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Journal of Environmental Radioactivity 141 (2015) 38e43

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Journal of Environmental Radioactivity

journal homepage: www.elsevier .com/locate / jenvrad

137Cs concentrations in foliose lichens within Tsukuba-city as areflection of radioactive fallout from the Fukushima Dai-ichi NuclearPower Plant accident

Yoshihito Ohmura a, *, Kimiyo Matsukura b, Jun-ichi P. Abe b, Kentaro Hosaka a,Masanori Tamaoki c, Terumi Dohi d, Makoto Kakishima e, f, Mark R.D. Seaward g

a Department of Botany, National Museum of Nature and Science, 4-1-1 Amakubo, Tsukuba, Ibaraki 305-0005, Japanb Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Ten-noudai, Tsukuba, Ibaraki 305-8572, Japanc Center for Environmental Biology and Ecosystem Studies, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japand Headquarters of Fukushima, Japan Atomic Energy Agency, 6-6 Sakae-machi, Fukushima 960-8031, Japane Faculty of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Ten-noudai, Tsukuba, Ibaraki 305-8572, Japanf Engineering Research Center of Chinese Ministry of Education for Edible and Medicinal Fungi, Jilin Agricultural University, Changchun, Jilin Province130118, Chinag Department of Archaeological, Geographical & Environmental Sciences, University of Bradford, Bradford BD7 1DP, UK

a r t i c l e i n f o

Article history:Received 1 August 2014Received in revised form2 November 2014Accepted 19 November 2014Available online

Keywords:BiomonitoringRadionuclide accumulationJapanDirinaria applanataPhyscia orientalis

* Corresponding author.E-mail address: ohmura-y@kahaku.go.jp (Y. Ohmu

http://dx.doi.org/10.1016/j.jenvrad.2014.11.0140265-931X/© 2014 Elsevier Ltd. All rights reserved.

a b s t r a c t

137Cs concentrations in ten species of foliose lichens collected within Tsukuba-city in August 2013 rangedfrom 1.7 to 35 kBq/kg. The relationships between 137Cs in two dominant species, Dirinaria applanata andPhyscia orientalis, and the air dose rate (mSv/h) at the sampling sites were investigated. 137Cs in P. ori-entalis measured about 1 year after the Fukushima nuclear accident was correlated (r2 ¼ 0.80) moreclosely with the air dose rate than those measured after about 2 years (r2 ¼ 0.65), possibly demonstratingits continued value as a biomonitor to reflect ambient fall-out levels. In contrast, those of Dirinariaapplanata were not correlated with the air dose rate in either year.

© 2014 Elsevier Ltd. All rights reserved.

1. Introduction

A substantial quantity of radionuclides was released into theatmosphere as a result of the Fukushima Dai-ichi Nuclear PowerPlant (FNPP) accident on 11 March 2011. Lichens are known to be amost effective tool to monitor aerial radionuclide depositions bothspatially and temporally, as demonstrated by investigations un-dertaken as a result of the Chernobyl NPP accident in April 1986(Seaward, 2002), when, for example, Cladonia stellaris (Opiz) Pou-zar& V�ezda, Hypogymnia physodes (L.) Nyl., Pseudevernia furfuracea(L.) Zopf, and Umbilicaria spp. were used as the biomonitors (e.g.Eckl et al., 1986; Seaward et al., 1988; Heinrich et al., 1989a, 1989b;

ra).

Puhakainen et al., 2007). Since these particular species do not occuraround the FNPP, except in limited areas of high mountains, it isimpossible to make direct comparisons with data derived fromEuropean or North American biomonitoring programmes; howev-er, there are appropriate local lichens to establish suitable long-term monitoring of aerial radionuclides depositions. Unfortu-nately, there are no baseline data on radionuclide levels in lichensprior to the FNPP accident for the region affected, or likely to havebeen affected; furthermore, from a geographic point of view, suchlevels have only been reported from Tsukuba-city which is locatedabout 170 km south of the FNPP (Ohmura et al., 2013).

The primary purpose of this study was to investigate the rela-tionship between 137Cs concentrations in foliose lichens collectedwithin Tsukuba-city on August 2013 and the air dose rate (mSv/h) attheir sampling sites measured about 1 and 2 years after the FNPPaccident.

Y. Ohmura et al. / Journal of Environmental Radioactivity 141 (2015) 38e43 39

2. Materials and methods

2.1. Study area

Tsukuba-city, covering an area of 284.1 km2, is located about170 km south of the FNPP. On 15 March 2011, four days after theaccident, the maximum air dose rate in the city was 2.5 mSv/h. Twoand half years later, the air dose rate was less than 0.17 mSv/hthroughout the city (Tsukuba, 2013).

Approximately 1 year after the FNPP accident the air dose rates(measured during 26 December 2011 to 10 February 2012) werelower (<0.15 mSv/h) in northern parts and higher (0.27e0.30 mSv/h)

Fig. 1. Sampling sites in Tsukuba-city. F

in southern parts of the city, but about 2 years after the accident(measured during 8 December 2012 to 18 January 2013) these airdose rates were significantly reduced to <0.10 mSv/h in northernparts and 0.20e0.23 mSv/h in southern parts.

Forty-two sites located in 25 public parks at elevations of8e31 mwere investigated throughout Tsukuba-city (Fig. 1, Table 1)during 6e8 August 2013.

2.2. Lichen samples

Fifty samples of foliose lichens were collected from tree trunks(e.g. Pinus thunbergii Parl., Prunus � yedoensis Matsum., Quercus

or details of localities see Table 1.

Table 1Summary of site and sample characteristics. Sampling sites 1e8 were investigated on 6 August 2013, sites 9e27 on 7 August 2013, and sites 28e42 on 8 August 2013.*Corresponding to the numbers in Fig. 1. ** Data cited from Tsukuba (2013). *** CC ¼ Candelaria concolor, DA ¼ Dirinaria applanata, FC ¼ Flavoparmelia caperata, HC ¼Hyperphyscia crocata, PA ¼ Parmotrema austrosinense, PB ¼ Punctelia borreri, PC ¼ Parmotrema clavuliferum, PO ¼ Physcia orientalis, PS ¼ Phaeophyscia spinellosa, PT ¼ Par-motrema tinctorum.

Air dose rate (mSv/h)**

Samplingsite*

Locality inTsukuba-city

Elevation(m)

26 Dec 2011to 10 Feb 2012

8 Dec 2012to 18 Jan 2013

Lichenspecies***

Substrate [growth positionof lichen: facing direction,height (cm)]

Specimenvoucher

Dryweight(g)

137Cs concentration(Bq/kg, dry weight)

1 Kukizaki-Undo Park 15 0.219 0.183 DA Cinnamomum camphora[N to W, 40e170]

YO9826 12.57 13100 ± 120

2 23 0.219 0.183 PO C. camphora[S to E, 40e130]

YO9827 11.77 20000 ± 150

3 Hanare Park 25 0.188 0.147 DA Zelkova serrata[N to W, 50e150]

YO9828 10.68 7700 ± 90

PO Z. serrata[N to W, 50e150]

YO9829 6.34 26400 ± 210

PC Z. serrata[N to W, 50e150]

YO9830 4.78 8500 ± 150

4 24 0.188 0.147 PS Horizontal surface ofconcrete on a pavement

YO9831 15.99 25100 ± 140

5 Yatabe BaseballGround

10 0.146 0.115 PO Z. serrata[N to E, 30e130]

YO9832 6.88 20400 ± 190

6 Koyadai Park 23 0.206 0.15 DA Z. serrata[N to W, 90e150]

YO9833 8.09 16900 ± 160

DA Z. serrata[N to W, 90e150]

YO9834 8.66 10100 ± 120

7 Kukizaki Family Park 19 0.231 0.2 PO Z. serrata[N to E, 30e160]

YO9835 9.26 30200 ± 210

8 Kokaigawa Sports Park 15 0.127 0.112 DA Wisteria floribunda[N to E, 50e150]

YO9836 9.00 9300 ± 110

9 Matsumi Park 29 0.114 0.109 PT Pinus densiflora[N, 60e100]

YO9837 7.37 4400 ± 90

10 Katsuragi Park 25 0.118 0.099 PS Horizontal surface ofconcrete on a pavement

YO9838 21.95 6200 ± 60

11 24 0.118 0.099 PO Quercus myrsinaefolia[NW to E, 30e70]

YO9839 8.84 5000 ± 80

12 23 0.118 0.099 DA Z. serrata[NW, 50e130]

YO9840 10.04 9400 ± 110

HC Z. serrata[NE, 50e200]

YO9841 8.79 9100 ± 110

13 Tsukuba EXPO Center 25 0.118 0.109 PO Z. serrata[NE, 150]

YO9842 12.35 8700 ± 100

14 26 0.118 0.109 CC Z. serrata[E, 150]

YO9843 10.93 9900 ± 110

PO Z. serrata[N, 150]

YO9844 11.61 9600 ± 100

15 25 0.118 0.109 DA Z. serrata[N, 150]

YO9845 11.68 7400 ± 90

16 Namiki Park 22 0.172 0.149 DA Z. serrata[NW, 150]

YO9846 12.30 11600 ± 110

17 22 0.172 0.149 PO Z. serrata[W to N to E, 100e170]

YO9847 11.74 15300 ± 130

18 21 0.172 0.149 PO Z. serrata[NE, 100e150]

YO9848 8.04 14100 ± 140

19 Umezono Park 26 0.205 0.168 PO Prunus mume[NE, 100e150]

YO9849 14.69 31700 ± 170

20 25 0.205 0.168 HC Q. myrsinaefolia[S to W to N, 20e100]

YO9850 23.67 8900 ± 70

21 Saginuma-Jido Park 27 0.198 0.159 PO Z. serrata[NE, 50e100]

YO9851 12.21 35400 ± 190

22 Higashimukai-Jido Park 25 0.16 0.115 DA Liquidambar styraciflua[NE, 60e150]

YO9852 12.55 20400 ± 150

23 Teshirogi Park 25 0.16 0.115 DA Z. serrata[E, 130e180]

YO9853 11.86 18300 ± 150

24 Gojyutsuka-Jido Park 26 0.128 0.111 DA Z. serrata[SE, 50e100]

YO9854 11.00 11400 ± 120

25 Ninomiya Park 27 0.163 0.141 HC Z. serrata[NW, 50e180]

YO9855 12.70 10500 ± 100

26 27 0.163 0.141 PO Z. serrata[W, 50e120]

YO9856 9.99 18100 ± 150

27 Takezono Park 25 0.118 0.109 DA Z. serrata[NW to E, 30e70]

YO9857 15.57 10400 ± 100

28 Nakane-Fureai Park 8 0.114 0.109 HC Q. myrsinaefolia[all directions, 30e150]

YO9858 19.21 2800 ± 50

Y. Ohmura et al. / Journal of Environmental Radioactivity 141 (2015) 38e4340

Table 1 (continued )

Air dose rate (mSv/h)**

Samplingsite*

Locality inTsukuba-city

Elevation(m)

26 Dec 2011to 10 Feb 2012

8 Dec 2012to 18 Jan 2013

Lichenspecies***

Substrate [growth positionof lichen: facing direction,height (cm)]

Specimenvoucher

Dryweight(g)

137Cs concentration(Bq/kg, dry weight)

29 10 0.114 0.109 PA Prunus � yedoensis[NE, 20e90]

YO9859 15.60 9400 ± 90

DA P. � yedoensis[NW to NE, 20e180]

YO9860 5.08 14400 ± 200

30 Hanabatake Park 30 0.112 0.096 DA Z. serrata[SW, 50e110]

YO9861 11.45 8300 ± 100

31 Oike Park 22 0.117 0.103 DA Z. serrata[N to NE, 30e120]

YO9862 11.12 15700 ± 140

32 23 0.117 0.103 FC P. � yedoensis[NE, 130e150]

YO9863 8.97 9300 ± 120

PA P. � yedoensis[NE, 100e170]

YO9864 5.46 9500 ± 160

DA P. � yedoensis[NE, 150]

YO9865 20.12 7400 ± 80

33 23 0.117 0.103 PC P. � yedoensis[NE, 160e190]

YO9866 7.69 8200 ± 120

34 23 0.117 0.103 PT P. � yedoensis[N, 100e120]

YO9867 8.45 3000 ± 80

35 Tsukuba-Hokubu Park 31 0.101 0.096 DA Z. serrata[NE, 10e70]

YO9868 10.38 4300 ± 80

36 Okubo Park 29 0.103 0.093 PB Z. serrata[NE, 160e190]

YO9869 5.84 7300 ± 130

37 29 0.103 0.093 PO Z. serrata[N to NE, 50e120]

YO9870 10.93 5500 ± 80

38 Daiyama Park 24 0.111 0.095 PO Z. serrata[E, 30e90]

YO9871 8.91 8800 ± 110

39 24 0.111 0.095 DA Z. serrata[NE, 40e140]

YO9872 11.77 8600 ± 100

40 Kawaguchi Park 24 0.103 0.093 PT P. mume var. purpurea[W, 40e80]

YO9873 6.58 1700 ± 60

41 23 0.103 0.093 PO P. mume var. purpurea[W to N to E, 100e180]

YO9874 14.11 5500 ± 70

42 Hachinosu Park 25 0.127 0.107 PO Z. serrata[E, 10e60]

YO9875 8.70 10600 ± 120

Y. Ohmura et al. / Journal of Environmental Radioactivity 141 (2015) 38e43 41

myrsinaefolia Blume and Zelkova serrata (Thunb.) Makino) at aheight of between 0.1 and 2.0 m from the ground or from stonepavements (Table 1).

Lichen identification undertaken in the field with the aid of ahand-lens (D36, Zeiss) was confirmed in the laboratory bymeans ofa dissecting stereomicroscope (SZX16, Olympus) and chemical ex-amination by thin layer chromatography using the “solvent B sys-tem” (Culberson and Kristinsson, 1970; Culberson and Johnson,1982).

All voucher specimens are housed in the National Museum ofNature and Science, Tsukuba, Japan (herbarium code: TNS).Collection data are summarized in Table 1.

2.3. Radionuclide measurement

The lichen samples were dried at 40 �C for 48 h and ground intoa powder (4.78e23.67 g dry weight, Table 1) by means of a mill(LM-PLUS, Osaka Chemical Co.). Each sample was placed in a cy-lindrical 100 mL plastic bottle (6.5 cm high, 5 cm diameter; U-8, ASONE) for radionuclide measurement and the 137Cs concentrations(Bq/kg, dry weight) determined at the Center for Research in Iso-topes and Environmental Dynamics, University of Tsukuba, using alow background gamma-ray detector (IGC25190, Princeton GammaTech; MSA7800, SEIKO EG&G) for 5000 s. The unique energy of theg-ray (661 KeV for 137Cs) allowed identification and quantificationof the radionuclides. Air dose rate measurements (mSv/h) at a

height of 0.5 m from the ground for the sampling sites were ob-tained from Tsukuba (2013).

3. Results

Ten species of foliose lichens were collected from the study area,each in sufficient quantity for radiocaesium measurement. Themost abundant species was Dirinaria applanata (F�ee) D.D. Awasthi(collected from 17 of 42 sampling sites), followed by Physcia ori-entalis Kashiw. (16), Hyperphyscia crocata Kashiw. (4), Parmotrematinctorum (Despr. ex Nyl.) Hale (3), P. austrosinense (Zahlbr.) Hale(2), P. clavuliferum (R€as€anen) Streimann (2), Phaeophyscia spinellosaKashiw. (2), Candelaria concolor (Dicks.) Arnold (1), Flavoparmeliacaperata (L.) Hale (1), and Punctelia borreri (Sm.) Krog (1) (Table 1).

137Cs concentrations in the ten species (50 samples) shown inTable 1 ranged from 1700 ± 60 to 35400 ± 190 Bq/kg, the lowestvalue being detected in Parmotrema tinctorum at a lower air doserate location (site 40) and the highest in Physcia orientalis at ahigher air dose rate location (site 21).

The relationships between the 137Cs concentrations in the twodominant species, Dirinaria applanata and Physcia orientalis onZelkova serrata, and the air dose rate measured after about 1 and 2years after the FNPP accident at the sampling places were investi-gated; the coefficients (r2) for Physcia orientaliswere determined as0.80 and 0.65 after about 1 and 2 years after the FNPP accidentrespectively (Fig. 2). In contrast, no statistically significant

Fig. 2. The relationship between the 137Cs concentration in Physcia orientalis on Zelkova serrata and air dose rate at the sampling sites: (a) air dose rate measured during 26 Dec 2011to 10 Feb 2012, (b) air dose rate measured during 8 Dec 2012 to 18 Jan 2013.

Y. Ohmura et al. / Journal of Environmental Radioactivity 141 (2015) 38e4342

correlations were detected for Dirinaria applanata in either year(r2 ¼ 0.17 and 0.08 respectively) (Fig. 3).

4. Discussion

Radionuclide accumulation in lichens depends on species, sub-strata and habitats, as well as spatial and temporal factors(Seaward, 2002). Therefore, such factors should be considered inestablishing a protocol for the collection of lichens and measure-ment of their radionuclide uptake in spatial and temporal bio-monitoring programmes. 137Cs concentrations in lichens at thesame location, and therefore subjected to the same air dose rate,varied significantly according to the species and the habitat; forexample, on the trunks of Zelkova serrata at Hanare Park (site 3),137Cs levels were 7700 ± 90 Bq/kg in Dirinaria applanata,8500 ± 150 Bq/kg in Parmotrema clavuliferum and 26400 ± 210 Bq/kg in Physcia orientalis; on the trunks of Zelkova serrata at NinomiyaPark (sites 25, 26), levels were 10500 ± 100 Bq/kg in Hyperphysciacrocata and 18100 ± 150 Bq/kg in Physcia orientalis; and on thetrunks of Cinnamomum camphora at Kukizaki-Undo Park (sites 1, 2),levels were 13100 ± 120 Bq/kg in Dirinaria applanata and

Fig. 3. The relationship between the 137Cs concentration in Dirinaria applanata on Zelkova s2011 to 10 Feb 2012, (b) air dose rate measured during 8 Dec 2012 to 18 Jan 2013.

20000 ± 150 Bq/kg in Physcia orientalis. Even at the same site, thesame lichen species with similar orientation and at same height onthe respective trunks of the same tree species, the 137Cs level var-ied; in the case of Dirinaria applanata on Zelkova serrata at KoyadaiPark (site 6), for example, the values were 10100 ± 120 and16900 ± 160 Bq/kg. Furthermore, for the same species but ondifferent substrata, the 137Cs level varied significantly, as, forexample, Dirinaria applanata at Oike Park (sites 31, 32), where itwas 7400 ± 80 Bq/kg on Prunus � yedoensis and 15700 ± 140 Bq/kgon Zelkova serrata.

In spite of such variations among the species examined, 137Cslevels in Physcia orientalis showed a strong positive correlationwiththe air dose rate, while the relationship for Dirinaria applanatawasunsupported statistically. This difference between the species wasunexpected since they both belong to the same family, Physciaceae,and their gross morphologies are very similar, having a foliosethallus, with soralia, adnate to the substrate; their ecological nichesare also similar, and they sometimes grow together. However, theanatomical structure of the thallus and the secondary substances inthese species are remarkably different: D. applanata has a proso-plectenchymatous lower cortex and contains divaricatic acid as the

errata and air dose rate at the sampling sites: (a) air dose rate measured during 26 Dec

Y. Ohmura et al. / Journal of Environmental Radioactivity 141 (2015) 38e43 43

major substance in the medulla, while Physcia orientalis has aparaplectenchymatous lower cortex and contains no divaricaticacid in the medulla (Kashiwadani, 1975, 1985). It is still uncertainwhether these differences are related to the nature of radionuclideaccumulation in their thalli. The differences in radionuclide uptakeand biological half-life have been reported in various species (e.g.Hanson, 1971; Puhakainen et al., 2007; Iurian et al., 2011) whichmay be influenced by structural differences in lichens and variousenvironmental factors (Hanson, 1971; Cevik and Celik, 2009).Clearly, all these factors need to be investigated in terms of thebiomonitoring value of lichens used to evaluate the nature andextent of the fallout around Fukushima.

137Cs levels in P. orientalis showed a higher correlation with theair dose rate measured about 1 year after the FNPP accident(r2 ¼ 0.80) than those measured about 2 years after the accident(r2 ¼ 0.65), suggesting that this species still reflects the distributionof radioactive contamination caused by the fallout. The air doserates in the radioactive contaminated areas in/around Fukushimahave been dramatically reduced due to the physical half-life of 134Cs(about 2 years) and to decontamination activities by national andlocal governments (Ministry of the Environment, 2014); clearly,137Cs, with a physical half-life of about 30 years, will be environ-mentally influential over a much longer period. Furthermore, thespeed of the reduction in air dose rate varies according to theenvironment, being, for example, fast in urban areas and slow inforested areas (Saito, 2013, 2014). Therefore, it has proved difficultto obtain a detailed pollution map for the local area, there beingonly a poorly conducted radioactive contamination survey in 2011and subsequent years. Undoubtedly, earlier measurements of 137Cslevels in the locally dominant P. orientalis would have beeninvaluable for monitoring the temporal and spatial impact ofradioactive fallout in and around Fukushima.

Acknowledgments

We are most grateful to Tsukuba-city for permission to conductthis investigation and to Dr H. Matsumoto for giving us the op-portunity to measure radionuclides at the Center for Research inIsotopes and Environmental Dynamics, University of Tsukuba. Thisstudy was partly funded by a Grant-in-Aid of the Japan Society for

the Promotion of Science (no. 24651043) and the Ministry of theEnvironment, Government of Japan.

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