The biological impacts of ingested radioactive materials on the pale grass blue butterfly

OPEN SUBJECT AREAS: ENVIRONMENTAL SCIENCES RISK FACTORS ENVIRONMENTAL HEALTH The biological impacts of ingested radioactive materials on the pale grass blue butterfly Chiyo Nohara1, Atsuki Hiyama1, Wataru Taira1, Akira Tanahara2 & Joji M. Otaki1 1 Received 17 January 2014 Accepted 22 April 2014 Published 15 May 2014 Correspondence and requests for materials should be addressed to J.M.O. () The BCPH Unit of Molecular Physiology, Department of Chemistry, Biology and Marine Science, Faculty of Science, 2Instrumental Research Center, University of the Ryukyus, Okinawa 903-0213, Japan. A massive amount of radioactive materials has been released into the environment by the Fukushima Dai-ichi Nuclear Power Plant accident, but its biological impacts have rarely been examined. Here, we have quantitatively evaluated the relationship between the dose of ingested radioactive cesium and mortality and abnormality rates using the pale grass blue butterfly, Zizeeria maha. When larvae from Okinawa, which is likely the least polluted locality in Japan, were fed leaves collected from polluted localities, mortality and abnormality rates increased sharply at low doses in response to the ingested cesium dose. This dose-response relationship was best fitted by power function models, which indicated that the half lethal and abnormal doses were 1.9 and 0.76 Bq per larva, corresponding to 54,000 and 22,000 Bq per kilogram body weight, respectively. Both the retention of radioactive cesium in a pupa relative to the ingested dose throughout the larval stage and the accumulation of radioactive cesium in a pupa relative to the activity concentration in a diet were highest at the lowest level of cesium ingested. We conclude that the risk of ingesting a polluted diet is realistic, at least for this butterfly, and likely for certain other organisms living in the polluted area. E nvironmental pollution by artificial radionuclides released from the collapsed Fukushima Dai-ichi Nuclear Power Plant (NPP) has often been evaluated based on radioactivity concentrations in environmental samples collected from the polluted area, such as soil and forest litter1–3. The accumulation of radionuclides in the bodies of wild and domesticated organisms and in agricultural products has also been documented4–11. However, the biological impacts of this pollution on the health and disease of wild organisms have not been examined sufficiently. A field study indicated that the abundance of insects, especially butterflies, has decreased12,13, suggesting that the pollution might have had a fatal effect on butterflies. Another study indicated a high incidence of morphological abnormality in gall-forming aphids14. Consistent with these studies, we have demonstrated that the Japanese pale grass blue butterfly, Zizeeria maha (Yamato shijimi in Japanese), was affected physiologically and genetically in the polluted area, likely due to the artificial radionuclides released from the Fukushima Daiichi NPP15,16. In one of a series of experiments, we have shown a decrease in the survival rate of this butterfly in accordance with the level of radioactivity of cesium in the diet (i.e., the leaves of the host plant, Oxalis corniculata)15,16 under our standard rearing conditions17. In this experiment, host plant leaves were collected from 5 different localities with different pollution levels (Ube, Hirono, Fukushima, Iitate-flatland, and Iitate-montane) (Table 1) and were given to larvae that were obtained in the laboratory from field-caught females from Okinawa15, which is likely the least polluted locality in Japan. However, the amount of food and the dose of artificial radioactive cesium ingested by these larvae remain to be determined. Furthermore, the amount of radioactivity retained and accumulated by pupae has not been examined. In the present study, we quantified the amount of radioactive cesium consumed by larvae over their lifetimes. Based on these data, simple mathematical models were employed to obtain the radioactive cesium doses resulting in a 50% mortality rate and a 50% abnormality rate. We also quantified how much radioactive cesium was retained and accumulated in pupae. Finally, we discussed the possible risks of a polluted diet for butterflies and other organisms living in the polluted area. Results Quantification of ingested doses. We first investigated the leaf weight consumed by larvae in the larval stage (Fig. 1). Dietary consumption curves for 5 larvae were largely sigmoidal: approximately 4 days before reaching the SCIENTIFIC REPORTS | 4 : 4946 | DOI: 10.1038/srep04946 1 www.nature.com/scientificreports Table 1 | Summary of data for the internal exposure experiment*1 Ube Hirono Fukushima Iitate-flatland Iitate-montane Distance from the NPP [km] 966.0 20.7 61.1 40.0 33.7 Collection site for the host Higashisue, Oaza Futatsunuma Park Takahata (Okabe); Ainosawa Campsite; Nagadoro plant (Kounan-kita) Hanamiyama Omori Fukaya; Onishi Iitoi Collection prefecture for Yamaguchi Prefecture Fukushima Prefecture the host plant Collection site for the pale Nishihara, Okinawa Island, Okinawa Prefecture grass blue butterfly Ground radiation 0.18 1.06 3.57 6.22 18.9 dose [mSv/h] 2.33 (60.01) 3 104 Activity of 137Cs in the host 5.4 (60.2) 3 1021 7.79 (60.08) 3 102 4.21 (60.04) 3 103 5.47 (60.05) 3 103 2 plant [Bq/kg]* Activity of 134Cs in the host 4.5 (60.1) 3 1021 6.73 (60.07) 3 102 3.65 (60.03) 3 103 4.70 (60.05) 3 103 2.02 (60.01) 3 104 plant [Bq/kg]*2 Summation of cesium 0.99 1,452 7,860 10,170 43,500 activity in the host plant [Bq/kg] 85 108 100 103 Number of larvae reared 146*3 Number of pupae 154 58 70 67 81 obtained Number of adults eclosed 139 62 53 41 56 0.035 6 0.005 0.037 6 0.006 0.033 6 0.006 0.029 6 0.007 0.033 6 0.008 Average pupal weight 6 SD [g]*4 Total leaves ingested per 0.39 0.42 0.37 0.33 0.37 larva [g] 0.38 0.40 0.36 0.32 0.36 Contaminated leaves ingested per larva [g]*5 Radiation dose ingested 0.00038 0.58 2.8 3.3 16 per larva [Bq] 0.048 0.23 0.28 1.3 Dose rate of ingestion per 3.2 3 1025 day per larva [Bq/d] Mortality rate [%] 4.8 31.8 58.3 63.0 46.6 Abnormality rate [%] 6.2 45.9 73.1 75.0 72.8 *1. Part of this information is also available in Supplementary Table 8 in Hiyama et al. (2012)15. *2. Activity values at the time of larval ingestion (fixed at 22 July 2011 for simplicity) were calculated based on measured values obtained on 26 December 2011 as shown in Hiyama et al. (2012)15, assuming that 137Cs and 134Cs were released at a 151 activity ratio on 15 March 2011 in a single burst from the Fukushima Dai-ichi NPP. *3. This number was underestimated because larvae not counted at the earlier stage were found later. *4. Pupal weight was measured within 24 hours postpupation. *5. Because leaves from the 5 localities were given from the 6th day post-hatching, the ingested contaminated leaves correspond to 97.16% of the total amount of leaves ingested. 100% consumption level, the amount of i (...truncated)