Discovery of radioactive silver (110mAg) in spiders and other fauna in the terrestrial environment after the meltdown of Fukushima Dai-ichi nuclear power plant

Hiromi NAKANISHI; Atsushi MORI; Kouki TAKEDA; Houdo TANAKA; Natsuko KOBAYASHI; Keitaro TANOI; Takashi YAMAKAWA; Satoshi MORI

doi:10.2183/pjab.91.160

Abstract

Six months after the explosion of TEPCO’s Fukushima Dai-ichi nuclear power plant, radioactive silver (^110mAg), was detected in concentrations of 3754 Bq/kg in Nephila clavata (the orb-web spider; Joro-gumo in Japanese) collected at Nimaibashi, Iitate village in Fukushima Prefecture, whereas ^110mAg in the soil was 43.1 Bq/kg. A survey of 35 faunal species in the terrestrial environment during the 3.5 years after the accident showed that most of Anthropoda had two orders higher ^110mAg in their tissues than soils, although silver is not an essential element for their life. However, tracing of the activity of ^110mAg detected in spider Atypus karschi collected regularly at a fixed location showed that it declined much faster than the physical half-life. These results suggest that ^110mAg was at once biologically concentrated by faunal species, especially Arthropoda, through food chain. The factors affecting the subsequent rapid decline of ^110mAg concentration in faunal species are discussed.

Introduction

After the Great East Japan Earthquake and resulting Tsunami on March 11, 2011, a sequential meltdown of the nuclear fuels occurred at the Fukushima Dai-ichi nuclear power plant (NPP) of Tokyo Electric Power Company (TEPCO), following the discharge of enormous amounts of radioactive materials into the environment. The main components were ¹³¹I, ¹³³I, ¹³⁴Cs and ¹³⁷Cs, whose total amounts were estimated to be 1.5 × 10¹⁷ Bq for ¹³¹I, 1.2 × 10¹⁶ Bq for ¹³⁷Cs, and also 6.3 × 10¹⁷ Bq in iodine equivalent.¹⁾ Roughly half of the discharged activity had precipitated in soils and entered inland waters, where it was incorporated into flora and fauna in the terrestrial environment.²⁾ Among a number of attempts to reveal the scale and distribution of the fallout, our group also started to survey local and biological contamination with the radioactivity in the vicinity of the TEPCO’s NPP. On Sept. 20, 2011, we visited one of the heavily contaminated area, Iitate village in Fukushima Prefecture, where had already been declared to be the “planned evacuation zone”. It was a stormy day with heavy rain of typhoon and we had to abandon our original plan to collect vegetation samples, instead we collected the orb-web spider Nephila clavata (Joro-gumo in Japanese), which nested in abundance in a bamboo forest. Our initial conjecture was that the spiders might be contaminated with radioactive cesium reflecting contamination of the food chain. Unexpectedly, however, germanium-semiconductor analysis in the laboratory of the N. clavata specimens showed a sharp peak (657.8 keV) of ^110mAg distinct from the ¹³⁷Cs peak (661.7 keV). This was the beginning to recognize marked biological concentration of ^110mAg in the field fauna during this accident, which was publicized preliminary.³⁾

In fact, radioactive silver, ^110mAg (half-life: 249.95 days), first attracted attention as the atomic weapon detritus, whose distinct biological accumulation was detected in the digestive tissues of a marine crustacean and mussels, barnacles, and fishes from the Pacific Ocean due to the repeated test explosions at Entwetok Atoll, Bikini Atoll etc., from 1946 to 1963.⁴⁾^,⁵⁾ ^110mAg had also been detected as a minor radioactive nuclide contained in wastewater from NPPs, however, the Chernobyl accident on April 26, 1986 caused its discharge in a large amount into the environment. For example, in Cumbria, northwestern England located ∼2000 km from Chernobyl, all vegetation in 18 varietal soils sampled in May 1986 was contaminated with ^110mAg with concentrations ranging from 190 to 480 Bq/kg of dryweight (DW).⁶⁾ Many studies were conducted on the metabolism of ^110mAg in the fallout of the accident by aquatic biota especially in oceans.⁷⁾^–⁹⁾ Studies on cattle such as oxen, lambs and sheep revealed that distinct accumulation of ^110mAg was rather restricted to liver with the biological half-life of 35 days in the case of sheep.⁶⁾^,¹⁰⁾^–¹²⁾ In contrast to these studies, contamination of terrestrial wild fauna involving small insects and animals remained very scarce.

Even in the accident at TEPCO’s NPP, studies on the contamination of fauna were mostly restricted to cattle. After the accident, ^110mAg was detected in the liver of cattle at a concentration of 177 ± 176 Bq/kg,¹³⁾ and a 3-month supply of clean hay as fodder to the contaminated cattle failed to decrease its contents in liver significantly.¹⁴⁾ In contrast, no published studies exist on the dynamics of ^110mAg in small faunal species comprising the food chain in terrestrial environments. Therefore, we conducted successive surveillance of ^110mAg in spiders as well as several small animals and insects during our visits to Fukushima once a month until November 2014. The obtained results confirmed the reproducible accumulation of ^110mAg in small faunal species. Here, we describe the contamination of 35 of these species by ^110mAg and ¹³⁷Cs (or ¹³⁴Cs) fallout and the fates of those radionuclides in the bodies of the orb-web spider N. clavata and the ground spider Atypus karschi in the 3.5 years after the NPP accident.

Materials and methods

Sampling of fauna species and soils.

From Sept. 20, 2011 until Nov. 3, 2014, we collected 35 faunal species from Benten-yama and Hanami-yama in Fukushima city, Oguni, Miyuki-yama and Ryozen in Date city, Tsushima and Akougi in Namie town, Yamakiya in Kawamata town and Nimaibashi, Iitoi, Hiso, Maeda, Sasu, Usuishi and Nagadoro in Iitate village in Fukushima Prefecture (Fig. 1). The sampling sites were located more than 30 km from Fukushima Dai-ichi NPP. Most of the collected species were separately stored in plastic 100-mL cups to avoid their preying on each other. Names of all collected species are listed in Table 3. The collected fauna were starved at room temperature for ∼3 weeks in the U8-cups, which were stored in desiccators. During the starvation process, some of the fauna excreted feces and urine before their death. Starvation was necessary to allow measurement of the true radioactivity in the body tissues of the collected fauna, after they had excreted residual, non-metabolized contamination in their feces and urine. For some of the fauna, the radioactivity in the desiccated feces was also measured.

Fig. 1.

A map of ^110mAg concentration in soil (as of June 14, 2011)²¹⁾ and sampling sites. 1: Benten-yama, 2: Oguni, 3: Nimaibashi, 4: Iitoi, 5: Hiso, 6: Tsushima, 7: Maeda, 8: Miyuki-yama, 9: Ryozen, 10: Yamakiya, 11: Sasu, 12: Usuishi, 13: Nagadoro, 14: Hanami-yama, 15: Akougi.

Our visit to the Hiso on Oct. 13, 2013 coincided with the pregnancy phase of N. clavata females. We collected 85 of the pregnant spiders, separately storing them in U8-cups. These spiders were starved under dark conditions until some of them had spun webs and shed their egg sacs into the cups. Spider bodies, excrement (feces + urine), web thread, and egg sacs were separately collected and their radioactivity was measured. We also collected soil from the sites where N. clavata and A. karschi had been sampled. Surface soils were collected from an area of 10 × 10 × 2 cm. A vertical depth of 2 cm was chosen because >95% of nuclear fallout accumulates within a vertical depth of 2 cm from the soil surface.¹⁵⁾^,¹⁶⁾

Measurement of radioactivity.

The detection of the discharged ^110mAg in the atmospheric dust from the TEPCO’s NPP was first recognized by several institutions from March to May in 2011,¹⁷⁾^–¹⁹⁾ and its total amount was estimated to be 4.04–6.41 × 10¹⁵ Bq in the cores of Units 1–3 of the NPP.²⁰⁾ The Ministry of Education, Culture, Sports, Science and Technology, Japan, published a rough distribution map of ^110mAg in soils on Oct. 31, 2011 (Fig. 1),²¹⁾ and its distribution in surface soils in a wide area around the power plant²²⁾^–²⁴⁾ as well as the vertical distribution profile in Fukushima soils¹⁶⁾ were described a year later the accident.

The aerial dose (µSv/h) was measured in the contaminated fields at a height of 1 m from the sampling sites using an Aloka γ-survey meter (TCS-172; Hitachi-Aloka, Tokyo, Japan). In the laboratory, all materials were analyzed on germanium-semiconductor detectors (GEM type and GMX type, Seiko EG&G, Tokyo, Japan). The counting time was set at 220,000 s. ^110mAg, ¹³⁷Cs, and ¹³⁴Cs activities were determined using the γ-ray detector, detecting peaks at 884.7, 661.7, and 604.7 keV, respectively. Multiple number of animals in each sample (Table 3) was put together in a cup and measured. Therefore no statistical errors were expressed in Tables. The concentration of the measured radioactivity was expressed as Bq/kgDW. Radioactivity in snakes, slugs, and tadpoles, all of which had high water content, and melted during starvation process was measured without desiccation of the specimens and expressed as Bq/kgFW, where FW is the fresh weight.

Imaging analysis.

N. clavata specimens were gently flattened between paper towels, allowed to air-dry completely, and then exposed to BAS imaging plates (IP-plate; FujiFilm, Tokyo, Japan). An image of the vertical distribution of the radioactivity in the soil profile was obtained by exposing the vertical soil layer collected in a lunchbox (13 × 7.5 × 6 cm) to an IP-plate. In both cases, polyethylene film was placed between the sample and the IP-plate to avoid chemical- or water-related disturbances of the sensitivity of the IP-plate to the samples. After ∼1 month of exposure, the IP-plates were scanned using an Image-analyzer (FLA-5000; FujiFilm). The feces of lizards and other fauna were observed by digital microscopy (KEYENCE VH-6300).

Results

Detection of ^110mAg in N. clavata.

Figure 2 shows the γ-radiation from N. clavata (sample no. 3 in Table 3) detected by Ge-semiconductor analysis. Energy peaks corresponding to ¹³⁷Cs (661.7 keV), ^110mAg (657.8 keV), and three other peaks characteristic of ^110mAg (884.7, 937.5, and 1384 keV) were obtained from the same sample. The radioactivity ratio of ^110mAg/¹³⁴Cs/¹³⁷Cs was 1/1.12/1.50.

Fig. 2.

Germanium-semiconductor detector measurement of N. clavata collected at Nimaibashi on Nov. 9, 2011.

Concentration of radioactivity in N. clavata and A. karschi.

We collected N. clavata and surface soils from three different locations in Fukushima Prefecture and calculated the radioactivity concentration ratios, defined as (^110mAg Bq/kg N. clavata)/(^110mAg Bq/kg soil). A similar ratio was calculated for ¹³⁷Cs. As shown in Table 1, the radioactivity concentration ratios were 27.8, 74.5, and 87.3 for ^110mAg and 0.036, 0.078, and 0.071 for ¹³⁷Cs at Oguni, Benten-yama, and Nimaibashi, respectively. These data were then used to calculate the radioactivity concentration ratios of ^110mAg to ¹³⁷Cs, defined as (^110mAg Bq/kg spider/^110mAg Bq/kg soil)/(¹³⁷Cs Bq/kg spider/¹³⁷Cs Bq/kg soil). The values were 774, 960, and 1234, at Oguni, Benten-yama, and Nimaibashi, respectively.

Table 1. Radioactivity concentration ratio between soil and Nephila clavata or Atypus karschi. To calculate the concentration ratio, the spider’s radioactivity, as shown in Table 3b, was divided by the corresponding soil radioactivity data shown in Table 6. The results obtained using the ¹³⁴Cs and ¹³⁷Cs data were almost the same (data not shown)

Species	Sampling place (Sample no. in Table 3)	Ratio of the radioactivity concentrations: Spider (Bq/kg)/Soil (Bq/kg)		^110mAg : ¹³⁷Cs ratio (a)/(b)
Species	Sampling place (Sample no. in Table 3)	^110mAg (a)	¹³⁷Cs (b)	^110mAg : ¹³⁷Cs ratio (a)/(b)
Nephila clavata
	Oguni (2)	27.8	0.036	774
	Benten-yama (1)	74.5	0.078	960
	Nimaibashi (3)	87.3	0.071	1234
Atypus karschi
	Benten-yama (16)	448	1.30	344
	Iitoi (14)	166	0.45	369

We also measured the radioactivity concentration ratio in A. karschi living only on the soil surface as a ground spider, which would have received ^110mAg directly from the soil-based food chain, while N. clavata resides in aerial webs mainly depending on flying preys. As shown in Table 1, the concentration ratios of ^110mAg and ¹³⁷Cs in A. karschi in samples collected at Benten-yama and Iitoi were 448 and 166, and 1.30 and 0.45, respectively, corresponding to ^110mAg to ¹³⁷Cs radioactivity concentration ratios of 344 and 369 (Table 1). Thus, in both spider species, the concentration ratio of radioactive ^110mAg was two–three orders higher than that of ¹³⁷Cs.

Distribution of radionuclides in the body, thread, excrement, and egg sac of N. clavata.

Figure 3 shows the lifestyle of the female N. clavata spiders in the U8-cups. All N. clavata collected from Hiso on Oct. 13, 2013 were pregnant. During starvation in the U8-cups incubated at room temperature, one N. clavata delivered one egg sac containing many larval spiders (Fig. 3a). The egg sac was covered with a silky thread and hung on the web strung across the cup interior (Fig. 3d). Table 2 shows that the spider’s body and excrement contained equivalent concentrations of ^110mAg, whereas the concentration in the egg sacs was more than twofold higher. Web silk did not contain ^110mAg. However, the concentration of ¹³⁷Cs (and ¹³⁴Cs) in the spiders’ body and thread was nearly the same. Cesium might be incorporated as a contaminant into thread, replacing potassium. Spider excrement contained 4.5 times more ¹³⁷Cs (and ¹³⁴Cs) than measured in the spider body. Concentrated radioactivity was observed possibly at the midgut gland of N. clavata, while with lower concentrations of radioactivity in other body parts (Fig. 4).

Fig. 3.

N. clavata. a: egg sac; b: web threads collected from the spiders; c: feces and urine collected from the spiders; d: dead body of N. clavata after release of the egg sac. An egg sac covered with a silky thread is shown. These threads usually had adhered dried residual materials. e: N. clavata during pregnancy.

Table 2. Distribution of radionuclides derived from Nephila clavata into four parts. It was sampled at Hiso on Oct. 13, 2013 (sample no. 9 in Table 3). See the culture conditions of N. clavata in the U8-cup in the Materials and methods. Figures of each part are shown in Fig. 3

N. clavata	Radioactivity (Bq/kg)
N. clavata	^110mAg	¹³⁴Cs	¹³⁷Cs
Whole body	78.5	546	1339
Excrement (feces + urine)	70.1	2480	6040
Thread	n.d.	756	1330
Egg sacs	150	155	395

n.d.: not detected.

Fig. 4.

Autoradiograph of Nephila clavata. Collected at Nimaibashi on Sep. 20, 2011 (A) and at Hiso on Oct. 13, 2014. Sample A contained ^110mAg, but sample B did not.

Radionuclide contents in N. clavata during the 3.5 years after the NPP accident.

Figure 5 shows the trend in the radionuclide contents of N. clavata over the sampling period. Although the dates and sites of N. clavata collection differed, the concentration of ^110mAg in the spiders clearly decreased rapidly within 3.5 years after the NPP accident, except in sample no. 11, which still had a detectable amount of ^110mAg and a very high amount of ¹³⁷Cs (and ¹³⁴Cs). This sample was collected at Tsushima, where aerial doses were higher (8.2 µSv/h) than those (1.3–4.6 µSv/h) at other sampling sites (Table 3a).

Fig. 5.

Decay of ^110mAg (red), ¹³⁴Cs (green), and ¹³⁷Cs (blue) over time in Nephila clavata. The data shown in Table 3a (sample nos. 1–12) were used. Spiders 1–4, 5–8, 9, 10, and 11, 12 were collected in 2011, 2012, 2013 and 2014, respectively. Sample 11 was collected on Oct. 13, 2014 from Tsushima in Namie town, where researchers were not permitted to enter for 3 years after the NPP disaster because of the high level of aerial radiation.

Table 3a. Radioactivity of faunal species collected from Sept. 20, 2011 to Nov. 3, 2014 at the sampling sites. Indicated number of animals in each sample was put together in a cup and measured

Sample number	Faunal species	Number of measured samples	Radioactivity (Bq/kgDW)			Date of sampling	Sampling place	Aerial dose (µSv/h)	¹³⁴Cs /¹³⁷Cs	^110mAg /¹³⁷Cs
Sample number	Faunal species	Number of measured samples	^110mAg	¹³⁴Cs	¹³⁷Cs	Date of sampling	Sampling place	Aerial dose (µSv/h)	¹³⁴Cs /¹³⁷Cs	^110mAg /¹³⁷Cs
1	Nephila clavata (silk spider)	5	731	989	1052	2011/9/20	Benten-yama	3.5	0.94	0.70
2	Nephila clavata (silk spider)	6	707	949	1180	2011/10/18	Oguni	2.1	0.80	0.60
3	Nephila clavata (silk spider)	6	1398	1559	2096	2011/11/9	Nimaibashi	3.2	0.74	0.67
4	Nephila clavata (silk spider)	10	400	980	1340	2011/11/9	Benten-yama	4.3	0.73	0.30
5	Nephila clavata (silk spider)	5	n.d.	772	1653	2012/7/11	Hiso	4.3	0.47	n.d.
6	Nephila clavata (silk spider)	4	n.d.	512	1093	2012/7/11	Hiso	4.6	0.47	n.d.
7	Nephila clavata (silk spider)	6	n.d.	538	1077	2012/7/11	Hiso	4.4	0.50	n.d.
8	Nephila clavata (silk spider)	3	226	993	2163	2012/7/11	Oguni	1.3	0.46	0.10
9	Nephila clavata (silk spider)	35	78.5	546	1339	2013/10/13	Hiso	4.5	0.41	0.059
10	Nephila clavata (silk spider)	14	48.4	107	385	2013/11/5	Hiso	3.5	0.28	0.13
11	Nephila clavata (silk spider)	4	139	2369	8965	2014/10/13	Tsushima	8.2	0.26	0.016
12	Nephila clavata (silk spider)	8	18.2	378	1395	2014/10/13	Hiso	3.1	0.27	0.013
13	Araneus ventricosus (Onigumo)	2	162	424	508	2011/11/9	Benten-yama	2.3	0.83	0.32
14	Atypus karschi (ground spider)	8	3211	6346	8016	2011/10/18	Iitoi	5.4	0.79	0.40
15	Atypus karschi (ground spider)	12	618	1912	3169	2012/5/5	Iitoi	4.5	0.60	0.20
16	Atypus karschi (ground spider)	10	2866	11464	17445	2012/5/1	Benten-yama	4.5	0.66	0.16
17	Atypus karschi (ground spider)	13	232	1383	2932	2013/6/5	Iitoi	3.7	0.47	0.079
18	Atypus karschi (ground spider)	4	n.d.	360	1206	2014/10/13	Iitoi	2.7	0.30	n.d.
19	Atypus karschi (ground spider)	4	86.8	513	1800	2014/11/2	Maeda	3.1	0.29	0.048
20	Atypus karschi (ground spider)	4	n.d.	436	686	2014/11/2	Iitoi	2.9	0.64	n.d.
21	Argiope amoena (Koganegumo)	10	140	174	436	2012/9/27	Miyuki-yama	4.6	0.40	0.32
22	Spider (Unknown)	1	182	1218	2506	2012/9/16	Hiso	4.2	0.49	0.073
23	Doricus herensis (Seaka-gomimushi)	6	491	1006	1271	2012/3/30	Benten-yama	2.5	0.79	0.39
24	Armadillidium vulgare (pill bug)	23	2099	8073	10759	2011/11/9	Iitoi	2.7	0.75	0.20
25	Armadillidium vulgare (pill bug)	25	3906	26734	34842	2011/11/9	Benten-yama	3.0	0.77	0.11
26	Aphaenogaster famelica (ant)	20	n.d.	11360	14768	2011/11/9	Maeda	4.2	0.77	n.d.
27	Aphaenogaster famelica (ant)	10	n.d.	6233	7672	2011/11/10	Benten-yama	2.8	0.81	n.d.
28	Aphaenogaster famelica (ant)	32	317	871	1271	2012/6/16	Ryozen	2.1	0.69	0.25
29	Oligochaeta (earthworm)	1	20.8	357	476	2011/11/9	Benten-yama	3.8	0.75	0.044
30	Euhadra (snail: Maimai)	43	3118	11466	14778	2012/7/12	Yamakiya	5.1	0.78	0.21
31	Bufo japonicus formosus (frog: Hikigaeru)	1	426	5709	12130	2012/6/15	Iitoi	5.5	0.47	0.035
32	Rana rugosa (frog: Tsuchigaeru)	5	206	17785	23544	2012/3/30	Iitoi	4.5	0.76	0.0087
33	Frog (unknown)	1	53	6519	18544	2013/6/5	Hiso	3.5	0.35	0.0029
34	Frog (unknown)	1	74.6	2584	7671	2013/11/10	Hiso	3.7	0.34	0.010
35	Lacertidae (lizard)	4	n.d.	11500	14700	2011/10/18	Iitoi	5.1	0.78	n.d.
36	Lacertidae (lizard)	3	n.d.	3300	4900	2012/9/27	Iitoi	4.5	0.67	n.d.
37	Lacertidae (lizard)	1	n.d.	431	1338	2014/10/13	Iitoi	2.7	0.32	n.d.
38	Elaphe climacophora (snake)^‡	1	18.2	274	504	2012/7/11	Oguni	2.2	0.54	0.036
39	Patanga japonica (locust)	8	25.7	816	829	2011/10/18	Nimaibashi	3.5	0.98	0.031
40	Patanga japonica (locust)	4	n.d.	111	251	2013/4/30	Oguni	2.3	0.44	n.d.
41	Diestrammena apicalis (Kamadouma)	4	65	1348	2563	2011/11/9	Benten-yama	2.2	0.53	0.025
42	Thereuonema tuberculata (millipede: Geji)	3	578	1724	2550	2011/11/9	Benten-yama	2.0	0.68	0.227
43	Meghimatium bilineatum (slug)^‡	5	165	2833	5095	2012/9/27	Oguni	3.4	0.56	0.032
44	Meghimatium bilineatum (slug)^‡	6	233	6856	13272	2012/7/11	Benten-yama	3.3	0.52	0.018
45	Allomylina dichotoma (female)(beetle)	1	n.d.	845	1445	2012/7/12	Benten-yama	1.4	0.58	n.d.
46	Allomylina dichotoma (male)(beetle)	1	n.d.	580	1007	2012/7/12	Benten-yama	1.3	0.58	n.d.
47	Cerambycidae (longicorn: Kamikiri)	1	n.d.	70.1	105	2012/8/16	Benten-yama	1.2	0.67	n.d.
48	Graptopsaltria nigrofuscata (Aburazemi)	10	n.d.	699	1196	2012/8/17	Benten-yama	1.5	0.58	n.d.
49	Pentatoma japonica (Kamemushi)	4	n.d.	129	207	2012/6/15	Maeda	4.0	0.62	n.d.
50	Vespa mandarinia (hornet: Suzumebachi)	4	273	8206	11320	2011/11/9	Iitoi	4.5	0.72	0.024
51	Apis cerana japonica Rad (honeybee)	7	n.d.	354	805	2013/6/5	Sasu	1.2	0.44	n.d.
52	Rhopalocera (butterfly: Unknown)	10	n.d.	91	250	2013/6/5	Usuishi	2.1	0.36	n.d.
53	Rhopalocera (butterfly: Monshirocyo)	5	n.d.	2418	3300	2011/11/10	Sasu	2.5	0.73	n.d.
54	Anotogaster sieboldii (dragonfly)	5	838	7980	18800	2012/8/17	Hiso	4.5	0.42	0.045
55	Sympetrum croceolum (dragonfly)	6	180	637	1490	2012/6/15	Sasu	2.5	0.43	0.12
56	Sympetrum frequens (dragonfly)	4	610	2755	3487	2011/9/20	Iitoi	5.2	0.79	0.17
57	Palaemon paucidens (river shrimp)	35	81.7	746	2387	2014/5/30	Nagadoro	6.2	0.31	0.034
58	Geothelphusa dehaani (crab: Sawagani)	3	162	172	230	2012/3/30	Hanami-yama	1.8	0.75	0.70
59	Geothelphusa dehaani (crab: Sawagani)	3	185	10800	30600	2014/5/30	Akougi	8.0	0.35	0.0060
60	Geothelphusa dehaani (crab: Sawagani)	5	664	5450	14100	2013/7/8	Hiso	5.5	0.39	0.047
61	Bellamya quadrata histrica (Tanishi)	12	10.2	246	483	2012/6/15	Benten-yama	1.0	0.51	0.021
62	Cybister japonicus (Gengoro)	8	46.7	142	257	2012/8/17	Benten-yama	1.2	0.55	0.18
63	tadpole^‡	86	n.d.	63.4	147.1	2013/6/5	Iitoi	3.0	0.43	n.d.
64	Cynops pyrrhogaster (Akaharaimori)	2	n.d.	484	1760	2014/10/13	Sasu	0.8	0.28	n.d.
65	Epimorpha (centipede: Mukade)	1	425	883	3289	2014/11/3	Akougi	6.9	0.27	0.13

^‡: measured without desiccation and expressed as Bq/kgFW. n.d.: not detected, not determined.

Amounts of ^110mAg, ¹³⁴Cs, and ¹³⁷Cs in various faunal species.

Table 3a shows the original ^110mAg, ¹³⁴Cs, and ¹³⁷Cs data obtained at the faunal sampling times between Sept. 20, 2011 and Nov. 3, 2014, and Table 3b presents the decay-corrected data of Table 3a with reference to March 15, 2011, when the NPP discharged gaseous materials and the plume spread to the northwest. The γ-ray peak patterns of most of the faunal samples collected in 2011–2012 were similar to that of N. clavata (Fig. 2, Table 3a). As shown in the column “^110mAg Bq/kg” of Table 3b, silk spiders (sample no. 11), ground spiders (14, 16), pill bugs (24, 25), snails (30), dragonflies (54), crabs (60) and centipede (65) contained more than 5000 Bq/kg, whereas silk spiders (1, 2, 3, 4), ground spiders (15, 17, 19), other spiders (21, 22), the beetle Seaka-gomimushi (23), ants (28), frogs (34), millipedes (42), slugs (44), dragonflies (56), and river shrimp (57) contained 1000–5000 ^110mAg Bq/kg. In contrast, ^110mAg was not detectable in lizards, locusts, beetles, longicorn beetles, honeybees, butterflies, tadpoles, and newts, although ¹³⁷Cs (or ¹³⁴Cs) was detected in all of them. Table 3b also shows that ground spiders, pill bugs, ants, snails, frogs, lizards, slugs, hornets, crabs, and dragonflies contained more than 10,000 ¹³⁷Cs Bq/kg. The ^110mAg/¹³⁷Cs ratios of silk spiders, Argiope amoena, Seaka-gomimushi, millipedes, river shrimp, crabs, and the diving beetle Gengoro were above 1.0. Note that all of those species are members of Arthropoda.

Table 3b. Decay corrected data of Table 3a. All data of Table 3a was corrected following physical half-life of each nuclide to the date Mar. 15, 2011

Sample number	Faunal species	Bq/kgDW			^110mAg/¹³⁷Cs
Sample number	Faunal species	^110mAg	¹³⁴Cs	¹³⁷Cs	^110mAg/¹³⁷Cs
1	Nephila clavata (silk spider)	*1640	1293	1072	^†1.5
2	Nephila clavata (silk spider)	*1559	1286	1201	^†1.3
3	Nephila clavata (silk spider)	*3754	2163	2144	^†1.8
4	Nephila clavata (silk spider)	*1074	1360	1370	0.78
5	Nephila clavata (silk spider)	n.d.	1524	1709	n.d.
6	Nephila clavata (silk spider)	n.d.	1011	1130	n.d.
7	Nephila clavata (silk spider)	n.d.	878	1129	n.d.
8	Nephila clavata (silk spider)	986	1618	2237	0.44
9	Nephila clavata (silk spider)	n.d.	878	1129	n.d.
10	Nephila clavata (silk spider)	495	259	409	^†1.2
11	Nephila clavata (silk spider)	**5167	7852	9734	0.53
12	Nephila clavata (silk spider)	677	1253	1515	0.45
13	Araneus ventricosus (Onigumo)	344	544	517	0.67
14	Atypus karschi (ground spider)	**6811	8142	8154	0.84
15	Atypus karschi (ground spider)	*1955	2800	3253	0.61
16	Atypus karschi (ground spider)	**9852	17261	^#17942	0.55
17	Atypus karschi (ground spider)	*2089	2863	3082	0.68
18	Atypus karschi (ground spider)	n.d.	1193	1309	n.d.
19	Atypus karschi (ground spider)	*3832	1800	1960	2.0
20	Atypus karschi (ground spider)	n.d.	1630	784	n.d.
21	Argiope amoena (Koganegumo)	*1260	360	458	^†2.8
22	Spider (Unknown)	*1639	2523	2634	0.62
23	Doricus herensis (Seaka · gomimushi)	*1469	1447	1303	^†1.1
24	Armadillidium vulgare (pill bug)	**5482	11097	^#10997	0.50
25	Armadillidium vulgare (pill bug)	**13998	40812	^#35869	0.39
26	Aphaenogaster famelica (ant)	n.d.	14942	^#15049	n.d.
27	Aphaenogaster famelica (ant)	n.d.	9214	7831	n.d.
28	Aphaenogaster famelica (ant)	*1234	1366	1311	0.94
29	Oligochaeta (earthworm)	46	464	485	0.095
30	Euhadra (snail: Maimai)	**14504	19084	^#15304	0.95
31	Bufo japonicas (frog: Hikigaeru)	*5517	13341	^#12858	0.43
32	Rana rugosa (frog: Tsuchigaeru)	650	26026	^#24957	0.026
33	Frog (unknown)	778	15878	^#19713	0.039
34	Frog (unknown)	*1095	6294	8155	0.13
35	Lacertidae (lizard)	n.d.	13949	^#14926	n.d.
36	Lacertidae (lizard)	n.d.	5507	5320	n.d.
37	Lacertidae (lizard)	n.d.	1429	1452	n.d.
38	Elaphe climacophora (snake)^‡	85.8	458	522	0.16
39	Patanga japonica (locust)	57.6	1066	844	0.068
40	Patanga japonica (locust)	n.d.	236	264	n.d.
41	Diestrammena apicalis (Kamadouma)	382	2424	2668	0.14
42	Thereuonema tuberculata (millipede: Geji)	*3329	3080	2654	^†1.3
43	Meghimatium bilineatum (slug)^‡	932	5029	5300	0.18
44	Meghimatium bilineatum (slug)^‡	*1130	11570	^#13758	0.082
45	Allomylina dichotoma (female beetle)	n.d.	1413	1497	n.d.
46	Allomylina dichotoma (male beetle)	n.d.	970	1043	n.d.
47	Cerambycidae (longicorn)	n.d.	117	109	n.d.
48	Graptopsaltria nigrofuscata (Aburazemi)	n.d.	1503	1239	n.d.
49	Pentatoma japonica (Kamemushi)	n.d.	236	216	n.d.
50	Vespa mandarinia (hornet: Suzumebachi)	649	10933	^#11545	0.056
51	Apis cerana japonica Rad (honeybee)	n.d.	789	851	n.d.
52	Rhopalocera (butterfly: Unknown)	n.d.	206	264	n.d.
53	Rhopalocera (butterfly: Monshirocyo)	n.d.	4324	3434	n.d.
54	Anotogaster sieboldii (dragonfly)	**8177	16979	^#19774	0.41
55	Sympetrum croceolum (dragonfly)	849	1065	1543	0.55
56	Sympetrum frequens (dragonfly)	*3465	4899	3628	0.96
57	Palaemon paucidens (river shrimp)	*2688	2375	2585	^†1.0
58	Geothelphusa dehaani (crab: Sawagani)	970	311	240	^†4.0
59	Geothelphusa dehaani (crab: Sawagani)	4625	31384	32926	0.14
60	Geothelphusa dehaani (crab: Sawagani)	**11039	13825	^#15084	0.73
61	Bellamya quadrata histrica (Tanishi)	58.8	439	503	0.12
62	Cybister japonicus (Gengoro)	274	255	268	^†1.0
63	tadpole^‡	n.d.	135	155	n.d.
64	Cynops pyrrhogaster (newt: Akaharaimori)	n.d.	484	1760	n.d.
65	Epimorpha (centipede: Mukade)	**18782	3099	3595	^†5.2

*: 1000–5000 ^110mAg Bq/kg. **: >5000 ^110mAg Bq/kg. ^#: >10000 ¹³⁷Cs Bq/kg. ^†: >1.0 of ^110mAg/¹³⁷Cs. ^‡: expressed as Bq/kgFW. n.d.: not detected, not determined.

^110mAg/¹³⁷Cs ratio of feces and soil.

The feces of some of the fauna were collected and the radioactivity content was measured. As shown in Table 4, earthworms, lizards, Seaka-gomimushi, and dragonflies (Akiakane) concentrated ^110mAg in their feces, based on feces/soil radioactivity ratios of 15, 746, 45, and 101, respectively. The feces of earthworms, ground spiders, and lizards also contained ¹³⁷Cs (feces/soil ratios of 18, 19, and 4.3, respectively). The ^110mAg/¹³⁷Cs ratios in the feces of lizards and dragonflies were 0.23 and 0.46, respectively, which were two orders of magnitude higher than in any of the contaminated soils examined (see ^110mAg/¹³⁷Cs in Table 6). Thus, lizards and dragonflies concentrated large amounts of ^110mAg, which they ingested via the soil-based food chain.

Table 4. ^110mAg/¹³⁷Cs radioactivity ratio in the feces of some of the studied faunal species and the radioactivity concentration ratio for their feces vs. soil. All data are calculated after decay correction to the date Mar. 15, 2011

Feces secreted from fauna	Radioactivity (Bq/kg)			^110mAg/¹³⁷Cs	Sampling date	Radioactivity ratio feces/soil
Feces secreted from fauna	^110mAg	¹³⁴Cs	¹³⁷Cs	^110mAg/¹³⁷Cs	Sampling date	^110mAg	¹³⁴Cs	¹³⁷Cs
earthworm (1)	536	163000	267000	0.0020	2013/2/22	15	9.0	13
earthworm (2)	n.d.	569000	593000	n.d.	2011/10/18	n.d.	15	18
Atypus karschi	n.d.	271000	337000	n.d.	2011/10/18	n.d.	17	19
lizard	17700	58300	77100	0.23	2011/10/18	746	4.0	4.3
Seaka gomimushi	1460	20900	23500	0.062	2011/11/30	45	0.79	1.3
dragonfly	2510	4230	5420	0.46	2011/11/9	101	0.27	0.30
locust	n.d.	4480	4840	n.d.	2011/11/9	n.d.	0.17	0.17

n.d.: not detected, not determined. Earthworm (2), Atypus karschi and lizard correspond to no. 29, no. 14 and no. 35 in Table 3, respectively. Other specimens are different from those listed in Table 3.

Radionuclide contents of A. karschi during the 3.5 years after the NPP accident.

A. karschi was collected as the representative spider to monitor radionuclide accumulation in spider bodies in the area of Iitoi, Iitate village, from Oct. 18, 2011 to Oct. 13, 2014. As an inhabitant of the surface soil, A. karschi was assumed to more directly reflect soil radionuclides available through the food chain than N. clavata, which mostly resides in aerial webs. The fixed sampling site, where the aerial rate of radioactivity accumulation was 5.37 µSv/h on the first sampling date, Oct. 18, 2011, but had decreased to 2.75 µSv/h on the fourth sampling date, Oct. 13, 2014. As shown in Table 5, during the 6 months from Oct. 18, 2011 to May 5, 2012, the radioactivity of ^110mAg, ¹³⁴Cs, and ¹³⁷Cs decayed from 3211 to 618 Bq/kg, 6346 to 1912 Bq/kg, and 8016 to 3169 Bq/kg, respectively. If each radionuclide found in A. karschi on Oct. 18, 2011 had decayed following its physical half-life, then the values on May 5, 2012 should have been 1859, 5294, and 7916 Bq/kg, respectively. However, the detected radioactivity was far less. Moreover, on Oct. 13, 2014, ^110mAg was no longer detected in A. karschi, although ¹³⁷Cs and ¹³⁴Cs were still present in large amounts.

Table 5. Concentration of radionuclides in Atypus karschi during the 3.5 years after the NPP disaster. Sampling was carried out on Oct. 18, 2011, May 5, 2012, June 5, 2013, and Oct. 13, 2014 that correspond to the sample nos. 14, 15, 17 and 18 in Table 3a, respectively, at the fixed observation site in Iitoi. Parentheses indicate the calculated data based on the assumption that the radioactivity in the samples collected on the first sampling date (Oct. 18, 2011) decayed following the physical half-life of each radionuclide

Date of sampling	Radionuclides (Bq/kg)
Date of sampling	^110mAg	¹³⁴Cs	¹³⁷Cs
2011/10/18	3211	6346	8016
2012/5/5	618 (1859)	1912 (5294)	3169 (7916)
2013/6/5	232 (742)	1383 (3909)	2932 (7754)
2014/10/13	0 (144)	360 (2184)	1206 (7469)

Radioactivity in soils.

In contrast, the γ-ray traces of all surveyed soils showed very low peaks for ^110mAg. ^110mAg was detected in soils at concentrations between 22 and 238 Bq/kg (Table 6). For example, the radioactivity ratio of ^110mAg/¹³⁴Cs/¹³⁷Cs in Nimaibashi soil collected on the same day as N. clavata was 1/675/703, which was very different from that of N. clavata (1/1.12/1.50. See Results). The radioactivity ratio of ^110mAg/¹³⁷Cs was between 0.0014 and 0.0023. These values were almost the same as those of the riverbed sediments of the four sampling locations of Nitta River (0.0016–0.0036), Takanokura Dam (0.008) of the Nitta River, and Tetsuzen Dam (0.01) of Ota River.¹⁶⁾ These sampling places are located in Minamisoma city, Fukushima Prefecture and to the northwest from Fukushima Dai-ichi NPP. The almost constant ^110mAg/¹³⁷Cs ratios in those soils suggested that our research area (100 km × 60 km) was contaminated with ^110mAg and ¹³⁷Cs (and ¹³⁴Cs) all at once shortly after the release of huge amount of radioactivity on March 15, 2011, with contamination occurring by precipitation. Figure 6 shows the autoradiograph of the forest soil profile at Tsushima. Radioactivity is distributed within 2 cm of the top soil, which includes a litter layer of ∼1 cm at the surface.

Table 6. Concentration of soil radioactivity and the ^110mAg/¹³⁷Cs ratio. All data was corrected following physical half-life of each nuclide to the date Mar. 15, 2011

	Soils	Radioactivity (Bq/kg) in soils			^110mAg/¹³⁷Cs
	Soils	^110mAg	¹³⁴Cs	¹³⁷Cs	^110mAg/¹³⁷Cs
1	Oguni	56	32000	33400	0.0017
2	Hanami-yama	42	25600	26500	0.0016
3	Benten-yama	22	12900	13800	0.0016
4	Tsushima	238	105900	108000	0.0022
5	Iitoi	41	17200	18100	0.0023
6	Nimaibashi	43	29100	30300	0.0014
7	Hiso	37	18200	21300	0.0017

Fig. 6.

Radioactivity image of the forest soil profile of Tsushima. See the data for soil no. 4 in Table 6.

Discussion

During our field research on the contamination of flora in Ibaraki,²⁵⁾ and Fukushima,²⁶⁾ we coincidentally detected large amounts of ^110mAg in the spider N. clavata (Fig. 2). This finding was subsequently confirmed in other faunal species. Among the many species surveyed (Table 3a), those belonging to Arthropoda contained more ^110mAg and had a higher radioactivity ratio (^110mAg/¹³⁷Cs > 1) than faunal species from other phyla, when decay was corrected to the date of release of these radioactivity, March 15, 2011 (Table 3b). In contrast, ^110mAg concentrations in soils were very low, along with the ^110mAg/¹³⁷Cs ratio in soils (0.0014–0.0023) (Table 6) compared to the concentrations of these two radionuclides in all faunal species in which ^110mAg were detected (Table 3b).

In both spider species (N. clavata and A. karschi), the radioactivity concentration ratio of ^110mAg was three orders of magnitude higher than that of ¹³⁷Cs (Table 1). The most plausible explanation for this unexpected result is that ¹³⁷Cs was more rapidly bound to soil clay minerals, especially mica¹⁵⁾ or illite,²⁷⁾ than ^110mAg, resulting in less ¹³⁷Cs available to flora and/or fauna in the soil. Indeed, the ¹³⁷Cs content of most of the vegetables and rice in Fukushima Prefecture has decreased very quickly in the 3 years since the NPP accident.²⁸⁾ Alternatively, the Ag-transporter activity of both spiders may be much higher than their Cs-transporter activity, resulting in the more efficient uptake of ^110mAg. Otherwise, as mentioned later the binding activity of ^110mAg to hemocyanin in lymph fluid in both spiders may be very strong, thus ^110mAg may be more slowly metabolized than radioactive Cs to be excreted. Another explanation is that ^110mAg is more quickly turned over through the food chain to spiders in terrestrial environments than ¹³⁷Cs. To confirm the latter three possibilities will require advanced biochemical and molecular biological works on mineral (Ag and/or Cs) transporters in flora and fauna.

Although we could not segregate the radioactivity sources in the labeling image of N. clavata and thus unable to localize ^110mAg and ¹³⁷Cs (or ¹³⁴Cs) anatomically, the image shown in Fig. 4 suggests that ^110mAg is circulated in the lymph fluid, thus binding to hemocyanin, the O₂ carrier protein that also plays an important role in metal transport and distribution in decapod crustaceans.²⁹⁾ The trunk, head, and legs of N. clavata, as depicted in Fig. 4B, were probably labeled mainly with radioactive Cs. Autoradiographs (BAS-images) of many small animals collected from the contaminated field were taken by one of the authors (S. Mori) and published online.³⁰⁾^,³¹⁾ The muscles of frog and snake are very strongly labeled with radioactive Cs.³²⁾ These observations are consistent with the very low ^110mAg/¹³⁷Cs ratio of those fauna (see the ^110mAg/¹³⁷Cs ratio of snake no. 38 and frog nos. 32–34 in Table 3a).

The fact that the concentration of ^110mAg in the egg sac of N. clavata (Fig. 3a) was more than twice that of the spider’s body (Table 2) suggests that ^110mAg was transferred from the female spider to the egg sac. Because one egg sac incubates hundreds of larval spiders, separating them from the fragile sac after it was crushed was difficult (Fig. 3a). Thus, the portion of ^110mAg transferred from female spiders to its larvae could not be determined.

In Arthropoda and Mollusca that inhabit the sea, such as crab, octopus, and squid, etc., ^110mAg was suggested to replace copper in the active center of hemocyanin. It is reported that the regeneration of holohemocyanin by the combination of apoprotein with added cuprous chloride was inhibited by Ag⁺,³³⁾ although this has yet to be proven more directly using ^110mAg. The same may be true in the case of land fauna species living in freshwater, such as river shrimp, crab, and diving beetle Gengoro, whose ^110mAg contents and ^110mAg/¹³⁷Cs ratios were relatively high (Table 3). The amount of ^110mAg concentrated by phytoplankton or zooplankton may be a determining factor, as both would serve as the primary source of ^110mAg in the food chain of freshwater ecosystems. It was interesting that snail (sample no. 30 in Table 3) belonging to Mollusca had also relatively high ^110mAg content and ^110mAg/¹³⁷Cs ratio.

^110mAg was not detectable in lizards, locusts, beetles, longicorn beetles, honeybees, butterflies, tadpoles, and newts, which may have been due to very low Ag-transporter activity in the digestive organs of these species. The lizards were collected at the same fixed point where we also collected the ground spider A. karschi annually. As shown in Fig. 7, a major component of lizard feces comprised fragmented A. karschi. This spider highly concentrated ^110mAg in its body (sample nos. 14–20 in Table 3a), whereas the lizard did not (sample nos. 35–37 in Table 3a). This high amount of ^110mAg in the feces of lizards suggests that the lizards excreted highly concentrated ^110mAg without absorption of the radionuclide from the digested A. karschi. Thus, lizards may have very low intestinal Ag-transporter activity. A. karschi, however, almost completely absorbed ^110mAg into its body from unknown foods because no detectable ^110mAg was found in the feces of this spider (Table 4).

Fig. 7.

Body fragments of Atypus karschi were the major components of the feces of the lizards collected at the observation site in Iitoi. The digital microscopy photo was taken on Jan. 30, 2012.

The radioactivity image of the soil profile (Fig. 6) agrees with the results of Lepage et al.¹⁶⁾ (see Figs. 5, 7 and 8 in their recent report). Although we could not differentiate ^110mAg from ¹³⁷Cs and ¹³⁴Cs in the image, the three radionuclides seemed to have co-localized in the topsoil within a depth of 2 cm. Silver tends to concentrate in the surface litter plus humus horizon, suggesting that it mixes with organic matter. Increased acidity facilitates the removal of Ag from this horizon, whereas at a pH above 4, Ag is relatively immobile.³⁴⁾ If we define “the residence half time for ^110mAg in soil” as the time required for one-half of an acute ^110mAg deposit to pass through the soil layer of interest, the residence half time resulting from the migration velocity of Ag⁺ within the 5-cm soil top layer would be 33 ± 3 years.¹²⁾ Therefore, the vertical migration of ^110mAg may be highly dependent on the soil type.

This study shows that faunal concentrations of ^110mAg released during the Fukushima Dai-ichi NPP accident are decreasing more rapidly than the physical half-life of the radionuclide in the contaminated terrestrial environment of Fukushima (Fig. 5, Table 5). Due to the Chernobyl and Fukushima disasters, the precise physicochemical dynamics of radioactive Cs with soil minerals have received considerable attention from soil scientists around the world.¹⁵⁾^,²⁷⁾ However, studies on the biological dynamics of radioactive Cs in the “soil sphere” are lacking. Clarification of not only the physicochemical dynamics of soil minerals, but also the biological dynamics of ^110mAg in the “soil sphere”, will likely provide the information needed to explain why faunal concentrations of ^110mAg released by the Fukushima Dai-ichi NPP meltdown are decreasing faster through the food chain than predicted by their physical half-life.

Acknowledgments

We thank Prof. Naoko K. Nishizawa (Ishikawa Prefectural University) for critical reading of this manuscript, and Prof. Tomoko Nakanishi (The University of Tokyo) for supplying the facilities for radioisotope studies by S.M., and Mr. Masamichi Kagaya for assisting the sampling of faunal species and soils at Namie town. We are deeply indebted to the Aichi Steel Corporation for financial funding of this study.

References

1) Tanaka, S. (2012) Accident at the Fukushima Dai-ichi Nuclear power station of TEPCO. — Outline & lessons learned —. Proc. Jpn. Acad., Ser. B 88, 471–484.
2) MEXT (2011) Extension Site of the Distribution Map for Radiation Dose at http://ramap.jmc.or.jp/map/eng/, last accessed, Jan. 30, 2015.
3) Mori, S. (2011) http://moribin.blog114.fc2.com/blog-entry-1306.html, last accessed, Jan. 30, 2015 (in Japanese).
4) Seymour, A.H. (1963) Radioactivity of marine organisms from Guam, Palau and the Gulf of Siam, 1958–1959. In Radioecology (eds. Schultz, V. and Klement, A.W., Jr.). Reinhold, New York, pp. 151–157.
5) Folsom, T.R., Grismore, R. and Young, D.R. (1970) Long-lived γ-ray emitting nuclide silver-108m found in Pacific marine organisms and used for dating. Nature 227, 941–943.
6) Beresford, N.A. (1989) The transfer of Ag-110m to sheep tissues. Sci. Total Environ. 85, 81–90.
7) Boccolini, A., Gentilli, A., Guidi, P., Sabbatini, V. and Toso, A. (1988) Observations of silver-110m in the marine mollusc Pinna noblis. J. Environ. Radioact. 6, 191–193.
8) Boisson, F., Hutchinis, D.A., Fowler, S.W., Fisher, N.S. and Teyssie, J.-L. (1997) Influence of temperature on the accumulation and retention of 11 radio nuclides by the marine alga Fucus vesiculosus (L.). Mar. Pollut. Bull. 35, 313–321.
9) Zalewska, T. and Saniewski, M. (2011) Bioaccumulation of gamma emitting radionuclide in red algae from the Baltic Sea under laboratory conditions. Oceanologia 53, 631–650.
10) Jones, G.D., Forsyth, P.D. and Appleby, P.G. (1986) Observation of Ag-110m in Chernobyl fallout. Nature 322, 313.
11) Martin, C.J., Heaton, B. and Thompson, J. (1989) Cesium-137, ¹³⁴Cs and ^110mAg in lambs grazing pasture in NE Scotland contaminated by Chernobyl fallout. Health Phys. 56, 459–464.
12) Handl, J., Kallweit, E., Henning, M. and Szwec, L. (2000) On the long-term behaviour of ^110mAg in the soil-plant system and its transfer from feed to pig. J. Environ. Radioact. 48, 159–170.
13) Fukuda, T., Kino, Y., Abe, Y., Yamashiro, H., Kuwahara, Y., Nihei, H., Sano, Y., Irisawa, A., Shimura, T., Fukumoto, M., Shinoda, H., Obata, Y., Saigusa, S., Sekine, T., Isogai, E. and Fukumoto, M. (2013) Distribution of artificial radionuclides in abandoned cattle in the evacuation zone of the Fukushima Daiichi Nuclear Power Plant. PLoS ONE 8, e54312.
14) Ito, N. (2012) Conquest of the effects on agricultural products by the disaster of Fukushima No. 1 Nuclear Power Plant (NPP) — Studies on the active use of the contaminated livestock within 20 km area from NPP. Journal of the Japan Veterinary Medical Association 65, 645–652 (in Japanese).
15) Ogasawara, S., Nakao, A. and Yanai, J. (2013) Radiocesium interception potential (RIP) of smectic and kaolin reference minerals containing illite (micaceous mineral) as impurity. Soil Sci. Plant Nutr. 59, 852–857.
16) Lepage, H., Evrard, O., Onda, Y., Patin, J., Chartin, C., Lefèvre, I., Bonté, P. and Ayrault, S. (2014) Environmental mobility of ^110mAg: lessons learnt from Fukushima accident (Japan) and potential use for tracking the dispersion of contamination within coastal catchments. J. Environ. Radioact. 130, 44–55.
17) KEK (2011) http://legacy.kek.jp/quake/radmonitor/GeMonitor6.html, last accessed, Jan. 30, 2015 (in Japanese).
18) RIKEN (2011) http://www.radiochem.org/kinkyu/49.pdf, last accessed, Jan. 30, 2015.
19) UNSCEAR (2011) http://www.unscear.org/docs/reports/2013/UNSCEAR_2013A_B-1_CTBTO_particulates_air_2014-07.xlsx, last accessed, Jan. 30, 2015.
20) Povinec, P.P. (2013) Fukushima Dai-ichi Nuclear Power Plant. In Fukushima Accident: Radioactivity Impact on the Environment (eds. Povinec, P.P., Hirose, K. and Aoyama, M.). Elsevier, Amsterdam, pp. 31–54.
21) MEXT (2011) Preparation of Distribution Map of Radiation Doses, etc. (Maps of Concentration of Tellurium 129m and Silver 110m in Soil) by MEXT at http://radioactivity.nsr.go.jp/en/contents/5000/4168/24/1750_1031e_2.pdf, last accessed, Jan. 30, 2015.
22) Watanabe, T., Tsuchiya, N., Oura, Y., Inoue, C., Hirano, N., Yamada, R., Yamasaki, S., Okamoto, A., Nara, F.W. and Nunohara, K. (2012) Distribution of artificial radionuclides (^110mAg, ¹²⁹Te, ¹³⁴Cs, ¹³⁷Cs) in surface soils from Miyagi Prefecture, northeast Japan, following the 2011 Fukushima Dai-ichi nuclear power plant accident. Geochem. J. 46, 279–285.
23) Tazoe, H., Hosoda, M., Sorimachi, A., Nakata, A., Yoshida, M.A., Tokonami, S. and Yamada, M. (2012) Radioactive pollution from Fukushima Daiichi Nuclear Power Plant in the terrestrial environment. Radiat. Prot. Dosimetry 152, 198–203.
24) Petit, G.L., Douysset, G., Ducros, G., Gross, P., Achim, P., Monport, M., Raymond, P., Pontillon, Y., Jutier, C., Blanchard, X., Taffary, T. and Moulin, C. (2014) Analysis of radionuclide releases from the Fukushima Dai-Ichi Nuclear Power Plant Accident. Part I. Pure Appl. Geophys. 171, 629–644.
25) Mori, S., Hirato, A., Tanoi, K., Takeda, K., Yamakawa, T. and Nakanishi, H. (2012) Radioactive cesium flow in Rhus vernicifera. Soil Sci. Plant Nutr. 58, 611–617.
26) Nakanishi, H., Tanaka, H., Takeda, K., Tanoi, K., Hirose, A., Nagasaka, S., Yamakawa, T. and Mori, S. (2014) Radioactive cesium distribution in bamboo (Phyllostachy reticulate (Rupr) K. Koch) shoots after the TEPCO Fukushima Daiichi Nuclear Power Plant disaster. Soil Sci. Plant Nutr. 60, 801–808.
27) Vandebroek, L., Hees, M.V., Delvaux, B., Spaargaren, O. and Thiry, Y. (2012) Relevance of radio cesium interception potential (RIP) on a worldwide scale to assess soil vulnerability to ¹³⁷Cs contamination. J. Environ. Radioact. 104, 87–93.
28) Monitoring information by Fukushima Prefecture available at http://www.new-fukushima.jp/monitoring/en/, last accessed, Jan. 30, 2015.
29) Rtal, A., Nonnotte, L. and Truchot, J.P. (1996) Detoxification of exogenous copper by binding to hemolymph proteins in the shore crab, Carcinus maenas. Aquat. Toxicol. 36, 239–252.
30) Mori, S. (2013) http://moribin.blog114.fc2.com/blog-entry-1631.html, last accessed, Jan. 30, 2015 (in Japanese).
31) Mori, S. (2014) http://moribin.blog114.fc2.com/blog-entry-1907.html, last accessed, Jan. 30, 2015 (in Japanese).
32) Mori, S. (2014) Reconstruction of the destroyed agriculture with evolution of agricultural sciences. Trends in the Science 19 (7), 56–59 (in Japanese).
33) Moore, C.H., Henderson, R.W. and Nichol, L.W. (1968) An examination of the polymerization behavior of Jasus lalandii haemocyanin and its relation to the allosteric binding of oxygen. Biochemistry 7, 4075–4085.
34) Boyle, R.W. (1968) The geochemistry of silver and its deposits. Geological Survey of Canada Bulletin 160, Geological Survey of Canada, Ottawa.

Corresponding author

Register with J-STAGE for free!