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Distribution of radioactive cesium in soil and its uptake byherbaceous plants in temperate pastures with differentmanagement after the Fukushima Dai-Ichi Nuclear PowerStation accidentShin-ichiro Oguraa, Takae Suzukia & Masanori Saitoa

a Graduate School of Agricultural Science, Tohoku University, Osaki, 989-6711, JapanPublished online: 26 Nov 2014.

To cite this article: Shin-ichiro Ogura, Takae Suzuki & Masanori Saito (2014) Distribution of radioactive cesium in soil and its uptake byherbaceous plants in temperate pastures with different management after the Fukushima Dai-Ichi Nuclear Power Station accident, SoilScience and Plant Nutrition, 60:6, 790-800, DOI: 10.1080/00380768.2014.954269

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ORIGINAL ARTICLE

Distribution of radioactive cesium in soil and its uptake byherbaceous plants in temperate pastures with different managementafter the Fukushima Dai-Ichi Nuclear Power Station accident

Shin-ichiro OGURA, Takae SUZUKI and Masanori SAITOGraduate School of Agricultural Science, Tohoku University, Osaki, 989-6711, Japan

Abstract

The accident at Fukushima Dai-Ichi Nuclear Power Station (NPS) extensively contaminated the agriculturalland in the Tohoku region of Japan with radioactive cesium [sum of cesium-134 (134Cs) and cesium-137(137Cs)]. We evaluated the status of radioactive cesium (Cs) contamination in soil and plants at the Field ScienceCenter of Tohoku University, northern Miyagi prefecture, 150 km north of the NPS. In seven pastures withdifferent management, we examined: (1) the distribution of radioactive Cs in soil, (2) the concentration ofradioactive Cs in various herbaceous plant species and (3) the change in radioactive Cs content of plants as theymatured. We collected samples of litter, root mat layer (root mat soil and plant roots), and subsurface soil(0–5 cm beneath the root mat) at two to three locations in each pasture in December 2011 and May 2012. Theaboveground parts of herbaceous plants (four grasses, two legumes, and one forb species) were collected fromMay 9 to June 20, 2012, at 14-d intervals, from one to five fixed sampling locations in each pasture. Thedistribution of radioactive Cs in soil differed among pastures to some degree: a large proportion of radioactiveCs was distributed in the root mat layer. Pasture management greatly influenced the radioactive Cs content ofherbaceous plants (p < 0.001); plant species had less influence. Radioactive Cs content was highest(> 3 kBq kg−1 dry weight) on May 9 and significantly decreased with maturity (p < 0.001) for most of thepastures, whereas it remained low (0.04–0.18 kBq kg−1 dry weight) throughout the measurement period in thepasture where composted cattle manure was applied. The soil-to-plant transfer factor was negatively correlatedto pH(H2O) (R2 = 0.783, p < 0.001) and exchangeable K content (R2 = 0.971, p < 0.001) of root mat soils,which suggests that surface application of composted cattle manure reduces plant uptake of radioactive Cs byincreasing the exchangeable K content of the soil. The radioactive Cs content of plants decreased with plantmaturity; its degree of decrease (May 9 to June 6) was smaller in legumes (80.6%) than grasses (55.5%) and theforb (58.6%). Radioactive Cs content decreased with plant maturity; also, the proportion remaining in theaboveground plant was higher in legumes (80.6%) than grasses (55.5%) and the forb (58.6%).

Key words: herbage, pasture management history, plant taxa, radioactive cesium, root mat soil.

INTRODUCTION

The Great East Japan Earthquake on March 11, 2011,followed by the tsunami, triggered the accident at the

Fukushima Dai-Ichi Nuclear Power Station (NPS). Theradioactive fallout was dispersed by wind through sev-eral regions in eastern Japan, and was deposited duringrainfall and snowfall after the accident (Chino et al.2011; MEXT 2011; Katata et al. 2012; Terada et al.2012). The radioactive fallout extensively polluted agri-cultural land, including permanent pastures and mea-dows, with radioactive cesium [the sum of cesium-134(134Cs) and cesium-137 (137Cs)].Extensive investigation of radioactive cesium (Cs) pol-

lution of agricultural land after the Chernobyl disasterand atmospheric bomb testing showed that radioactiveCs fallout deposited on the soil surface remains in the

Correspondence: M. SAITO, Graduate School of AgriculturalScience, Tohoku University, Osaki, 989–6711, Japan. Tel:+81-229-84-7360. Fax: +81-229-84-6490. Email: msaito@bios.tohoku.ac.jpSubmission to Special Section “Contamination of Agro-Environment and Forestry with Radio-nuclides from FukushimaDaiichi Nuclear Power Station”Received 9 December 2013.Accepted for publication 10 August 2014.

Soil Science and Plant Nutrition (2014), 60, 790–800 http://dx.doi.org/10.1080/00380768.2014.954269

© 2014 Japanese Society of Soil Science and Plant Nutrition

Fukushima Special Section Papers

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litter layer or soil surface of non-cultivated land such aspasture (Riise et al. 1990; Varskog et al. 1994).Consequently, the radioactive Cs accumulated in thesurface or litter layer is readily taken up by herbaceousplant roots that are distributed in these layers, resultingin relatively higher soil-to-plant transfer factors (TFs) inpastures than in tilled fields (IAEA 2010).Plant uptake of radioactive Cs is affected by the phy-

sical and chemical factors of soil (Zhu and Smolders2000; Ehlken and Kirchner 2002). For example, uptakeof radioactive Cs by plants was increased by an increasein soil nitrogen (N) content and a decrease in potassium(K) content (Evans and Dekker 1969; Belli et al. 1995).Soil organic matter content also increases radioactive Csuptake by plants (van Bergeijk et al. 1992; Absalom et al.1996; Sanchez et al. 1999; Grytsyuk et al. 2006; Tulinaet al. 2010), due to the lack of sufficient clay minerals tofix radioactive Cs (Rigol et al. 2002). These studiessuggest that pasture management, such as fertilizationand usage (e.g., herbivore grazing, cutting), affects soil-to-plant transfer of radioactive Cs. In addition, uptake ofradioactive Cs is known to differ among plant species(e.g., Broadley and Willey 1997; Willey and Martin1997). The radioactive Cs content of herbage decreasedwith maturity in ryegrass, whereas it increased inlegumes (Paasikallio and Sormunen-Cristian 2002).However, it is unclear whether the findings in Europe

after the Chernobyl accident are relevant to the status inJapan after the NPS accident. In particular, the contam-ination status of pastures has not been documented aswell as that of arable land (Tsuiki and Maeda 2012).The aim of this study was to measure radioactive Cs inthe belowground and aboveground parts of plants fromtemperate pastures under different management history,and to examine whether (1) the radioactive Cs content ofsoils and plants differ with pasture management history,(2) the radioactive Cs content of plants differs amongplant species or plant taxa and (3) the radioactive Cscontent of plants decreases with maturity.

MATERIALS AND METHODS

Study areaThe study was conducted in temperate pastures of theField Science Center (FSC) at the Graduate School ofAgricultural Science, Tohoku University, Japan (38°44’N,140°15’E, 300 m elevation above sea level). The FSC is150 km from the Tokyo Electric Power Company’s NPS(Fig. 1). The soil is classified as a Haplic, non-allophanicAndosol according to Soil Classification for CultivatedSoils in Japan (Classification Committee of CultivatedSoils 1996), or as an Alic Hapludands in Soil Taxonomy(Soil Survey Staff 1999).

Seven pastures with different size and managementhistory were studied (Table 1). Two pastures (5–2 and14–2) were used as grazing paddocks for sheep andcattle, respectively, and the others were used as cuttingmeadows. In spring 2010, chemical fertilizer was appliedto six pastures, and only composted cattle manure wasapplied to the surface of the seventh pasture (9–2). Allpastures were abandoned and received no management(i.e., cultivation, fertilization, animal grazing, cutting,etc.) after the earthquake.

Pasture measurement and collection of herbageTwo to five sampling sites (radius 10 m) were system-atically allocated within each pasture at least 50 m apartfrom each other. The position of each site was recordedby a global positioning system (eTrex®, personalnavigator®, GARMIN, Olathe, USA).Four grasses (Dactylis glomerata L., Phalaris arun-

dinacea L., Lolium perenne L., and Anthoxanthumodoratum L.), two legumes (Trifolium repens L. andT. pratense L.) and one forb weed (Rumex obtusifoliusL.) were chosen as the target plant species (Table 1).These species were dominant in the individual pas-tures. Pasture air radiation dose rate, leaf mass heightand ear height were measured and samples collected on

FSC, Tohoku Univ.

Fukushima Dai-Ichi

Nuclear Power Plant

100 km

Sea of Japan

Pacific Ocean

Figure 1 Locations of the Fukushima Dai-Ichi Nuclear PowerPlant and the Tohoku University Field Science Center (FSC)sampling site.

Radioactive Cs in pastures 791

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Tab

le1

The

area,year

established,

man

agem

entan

dsamplingdesign

foreach

pasture

Pasture

number

Area

(ha)

Estab

lished

year

Usage

Chemical

fertilizer†

N-P

2O

5-K

2O

(kgha

−1y−

1)

Com

posted

cattle

man

ure†

,‡(M

gha

−1)

Targetedplan

tspeciesan

dtaxa

§

Num

berof

location

sforherbag

esampling

5-2

3.0

1986

Grazing

,sheep

106-53

-53

–Antho

xanthu

mod

oratum

L.(G)

4Trifoliu

mrepens

L.(L)

9-1

2.1

2000

Cutting

213-79

-79

4Pha

larisarun

dina

ceaL.(G

)3

Rum

exob

tusifoliu

sL.(F)

9-2

1.3

2010

Cutting

–30

Dactylis

glom

erataL.(G

)3

Trifoliu

mpratense

L.(L)

13-1

2.8

1992

Cutting

121-45

-45

4Dactylis

glom

erataL.(G

)4

Pha

larisarun

dina

ceaL.(G

)Rum

exob

tusifoliu

sL.(F)

14-2

3.6

1991

Grazing

,cattle

106-53

-53

–Dactylis

glom

erataL.(G

)3

Lolium

perenn

eL.(G

)1

Trifoliu

mrepens

L.(L)

4

18-2

4.0

1996

Cutting

91-30-30

–Dactylis

glom

erataL.(G

)5

Rum

exob

tusifoliu

sL.(F)

220.6

2000

Cutting

77-26-26

4Pha

larisarun

dina

ceaL.(G

)2

†So

ilam

endm

entcompo

sition

(nitrogen[N]-ph

osph

ate[P 2O

5]-po

tassium

oxide[K2O])an

dtheam

ount

appliedin

2010

.‡The

man

urecontained80

-145

-528

N-P

2O

5-K

2O

(kgha

−1).

§Plan

ttaxa

wereclassified

asgrasses(G

),legu

mes

(L)or

forb

(F).

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May 9, May 23, June 6 and June 20, 2012; only D.glomerata was collected on June 20. Leaf mass andplant height were measured for each plant species.Ear height was measured for grass species when earemergence was observed. The plants were cut at 3 cmabove the soil surface, air-dried at 70°C for 72 h, andmilled through a 2-mm screen to produce homoge-neous samples. All samples were stored dry until ana-lysis of radioactive Cs concentrations.

Air radiation dose rate of pasturesAir radiation dose rates (μSv h−1) were measured withan environmental radiation monitor (γ survey meterTCS-172B, Hitachi-Aloka Medical, Ltd., Tokyo,Japan) at 1 m above the ground surface at eachlocation. Air radiation was measured on the sameday as pasture measurement, or the following day ifit rained.

Soil collection and analysisSoil samples were collected from two to three locationsin each pasture in December 2011 and May 2012. Afterharvesting the aboveground part of the plants, a quadrat(28 × 28 cm) was set, litter on the soil surface wascollected, and then soil samples were collected. In thisstudy, root mat soil was defined as the surface soil layerthat was tightly bound with plant roots and easily sepa-rated from the subsurface layer. The depth of root matsoil differed between sampling sites, and depended onthe development of a tightly bound root layer.Subsurface soil, 0–5 cm depth immediately beneath ofthe root mat layer, was collected with a core sampler(5 cm height, 100 mL in volume). The root mat layer wasair-dried and separated into roots and soil, which wedesignated “root” and “root mat soil”, respectively.Soil samples (root mat soil and subsurface soil) weresieved to 2 mm. Litter and roots were oven-dried at70°C for 72 h and ground to pass through a 2-mmscreen.Radioactive Cs, pH(H2O), and exchangeable K of root

mat soil and subsurface soil samples were measured. Soilexchangeable K was extracted with a mixture of 0.05 Mammonium acetate and 0.0114 M strontium chloride (soil:extractant = 1:200) (Committee for Soil EnvironmentAnalysis 1997) and measured using an atomic absorptionspectrophotometer (Hitachi Z-2300, Hitachi Co., Japan).

Measurement of radioactive Cs content of samplesThe activity concentrations of 137Cs and 134Cs in driedsoil and plant samples were determined with a gammacounter (WIZARD2® 2480, PerkinElmer, Waltham,

USA) equipped with a sodium iodide (NaI) detector.We used either the measurement protocol provided byPerkin Elmer, Japan, or the protocol of Yin et al. (2012).Both protocols gave identical values. Each sample wasloaded into a 20-mL plastic vial, weighed and measuredfor 600–1800 s. The average radioactive Cs concentra-tion of duplicate samples was expressed as the totalactivity of 134Cs and 137Cs per unit of dry weight (drywt.; Bq kg−1 dry wt.). The standard deviation of eachmeasurement with the gamma counter was less than10%. All measured activities were corrected for radio-active decay to May 9, 2012, for estimates of soil-to-plant transfer. The measured activities of plant sampleswere corrected for each sampling date to compare the Csconcentrations in plants as they matured.

Data analysisRadiocesium concentrations in soil and plant samplesand soil properties for each pasture were summarized asgeometric means. The total amount of radioactive Csfallout (kBq m−2) was evaluated as the sum of theproducts of radioactive Cs contents (Bq kg−1 dry wt.)and the amounts of material (kg dry wt. m−2) for eachcompartment (litter, plant roots, root mat soil and sub-surface soil).Plant species were classified into three taxa (i.e., grasses,

legumes and a forb) before statistical analysis. A generallinear model was used to analyze the factors affecting theradioactive Cs content of the plants. Radioactive Cs con-tents were logarithmically transformed to fit a normaldistribution. The main effects were pasture, samplingdate and plant taxa. The interactions included in thismodel were pasture × sampling date, pasture × planttaxa and sampling date × plant taxa.The change in radioactive Cs content of the above-

ground part of each plant species from each pasturewas evaluated as the plants matured by calculating theproportion of radioactive Cs content on each samplingdate to the content on May 9, 2012. The relativevalues were analyzed by a general linear model forthe main effects of sampling date and plant taxa andthe interaction between them. All the analyses wereperformed with IBM® SPSS® statistics v. 21 (IBMCorporation, New York, USA) (IBM Corporation2012).Pearson’s correlation analysis was performed to test

whether the K content of root mat soil was related tothat of subsurface soil. Regression analysis was per-formed to assess the relationship between soil-to-planttransfer factor of radioactive Cs (TF) and soil charac-teristics for each plant species. TF was defined asfollows:

Radioactive Cs in pastures 793

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where all radioactive Cs contents of litter, root mat soil,roots from the root mat and subsurface soil are included inthe denominator, and the concentration is expressed as aweighted average of these components. This is because theradioactive Cs in any of these components may be a sourceof plant uptake, and because we could neither differentiateliving roots from dead root tissues nor remove all fine soilparticles in the rhizoplane. Hence, the definition of TF inthe present work is a little different from that widely usedin the literature (IAEA 2010).

RESULTS

Distribution of radioactive Cs and chemicalcharacteristics of the pasture soilsThe pattern of dry-matter distribution between the com-partments differed among pastures (Table 2). For exam-ple, in pasture 22, which was used as a cutting meadow,a large proportion of dry matter was in the root matlayer because of the well-developed root mat. The thick-ness of the root mat in pasture 22 was 4–5 cm, whereasin pastures 9–1, 9–2 and 13–1 it was only about 1 cmbecause of poorly developed root mats. Subsurface soilaccounted for the highest proportion of belowgrounddry material (19.1–29.7 kg m−2), whereas the proportionin litter was the lowest (0.05–0.37 kg m−2).Radioactive Cs contents tended to be higher in

the litter (2.13–11.87 kBq kg−1 dry wt.) and roots(4.00–9.66 kBq kg−1 dry wt.) than in root mat soil(0.54–6.68 kBq kg−1 dry wt.) and subsurface soil(0.01–0.50 kBq kg−1 dry wt.) (Table 2). The distributionof radioactive Cs differed among pastures (Fig. 2). Forexample, 35.9–43.3% of radioactive Cs was in the sub-surface soil from pastures 5–2, 9–1, and 9–2, whereas itwas 1.1–7.1% in pastures 14–2 and 22. The relativedistribution of radioactive Cs was low in the litter(0.3–5.6%). The soil fractions (i.e., root mat soil andsubsurface soil) contained 18.4–84.5% of radioactiveCs per area, in which the root mat soil tended to accu-mulate more radioactive Cs (17.3–59.3%) than the sub-surface soil (1.1–43.3%).The total average radioactive Cs fallout was

31.3 kBq kg−1, with a range of 26.8–42.2 kBq m−2

(Table 2). These values are comparable with those pre-dicted from the radioactive Cs distribution map producedwith aerial monitoring data (MEXT 2011; JAEA 2013).

The soil pH(H2O) was 4.6–6.5 and the exchangeableK content was 0.09–4.27 cmol kg−1 dry wt. (Table 2).Both values were high in pasture 9–2 where compostedcattle manure was applied. The exchangeable K contentsin root mat soils were significantly correlated with thosein subsurface soils (r = 0.987, p < 0.001).

Maturity of the target plant speciesLeaf mass and plant height increased in all plant speciesover the sampling period in 2012 (Fig. 3). Ear emergencewas observed from May 23 for A. odoratum and fromJune 6 for D. glomerata and P. arundinacea. Bloomingwas observed from June 6 for R. obtusifolius and T.repens.

Air radiation dose rate of the pasturesAir radiation dose rate was almost constant throughoutthe sampling period. Relatively high values wererecorded in pastures 13–1, 14–2 and 18–2 (0.158–0.178 μSv h−1); the lowest value was in pasture 5–2(0.140 μSv h−1).

Radioactive Cs content in herbageRadioactive Cs content in collected plants varied amongthe pastures (Fig. 4). The effects of pasture (p < 0.01) andsampling date (p < 0.001) were significant, but Cs con-tents did not differ significantly among plant taxa(p > 0.10). There were no significant interactions ofpasture × sampling date, pasture × plant taxa and sam-pling date × plant taxa (Table 3).High radioactive Cs content was recorded in pastures

14–2 (2.85–3.98 kBq kg−1) and 22 (4.27 kBq kg−1) onMay 9 (Fig. 4). Radioactive Cs contents were also highon May 9 in P. arundinacea in pasture 9–1(3.51 Bq kg−1). In contrast, radioactive Cs content wasvery low in plants collected from pasture 9–2 (0.04–0.18 kBq kg−1) throughout the sampling period.The radioactive Cs content decreased with maturity

in all sampled plants (Fig. 4). The tendency was clearlyobserved in pastures 9–1, 14–2 and 22, wherethe radioactive Cs content of herbage was high onMay 9.The relative values of the radioactive Cs content sig-

nificantly decreased with maturity of plants (p < 0.001),

TF ¼ radioactive Cs content of the aboveground part of the plant ðBqkg�1dry wt:Þ=

radioactive Cs content of the soil ðBqkg�1 dry wt:Þ (1)

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but the extent differed among plant taxa (p = 0.05)(Fig. 5). There was no significant interaction betweenmaturity and plant taxa. Relative to the radiation inthe grasses and the forb (R. obtusifolius) on May 9, theradiation by May 23 had decreased to 69.7–72.9% andby June 6 to 55.5–58.6%. In contrast, radiation inlegumes on June 6 was still 80.6% of that on May 9.

Relationship between TF and soil characteristicsThe soil-to-plant TF varied among pastures, but wasalmost constant among plant species within the samepasture (Table S1). The lowest TF value (0.11) wascalculated for pasture 9–2, where composted cattle man-ure was applied. The highest value (6.23) was calculatedfor pasture 22, which was used as a cutting meadow.The variation of TF was well explained by both pH(H2O) (R2 = 0.783, p < 0.001) and exchangeable Kcontent (R2 = 0.971, p < 0.001) in root mat soil (Fig. 6).

DISCUSSION

The accident at NPS released a substantial amount ofradioactive cesium, thereby contaminating soil over awide area. The survey conducted by the Ministry ofEducation, Culture, Sports, Science, and Technology(MEXT), Japan, estimated that the contamination levelsbroadly ranged from less than 10 kBq m−2 to more than3000 kBq m−2 (MEXT 2011). For our study area, theyestimated the contamination level to be 10–30 kBq m−2

for both radionuclides of 134Cs and 137Cs (JAEA 2013),which is comparable to our measurements (29.4–42.2 kBq m−2).At all locations in our study area, the root mat layer

(plant roots and root mat soil) accumulated a large pro-portion of the deposited radioactive Cs. In the soilT

able

2The

drymatterdistribu

tion

,meanpH

(H2O),exchan

geab

lepo

tassium

(K)concentrationan

dradioa

ctivecesium

(Cs)

fallo

utan

dcontentof

each

compa

rtmentin

the

pastures

Dry

matterdistribu

tion

(kgm

−2)

pH(H

2O)

Excha

ngeableK

concentration

(cmol

kg−1drywt)

Total

radioa

ctive

Csfallo

ut†

(kBqm

−2)

Rad

ioactive

Cscontent†

(kBqkg

−1drywt)

Pasture

number

Litter

Roo

tsRoo

tmat

soil

Subsurface

soil

Roo

tmat

soil

Subsurface

soil

Roo

tmat

soil

Subsurface

soil

Litter

Roo

tsRoo

tmat

soil

Subsurface

soil

5-2

0.05

1.69

2.07

18.95

5.1

4.9

1.39

0.57

32.4

2.12

5.15

4.24

0.46

9-1

0.09

0.72

1.14

19.03

5.1

5.1

0.93

0.24

29.7

9.38

9.66

6.68

0.43

9-2

0.37

0.71

1.92

27.50

6.5

6.2

4.27

2.62

42.2

2.55

6.06

6.85

0.50

13-1

0.14

0.98

1.31

20.79

4.7

4.6

0.79

0.24

26.8

9.58

9.42

4.91

0.25

14-2

0.11

2.29

4.68

25.94

4.9

5.0

0.41

0.09

28.7

11.87

5.74

1.90

0.06

18-2

0.19

0.45

3.33

26.73

4.8

4.9

1.06

0.27

33.2

10.01

8.14

4.47

0.18

220.07

5.72

7.16

29.56

4.7

4.7

0.24

0.13

29.4

4.44

4.00

0.54

0.01

†Rad

ioactivities

werecorrectedforradioa

ctivedecayto

May

9,20

12.

Allvalues

aregeom

etricmeans.

TotalradioactiveCs fallout(kBq m–2)

32.4

29.7

42.2

26.8

28.7

33.2

29.4

PastureNo.

5–2

9–1

9–2

13–1

14–2

18–2

22

0 0.2 0.4 0.6 0.8 1

Litter Plant roots Rootmat soil Subsurface soil

Figure 2 Relative distributions of radioactive cesium (Cs) inlitter, plant roots, root mat soil and subsurface soil in theseven sampled pastures. Radioactivities were corrected forradioactive decay to May 9, 2012.

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fractions, a higher proportion of radioactive Cs was in theroot mat soil than in the subsurface soil (Fig. 2). Studies innortheastern Japan after the Fukushima accident showedhigh radioactive Cs contents in the top layer of untilled

arable soils (Koarashi et al. 2012; Yamaguchi et al. 2012;Shiozawa 2013). Many studies conducted after theChernobyl accident indicated that vertical migration ofradioactive Cs was very slow, and most radioactive Cs

0

20

40

60

80

100

120

140

Grasses Broad leaves

Sampling date

June 20June 6May 23May 9 June 20June 6May 23May 9

L. perenneA. odoratum ,P. arundinacea,D. glomerata ,

R. obtusifolius ,

T. pratense , T. repens.

Grasses:

Legumes:

Forb:

Pla

nt h

eigh

t an

d ea

r he

ight

(cm

)

Figure 3 Plant height (solid line and symbols) and ear height (dashed line and open symbols) of the seven herbaceous plants (Dactylisglomerata L., Phalaris arundinacea L., Anthoxanthum odoratum L., Lolium perenne L., Trifolium pratense L., Trifolium repens L.and Rumex obtusifolius L.). Vertical bars represent standard deviation (n = 4 for D. glomerata, n = 3 for P. arundinacea and R.obtusifolius, and n = 2 for A. odoratum and T. repens).

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Figure 4 Geometric mean of radioactive cesium (Cs) content of the aboveground part of the seven herbaceous plants (Dactylisglomerata L., Phalaris arundinacea L., Anthoxanthum odoratum L., Lolium perenne L., Trifolium pratense L., Trifolium repens L.and Rumex obtusifolius L.) in each pasture. The number in each graph is the pasture name. No vertical bars are shown because thegeometrical standard deviation is small.

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was present in the upper soil layers (e.g., Almgren andIsaksson 2006). Furthermore, biorecycling of radioactiveCs found in forest ecosystems (Kruyts and Delvaux 2002)might also occur in pasture ecosystems. Radioactive Csdeposited onto a pasture surface may be taken up by rootsdeveloped in the root mat layer; then the radioactive Csabsorbed by plants may fall onto the pasture surface layeras dead tissues, unless the aboveground part of the plantis removed by harvesting or grazing.The radioactive Cs content of the aboveground part

of plants differed between pastures, despite the similar-ity in total radioactive Cs fallout. Many studies haveshown that plant uptake of radioactive Cs is higher

from soil rich in organic matter (van Bergeijk et al.1992; Absalom et al. 1996; Sanchez et al. 1999;Grytsyuk et al. 2006); this is because organic matterdecreases the affinity of clay for Cs, which increases Csmobility (Dumat et al. 1997; Sanchez et al. 1999;Staunton et al. 2002). The soil used in our study wasan Andosol, which is rich in organic matter (Nanzyo2002). However, very low radioactive Cs content inherbaceous plants was observed in pasture 9–2, inwhich composted cattle manure was applied to thesurface (Fig. 4). Soil-to-plant TF was negatively relatedto pH(H2O) and exchangeable K content in soil in allthe pastures (Fig. 6). It is well known that plant uptakeof radioactive Cs is suppressed in soil with a highexchangeable K content; in fact, the ability of K tosuppress radioactive Cs uptake is larger than the abilityof organic matter to promote it (Shaw and Bell 1991;Belli et al. 1995; Sanchez et al. 1999; Rigol et al. 2002).This is because K+ can compete with Cs for absorptionby plant roots (Robison and Stone 1992; Roca andVallejo 1995; Zhu and Smolders 2000; Ciuffo et al.2003). The high soil exchangeable K content in pasture9–2 indicates that surface application of compostedcattle manure greatly reduced plant radioactive Csuptake by increasing exchangeable K content in thesoil. It remains uncertain whether pH(H2O) is directlyrelated to radioactive Cs uptake by plants.In our study, radioactive Cs content significantly

decreased with maturity of the aboveground part ofplants; in addition, the extent of decrease was less inlegumes than in the grasses and the forb R. obtusifolius.Paasikallio and Sormunen-Cristian (2002) reported thatradioactive Cs concentrations decreased in ryegrass andincreased in clover and alfalfa with time during thegrowth period. They suggested that more ammonium(NH4

+) was available in legumes at the later stage of

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Figure 5 Relative radioactive cesium (Cs) content of the above-ground part of grasses (Dactylis glomerata L., Phalaris arundi-nacea L., Anthoxanthum odoratum L. and Lolium perenne L.;n = 9), legumes (Trifolium pratense L. and Trifolium repens L.;n = 3) and the forb (Rumex obtusifolius L.; n = 3) with maturity.The values are presented as the percentage of radioactive Cscontent on each sampling date relative to that on May 9.

Table 3 Results for the general linear model used to analyze the factors affecting the radioactive cesium (Cs) content of theaboveground part of plants†

Factors Degree of freedom Mean square F value Probability

Intercept Model 1 1351.02 256.67 0.000Error 6 5.26

Pasture Model 6 6.40 20.58 0.006Error 4 0.31

Sampling date Model 3 0.79 11.69 0.000Error 24 0.07

Plant taxa Model 2 0.28 0.89 0.481Error 4 0.31

Pasture × sampling date Model 15 0.07 0.99 0.511Error 14 0.07

Pasture × plant taxa Model 4 0.31 4.61 0.014Error 14 0.07

Sampling date × plant taxa Model 4 0.07 1.04 0.422Error 14 0.07

† Radioactive Cs contents were logarithmically transformed to fit normal distribution before the statistical analysis.

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growth due to symbiotic N fixation, and that the NH4+

availability may result in the relatively higher radioactiveCs uptake in legumes than grasses and other forbs. It iswell known that NH4

+ in soil increases the radioactiveCs content of plants (Evans and Dekker 1969; Shaw andBell 1991; Belli et al. 1995; Sanchez et al. 1999; Rigolet al. 2002), because NH4

+ effectively mobilizes Cs insoils (Jackson et al. 1965; Sanchez et al. 1999).However, it is uncertain whether N fixation in legumesis related to uptake of radioactive Cs. To clarify thetemporal change in concentration of radioactive Cs inplants, it may be necessary to clarify the change in con-centration of K and other nutrients.In conclusion, pasture management history and plant

maturity were major factors affecting radioactive Cscontent in the aboveground part of plants. Surface appli-cation of composted cattle manure reduced radioactiveCs uptake by plants by increasing the exchangeable Kcontent of the soil; however, increased exchangeable Kcontent may reduce herbage quality by degrading themineral balance (Kayser and Isselstein 2005). Plantmaturity reduced the Cs content of plants, but late har-vesting can decrease the nutritive value and digestibilityof herbage. However, both application of compostedcattle manure and late harvesting would be effectivemanagement strategies to produce forage with radioac-tive Cs contents that are below the contamination limitfor animal feed (MAFF 2013).

SUPPLEMENTARY MATERIAL

The supplementary material for this article is availableonline from: http://dx.doi.org/10.1080/00380768.2014.954269.

ACKNOWLEDGMENTS

We thank the staff and students at the Laboratory ofLand Ecology and the Laboratory of EnvironmentalCrop Science, FSC, Tohoku University, for useful adviceand support with field sampling and measurements. Thepresent work was in part supported by TohokuUniversity and JSPS KAKENHI Grant No. 26511003.

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