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      Ingestion of radioactively contaminated diets for two generations in the pale grass blue butterfly

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          Abstract

          Background

          The release of radioactive materials due to the Fukushima nuclear accident has raised concern regarding the biological impacts of ingesting radioactively contaminated diets on organisms. We previously performed an internal exposure experiment in which contaminated leaves collected from polluted areas were fed to larvae of the pale grass blue butterfly, Zizeeria maha, from Okinawa, which is one of the least polluted localities in Japan. Using the same experimental system, in the present study, we further examined the effects of low-level-contaminated diets on this butterfly. Leaves were collected from two localities in Tohoku (Motomiya (161 Bq/kg) and Koriyama (117 Bq/kg)); two in Kanto (Kashiwa (47.6 Bq/kg) and Musashino (6.4 Bq/kg)); one in Tokai (Atami (2.5 Bq/kg)); and from Okinawa (0.2 Bq/kg). In addition to the effects on the first generation, we examined the possible transgenerational effects of the diets on the next generation.

          Results

          In the first generation, the Tohoku groups showed higher rates of mortality and abnormalities and a smaller forewing size than the Okinawa group. The mortality rates were largely dependent on the ingested dose of caesium. The survival rates of the Kanto-Tokai groups were greater than 80%, but the rates in the Tohoku groups were much lower. In the next generation, the survival rates in the Tohoku groups were below 20%, whereas those of the Okinawa groups were above 70%. The survival rates in the second generation were independent of the locality of the leaves ingested by the first generation, indicating that the diet in the second generation was the determinant of their survival. Moreover, a smaller forewing size was observed in the Tohoku groups in the second generation. However, the forewing size was inversely correlated with the cumulative caesium dose ingested throughout the first and second generations, indicating that the diet in the first generation also influenced the forewing size of the second generation.

          Conclusions

          Biological effects are detectable under a low ingested dose of radioactivity from a contaminated diet. The effects are transgenerational but can be overcome by ingesting a non-contaminated diet, suggesting that at least some of the observed effects are attributable to non-genetic physiological changes.

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          Most cited references19

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          The biological impacts of the Fukushima nuclear accident on the pale grass blue butterfly

          The collapse of the Fukushima Dai-ichi Nuclear Power Plant caused a massive release of radioactive materials to the environment. A prompt and reliable system for evaluating the biological impacts of this accident on animals has not been available. Here we show that the accident caused physiological and genetic damage to the pale grass blue Zizeeria maha, a common lycaenid butterfly in Japan. We collected the first-voltine adults in the Fukushima area in May 2011, some of which showed relatively mild abnormalities. The F1 offspring from the first-voltine females showed more severe abnormalities, which were inherited by the F2 generation. Adult butterflies collected in September 2011 showed more severe abnormalities than those collected in May. Similar abnormalities were experimentally reproduced in individuals from a non-contaminated area by external and internal low-dose exposures. We conclude that artificial radionuclides from the Fukushima Nuclear Power Plant caused physiological and genetic damage to this species.
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            The effects of natural variation in background radioactivity on humans, animals and other organisms.

            Natural levels of radioactivity on the Earth vary by more than a thousand-fold; this spatial heterogeneity may suffice to create heterogeneous effects on physiology, mutation and selection. We review the literature on the relationship between variation in natural levels of radioactivity and evolution. First, we consider the effects of natural levels of radiation on mutations, DNA repair and genetics. A total of 46 studies with 373 effect size estimates revealed a small, but highly significant mean effect that was independent of adjustment for publication bias. Second, we found different mean effect sizes when studies were based on broad categories like physiology, immunology and disease frequency; mean weighted effect sizes were larger for studies of plants than animals, and larger in studies conducted in areas with higher levels of radiation. Third, these negative effects of radiation on mutations, immunology and life history are inconsistent with a general role of hormetic positive effects of radiation on living organisms. Fourth, we reviewed studies of radiation resistance among taxa. These studies suggest that current levels of natural radioactivity may affect mutational input and thereby the genetic constitution and composition of natural populations. Susceptibility to radiation varied among taxa, and several studies provided evidence of differences in susceptibility among populations or strains. Crucially, however, these studies are few and scattered, suggesting that a concerted effort to address this lack of research should be made. © 2012 The Authors. Biological Reviews © 2012 Cambridge Philosophical Society.
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              Effects of food stress and density in different life stages on reproduction in a butterfly

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                Author and article information

                Contributors
                chiyodon@gmail.com
                wataira@gmail.com
                atsuki.hiyama@gmail.com
                tanahara@lab.u-ryukyu.ac.jp
                takatsuj@nagasaki-u.ac.jp
                otaki@sci.u-ryukyu.ac.jp
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                23 September 2014
                23 September 2014
                2014
                : 14
                : 1
                : 193
                Affiliations
                [ ]BCPH Unit of Molecular Physiology, Department of Chemistry, Biology and Marine Science, University of the Ryukyus, Okinawa, 903-0213 Japan
                [ ]Instrumental Research Center, University of the Ryukyus, Okinawa, 903-0213 Japan
                [ ]Graduate School of Fisheries Science and Environmental Studies, Nagasaki University, Nagasaki, 852-8521 Japan
                Article
                193
                10.1186/s12862-014-0193-0
                4171559
                25330067
                5a4dad4c-c3f4-45d4-bc75-03d03d6afcd5
                © Nohara et al.; licensee BioMed Central Ltd. 2014

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 23 May 2014
                : 19 August 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2014

                Evolutionary Biology
                fukushima nuclear accident,ingestion,internal exposure,low-dose exposure,pale grass blue butterfly,radioactive contamination,transgenerational effect

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