Effects of ionizing radiation on wildlife: What knowledge have we gained between the Chernobyl and Fukushima accidents?

Abstract

The recent events at the Fukushima Daiichi nuclear power plant in Japan have raised questions over the effects of radiation in the environment. This article considers what we have learned about the radiological consequences for the environment from the Chernobyl accident, Ukraine, in April 1986. The literature offers mixed opinions of the long-term impacts on wildlife close to the Chernobyl plant, with some articles reporting significant effects at very low dose rates (below natural background dose rate levels in, for example, the United Kingdom). The lack of agreement highlights the need for further research to establish whether current radiological protection criteria for wildlife are adequate (and to determine if there are any implications for human radiological protection). Integr Environ Assess Manag 2011;7:371–373. © 2011 SETAC

Editor's Note: This is 1 of 17 invited commentaries in the series “Challenges Posed by Radiation and Radionuclides in the Environment.” These peer-reviewed commentaries were prepared to address some of the environmental issues raised by the March 2011 nuclear power plant accident in Japan.

INTRODUCTION

Organisms have the inherent ability to repair radiation-induced damage, because they have evolved in the presence of natural radiation. Studies on the effects of ionizing radiation on wildlife conducted over 100 y (Whicker and Schultz 1982) demonstrated considerable variation in the response to radiation within and between different organism types. It is now widely accepted that, in general, mammals are the most sensitive organism group, with invertebrates and simpler organisms typically being relatively insensitive to radiation exposure. This can be related to the biological complexity of an organism. A number of reviews suggested that: 1) populations of terrestrial animals are unlikely to be detrimentally affected at dose rates <1 mGy d⁻¹, and 2) dose rates <10 mGy d⁻¹ to plants and aquatic animals are unlikely to be detrimental to populations. (The SI unit of absorbed dose is the Gray [Gy], where 1 Gy is equivalent to the absorption of 1 joule of energy per kilogram of matter [i.e., biological tissue in this case]). The exact wording and the implications of these reviews differs (see discussion in Howard et al. [2010]).

Worldwide, there has been renewed interest in the contribution that nuclear power could make to future energy needs and reduced CO₂ emissions. In the aftermath of the Fukushima accidents, there is a need for robust, unbiased scientific evaluation of the consequences of radioactivity for wildlife. Here, we review studies conducted in terrestrial ecosystems close to the Chernobyl nuclear power plant (NPP), in the Ukraine, since the 1986 accident.

ACUTE AND SHORT-TERM EXPOSURE OF WILDLIFE FOLLOWING THE CHERNOBYL ACCIDENT

Much of the area around the Chernobyl NPP was coniferous forest. Interception of radionuclides by the forest canopy resulted in high absorbed dose rates (predominantly beta-radiation). Mass mortality of pine trees was observed over an area of 600 ha with an estimated absorbed dose of between 60 and 100 Gy in June 1986 (Geras'kin et al. 2008). No seeds were produced for 5 to 7 y in a further 3800 ha of forest, which received doses of 30 to 40 Gy. Some effects (e.g., growth reduction) were observed at doses of 0.5 to 1.0 Gy. Up to 80% of the dose absorbed by trees occurred during the first month (Geras'kin et al. 2008). Subsequently, more radioresistant deciduous species have grown in the areas that experienced high pine mortality.

A 30-fold reduction in forest soil invertebrates was observed 3 to 7 km from the Chernobyl NPP. Arable soil invertebrate populations were less affected, perhaps because of the greater shielding of soil compared to forest litter. Invertebrates are relatively resistant to radiation but were exposed during their more radiosensitive early life-stages (Geras'kin et al. 2008). Within 2.5 y of the accident, numbers had more or less recovered, although diversity was lower than before the accident.

Radiation levels in the most contaminated sites probably led to the death of wild mammals, evident by low rodent numbers recorded in autumn 1986 (cited in Geras'kin et al. 2008). Numbers recovered by spring 1987, probably due to immigration.

The severe acute and short-term effects observed were the consequence of the Chernobyl reactor exploding, resulting in the release of significant components of its inventory (e.g., around 60% of ¹³¹I, 100% of ¹³³Xe, >30% of ¹³⁴Cs and ¹³⁷Cs). The Fukushima reactors have overheated but not exploded and, date (early April 2011), have not released large proportions of their inventory. Furthermore, once nuclear chain-reactions have stopped, the reactors will no longer produce the short-lived radionuclides that contributed so significantly to the wildlife doses around Chernobyl.

LONG-TERM CHRONIC EXPOSURE OF WILDLIFE IN THE AREA AROUND THE CHERNOBYL NPP

Twenty-five years after the Chernobyl accident, there is no consensus on the impact of the chronic exposure to radiation on wildlife in the area around the NPP from which people were evacuated in 1986 and which remains largely uninhabited. This area is commonly referred to as the Chernobyl exclusion zone. Some have suggested that the removal of humans, and cessation of associated activities, has led to the Chernobyl exclusion zone becoming a thriving and biologically diverse environment with many protected species (IAEA 2006). However, such observations can be criticized as being based largely on anecdotal evidence and not rigorous scientific study.

Although the removal of human inhabitants can be viewed as having had a positive net ecological consequence, there may still be detrimental consequences of radiation exposure. For instance, populations may be abundant, but do those in more contaminated areas have the same age structure and reproductive success as those less exposed to radiation? In some areas of the exclusion zone, organisms receive chronic dose rates above those expected to, for instance, impair reproductive success (Chesser et al. 2000). Authors describing the diversity in the exclusion zone recognize the potential for detrimental effects of chronic radiation exposure and recommend long-term studies.

Conversely, a group of workers has reported a variety of effects in a range of organisms at comparatively low dose rates within the exclusion zone (Mousseau and Møller 2011). Møller and Mousseau (2009) reported reduced numbers of aboveground invertebrates with increasing dose rate “around Chernobyl” in 2006 to 2008. Negative relationships were observed in the range (0.24–24) × 10^×3 mGy d^×1. The authors concluded that this has implications for overall ecosystem function, given the importance of plant-pollinating invertebrates, although no observations of vegetation diversity and abundance were reported. To put these dose rates into context, the estimated unweighted dose rate of terrestrial organisms in the United Kingdom due to naturally occurring ²³⁸U and ²³²Th series radionuclides and ⁴⁰K (Beresford, Barnett, et al. 2008) span and exceed the range over which Møller and Mousseau report order-of-magnitude reductions in invertebrate numbers. Even accepting that natural background radiation in northern Ukraine is comparatively low (Møller and Mousseau 2011), the dose rates over which significant reductions in invertebrate numbers and abundance were reported to be observed appear to be incredulously low. Wickliffe and Baker (2011) have similarly criticized this work and also commented that the dose rates reported are significantly lower than those reported by others in the exclusion zone.

Other observations by Møller, Mousseau, and coworkers include: reduced diversity and abundance of “forest” birds in areas with dose rates in excess of 1 mGy d⁻¹ (Møller and Mousseau 2007) and germline mutations, increased sperm deformities, reduced egg viability, albinistic or deformed feathers, and reduced survival rates (determined from annual return to nesting sites) in barn swallows (Hirundo rustica) (Mousseau and Møller 2011). In these articles, the authors report only external dose rates and do not consider internal exposure, which is likely to dominate in many organisms (Beresford, Gaschak, et al. 2008). There has been criticism of the barn swallow studies; Smith (2008) commented on the lack of consideration of confounding factors, poor dosimetry reporting, and inappropriate grouping of sites for data interpretation.

A number of studies have considered chromosomal and molecular effects of radiation on wildlife in the exclusion zone (IAEA 2006; Geras'kin et al. 2008). Ryabokon and Goncharova (2006) reported that chromosome aberrations in bone marrow cells of bank voles (Myodes glareolus) were correlated with radionuclide concentrations at 5 Belarusian sites. The rate of aberrations appeared relatively constant over the period 1986 to 1996 (approximately 22 generations), although estimated whole-body dose rates decreased with a half-life of 2.5 to 3 y (Ryabokon et al. 2005). Studies with offspring from females captured at the sites and raised under laboratory conditions showed similar levels of chromosomal aberrations. This highlights a problem when interpreting results from Chernobyl: are the observed effects a consequence of chronic exposure or a residual consequence of the high short-term exposures?

Geras'kin et al. (2008) quote work by Ryabokon and coworkers that showed increased micronuclei frequency in polychromatic erythrocytes in bank voles in 1996. Conversely, Rodgers and Baker (2000) found no significant increase of micronuclei in polychromatic erythrocytes of bank voles with dose rates up to 86 mGy d⁻¹ in 1997 and suggested that this may indicate that the population had evolved to be “radioresistant.” Matson et al. (2000) found significantly greater genetic diversity in bank vole populations, with an estimated dose rate of 86 mGy d⁻¹ compared to a reference site. Although increased mutation rates may have contributed to this, the authors suggest that immigration into areas where populations had been significantly reduced after the accident may also be a factor.

DISCUSSION

Some of the observations from the Chernobyl exclusion zone (Mousseau and Møller 2011) have potential implications for our understanding of the effects of radiation on wildlife (and potentially humans) and the regulation of radioactive substances. However, such results have been questioned (Smith 2008; Wickliffe and Baker 2011) with, in our opinion, some justification, especially given the dosimetry approaches used. However, it is agreed that there is a need for coordinated and long-term research on the consequences of exposure to ionizing radiation in the vicinity of Chernobyl, taking into account spatial and temporal issues. Although the Chernobyl accident was a catastrophe to those people in the former Soviet Union whose lives were affected, it offers the radioecological community a unique opportunity to study the environmental effects of radiation. After 25 y, it is an opportunity we have yet to effectively exploit. Especially after the Fukushima releases, it is important, in the context of the energy debate and climate change, to have robust scientific evidence on the environmental risks associated with nuclear power generation.

Detailed inventories of the releases from the Fukushima complex are not yet available. Looking ahead, future research in the Chernobyl exclusion zone, and indeed in areas that have received deposition from the Fukushima releases, should adopt a “whole-ecosystem” approach. If this approach is to be successful, scientists will be challenged by the need to consider basic monitoring of biodiversity and similar ecosystem-level indices through to state-of-the-art cytogenetic approaches. A related challenge will be the need to include tools capable of supporting robust estimates of exposure in order to evaluate the overall impact to the environment.