Ingestional and transgenerational effects of the Fukushima nuclear accident on the pale grass blue butterfly

Abstract

One important public concern in Japan is the potential health effects on animals and humans that live in the Tohoku-Kanto districts associated with the ingestion of foods contaminated with artificial radionuclides from the collapsed Fukushima Dai-ichi Nuclear Power Plant. Additionally, transgenerational or heritable effects of radiation exposure are also important public concerns because these effects could cause long-term changes in animal and human populations. Here, we concisely review our findings and implications related to the ingestional and transgenerational effects of radiation exposure on the pale grass blue butterfly, Zizeeria maha, which coexists with humans. The butterfly larval ingestion of contaminated leaves found in areas of human habitation, even at low doses, resulted in morphological abnormalities and death for some individuals, whereas other individuals were not affected, at least morphologically. This variable sensitivity serves as a basis for the adaptive evolution of radiation resistance. The distribution of abnormality and mortality rates from low to high doses fits well with a Weibull function model or a power function model. The offspring generated by morphologically normal individuals that consumed contaminated leaves exhibited high mortality rates when fed contaminated leaves; importantly, low mortality rates were restored when they were fed non-contaminated leaves. Our field monitoring over 3 years (2011-2013) indicated that abnormality and mortality rates peaked primarily in the fall of 2011 and decreased afterwards to normal levels. These findings indicate high impacts of early exposure and transgenerationally accumulated radiation effects over a specific period; however, the population regained normality relatively quickly after ∼15 generations within 3 years.

Keywords: Fukushima nuclear accident; adaptive evolution; ingestional effect; internal exposure; natural selection; pale grass blue butterfly; radiation resistance; radiation sensitivity; transgenerational effect.

Fig. 1.

Pale grass blue butterfly in the Tohoku district. (a) A pair of pale grass blue butterflies in Minami-soma City, Fukushima Prefecture. Pictured in August 2014. (b) An adult individual caught in Okuma Town, Fukushima Prefecture and pictured in the laboratory, Okinawa Prefecture. Pictured in August 2014. (c) A pair of pale grass blue butterflies in Yuriage, Natori City, Miyagi Prefecture. Pictured in May 2013.

Fig. 2.

Pale grass blue butterfly and its host plant in Okinawa (Nanjo City) in August 2015. (a, b) A typical habitat, where numerous butterflies are found: the ground is stony and covered with the host plant. (c) A male butterfly flying close to the ground of the host plant field (red arrow). The butterfly is flying at the height of the shoes of the photographer. The shadow of the photographer (who is standing straight) can be observed. (d) The host plant with a hand of the photographer, indicating the size of the plant. (e, f) A female butterfly in this habitat.

Fig. 3.

Survival rate (percentage survival) of the internal exposure experiments. (a) The effects on the first generation, which include relatively high contamination levels [34] (the first set of experiments, shown in dark blue bars) and relatively low contamination levels [38] (the second set of experiments, shown in light blue bars). (b) The effects on the second generation [38]. For example, ‘O-K’ indicates that leaves from Okinawa were given in the first generation (defined as F₁) and leaves from Koriyama were given in the second generation (defined as F₂).

Fig. 4.

Time course of the three types of ‘abnormality rates’ (percentage abnormal) of butterflies from Fukushima City over 3 years (2011–2013). Peaks in abnormality rates are present in the fall of 2011 and the spring of 2012. All of the abnormality rates then decrease to a normal level. The normal abnormality rates of adults are ∼10% or less [36, 39]. In Hiyama et al. (2015) [39], ‘morphological abnormalities of field-caught adults’ is defined as the ‘adult abnormality rate of the P generation’ or ‘aAR(P)’. ‘Morphological abnormalities of adults in the offspring generation’ is defined as the ‘adult abnormality rate of the F₁ generation’ or ‘aAR(F₁)’. ‘Deaths of larvae, prepupae and pupae and morphological abnormalities of adults in the offspring generation’ is defined as the ‘total abnormality rate’ or ‘tAR(F₁)’.

Fig. 5.

Interpretations of morphological examinations. (a) Judgment criteria regarding the nature of damage based on the generations examined. All of the morphological changes in the first generation can be attributed to physiological damage because the first generation directly received irradiation. Morphological changes observed in the laboratory reared (F₁) generations from the first and fifth generations can be attributed to genetic damage because physiological damage did not occur in the clean laboratory environment; however, some of these changes may have been epigenetic. Morphological changes in the fifth generation may be a mixture of physiological and genetic damages. (b) Judgment criteria regarding the potential major causal materials. When abnormality rates are correlated with distance from the NPP, these abnormalities can be attributed to short-lived radionuclides because they are distributed in a concentric fashion. When abnormality rates are correlated with the measured ground radiation doses, these abnormalities can be attributed to the radioactive cesium species. (c) Summary of morphological examinations. Physiological (somatic) damage in the first generation is clearly detected. Genetic (germline) damage in the first and fifth generations is also clear, based on the results of the offspring generations. Genetic damage is likely caused by short-lived radionuclides, based on the correlation with distance. Abnormalities in the first generation may be caused by both short-lived radionuclides and cesium, which did not exhibit a clear correlation. Abnormalities in the fifth generation may primarily be caused by cesium.

Fig. 6.

Mathematical analyses of the total abnormality rates (including the deaths of larvae, prepupae, and pupae and the morphological abnormalities of adults), which were obtained from high [34] and low [38] contamination levels, in response to cesium radioactivity ingested by Okinawa larvae. The horizontal axis represents ingested cesium radioactivity per larva [Bq/body]. (a) AIC improvement index. The highest AIC improvement index is obtained when the Koriyama data point is excluded as an outlier. (b) A Weibull model (type 2, 4 parameters) is the best mathematical fit when the Koriyama data point is excluded. The distribution pattern is loosely sigmoidal. The threshold is approximately 10 mBq/body, and the saturation point is approximately 10 Bq/body. (c) A power function model is the best mathematical fit when the Koriyama and Iitate-montane data points are excluded.