s after the imple-
mentation of a sewage treatment plant (Igarashi et al., 2000). In
Lake Oshima-Ohnuma, OC MARs increased after the 1960s, espe-
cially after the 1980s, and did not show a decreasing trend. In fact,
earlier studies have reported a decline of water quality between
1977 and 1996 (Yoshimura et al., 2000) and a gradual increase of
the chemical oxygen demand (COD) in lake water since the
farmland and urban area in the watershed (Ishikawa, 2000). The
sediments of Lake Kizaki showed that OC concentrations increased
in the 1970s. This is in agreement with earlier reports of oxygen
concentration increase and phytoplankton composition change in
lake surface water in the 1970s, both of which indicate the occur-
rence of eutrophication due to increased loads of sewage water
(Hayashi, 2001; Kiyosawa, 2001).
In contrast to the lowland lakes, the mountain lakes did not
demonstrate such increasing trends in either OC concentrations
or MARs. The sediments of Lake Rausu showed relatively constant
OC concentrations and MARs, indicating that the environment
surrounding this lake, the Shiretoko World Heritage area, has
been well preserved over the last century. In Lake Niseko-
Ohnuma, the OC concentrations decreased in the early 1900s,
although the OC MARs increased after 1950. This indicates an
increase in deposition rates of inorganic materials into the sedi-
ments, although the cause is unclear. Both the OC concentration
and MAR peaked in approximately the early 1970s in Lake
Mikuri-ga-ike. The same change in accumulation rates have been
reported in two previous studies (Fukuzawa, 2006; Hosono et al.,
2016). Fukuzawa (2006) suggested that the changes were caused
by soil erosion associated with a rapid increase in the number of
mountain-climbers in the early 1960s and later development of
mountain trails around the lake.
 F. Hyodo et al. / Organic Geochemistry 103 (2017) 125–135
r2 = 0.657
r2 = 0.399 p = 0.027
p = 0.128
S/V
y = 1.21x + 0.62
C/V
r2 = 0.218 r2 = 0.001
p = 0.291 p = 0.878
y = 1081x -352
LPVI
r2 = 0.704
p = 0.018
r2 = 0.595
p = 0.042
y = 885x + 193
Angiosperm/Vegetation Grass/Vegetation
Fig. 6. Relationship of S/V, C/V and LPVI to the proportions of angiosperm and grass
to watershed vegetation in the watersheds of the seven lakes. Regression lines are
shown for the significant relationships. In these analyses, the mean values of all the
depth of each lake were used.
4.2. Historical changes in the lignin phenol composition in each lake
The lignin phenol concentration normalized to OC decreased in
the sediments of two lowland lakes, Akan and Kizaki, during the
periods with increased OC MARs, likely indicative of a greater con-
tributions of aquatic primary production to the sedimentary
organic matter (Hyodo et al., 2008). Despite the changes in OC con-
centrations and MARs, the lignin phenol concentrations did not
exhibit large changes in the lowland lake, Oshima-Ohnuma, and
in the mountain lakes, Niseko-Ohnuma and Mikuri-ga-ike. These
results indicate that the relative contributions of terrestrial organic
matter input to the sediments were relatively constant during
these periods in these lakes. In Lake Oshima-Ohnuma, the cause
of the increased OC concentrations and MARs could therefore be
the enhanced inputs of terrestrial organic matter as well as
eutrophication.
The lignin parameters, S/V, C/V, LPVI and (Ad/Al)v of the lake
sediments examined did not show consistent trends during the last
century, except for those in Lake Akan. In Lake Akan, the LPVI
showed an increasing trend from 1930 to 2010, which may indi-
cate the development of broad-leaved forests (e.g., birch) in the
watershed. This may reflect the regulation of timber-harvesting
in 1934, when the area including the watershed became a desig-
nated National Park (Igarashi et al., 2000). The values of (Ad/Al)v
in the analyzed sediments showed no clear trend with depth, indi-
cating that the degree of oxidative degradation in the terrestrial
organic matter flowing into the lakes was unchanged over the last
century.
133
4.3. Comparison of lignin phenol compositions among lakes and their
relation to watershed vegetation
The mean lignin phenol concentrations in the sediments of the
mountain lakes, Rausu and Niseko-Ohnuma (1.6 mg/100 mg-OC),
were higher than those of the lowland lakes and one mountain
lake, Lake Mikuri-ga-ike (0.7 mg/100 mg-OC). This is possibly due
to the greater contribution of aquatic production to the total input
into the eutrophic or mesotrophic lowland lakes. In the case of
Lake Mikuri-ga-ike, it is located at a high altitude of 2407 m, which
is above the tree line. Therefore, the low lignin phenol concentra-
tions may be accounted for by low terrestrial productivity.
The S/V and C/V ratios of the sediments also differed signifi-
cantly among the lakes examined. The S/V ratios in the sediments
(1.5) of Lake Niseko-Ohnuma, whose watershed is covered by bam-
boo grass and birch, are one of the highest values reported so far
for lake sediments. Such high values have been reported for other
lake sediments, such as those from Lake Malawi during the
Younger Dryas (a cooling event at the end of the last glaciation per-
iod) (Castañeda et al., 2009), and from a peat in Indonesia (Tareq
et al., 2004). The C/V ratios of the sediments of Lake Mikuri-ga-
ike showed the highest value (0.7) out of all the lakes examined,
which agrees with the fact that this lake is located above the tree
line and thus the productivity of woody-tissues is limited. The LPVI
of Lake Niseko-Ohnuma sediments showed the highest values
(approximately 800) out of all the lakes examined, reflecting the
dominance of grass species (e.g., bamboo grass) in the watershed
vegetation. Such high values have been observed in Lake Malawi
for the Younger Dryas period (Castañeda et al., 2009). The lowest
values (200) of LPVI in this study are found in Lake Akan, which
is surrounded by both conifer forests and mixed forests. The values
are still much higher compared to those (2–3) in the boreal lake
sediments (Chmiel et al., 2015).
The degree of oxidative degradation of lignin was the highest in
the mountain lake, Mikuri-ga-ike with the value of (Ad/Al)v being
1.0. Such high (Ad/Al)v values were also reported from Lake Wien
in Alaska (Hu et al., 1999). Fresh plant materials generally have
(Ad/Al)v of 0.1–0.3 (Hedges et al., 1988; Opsahl and Benner,
1995). Microbial degradation of plant substrates can increase the
value up to 0.5, and humic substances could have (Ad/Al)v of
0.6–2.0 (Ertel and Hedges, 1984; Ertel et al., 1986). It is known that
the accumulation of soil organic matter including humic sub-
stances becomes greater in low-temperature environments
(Chapin et al., 2002). Therefore, in Lake Mikuri-ga-ike the relative
contribution of soil organic matter to terrestrial OC input might
be larger than that in other lakes. Note that the microbial degrada-
tion of lignins could lead to a decrease in both S/V and C/V ratios,
due to the preferential degradation of syringyl and cinnamyl phe-
nols over vanillyl phenols (Hedges et al., 1988; Opsahl and Benner,
1995).
Teisserenc et al. (2010) found a good correlation between the
S/V ratios of twelve lake sediments and the proportions of angios-
perm vegetation in watersheds of a boreal ecosystem. In the
present study, the S/V ratio had a positive relationship with the
proportions of angiosperm to watershed vegetation, although it
was not significant. Rather, the ratio had a significant positive rela-
tionship with the proportions of grass to watershed vegetation in
our results. The lack of a significant relationship of S/V ratios
may be due to the smaller sample size in this study compared to
the previous study, or due to differences in climate regions (boreal
vs. cool-temperate regions). The LPVI index had a better correlation
with the proportions of angiosperm and grass to watershed vege-
tation, which indicates that lignin phenol compositions can be
used as indicators of past vegetation in watersheds in temperate
forest ecosystems as well.
134 F. Hyodo et al. / Organic Geochemistry 103 (2017) 125–135
5. Conclusions
Our results demonstrated that the increased OC input into the
sediments of lowland lakes over the last century, especially in
the 1960s, was due not only to eutrophication, but also to an
enhanced level of terrestrial OC input. This increasing trend in
OC concentration and MAR in sediments was not clearly observed
in the mountain lakes. However, in two of the three mountain
lakes, the OC concentrations and MARs varied over the last century.
The lignin phenol compositions suggest that the lake watersheds
examined in this study, except for Lake Akan, maintained similar
vegetation types during the last century. Further studies are neces-
sary to examine changes in pollen compositions in Lake Akan sed-
iments to confirm these results. The present study shows that
lignin phenols are helpful for investigating recent as well as past
changes in terrestrial organic matter input into lake environments
and watershed vegetation.
Acknowledgements
We thank Atsuko Tanaka and Takashi Otoda for helping with
sample analyses. We also thank two anonymous reviewers and
the editor for their helpful comments. This study was supported
by grants from the Ministry of the Environment, Japan (the
Environment Research and Technology Development Fund, No.
D-1002), Special Coordination funds for Promoting Sciences and
Technology from the MEXT Japan, and from Research Institute for
Humanity and Nature (project number D-04).
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.orggeochem.
2016.11.001.
Associate Editor—Philip Meyers
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