Radioactive Cesium Contamination of Arthropods and Earthworms After the Fukushima Daiichi Nuclear Power Plant Accident

To understand the behavior of radioactive cesium ( 134 Cs+ 137 Cs) in terrestrial invertebrates, chronological changes in the concentration of radioactive Cs in arthropods from different trophic levels were investigated after the Fukushima Daiichi Nuclear Power Plant accident. In addition, the level of radioactive Cs in earthworms, representing the detritivores, was also investigated. The median radioactive Cs concentration in the rice grasshopper ( Oxya yezoensis ) and the Emma field cricket ( Teleogryllus emma ) was 0.46 and 0.15 Bq/g fresh weight (fw) in 2012, respectively, which dropped continuously to 0.05 and 0.01 Bq/g fw in 2016. In contrast, no significant reduction in radioactive Cs concentration was observed in the Jorô spider ( Nephila clavata ) in which the concentration was 0.31 Bq/g fw in 2012 and remained at 0.14 Bq/g fw in 2016. The comparison of radioactive Cs concentration at each trophic level showed that the amount in detritivorous earthworms was 85 times higher than in herbivorous grasshoppers. This suggests that detritus food web could be a primary pathway for migration of radioactive Cs through food webs.


Introduction
The accident at TEPCO's Fukushima Daiichi Nuclear Power Plant (FNPP) caused serious radioactive contamination across a wide area of eastern Japan. There is concern about the effect on the environment of cesium-134 ( 134 Cs) and Cs-137 ( 137 Cs), with the relatively long half-life ( 134 Cs, 2.06 years; 137 Cs, 30.17 years). In Fukushima Prefecture, approximately 71% of the total land area is covered with forests [1]. Therefore, a large proportion of the radioactive Cs ( 134 Cs+ 137 Cs) released into the atmosphere was deposited onto the forested areas. Over time, the radioactive Cs accumulates in the soil surface layer and is maintained long-term in the soil organic layer. Thus, the organic layer of soil represents a major pool of radioactive Cs in forest ecosystems [2]. Radioactive Cs can then circulate throughout the forest ecosystem by biological processes [3] as is in the same elemental family as potassium, an essential element for all organisms.
Arthropods have a large biomass and are important food sources for other organisms such as birds, amphibians, reptiles and mammals. Terrestrial arthropods are also important seasonal diets for freshwater fishes such as trout [4,5] and act as a trophic linkage across the forest-stream ecosystem [6]. This supports the hypothesis that terrestrial arthropods could be a carrier of radioactive Cs throughout the food web and a route of transfer or radioactive Cs between the forest and aquatic ecosystems.
Earthworms function as ecosystem engineers [7] to produce a homogenized organic soil layer. This bioturbation activity is an important factor in the long-term behavior of radioactive Cs in the soil [8]. Earthworms are also important food resources for various organisms. Therefore, determining radioactive Cs concentration in arthropods and earthworms is important for understanding the long-term behavior of radioactive Cs in the ecosystem and for radiation risk assessment for non-human species. However, the number of reports on radioactive contamination in arthropods and earthworms after the FNPP accident is limited (Table 4.1) [9][10][11][12][13][14][15][16][17][18][19].
We reported the chronological changes in radioactive Cs levels in common terrestrial arthropod species from different trophic levels after the FNPP accident. The report showed a continuous annual reduction of radioactive Cs in herbivorous grasshoppers and omnivorous crickets, in contrast to carnivorous spiders in which no significant reduction in radioactive Cs was observed from 2012 to 2014. These differences in radioactive Cs at each trophic level over time suggest that the level of contamination of the varied food resource pathways is different [15].
The present study shows the latest data on the chronological changes of radioactive Cs concentration in the arthropods over the 5-year period from 2012 to 2016. Furthermore, in order to investigate the detritus food web which has been suggested to act a major transfer pathway of radioactive Cs in the food web [10,16], detritivorous earthworms were investigated in 2014, and radioactive Cs concentration among species with different feeding habits was compared.

Sampling Site and Measurement of Ambient Dose Equivalent Rate
The sampling site is located 40.1 km northwest of FNPP (latitude, 37°41′35″ N; longitude, 140°44′08″ E; Fig. 4.1). This area is composed of a hilly and mountainous landscape with agricultural fields and residential areas surrounded by mountainous forests. Residents were still not permitted to live in this area during the study period from 2012 to 2016. Ambient dose equivalent rate was measured at multiple points on the sampling site using a NaI scintillation survey meter (TCS171, Hitachi, Ltd., Japan) placed 1 m above the ground, and the distance of each measurement point was at least 20 m.

Sampling of Arthropods and Earthworms
Three arthropod species, the rice grasshopper (Oxya yezoensis), the Emma field cricket (Teleogryllus emma) and the Jorô spider (Nephila clavata) were collected by sweep-net sampling and hand collection from September to October of each year between 2012 and 2016. For each arthropod species, we collected 20-200 individuals each year. Epigeic earthworms were collected by hand collection in October  [19] 2014. All of the sampled arthropods and earthworms experience a generational turnover once a year.

Measurement of Radioactive Cs Levels in Samples
Gamma-ray spectrometry was conducted using a high-purity germanium detector (GC-2020, Canberra Industries, and GEM30-70, ORTEC, USA) with a multichannel analyzer (MCA, DAS1000, Canberra Industries, and Easy-MCA-8k, ORTEC, USA). The counting efficiency of the detector was determined by measuring a certified mixed radioactive standard gamma volume source (MX033SPLU8, Japan Radioisotope Association, and 24FY039, Japan Chemical Analysis Center). All samples were placed into 100 ml plastic containers (U-8), and the radioactivity of the samples was obtained as Bq/g fresh weight (Bq/g fw).

Statistical Analyses
For changes in ambient dose equivalent rate and radioactive Cs concentration in arthropods and earthworms, the lower (Q 1 ) and upper (Q 3 ) quartiles and the interquartile range (IQR = Q 3− Q 1 ) were calculated. Differences in the values among years were analyzed with a Kruskal-Wallis test using R version 2.15.3 [20].

Ambient Dose Equivalent Rates at the Sampling Site
Ambient dose equivalent rate at the sampling site is shown in Fig. 4

Chronological Changes in Radioactive Cs Levels in Arthropods
The change in radioactive Cs concentration in three arthropod species over the 5-year investigation is shown in Fig. 4.3. The median concentration of radioactive Cs in grasshoppers significantly decreased from 0.46 to 0.05 Bq/g fw between 2012 and 2016 (Kruskal-Wallis test, P < 0.05; Fig. 4.3A). Field crickets also showed a significant decrease in radioactive Cs concentration from 0.15 to 0.01 Bq/g fw (P < 0.05; Fig. 4.3B). In contrast, the median concentration of radioactive Cs in Jorô spiders was not significantly different during the survey period (P = 0.14; Fig. 4

Comparison Between Different Feeding Habits and 137 Cs Concentration
Radioactive Cs concentration in grasshoppers, field crickets, Jorô spiders and earthworms was compared in 2014. The median of 137 Cs concentration in earthworms was 4.87 Bq/g fw, which was about 85 times higher than that of grasshoppers, and over 30 times higher than that of Jorô spiders, which showed the highest level of radioactive Cs among the three arthropod species examined (Fig. 4.4).

Discussion
The ambient dose equivalent rate at the sampling site significantly decreased from 2012 to 2016. The γ-ray contribution of 134 Cs to ambient dose equivalent rate is higher than 137 Cs [21], and the physical half-life of 134 Cs is shorter than that of 137 Cs. Therefore, the reduction in the ambient equivalent dose rate during the initial phase after the accident determined in the present study is mainly attributed to the physical half-life of 134 Cs, although the weathering effect may also contribute to the decrease. From 2015 to 2016, the decrease in ambient equivalent dose rate at the sampling site was only 4%, which was lower than the 29% decrease during the initial phase from 2012 to 2013. This suggests that the yearly rate of decrease in the ambient dose equivalent rate at the time of this study will remain for a long time even at the low levels.
The median radioactive Cs concentration in the grasshoppers and field cricket significantly decreased from 2012 to 2016. In contrast, the concentration in Jorô spiders did not differ significantly during the survey period. These trends are consistent with our previous report from 2012 to 2014 [15]. The radioactive Cs concentration in Jorô spiders showed relatively wide variation during the 5-year sampling period, and the median radioactive Cs concentration in Jorô spiders remained at 52% between 2012 and 2016. Different food resource pathways, such as grazing and detrital food web, likely caused this trend [22]. As herbivorous, grasshoppers rely on the grazing food web, and their radioactive Cs concentration showed a rapid decrease. These indicate that radioactive Cs transfer from the grazing food web is not a dominant long-term contributor in grasshoppers. In contrast, carnivorous web spiders rely on both the grazing and detritus food webs due to the variety of prey items captured by their orb web. The variation in radioactive Cs in Jorô spiders during the 5-year survey period indicated that they use both the grazing and detritus food webs. The relationship between feeding habits and radioactive Cs levels showed that earthworms, representing the detritivores, had radioactive Cs levels about 85 times higher than grasshoppers which rely on the grazing food web. We reported that the 137 Cs concentration in the earthworms remained stable from 2014 to 2016 [19]. These findings clearly indicate that the detritus food web is more highly contaminated than the grazing food web. High levels of 137 Cs accumulation flow up to higher trophic levels through the detritus food web [10]. Therefore, the high levels of radioactive Cs concentration maintained in Jorô spiders during this study period could be explained by their food resources coming from the contaminated detritus food web. In forests, the biomass of aerial insects from the detrital food web increases in spring and autumn, and web spider depends on these aerial insects [23]. In the present study, Jorô spiders were collected in autumn between September and October; thus the food resources of Jorô spiders were relatively dependent on the detritus food web during the collection period. This study thus demonstrates that the detritus food web is the primary pathway for long-term movement of radioactive Cs through the food web. Moreover, the detritus food web makes a large contribution to the transfer and circulation of radioactive Cs within the ecosystem. From a long-term perspective, the behavior of radioactive Cs through the food web, including these invertebrate species, is important for understanding the environmental behavior of radioactive Cs and accurate radiation risk assessment for non-human species.

Conclusions
A 5-year study in arthropods showed variations in the chronological change of radioactive Cs concentration levels among arthropods of different trophic levels. The radioactive Cs concentration in both herbivorous grasshoppers and omnivorous field crickets significantly reduced from 2012 to 2016. In contrast, the level in carnivorous Jorô spiders did not change significantly during the survey period. This variance is likely caused by the difference in food resource pathways between the grazing food web and the detritus food web (Fig. 4.5). Detritivorous earthworms showed the highest radioactive Cs concentration, and the comparison between trophic levels and radioactive Cs concentration clearly showed high contamination in the detritus food web. This study demonstrates that the detritus food web is the primary pathway for long-term radioactive Cs movement through the food web. Long-term monitoring of terrestrial invertebrates is thus necessary to understand the behavior of radioactive Cs in the ecosystem and to contribute to risk assessment for non-human species. Transfer pathways of radioactive Cs in terrestrial invertebrates. Each species represents feeding habits of terrestrial invertebrates; thus each species does not always prey on each other directly. For example, web spider cannot prey earthworm, but they can prey detritivores such as flies (Diptera) which emerge from the same habitat of earthworm. Therefore, earthworm represents radioactive Cs contamination in detritivores, and the other three species also represent the contamination of each feeding habit Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.
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