Physics and Chemistry of the Earth 58–60 (2013) 57–67

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Physics and Chemistry of the Earth

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Mineralogical and geomicrobial examination of soil contamination byradioactive Cs due to 2011 Fukushima Daiichi Nuclear Power Plantaccident

1474-7065/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.pce.2013.04.010

⇑ Corresponding author. Tel.: +81 25 2626186.E-mail address: akai@geo.sc.niigata-u.ac.jp (J. Akai).

Junji Akai a,⇑, Nao Nomura b, Shin Matsushita b, Hisaaki Kudo c, Haruo Fukuhara d, Shiro Matsuoka e,Jinko Matsumoto f

a Department of Geology, Faculty of Science, Niigata University, Ikarashi-2, 8050, Niigata 950-2181, Japanb Graduate School of Science and Technology, Niigata University, Ikarashi-2, 8050, Niigata 950-2181, Japanc Department of Chemistry, Faculty of Science, Niigata University, Ikarashi-2, 8050, Niigata 950-2181, Japand Department of Biology, Faculty of Education, Niigata University, Ikarashi-2, 8050, Niigata 950-2181, Japane Department of Environmental Sciences, Faculty of Science, Niigata University, Ikarashi-2, 8050, Niigata 950-2181, Japanf Fukushima-Higashi High School, Fukushima, Japan

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

Article history:Available online 25 April 2013

Keywords:CesiumFukushimaLeavesRecirculationBacterial sorptionTEM

Soil contamination by radioactive Cs from Fukushima Daiichi Nuclear Power Plant accident was investi-gated. Absorption and desorption experiments of Cs were conducted for several phyllosillicates (kaolin-ite, sericite, montmorillonite, vermiculite, chrysotile and biotite), zeolite and solid organic matter (deadand green leaves). The results confirmed the characteristic sorption and desorption of Cs by these mate-rials. The 2:1 type phyllosilicate, especially, vermiculite and montmorillonite absorbed Cs well. Heatedvermiculite for agricultural use and weathered montmorillonite also adsorbed Cs. Leaves also absorbedCs considerably but easily desorbed it. In summary, the relative capacity and strength of different mate-rials for sorption of Cs followed the order: zeolite (clinoptilolite) > 2:1 type clay mineral > 1:1 type claymineral > dead and green leaves. Culture experiments using bacteria of both naturally living on deadleaves in Iitate village, Fukushima Pref. and bacterial strains of Bacillus subtillis, Rhodococus erythropolis,Streptomyces aomiensis and Actinomycetospora chlora were carried out. Non-radioactive 1% Cs solution(CsCl) was added to the culture media. Two types of strong or considerable bacterial uptakes of Cs werefound in bacterial cells. One is that Cs was contained mainly as globules inside bacteria and the other isthat Cs was absorbed in the whole bacterial cells. The globules consisted mainly of Cs and P. Based on allthese results, future diffusion and re-circulation behavior of Cs in the surface environment was discussed.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction mals. Clay minerals, especially 2:1 type clay minerals strongly ab-

The Fukushima Daiichi Nuclear Power Plant accident hascaused wide soil contamination by radioactive Cs as Chernobylaccident did (e.g., Ebihara et al., 2012; Watanabe et al., 2012;UNSCEAR, 2008). It is well known that sorption of radioactiveCs in soil does not go so deep: Most of the Cs is less than10 cm deep (e.g., Arapis et al., 1997; Ohno et al., 2012). This isdue to strong sorption of Cs by soil. Soil is fundamentally com-posed of minerals containing clay minerals and organic matters,and various organisms living in it.

Cesium has a similar nature to other alkali metals such as K andbinds weakly to organic and inorganic ligands. Organic materials insoil are derived from plants and microorganisms. Organisms in thesoil are plants, filamentous and single-celled bacteria, algae, fungi,and small invertebrates such as protozoa, worms, insects and ani-

sorb Cs (Sawhney, 1972; Comans et al., 1991; Comans and Hockley,1992; Maes and Cremers, 1986; Cornell, 1993; Bostick et al., 2002;Nakano et al., 2003).

Dissolution and extraction experiments have suggested that Csstrongly combined to clay minerals is not easily released in manykinds of solutions; for example water, acid and alkaline solutions.However, ammonium acetate releases Cs of ca. 15% and finallyca. 70% of Cs remains after treatment (Hou et al., 2003). The 2:1type clay minerals show stronger sorption ability than 1:1 typeclay minerals and frayed edge sites in clay minerals mainly absorbCs (Sawhney, 1972; Ebel, 1980; Kitamura et al., 2008). The Cs sorp-tion characteristics by zeolite, e.g., clinoptilolite, is well known(e.g., Bailey et al., 1999). Clinoptilolite, which is highly selectivefor Cs, is used for removal of Cs from contaminated waters (Cheli-shchev, 1995). Therefore, current method for treatment of Cs is byion exchange of clinoptilolite offering ion exchange sites, moderateresistance to radiometric degradation and low solubility.

58 J. Akai et al. / Physics and Chemistry of the Earth 58–60 (2013) 57–67

In general, the role of bacteria in surface environments isimportant due to the interaction between microbe and minerals.Regarding Cs contamination, bacterial behaviour has been re-viewed by Avery (1995, 2006). Because of the similarity of K andCs, both may be absorbed by the same metabolic pass. Escherichiacoli have characteristic K+ uptake transport systems which is re-lated to enzyme necessity and affinity of K+ (Bossemeyer et al.,1989). Appanna et al. (1996) suggested that Cs was immobilizedby Pseudomonas fluorescence as an insoluble precipitate when usingculture media containing ferric iron. However, the details for thesemicrobial processes are not fully clarified, and more varieties ofexamples in different conditions are needed to be collected forwide interpretation of natural processes and also for remediationpossibilities. Another algal and fungal model system of Cs sorptionis also suggested (Harvey and Patrick, 1967; DeRome and Gadd,1991). Later, Kato et al. (2000) suggested Cs uptake by Streptomyceslividans TK-24 and Streptomyces sp. TOHO-2. Uptake of Cs by ac-tively metabolizing microorganisms may be proved more effec-tively, but microbial biosorption has suggested low Cs uptakeover zeolite use (Macaskie, 1991).

Soil contamination by radioactive Cs from a reactor at the Fuku-shima Daiichi Nuclear Power Plant which resulted from meltdownof fuel rods, has spread over the wide area especially in FukushimaPrefecture. Regarding radioactive Cs behavior, many research stud-ies have been reported in relation to the Chernobyl accident andalso to nuclear weapons test effects in the 1960s (e.g., Lloyde andEncesah, 1999; Elles and Lee, 2002).

First, this study described the basic data of Cs contamination inFukushima. Second, fundamental experiments of Cs sorption anddesorption by various clay minerals and leaves were conducted.Some previous studies on sorption of Cs by typical clay mineralspecies have been carried out (e.g., Hou et al., 2003). Therefore, thisstudy examined the Cs sorption properties by more varieties ofphyllosilicate types. Sorption of Cs by leaves was also compara-tively conducted. Desorption characteristics of Cs by clay mineralshave been reported and are well known. Then, we carried out thedesorption experiments from leaves in details. Thirdly, in orderto clarify the bacterial role in the environment, culture experi-ments were carried out using both a natural bacterial mixture liv-ing on the dead leaves in Iitate village, Fukushima Pref. and on fourpure strains. These strains were randomly selected among verycommonly found types of bacteria in the surface environments.All of these results lead to a clarification of the detailed formationprocess of the so-called ‘hot spot’ where Cs is highly concentratedin local scales. Future diffusion and recirculation behaviour ofradioactive Cs in the surface environments, and the fate of Cs inthe future environments are finally discussed.

2. Materials and methods

This study is composed of sampling in the field and laboratoryexperiments. So-called ‘hot spot’, where Cs is highly concentratedlocally, were found in the field survey for sampling in Fukushimaprefecture. Using these samples, laboratory experiments wereconducted.

2.1. Materials

2.1.1. Soil and sandy dust specimens from highly Cs-concentratedareas

Soils beneath the rain drainspout from house roof in Date city(sampled by S. Sato): Radiation intensity of b and c rays measuredby the dosimeter (TGS-121/Aloka) was 60 lSv/h at the site and5 lSv/h at the position of 1 cm apart from the sample of ca.100 cc in the laboratory. Sandy dust sample on the housetop of

Tachibana High School in Fukushima City was collected by Mat-sumoto. They were collected 20th March 2011 and the c-ray mea-surements were carried out 25th March 2011. Radiation intensityof b and c rays measured by dosimeter (Gamma Scout) was3.8 lSv/h at the position of 1 cm apart from the sample of ca.100 cc in the Laboratory. The sample used for c ray spectroscopywas 0.695 g. A soil sample with some black dead leaves was col-lected from the street gutter at Iitate village where there is a so-called ‘hot spot’. The radiation intensity of b and c rays measuredby dosimeter at this point was 132 lSv/h (b and c rays)

2.1.2. Mineral and leaf samplesClay mineral species with their localities are shown below. 1.

Kaolinite in Kanpaku; 2. Kaolinite in Hakurou, Hokkaidou; 3. Ser-pentine (chrysotile) in Oheyama, Kyoto; 4. Montmorillonite inOdo, Niigata; 5. Weathered montmorillonite (kaolin–montmoril-lonite) in Hanetsu, Niigata; 6. Vermiculite (Materials importedfrom China), 7. Heated vermiculite of (6), 8. Biotite in Ishikawa,Fukushima Pref.; 9. Sericite in Nabeyama (with impurity of kaolinmineral), 10. Chlorite in Kamioka, Gifu Pref. (with impurity ofantigorite). Natural zeolite samples (mineral species, locality in Ja-pan) were also prepared as follows.

1. Clinoptilolite in Itaya, Yamagata; 2. Mordenite in Kamihoro,Iwamizawa, Hokkaido.

Leaf samples were used for sorption experiments. Varieties ofdead and green leaf samples were collected around Niigata Univer-sity, as follows; 1. Camellia (Camellia japonica), 2. Cherry tree‘Somei-yoshino’ (Cerasus yedoensis), 3.orange osmanthus (Osman-thus fragrans var. aurantiacus), 4. Reed (Phragmites australis), 5.Timothy, timothy grass (Phleum pretense), 6. Pine (Pinus thunbergii).

2.1.3. BacteriaThe natural bacterial mixtures living on dead leaves obtained

from the so-called ‘hot spot’ of a street gutter at Iitate village, Fuku-shima Prefecture were collected.

Pure bacterial strains of Rhodococus erythropolis (RIKEN BRC JCMNo. 9804), Streptomyces aomiensis (RIKEN BRC JCM No. 17986) andBacillus subtillis (RIKEN BRC JCM No. 18293) and Actinomycetosporachlora (RIKEN BRC JCM No. 17979) were obtained from JAPAN COL-LECTION OF MICROORGANISMS in RIKEN Bioresource Center.

2.2. Experimental methods

2.2.1. Radiation measurements and XRD analysisRadiation dosimeter of GM counter (Gamma Scourt) which

measure a, b and c rays was used for field and laboratory experi-ments. Radiation dosimeter of GM counter (TGS-121/Aloka) whichmeasure b and c rays were partly used for field use. c-ray spec-trometry was carried out for identification and determinations ofradioisotopes. This is composed of a high purity Ge coupled witha multi-channel pulse-height analyzer. The resolution is 2.0 keVat 1332 keV c-ray of 60Co. Autoradiography was carried out usingBlack and White film with sensitivity of ISO 400. Sandy dust parti-cles (Sample A) and Date soil sample (Sample B) were placed onthe film and kept for 5 days in a dark room to develop. XRD (X-ray Diffraction) analysis was carried out using Ultima IV (Rigaku)for powdered samples.

2.2.2. Sorption and desorption experiments by clay minerals, zeoliteand leaves

For phyllosilicates, 10 ppm and 1% Cs solution were prepared asnon-radioactive CsCl solution. 1% solution is too high in a concen-tration for accidental contamination by Cs but this experiment wasdesigned in order to check the fundamental capacity of sorption incomparison with other materials. Powdered phyllosilicate was putinto Cs solution. They were then stirred for 24 h and centrifuged for

J. Akai et al. / Physics and Chemistry of the Earth 58–60 (2013) 57–67 59

analysis. 1 g of phyllosilicate was put in 40 cc of 10 ppm or 1% Cssolution and stirred for 24 h. They were centrifuged and the Cs con-centration was measured by Atomic Absorption Spectrometer (AA-6200: Shimadzu).

Sorption experiments by zeolite samples were carried out forcomparison to clay minerals and leaf samples. Using 10 ppm and1% Cs solution (non-radioactive CsCl) and 1 g of zeolite, sampleswere put in 40 cc of 10 ppm or 1% Cs solution and stirred for24 h. The other conditions are the same as those described for clayminerals.

Dead and green leaves were collected, washed with distilledwater, and then air dried. The procedure was the same as inthe mineral sorption experiments. 1% and 10 ppm non-radioac-tive CsCl solutions were prepared. 5 g of the dried leaves wereput into the solutions (50 ml) and stirred for 24 h. The sampleswere centrifuged and the Cs concentration of the solution wasmeasured by Atomic Absorption Spectrometer (AA-6200:Shimadzu).

Sorption ratio was calculated based on the following equation:

Sorption ratio ð%Þ ¼ ðOriginal Cs content in solution� Remaining Cs content in solutionÞ=ðOriginal Cs content in solutionÞ � 100

Leave samples (1 g) were prepared by adsorbing Cs (1% Cs solu-tion; 50 cc) and drying. Then, they were immersed into varioustypes of solutions of 50 cc: Distilled water, NaOH (0.1 mol), HCl(0.1 mol), (NH4)2C2O4�H2O (0.1 mol), KCl (0.1 mol), H2SO4

(0.1 mol), HNO3 (0.1 mol).They were stirred for 1 h and centrifuged, and the Cs concentra-

tion was measured. Desorption ratio was calculated, using the fol-lowing equation:

Desorption ratio ð%Þ ¼ ðAbsorbed Cs content� Remaining Cs contentÞ=ðAbsorbed Cs contentÞ � 100

2.2.3. Bacterial culture experiments and TEM (Transmission ElectronMicroscopy) observations

The following culture media were prepared. Sakurai Mediumwas prepared as follows. 0.075 g of glucose, 0.3 g of polypeptonand 0.15 g of yeast extract were dissolved in 150 ml distilled water.Other Media for each corresponding bacterial strain was preparedas follows. For R. erythropolis, Bacto peptone (10 g), Yeast extract(5 g), Malt extract (5 g), Casamino acid (5 g), Glycerol (2 g), andMgSO4/7H2O were dissolved in 1 L of distilled water. For Strepto-mycesm aomiensis, Yeast extract (4 g), Malt extract (10 g) and Glu-cose (4 g) were dissolved in 1 L distilled water. For B. subtillis,Peptone (5 g), and Beef extract (3 g) were dissolved in 1 L distilledwater. For A. chlora, Yeast extract (1 g) and Oatmeal agar (20 g)were dissolved in 1 L distilled water. 1% Cs solution was prepared

Fig. 1. Autoradiograph of Cs-contaminated materials. (a) Sandy dust from a housetop of Tdrainspout from a house roof in Date City, Fukushima Prefecture.

by CsCl. 10 cc of Sakurai medium and 40 cc of 1% Cs solution weremixed and used for natural bacteria in Iitate village. A small pieceof muddy dead leaf (square of ca. 5 mm) was added to culture solu-tion as a natural bacterial source. They were cultured at room tem-perature (25 �C) for two weeks. Culture experiments of strains ofRIKEN BRC were carried out using 20 cc of corresponding mediumand 20 cc of 1% Cs solution. They were cultured at room tempera-ture (25 �C) for 2 weeks.

TEM–EDS (Energy Dispersive Spectrometer) analysis was car-ried out as follows. TEM of JEM 2010 was operated at 200 kV.The EDS system used was Voyager IV (Noran Inst). Dead leavesin Iitate village were immersed in a small quantity of distilledwater and a drop of it was placed on carbon-coated perforatedmicrogrid and dried for TEM observation. A drop of the culturedproducts was placed on carbon-coated perforated microgrid anddried.

3. Results

3.1. Analysis of sandy dust sample from Tachibana High School andsoil sample from Date city

The examined samples and obtained data in Fukushima City arevery fundamental as the early stage one of the Fukushima DaiichiNuclear Power Plant accident. The XRD analysis of the sandy dustsample from Tachibana High School showed that the constituentminerals were mainly quartz, feldspars, illite/mica, and very smallamounts of kaolin, vermiculite/chlorite and calcite. Soil samplecontained quartz, feldspars, illite/mica, vermiculite/smectite andvery small amounts of kaolin minerals. Furthermore, examinationby autoradiography was applied to both samples. Determinationof radioisotope nucleides by c-ray spectrometry was applied tothe sandy dust particles from Tachibana High School.

Autoradiography was applied to the sandy dust and soil sam-ples in the middle of May 2011. Black dots in Fig. 1a indicate thesand particles with high coating of radioactive elements. Stronglydarkened shadows are grains with highly absorbed radioactive Cs.

In Fig. 1b of soil specimens, rather continuous darkening isfound probably due to spacing between soil block sample and filmsurface. Strongly darkened grains are also found. Some white radialshadows are also found. There is a possibility that this is due toblocked radiation traces of b-ray by some mineral grains.

c-ray spectrum was measured for the sample from FukushimaCity. Fig. 2 shows the c-ray spectrum taken at March 29, 2011for the sandy dust of Tachibana High School in Fukushima City.The spectrum indicates the presence of 137Cs, 134Cs, 131I, 132Te,etc. which have already been reported (MITI, 2011). 137Cs, 134Csand 131I are most well known. 132Te was also found in the Fukushi-ma City sample. Although 132Te has a half-life of 3.2 days, the peakof 132Te was still persistent on 25th March 2011. This means that atthe initial stage, much more 132Te must be present. The boiling

achibana High School in Fukushima City. (b) Small block of soil sample beneath the

Fig. 2. c-ray Spectrum for the sandy dust of Tachibana High School in FukushimaCity.

60 J. Akai et al. / Physics and Chemistry of the Earth 58–60 (2013) 57–67

temperature of Te is 1380 �C and elements with relatively low boil-ing temperatures might be predominant. The radioactivity of 137Csin the sample was calculated to be 4.8 � 105 Bq/kg. The number ofCs atoms in the sample is 4.58 � 1011 which corresponds to theweight of Cs to be 105 pg (1.05 � 10�10 g). This is equal to150 ppt in concentration.

3.2. Sorption and desorption experiments by clay minerals, zeolite andleaves

3.2.1. Sorption experimentFundamental sorption experiments for varieties of phyllosili-

cates were carried out, adding previously reported results for 2:1type clay minerals (Sawhney, 1972; Ebel, 1980; Comans et al.,1991; Kitamura et al., 2008).

Fig. 3a and b indicate the results of sorption experiment of10 ppm and 1% Cs solutions for various clay mineral species,respectively. Slightly different sorption characteristics are found,but all kinds of phyllosilicates examined absorbed Cs well. 2:1 typeminerals strongly absorb Cs. Montmorillonite and vermiculiteshow stronger sorption properties among clay minerals. Heatedvermiculite of commercial use which is often used in agriculturalpurposes was also examined and adsorbed Cs as well as originalvermiculite.

Weathered montomorillonite also absorbed Cs as well as non-weathered montomorillonite. Some fluctuations may be due toimpurities contained in samples.

Sorption experiments of Cs by natural zeolite were conducted.Fig. 3c and d indicate the results of Cs sorption by zeolite. Zeoliteshows strong sorption characteristics for 10 ppm and 1% Cs solu-tion. At 1% solutions, a clear difference is found among zeolite,phyllosilicate and leaves; zeolite has still strong sorption abilitythan phyllosilicate and solid organic materials.

In order to assess sorption of Cs to dead and green leaves, sorp-tion experiments were carried out. Fig. 4 indicates the results ofsorption experiment of 10 ppm and 1% Cs solution for various deadand green leaves. At 1% solution, some fluctuations for each kind ofleaves are present, but all absorbed 8%–1.6% of Cs. At a 10 ppmsolution, 59–12.5% of Cs were absorbed. The general tendency isthat dead leaves absorb more than green leaves with some

exceptions. However, the difference is not so large, and both deadand green leaves absorb Cs considerably, in general. Depending onthe kinds of leaves, a little difference is found. The reason is not al-ways clear: some leaves are coated with wax-like materials, andthe degree of degradation is different in each leaf. These factorsmay influence the results. Green leaves have a still higher watercontent ratio than dead leaves. Therefore, a simple comparison be-tween green and dead leaves is difficult.

3.2.2. Desorption experiment by leavesCs-desorption experiments of absorbed Cs in leaves by using

distilled water and various chemical solutions showed that Cs is re-leased relatively easily (Fig. 5). This means that the combiningforce of Cs to leaves is not strong. In general, more Cs dissolvedfrom cherry leaves than pine leaves. There is a possibility that sur-face chemical conditions in leaves may be different, but more anal-yses are needed to verify this.

3.2.3. Culture experiments using naturally living bacterial mixture toabsorb Cs

For the first time, original bacteria in Iitate village (a so-called‘hot spot’ in the street gutter in Iitate village) was examined byTEM. Fig. 6a shows TEM image of predominant bacteria in thehighly Cs concentrated soil of 132 lSv/h (just on the dead leaf withsoil) indicating faint globules in bacterial cells. EDS spectrum(Fig. 6b) of the globule indicates the presence of Ca, P and smallamount of K. To check the bacterial behavior, culture experimentswere carried out using 1% Cs solution and Sakurai medium for sev-eral days. The products of the culture experiments were examinedby TEM–EDS. Fig. 7a shows the TEM image of predominantlygrown bacteria. The size of the bacteria is 1–2 lm in length and0.4–0.5 lm in width, and rod-shaped and linked together in chain.Gene analysis for these bacteria was not carried out. However, leafsamples were once boiled at 100 �C, and then cultured with Sakuraimedium; after this procedure, bacteria grew again. That is, thesebacteria have heat-resistant nature: thus, they are probablyspore-forming bacteria.

Bacteria in Fig. 7a indicates that Cs–P globules are contained in-side the bacterial body. The EDS spectrum (Fig. 7b) shows the ana-lytical results of the globules. The globules may be mostly Cs–Pcompound. Using quantitative analysis program in Voyager IV, Csconcentration in the globules was calculated to be Ca. 38 wt% whensupposed to be Cs phosphate. The spectrum of Fig. 9c indicatedcomposition of bacterial bodies other than the globule: Cs is alsocontained in relatively small quantities. These are the results ofculture for 5 days. In comparison, sorption of 10 ppm Cs solutionby bacteria also shows very small peak of Cs for the globules.

3.2.4. Culture experiments using various bacteria to absorb CsFig. 8 shows some examples of Cs uptake by various bacteria.

Considerable amounts of Cs were observed in EDS spectra. Glob-ules mainly composed of Cs and P phase, most likely Cs phos-phates, were also found in some cases (Fig. 8a, c, and e). B.subtillis cultured for 2 weeks contained globules of Cs and P, andRhodococcus of 5 days culture product and Streotomyces of 2 weeksculture product also showed globules in bacterial cells. On theother hand, Actinomycetospora showed bulk absorption of Cs wasfound in the whole bacterial body. The atomic number of Cs (55)is high, so Cs concentrated parts show darker contrast in TEMimages. Therefore, bacterial sorption of Cs is easily estimated viaTEM observation. Even if similar globules are found in both naturalbacteria in Iitate village and these pure RIKEN strains, the bacterialspecies from Iitate village is not determined. However, it is at leastreported that varieties of bacteria may absorb Cs in various waysand Cs-absorption by bacteria is widely found in natural surfaceconditions.

Fig. 3. Experimental results of sorption of Cs from non-radioactive CsCl solutions by various types of phyllosilicate and natural zeolite. (a) Cs solution of 10 ppm forphyllosilicate. (b) Cs solution of 1% for phyllosilicate. (c) Cs solution of 10 ppm for zeolite. (d) Cs solution of 1% for zeolite.

J. Akai et al. / Physics and Chemistry of the Earth 58–60 (2013) 57–67 61

4. Discussion

4.1. Characteristics of soil contamination in Fukushima case

Wide contamination by radioactive nuclides over Europe hasbeen spread by the Chernobyl accident (United Nations ScientificCommittee on the Effects of Atomic Radiation, 2008). The Fukushi-ma Daiichi Nuclear Power Plant accident occurred and radioactive

nucleides have spread again (MITI, 2011). This paper reports moreadditive data in Fukushima City, in the early stage of the accident.Especially, c-ray Spectrum for the sandy dust (collected 20thMarch 2011 and the measurement was carried out 25th March2011) showed relative abundance of 137Cs, 134Cs and 131I, etc.Furthermore, the presently observed low concentration of 132Teindicates that 132Te concentration was initially higher, becausehalf-life of 132Te is 3.2 days. 132Te changes to 132I. The boiling

Fig. 4. Experimental results of sorption of Cs from non-radioactive CsCl solutions by various types of dead and green leaves. (a) Cs solution of 10 ppm. (b) Cs solution of 1%.

Fig. 5. Experimental results of desorption of non-radioactive Cs from leaf samples of pine (upper bar) and cherry trees (lower darker bar) by water and various chemicalsolutions.

62 J. Akai et al. / Physics and Chemistry of the Earth 58–60 (2013) 57–67

temperatures of Te and Cs are 1380 �C and 670 �C respectively, andtherefore, evaporation was above these temperatures. These com-positional characteristics are unique to Fukushima Daiichi and sug-gest a slight added health problem by radioactive 132I of latersupply after 131I. Half-life of 132I is 2.3 h.

Autoradiography was preliminarily applied to sandy dust andthe results indicated the possibility of further wide use of thismethod to varieties of the contamination problem. For example,using these methods, vertical section of soil profile or sedimentsprofile in river and/or ocean sediments can be visually examined.

Fig. 6. TEM image and EDS spectrum of bacteria (a) TEM image of bacteria in the highly Cs concentrated soil in Iitate Village, Fukushima Pref. Faint globules in the bacterialcells were found. (b) EDS spectrum of the globule. It indicates the presence of Ca, P and a very small amount of K. The vertical scale is a log scale.

Fig. 7. TEM image and EDS spectra of cultured bacteria using a 1% non-radioactive Cs solution. (a) TEM image of predominantly grown bacteria. Cs-P globules are containedinside the bacterial body. (b) EDS spectrum of the globules. (c) EDS spectrum of bacterial body other than globules.

J. Akai et al. / Physics and Chemistry of the Earth 58–60 (2013) 57–67 63

4.2. Sorption and desorption characteristics

In order to understand the combined process of natural envi-ronment, we must know the details of each key material whichbring Cs widely. So, fundamental characteristics of each key

material for Cs were examined, on the basis of previous knowl-edges on clay minerals (Schulz et al.,1960; Dolcater, 1968; Sawh-ney, 1972; Ebel, 1980; Comans et al., 1991; Ishikawa, 2007;Kitamura et al., 2008: Tsukada et al., 2008). And with regard toplant organic matters, Schulz et al., 1960; Tsukada et al., 2008)

Fig. 8. TEM images and EDS spectra of cultured strains of Bacillus subtillis, Rhodococus erythropolis, Streptomyces aomiensis and Actinomycetospora chlora. (a) TEM image ofBacillus subtillis (cultured for two weeks). Cs–P globules are contained inside bacterial body. (b) EDS spectrum of the globules of Bacillus subtillis (a). (c) TEM image ofRhodococus erythropolis (cultured for 5 days). Globules are contained inside the bacterial body. (d) EDS spectrum of the bacteria (c). (e) TEM image of Streptomyces aomiensis(cultured for 2 weeks). Cs is absorbed in the bacterial body. (f) EDS spectrum of Streptomyces aomiensis (e). (g) TEM image of Actinomycetospora chlora (cultured for 2 weeks).(h) EDS spectrum of Actinomycetospora chlora (g).

64 J. Akai et al. / Physics and Chemistry of the Earth 58–60 (2013) 57–67

Fig. 9. Schematic model for the recirculation and fate of Cs in soils and the surface environment. Solid arrows indicate transfer of Cs. Arrows with dashed lines indicate somepossible routes of Cs recirculation. ⁄1, ⁄2, and ⁄3 indicate references relating to each process. ⁄1: Wauters et al. (1996), Elles (2002), Stauton and Roubaud (1997), Sawney(1972), Maes and Cremers (1986), Johnston and Tombacz (1990), Comans and Hockley (1992), Arapis et al. (1997). ⁄2: The present study: Sawhney (1972), Ebel (1980),Comans et al. (1991), Kitamura et al. (2008). ⁄3: Dolcater et al. (1968), Sawhney (1972), Ishikawa (2007), Schulz et al. (1960), Cornell (1993). ⁄4: The present study; Schulzet al. (1960), Ejeckam and Sheriff (2005), Tsukada et al. (2008). ⁄5: The present study; Appanna et al. (1996), Staunton et al. (2002). ⁄6: The present study; Appanna et al.(1996), Avery (1995), Bossemeyer et al. (1989), Tomioka et al. (1992), Derks and Borst-Pauwels (1979), Kato et al. (2000). ⁄7: Matisoff (1995), Avery et al. (1992, 1993), Perkinsand Godd (1993), Derks and Borst-Pauwels (1979), deRome and Gadd (1991), Harvey and Patrick (1967). ⁄8: IAEA (1995), Delvaux et al. (2000), Lembrechts (1993).

J. Akai et al. / Physics and Chemistry of the Earth 58–60 (2013) 57–67 65

and microbes (Derks and Borst-Pauwels, 1979; Bossemeyer et al.,1989; Tomioka et al., 1992; Avery, 1995; Appanna et al., 1996; Katoet al., 2000).

Sorption studies by phyllosilicate, zeolite and leaves showeddifferences in 10 ppm and 1%, although the actual concentrationof radioactive Cs following an accidental release may be in ppbor ppt level in the environment. Solid materials, for example, sandydust on the housetop of Tachibana High School contained Cs con-centrations of 150 ppt. When 1% concentration is applied, zeoliteabsorbs more Cs than phyllosilicate and leaves; and the differencesin Cs sorption capacity became clear. This study showed the resultsof Cs adsorption by varieties of phyllosilicates that are not fully re-ported in the previous reports. In general, 2:1 type minerals ab-sorbed more Cs than 1:1 type, although some samples containedimpurity minerals. Montmorillonite absorbed Cs well. Weatheredmontmorillonite (kaolin–montmorillonite) still showed a largesorption capacity. Dead and green leaves also showed a consider-able amount of Cs sorption, but relatively less than phyllosilicate.

Phyllosilicates strongly absorb Cs and do not release Cs easily,but leaves desorb Cs relatively easily. These characteristics deter-mine the Cs behavior in the environment. Slight differences amongthe leaf species, dead and green leaves are present, but it can begenerally said that all dead and green leaves absorb a considerableamount of Cs and release Cs even by water relatively easily.

4.3. Interaction between microbes and minerals

Interaction between microbes and minerals is an important as-pect for the surface environmental process. Biological process-re-lated Cs diffusion effect into the ground has been theoreticallysuggested in the study of the Chernobyl accident and soil contam-ination (Matisoff, 1995). In this study, geomicrobilogical effects onCs behaviour are also suggested. The bacteria found may obtainnutrients from dead leaves, etc. A previous study on the biowea-thering of biotite (Akai, 2008) indicated that bacteria actively ab-sorb K on the cleavage surface of biotite from Ishikawa,Fukushima Prefecture, Japan. Therefore, sorption of Cs instead ofK in Iitate village is suggested, and the observed results (Fig. 9a

and b) are reasonably interpreted. Other examples have been re-viewed by Appanna et al. (1996), where Cs was immobilized withthe cell pellet of Pseudomonas fluorescens in the presence of ferriciron. All the results of this study suggest that the bacterial absorp-tion and later transportation of Cs by bacteria may play some rolein the surface behavior of Cs.

4.4. Formation of a so-called ‘hot spot’

As is well known, Cs concentrated area (so-called ‘hot spot’) isformed in various scales in Japan: for several km to less than 1 min size. The following four steps are described as important forthe formation of a Cs ‘hot spot’. Step I: Cs is present probably asa fine solid phase or gaseous phase in emission from the powerplant accident. Step II: Cs may be present as a solution when thesolid Cs phase fell onto the ground or is in the air with water phase.Step III: Cs in the solution meets minerals or other materials, e.g.,plants and other organic materials containing dead and greenleaves, etc. Then, Cs is strongly absorbed to minerals and softly ab-sorbed to organic matters containing dead leaves. This is related tothe strong absorbing property of clay minerals and soft absorbingin organic matters for Cs. Step IV: Cs diffusion and recirculationbehavior are interpreted to be involved in the transportation ofCs as solid grains of minerals and some solid organic substances.These grains may be transported, accumulated and again depositedby water flow, wind, or artificial transportation, burning, etc. Largeparts of step IV correspond to the fundamental process of erosion,transportation and sedimentation in the surface area, as is the casein natural sedimentological processes in geology, containing com-ponents of human activity.

4.5. Recirculation process and the fate of Cs in the future

Based on the results of this study and previous literatures thefollowing fundamental schematic figure can be drawn (Fig. 9). Itsuggests the possible Cs diffusion and recirculation in the surfaceenvironment.

66 J. Akai et al. / Physics and Chemistry of the Earth 58–60 (2013) 57–67

When a Cs solution corresponding to the above mentioned stepIII meets minerals, it is strongly absorbed to these minerals con-taining phyllosilicates by the weak hydration energy (Johnstonand Tombacz, 1990; Elles and Lee, 2002). Then the Cs is ion-ex-changed with cations in interlayer sites, e.g., K in mica with time.The ion-exchangeable form of Cs is known to be reduced less than50% after 1 year, and relative abundances of Cs are estimated as fol-lows: Cs firmly fixed to minerals, is 70%, Cs in ion–exchangeablestate is 10% and Cs in a form that is combined to organic matter,is 20% (Tsukada et al., 2008). Cs is softly absorbed to organic mat-ter, e.g., dead leaves and fumus. The fate of the Cs in the organicmatter, especially in dead leaves, will be released later and theymay then be transferred to minerals or plants. The fate of Cs maydepend on soil types and relative abundance and quantities of con-stituent minerals.

Bacterial absorption of Cs has been reported (Avery, 1995;Derks and Borst-Pauwels, 1979). E. coli has several well-character-ized K uptake transport systems, which are required for enzymeactivation (Bossemeyer et al., 1989). Uptake of Cs by activelymetabolizing microorganisms has been proven successfully. Inbiomass of Rhizopus arrhizus and Penicillium chrysogenu, uptakeby an energy-independent process was suggested to be moreimportant than energy-dependent uptake (Harvey and Patrick,1967; deRome and Gadd, 1991). Cs is expected to persist in a mo-bile form in the environment with accumulation of the Cs bymicroorganisms, which may be related to passing radionuclideto higher trophic levels in the food chain (Avery, 1995). Bacteriamay attack and obtain nutrients from dead leaves etc. So Cs inor on the dead leaves may be transferred into bacteria. Cs mayalso get into plants. Other organisms such as cyanobacteria andeukaryotic algae Chlorella salina (Very et al., 1992, 1993) and fun-gi biomass (Perkins and Godd, 1993) also accumulate Cs. So,microorganisms able to absorb Cs may be ubiquitously habitedin surface conditions, often on dead leaves, etc. From the resultsof this study and previous reports, wide bacterial absorption ofCs was suggested for Fukushima area even if the quantity is notalways so much.

The relative strength of bonding to phyllosilicates is in the orderof Cs > NH4+ > K+ (Sawhney, 1972). If extreme K+ is supplied, K+ willbe used by plants, and the final Cs concentration in the plant maybecome low. But if extreme NH4 is used, then Cs will be released,and Cs will be absorbed more by plant.

Thus, Fig. 9 schematically sketches the future fate of Cs diffu-sion and recirculation in the environment. That is, Cs diffusesand is fixed to various materials (minerals, organic matter contain-ing leaves, bacteria, microorganisms, plants, etc.) when Cs encoun-ters them in the solution state. Then, absorbed Cs does not remainin the same materials but diffuses to some extent for a long time,according to strength of sorption. Weakly absorbed Cs, for exampleto green and dead leaves, may be transferred probably to 2:1 phyl-losilicate via bacteria or through natural decay. Cs-fixed clay min-erals may also behave as fine sedimentary grains in the surfacegeological process. Thus, a ‘hot spot’ where radioactive Cs is highlyconcentrated is formed and/or Cs will migrate into the environ-ment. Conditions for formation of the ‘hot spot’ depend on differ-ent situations in varieties of the sites. Correlations of each factor,such as the presence of clay minerals, dead and green leaves, mi-crobes, pore water depend on a variety of situations.

5. Summary

Soil contamination by radioactive Cs in Fukushima region wasexamined from the standpoint of environmental mineralogy. Add-ing to obtained fundamental data for Fukushima City in an earlystage, the following new points were clarified.

1. Comparative sorption experiments of Cs by wide varieties ofphyllosilicates containing serpentine, heated vermiculite andweathered montmorillonit, dead and green leaves, and zeolitewere carried out. Strength and capacity for sorption of Cs is inthe order of zeolite > 2:1 type clay > 1:1 type clay > leaves.

2. Desorption experiments by leaves were also carried out. Rela-tively easy release of Cs from leaves was observed.

3. Bacterial absorption of Cs was examined, based on cultureexperiments of a variety of bacteria using non-radioactive CsClsolutions. Two types of Cs uptake by bacteria were clearly foundin TEM observations. One type is the bulk absorption of Csinside bacteria bodies. Another type is Cs accumulation in theform of Cs–P globules. Cs concentrations in the globule is over30 wt%.

4. Thus, characteristics of important factors of phyllosilicates,organic matter containing dead leaves, bacteria and microor-ganisms, and plants, in recirculation of Cs were clarified in moredetail.

5. The future diffusion and recirculation behavior of Cs in the envi-ronment were discussed using a schematic model figure. Theconcrete process of ‘hot spot’ formation depends on each situa-tion of every environment.

Acknowledgments

We thank Mr. Shigeki Chiba of Hobara High School, FukushimaPref., Mr. Nobuo Kuromori of Chishitu-Kisho Kogyou Company andMr. Shinnichi Satoh of Fukushima University Student for their helpin collecting samples and Mr. Shoki Yamada of Niigata UniversityStudent for his help in drawing figures. We thank BAMI Co., Ltd.in Fukushima and NITTAI Co., Ltd. in Okayama for supplying ver-miculite samples, and JIHKURAITO Co., Ltd. in Yamagata for sup-plying the Itaya zeolite sample. We thank Dr. Hossain Anawar forhis kind and detailed comments to the manuscript to improvingit. This work was supported by Grants-in-Aid for Scientific Re-search by JSPS (Challenging Exploratory Research). We alsoacknowledge many citizens of Wakamiya Cho, Nihonmatsu City,and Fukushima Pref. for their cooperation in cleaning Cs-contami-nated spots and sampling. We appreciate careful and kind com-ments of anonymous reviewers for this manuscript.

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