Journal of Environmental Radioactivity 164 (2016) 104e112 Contents lists available at ScienceDirect Journal of Environmental Radioactivity journal homepage: www.elsevier.com/locate/jenvrad Radioactive contamination of arthropods from different trophic levels in hilly and mountainous areas after the Fukushima Daiichi nuclear power plant accident * Sota Tanaka a, 1, Kaho Hatakeyama a, 2, Sentaro Takahashi b,Taro^ Adati a, a Department of International Agricultural Development, Faculty of International Agriculture and Food Studies, Tokyo University of Agriculture, 1-1-1 Sakuragaoka, Setagaya, 156-8502 Tokyo, Japan b Division of Radiation Safety and Control, Kyoto University Research Reactor Institute, Kumatori, Sennan, Osaka 590-0494, Japan article info abstract Article history: In order to understand the influence of the Fukushima Daiichi nuclear power plant accident on the Received 12 April 2016 ecosystem in hilly and mountainous areas of Fukushima Prefecture, chronological changes in the levels of Received in revised form radiocesium in arthropod species were investigated. From 2012 to 2014, arthropods from different tro- 8 July 2016 phic levels were sampled and the air radiation dose rates at the sampling sites were analyzed. The air Accepted 11 July 2016 radiation dose rates showed a significant and constant reduction over the 2 years at the sampling sites in Fukushima. The median radiocesium concentration (134Cs þ 137Cs) detected in the rice grasshopper, Oxya yezoensis, and the Emma field cricket, Teleogryllus emma, dropped continuously to 0.080 and 0.078 Bq/g Keywords: fi Nuclear power plant accident fresh weight, respectively, in 2014. In contrast, no signi cant reduction in radioactive contamination was ^ Radiocesium observed in the Joro spider, Nephila clavata, in which the level remained at 0.204 Bq/g in 2014. A sig- Trophic level nificant positive correlation between radiocesium concentration and the air radiation dose rate was Grasshopper observed in the rice grasshopper, the Emma field cricket and the Joro^ spider. The highest correlation Cricket coefficient (r ¼ 0.946) was measured in the grasshopper. Spider © 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 1. Introduction are unstable even though surveys are conducted within a limited area and/or time span. This is likely due to Fukushima's ecological Five years after the accident at the Fukushima Daiichi nuclear characteristics which include a large proportion of hilly and power plant (hereafter referred to as FDNPP), approximately one mountainous regions, estimated at 82% of the prefectural area hundred thousand refugees remain unable to return home (Fukushima Prefectural Government, 2010). In fields backed by (Fukushima Prefectural Government, 2016), and many difficulties wooded hills or in small valleys, runoff from uphill can reconta- still exist for agricultural recovery in the disaster-affected areas. A minate the lowlands; however, there are still merits to conducting major factor behind this uninhabitability is the environmental measurements of the air radiation dose rate. These include the contamination by radionuclides, especially radioactive cesium as immediacy and convenience of estimating radioactive contamina- reported in several studies (e.g. Endo et al., 2013; Kamada et al., tion levels in the agroecosystem compared to measurements of soil 2012; Tsuiki and Maeda, 2012; Yoshihara et al., 2013). radionuclide deposition using a germanium semiconductor Although decontamination operations have continuously been detector. underway (Ministry of the Environment, 2016), their effects are Hilly and mountainous areas, as well as other farmlands in unstable. After decontamination, air radiation dose measurements Japan, are inhabited by a diverse range of organisms including aquatic and terrestrial animals, birds and plants, all of which are linked through their activities to the outside ecosystems. Arthro- * Corresponding author. pods in particular maintain relationships between multiple E-mail addresses: [email protected] (S. Tanaka), [email protected]. ecological guilds, such as terrestrial herbivores, omnivores, and jp (T. Adati). carnivores, through the food chain. In such an ecosystem, radio- 1 Present address: Division of Radiation Safety and Control, Kyoto University active contamination may differently influence the arthropod Research Reactor Institute, Kumatori, Sennan, Osaka 590-0494, Japan. 2 Present address: 38 Bakers Gully Road, Bight, Victoria 3741, Australia. species depending on their trophic level. By periodically http://dx.doi.org/10.1016/j.jenvrad.2016.07.017 0265-931X/© 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). S. Tanaka et al. / Journal of Environmental Radioactivity 164 (2016) 104e112 105 monitoring the amount of radionuclides in these arthropods, the Prefecture, at an altitude of 450e490 m and 40e46 km northwest overall dynamics of radionuclides within an ecosystem can be or north-northwest of the FDNPP. Site D, located in Kanagawa elucidated. If these data correlate with representative air radiation Prefecture about 270 km south-west of the FDNPP, was selected as doses, such as the mean and median values within that area, the control site. In the administrative division which includes sites arthropod species could be utilized as a novel environmental in- A and B, decontamination activities under the direct control of the dicator of radioactive contamination. Ministry of Environment began in September 2012, and by the end A high level of concern also exists pertaining to environmental of September 2014 included 14.4% of the target farmland and forest protection and the effects of radiation on wildlife. With regard to areas (Ministry of the Environment, 2014a, 2014b). In the subdivi- the influence of radioactive contamination in arthropods after the sion including site C, decontamination activities organized by the FDNPP accident, Møller et al. (2013) conducted field censuses of municipal office were carried out in paddy fields around the site birds and arthropods and reported a significant negative correla- beginning in November 2012 (Monma et al., 2015). Surveys were tion between animal population density and the air radiation dose carried out from September to October in 2012e2014. In 2012 and rate. Hiyama et al. (2012) reported that the lycaenid butterfly, 2013, surveys were conducted at all four sites, while the survey was Zizeeria maha, that emerged in contaminated areas in 2011 conducted only at site A in 2014. exhibited morphological abnormalities, and that those abnormal- ities were inherited by the next generation, which exhibited a fi higher proportion of abnormalities than the rst generation. 2.2. Air radiation dose rate Akimoto (2014) compared the morphology and viability of first instar nymphs in populations of gall-forming aphids from The air radiation dose rate at each site was measured with a NaI Fukushima and uncontaminated areas and found that the propor- (Tl) scintillation survey meter (Hitachi-Aloka TCS-172B) at a height fi tion of morphological abnormalities and mortality was signi cantly of 1 m above the ground surface. For each site, dose rates were higher in Fukushima populations than in those from control areas. measured at five points of approximately 20 m intervals in distance. Assuming these abnormalities are due to the FDNPP accident, the exposure dose rate should be estimated to clarify the effects of radiation on these organisms. In order to do so, the concentration of 2.3. Arthropod samples whole-organism radioactivity is the most important factor to quantify, as this parameter estimates the internal exposure of an At each sampling site, arthropods were collected by sweep-net individual organism (ICRP, 2009). sampling and hand collection. Samples were preserved in 70% Furthermore, radioactive contamination should be investigated ethanol in the field and refrigerated until sorted. Each sample was in multiple arthropod species belonging to different trophic levels identified and sorted by species. Prior to radioactive measurement, in the food web to determine the influence of the accident on the samples were weighed after air-drying for 10 min. regional ecosystem. From the 1970's to the early 1980's, in- vestigations into watershed contamination by effluents from a former reactor in the United States demonstrated a significant correlation between radiocesium concentrations in plants and ar- 2.4. Radioactive measurements thropods, suggesting producerÀherbivoreÀpredator associations in terrestrial and aquatic food webs (Anderson et al., 1973; Brisbin The radioactivity in arthropod samples was measured by et al., 1989). After the Chernobyl reactor accident in 1986, radio- gamma spectrometry with a high-purity germanium semi- cesium was detected in earthworms (142 Bq/kg fresh weight) and conductor detector (GC-2020, Canberra Industries) and a multi- in the Eurasian woodcock (730 Bq/kg fresh weight) that fed on channel analyzer (DSA1000, Canberra Industries) for 3600 to fi earthworms in Norway (Kålås et al., 1994). However, few field 10,800 s. The counting ef ciency of the detector was determined by fi studies have been conducted which analyze radioactive contami- measuring a certi ed mixed radioactive standard gamma volume nation in sympatric arthropod species with different food habits, source