Nutrient Imbalance of the Host Plant for Larvae of the Pale Grass Blue Butterfly May Mediate the Field Effect of Low-Dose Radiation Exposure in Fukushima: Dose-Dependent Changes in the Sodium Content

Abstract

The pale grass blue butterfly Zizeeria maha is sensitive to low-dose radioactive pollution from the Fukushima nuclear accident in the field but is also highly tolerant to radioactive cesium (137Cs) in an artificial diet in laboratory experiments. To resolve this field-laboratory paradox, we hypothesize that the butterfly shows vulnerability in the field through biochemical changes in the larval host plant, the creeping wood sorrel Oxalis corniculata, in response to radiation stress. To test this field-effect hypothesis, we examined nutrient contents in the host plant leaves from Tohoku (mostly polluted areas including Fukushima), Niigata, and Kyushu, Japan. Leaves from Tohoku showed significantly lower sodium and lipid contents than those from Niigata. In the Tohoku samples, the sodium content (but not the lipid content) was significantly negatively correlated with the radioactivity concentration of cesium (137Cs) in leaves and with the ground radiation dose. The sodium content was also correlated with other nutrient factors. These results suggest that the sodium imbalance of the plant may be caused by radiation stress and that this nutrient imbalance may be one of the reasons that this monophagous butterfly showed high mortality and morphological abnormalities in the field shortly after the accident in Fukushima.

Metabolomic Response of the Creeping Wood Sorrel Oxalis corniculata to Low-Dose Radiation Exposure from Fukushima’s Contaminated Soil

“…Additionally, other ecological field effect modes of action may also be valid and important [ 27 , 32 ]. For example, a sodium deficiency is probably an important mechanism of the ecological field effects [ 38 ]. Another possibility in the plant is a decrease in their levels of vitamins available for the larvae when irradiated.…”

“…The biological impacts of the Fukushima nuclear accident have been studied in contaminated fields, which have focused on many organisms, including birds such as the barn swallow and goshawk [ 5 , 6 , 7 ], Japanese monkeys [ 8 , 9 , 10 ], intertidal invertebrates [ 11 ], gall-forming aphids [ 12 , 13 ], and plants [ 14 , 15 , 16 , 17 , 18 ]. However, to the best of our knowledge, the most intensively studied species in both field and laboratory experiments is the pale grass blue butterfly Zizeeria maha [ 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 30 , 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 ]. This small butterfly is popular in Japan (except for in Hokkaido) and has been established as an excellent field indicator species for environmental assessments and evolutionary studies [ 39 , 40 , 41 ] and as an excellent model organism in the laboratory for developmental and physiological studies [ 42 , 43 , 44 , 45 ].…”

“…This field effect hypothesis is reasonable, considering that some plants have shown morphological and gene expression changes in response to radiation exposure due to the Fukushima nuclear accident [ 14 , 15 , 16 , 17 , 18 ]. Along this line, we discovered that the sodium content in the leaves of the host plant was inversely correlated with both the 137 Cs radioactivity concentration in the leaves and the ground radiation dose [ 38 ]. Since the sodium deficiency in herbivore animals generally results in serious pathological consequences, this could be a possible mechanism of the ecological field effect on these butterflies.…”

Metabolomic Profiles of the Creeping Wood Sorrel Oxalis corniculata in Radioactively Contaminated Fields in Fukushima: Dose-Dependent Changes in Key Metabolites

“…The plant may have experienced biochemical changes in leaves in response to radiation exposure, which has led to harmful consequences in butterflies. This field effect hypothesis is reasonable, considering that at least some plants responded to Fukushima pollution at the levels of gene expression and phenotype [24][25][26][27][28][29]. Physiological damage to butterflies is likely mediated by multiple pathways, but one of them includes biochemical plant changes in response to radiation exposure, such as changes in nutritional contents [28] and changes in secondary metabolites [29].…”

“…In the case of the Fukushima nuclear accident, some scientists began investigating the biological effects soon after the accident using various wild animals and plants because access to the polluted areas was not difficult from a political standpoint. There is now accumulating field-based evidence that the Fukushima nuclear accident impacted animals and plants, including birds [11][12][13], butterflies [14][15][16][17], aphids [18,19], Japanese monkeys [20][21][22], intertidal invertebrates [23], and plants [24][25][26][27][28][29], even at relatively low levels of anthropogenic radiation. However, the application of advanced technologies such as metabolomics in studies on Fukushima has not yet been sufficient.…”