Soil Microbes and Plant-Associated Microbes in Response to Radioactive Pollution May Indirectly Affect Plants and Insect Herbivores: Evidence for Indirect Field Effects from Chernobyl and Fukushima

The biological impacts of the nuclear accidents in Chernobyl (1986) and Fukushima (2011) on wildlife have been studied in many organisms over decades, mainly from dosimetric perspectives based on laboratory experiments using indicator species. However, ecological perspectives are required to understand indirect field-specific effects among species, which are difficult to evaluate under dosimetric laboratory conditions. From the viewpoint that microbes play a fundamental role in ecosystem function as decomposers and symbionts for plants, we reviewed studies on microbes inhabiting soil and plants in Chernobyl and Fukushima in an attempt to find supporting evidence for indirect field-specific effects on plants and insect herbivores. Compositional changes in soil microbes associated with decreases in abundance and species diversity were reported, especially in heavily contaminated areas of both Chernobyl and Fukushima, which may accompany explosions of radioresistant species. In Chernobyl, the population size of soil microbes remained low for at least 20 years after the accident, and the abundance of plant-associated microbes, which are related to the growth and defense systems of plants, possibly decreased. These reported changes in microbes likely affect soil conditions and alter plant physiology. These microbe-mediated effects may then indirectly affect insect herbivores through food-mass-mediated, pollen-mediated, and metabolite-mediated interactions. Metabolite-mediated interactions may be a major pathway for ecological impacts at low pollution levels and could explain the decreases in insect herbivores in Fukushima. The present review highlights the importance of the indirect field effects of long-term low-dose radiation exposure under complex field circumstances.