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Journal of Environmental Radioactivity 162-163 (2016) 347e357

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Journal of Environmental Radioactivity

journal homepage: www.elsevier.com/locate/jenvrad

Review

Ecological effects of exposure to enhanced levels of ionizing radiation

Stanislav A. Geras’kin Russian Institute of Radiology and Agroecology, Obninsk, Kaluga Region, 249032, Russia

a r t i c l e i n f o

Article history: Received 23 February 2016 Received in revised form 1 May 2016 Accepted 15 June 2016

Keywords: Ecosystems Populations Ionizing radiation Radiation accidents Indirect effects Radioadaptation

E-mail address: [email protected].

http://dx.doi.org/10.1016/j.jenvrad.2016.06.012 0265-931X/© 2016 Elsevier Ltd. All rights reserved.

a b s t r a c t

Irradiation of plants and animals can result in disruption of ecological relationships between the com- ponents of ecosystems. Such effects may act as triggers of perturbation and lead to consequences that may differ essentially from expected ones based on effects observed at the organismal level. Considerable differences in ecology and niches occupied by different species lead to substantial differences in doses of ionizing radiation absorbed by species, even when they all are present in the same environment at the same time. This is especially evident for contamination with a-emitting radionuclides. Radioactive contamination can be considered an ecological factor that is able to modify the resistance in natural populations. However, there are radioecological situations when elevated radioresistance does not evolve or persist. The complexity and non-linearity of the structure and functioning of ecosystems can lead to unexpected consequences of stress effects, which would appear harmless if they were assessed within the narrower context of organism-based traditional radioecology. Therefore, the use of ecological knowledge is essential for understanding responses of populations and ecosystems to radiation expo- sure. Integration of basic ecological principles in the design and implementation of radioecological research is essential for predicting radiation effects under rapidly changing environmental conditions.

© 2016 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 347 2. Large-scale studies of natural ecosystems externally exposed to radiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 348 3. Severe radiation accidents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 349 4. Indirect effects of radiation exposure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 350 5. Radioadaptation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 352 6. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356

1. Introduction

For assessment of radiation impact on the environment it is essential to understand the ecological effects that can be observed under different scenarios of radiation exposure. It is well known that effects of radiation initially appear at the molecular level. However, this knowledge cannot be directly extrapolated to populations and ecosystems since much more complex underlying mechanisms are involved in their response to stress (Clements and Rohr, 2009).

Most research of the biological effects of ionizing radiation have been conducted under laboratory conditions, generally based on single species, where biotic environmental factors are excluded and abiotic factors are controlled. Such an approach limits assessment of the real-world consequences of radiation exposure, because free- living organisms may be limited or constrained in their ability to cope with effects of ionizing radiation. Recent critical reviews (Br�echignac et al., 2012) have stressed that an ecosystem-level perspective on radioecology more important than ever. Radio- ecology should consider the consequences of both present and impending severe radiation accidents and change from a purely

S.A. Geras’kin / Journal of Environmental Radioactivity 162-163 (2016) 347e357348

descriptive to a predictive science. More thorough consideration of the ecological effects of ionizing radiation should improve our ability to predict how and when populations and ecosystems respond to radiation and recover from such exposure. A better understanding of radiation-induced population tolerance and its costs should facilitate identification of impacted communities and, thus, forecast the ecological consequences of radiation exposure and determine effectiveness of restoration.

Which are the patterns of radiation effects on structure, func- tion, and development of biological communities? Although spe- cies interactions are not the major structuring force in ecosystems, when factors as competition and predation are important, the relative strength of these interactions should influence the response of ecosystems to radiation exposure. Knowledge about the effects of radiation exposure at higher levels of biological or- ganization is mainly based on microcosm experiments (Fuma et al., 2012; Jones et al., 2004) and small-scale field observations, while large-scale field studies are rare. In this review I focus on ecological mechanisms that operate at the population and community levels. Such mechanisms may contribute to compensation or exacerbation of individual-level effects of stressors at higher levels of biological organization. Therefore, the main aim of this review is to assess available information about ecological effects of radiation exposure.

Table 2 Classification of plant communities by radiosensitivity (Henner et al., 2010).

Type of community The severity of effect of irradiation, Gya

Minor Intermediate Serious

Coniferous forest 0.9e9 9e17 >17 Deciduous forest 9e90 40e300 >90 Shrubs 9e40 40e170 >170 Rainforest 35e90 90e350 >350 Herbaceous species on rocks 70e90 90e350 >350 Old field 25e90 90e870 >870 Herbaceous cover under forest 170e350 350e520 >520 Pasture 9e90 90e870 >870 Herbaceous invaders 350e520 520e870 >870

a Original data in kR, values calculated with a conversion factor of 1Gy ¼ 115 R and adjusted to the nearest unity below 20, nearest 5 below 40 and nearest 10

2. Large-scale studies of natural ecosystems externally exposed to radiation

Experimental studies carried out in the USA, Canada, France and the USSR (Table 1) have provided information about the dynamics of radiation damage and recovery processes in different types of ecosystems (Alexakhin et al., 1994; Fabries et al., 1972; Guthrie and Duole, 1983; McCormick and Colley, 1966; Odum and Pigeon, 1970; Smirnov et al., 1983; Sparrow, 1966; Woodwell, 1967; Zavitovski, 1977). These studies have allowed estimation of radiation doses that lead to shifts in species composition. Generally, the structure of ecosystems changed as a function of dose. An effect stronger with higher radiation doses: the higher the dose, the simpler the structure of an ecosystem. Species within a community respond to radiation in accordance with their radiosensitivity and competition with other species. As a result, at intermediate dose rates the productivity of a community may increase, although with the completely different species composition (Smirnov et al., 1983).

Table 1 Large-scale studies of natural ecosystems externally exposed to radiation (Henner et al.,

Location Vegetation type Source type Expo

USA, Long Island NY

Mixed oak-pine forest 137Cs (350 TBq) 20 h Old-field community 60Co (115e144

TBq) 20 h

Winter-rye 60Co (115e152 TBq)

20 h

Canada, Manitoba

Boreal forest 137Cs (370 TBq) 19 h

USA Shortgrass plain 137Cs (324 TBq) Cont seas

USA, Wisconsin Deciduous forest 137Cs (56 TBq) 20 h USA Natural vegetation (Coniferous and

deciduous forest) reactor Vari

USA, Puerto Rico Tropical rainforest 134�137Cs (370 TBq)

Cont

Cadarache, France

Sclerophytic forest 137Cs (44 TBq) 20 h

USSR, South Urals

Pine/birch forest 1180 TBq Acut

USSR, South Urals

Grassland 1180 TBq Acut

Another consistent observation is the loss of larger, longer-lived plant species and the switch to smaller, more opportunistic taxa (Woodwell, 1967). Thus, the typical reactions of plant communities to irradiation at high doses are reductions in species diversity, changes in species dominance, reduction in productivity and changes in community structure. General outcomes of these ex- periments form the basis of classification for the main types of plant communities with respect to radiosensitivity (Table 2). It is evident that the most radiosensitive ecosystem is coniferous for- ests, while the most resistant is a meadow plant community.

Most of the available data concerning radiosensitivity of plants and animals are acquired in controlled conditions for individual species. Irradiation of ecosystems allowed comparison of such relative individual sensitivities with sensitivities recorded in eco- systems where they compete for resources and where fluctuating environmental parameters occur. Such comparison showed that species were more sensitive than predicted using laboratory- acquired values (Woodwell and Sparrow, 1963). The similar conclusion was drawn (Garnier-Laplace et al., 2013) when compared the range of variation of radiosensitivity of species from the Chernobyl exclusion zone with the statistical distribution established for terrestrial species chronically exposed to gamma external irradiation. This is a plausible hypothesis, considering that additional environmental stresses under field conditions super- imposed on the direct effects of radiations potentially results in increasing sensitivity. In addition, the duration of exposure is one of the major factors that distinguish situations of controlled exposure

2010).

sure mode Started on … Duration

/day Nov. 1961 18 yr /day 1962 2 yr

/day 1971 1 Growing season

/day 1969 14 yr þ 6/yr recovery

inuous/ onally

Apr. 1969 e

/day e 8 yr able flux of n, g 1959 e

inuous Jan. 1965

/day Jul. 1969 14 yr

e September of 1973; May of 1977

16 days in the autumn, 8 days in the spring

e MayeJune 1979 12 days

above.

S.A. Geras’kin / Journal of Environmental Radioactivity 162-163 (2016) 347e357 349

and field data. Except for organisms with short generation time, laboratory experiments are generally limited in time duration whereas wildlife is exposed across generations. As a result, the absorbed doses may be much higher in the field than in laboratory.

Another important conclusion from these experiments is that radiation is a form of stress that elicits community responses frequently similar to those observed under other forms of stress (Reyes et al., 2010; Woodwell, 1967). As a result, the changes observed in an ecosystem after irradiations are caused not only by radiation per se, but also by the inherent interactions between species within an ecosystem. This conclusion is emphasizing the importance of the structure of an ecosystem for maintaining con- ditions that allow for survival of its components. Therefore, the considerable insight into the basic nature of ecosystems and their ability to withstand or recover from stress can be obtained from observations of irradiated ecosystems.

However, temporal pattern of ecological succession in post- irradiated ecosystems is peculiar. For example, 47 years after cessation of irradiation of a mixed oak-pine forest (Brookhaven National Laboratory, the USA), we might have expected a recovery of the climax, pre-irradiation community. Initially irradiation resulted in five concentric zones of vegetation (Woodwell, 1967) that have retained their floristic heterogeneity and re-colonization by trees to a much smaller degree than expected (Stalter and Kincaid, 2009). Thus, it is probable that changes in a heavily irra- diated forest have exceeded the capacity of the ecosystem to recover.

3. Severe radiation accidents

The situation is different in case of radioactive fallout, and knowledge gained from previous studies is insufficient to explain the biota response. Why results of experiments with external irradiation of ecosystems can not be used to explain the changes from accidental release of radionuclides? Uptake of radionuclides in natural ecosystems during radiation accidents occurs through different pathways, while the aerial contamination is the prevailing one. In addition, there may be radionuclide release to the water environment, as in the case of the accident at NPP Fukushima Daiichi in 2011. Radionuclides that escaped to the environment during an accidental release enter the biotic and the abiotic chains of migration, leading to dynamic temporal and spatial distribution of radionuclides in ecosystems. Finally, this results in complicated space-time dynamics of exposure dose distribution in ecosystems (Table 3).

The most critical situation arises when the most radiosensitive components of an ecosystem receive maximum doses. Aerial contamination of coniferous forests is an example of such a radi- oecological situation. Coniferous trees generally have a high retention capacity and low turn-over rate for atmospherically dispersed contaminants (Tikhomirov and Shcheglov, 1994). As a consequence, the highest radionuclide concentrations and, corre- spondingly, exposure doses are received by the aboveground part

Table 3 The comparison of the absorbed dose distribution in ecosystems in case of radiation acc

External exposure of ecosystem Radiation accid

Source of exposure Point source Distributed sou Type of radiation g- or neutrons a-, b-, g- in diff Type of exposure External External and in Distribution of absorbed

doses in ecosystem Relatively uniform. Dose is decreased with the distance from the source

Extremely hete

Dose distribution over time

Uniform Intensive short- exposure in the

of plants, in particular, by needles. In case of the Chernobyl acci- dent, 90% of absorbed dose to critical organs of trees was due to b- irradiation from the deposited radionuclides and 10% due to g- irradiation (Arkhipov et al., 1994). The combination of increased radionuclide concentration (exposure doses) and low radio- resistance of conifers is responsible for the maximum radiation damage observed in this case. The “Red Forests” in Kyshtym and Chernobyl are striking examples.

Under the conditions of radioactive contamination, leaves, needles and apical meristems of trees are injured mostly in the middle and lower parts of crowns, in contrast with external exposure. The upper shoots remained viable even when 95% of the crowns were dried out (Krivolutsky et al.,1988). This is related with relatively rapid cleaning of the upper part of crowns under the influence of wind and precipitation.

Two month after the accident most radionuclides moved to the leaf litter and then remained in the upper 3e5 cm soil layer for a long time. This ecological niche is the habitat of forest invertebrates that have relatively radiosensitive juvenile stages. Ultimately, this causes an increased vulnerability of this component of forest eco- systems to radiation damage. Indeed, in the first years after the accident, inhabitants of the forest litter are severely affected at distances of 3e7 km from the Chernobyl NPP (Krivolutsky and Pokarzhevsky, 1992). The mean density of litter fauna was reduced from 104 individuals per 225 cm2 core at the control location to 2.2 at the 3-km site. Doses of 30 Gy had catastrophic effects on the invertebrate community, causing mortality of eggs and early life stages, as well as reproductive failure of adults. Such strong effect at the community level would not have been predicted from pre-Chernobyl data (Hinton et al., 2007). Even 16 years after the accident sampling for soil-surface and flying invertebrate spe- cies indicated a general loss of diversity with increasing levels of chronic exposure dose rates (up to 140 mGy/h), but with no asso- ciated loss of total biomass (Jackson et al., 2005). However, in the long run the situation was changed completely. In 2010e2011, ac- cording to (Bonzom et al., 2016), decomposition of uncontaminated leaf litter within the Chernobyl exclusion zone increased along with total dose rates (from 0.3 to 150 mGy/h) estimated for decomposers. These effects remained the same for the rapidly decomposing alder litter and the slowly decomposing birch litter. Therefore, species identity and quality of the leaf litter had no apparent impact on how radioactivity affected decomposition. These data indicate that radioactive contamination of forest ecosystems over more than two decades does not necessarily have detrimental effects on organic matter decay. Contrary to these findings, a study on leaf litter decomposition around Chernobyl (Mousseau et al., 2014) showed a negative relationship between litter mass loss and the level of ambient radiation (0.09e240 mGy/h). One of the most important differences between these studies was the range in radiation levels with much higher dose rates in (Mousseau et al., 2014). Actually, two the most contaminated sites in Mousseau et al. (2014) study appeared to drive the negative relationship between mass loss and radiation level. This might suggest a threshold in contamination,

ident and external irradiation.

ent

rce erent combinations ternal rogeneous

term exposure, followed by a slow decline in dose rate. Redistribution of radiation ecosystem components due to the migration of radionuclides

S.A. Geras’kin / Journal of Environmental Radioactivity 162-163 (2016) 347e357350

above which the decomposer abundance and community compo- sition might be affected more negatively by soil radioactive contamination.

In spring 2011 soil nematode assemblages from the forest sites in the Chernobyl Exclusion Zone were slightly impacted by chronic exposure with estimated dose rates ranging from 0.7 to 220 mGy/h (Lecomte-Pradines et al., 2014). However, this does not exclude the hypothesis that nematodes would be more strongly impacted immediately after the accident and that sensitive species did not recover.

The reconstruction of the absorbed dose rates by different birds species at 300 census sites in the 50-km northwest area affected by the accident at the Fukushima Daiichi nuclear power plant over 2011e2014 (from 0.3 to 97 mGy/h) has shown (Garnier-Laplace et al., 2015) that the overall bird abundance at Fukushima decreased with increasing total doses. This relationship was directly consistent with exposure levels found in the literature to induce physiological disturbances in birds. Among the 57 species constituting the observed bird community, 90% were likely chronically exposed at a dose rate that could affect their repro- ductive success.

Radiation effects in ecosystems depend on radiosensitivity of species and the distribution of absorbed doses within an ecosystem. However, dose distributions among components of an ecosystem are fundamentally different for external exposure and radioactive fallout (Table 3). As a consequence, doses absorbed by species, may vary by several orders of magnitude even when they are all present in the same environment at the same time. In particular, deposition of b-emitting radionuclides onto critical plant tissues results in larger doses received by plants than animals living in the same environment (Prister et al., 1982). Thus, in the first year after an accident doses to biota species varied significantly up to 250 times near the Borschevka settlement within the 30-km Chernobyl NPP zone (Fesenko et al., 2005). In addition, different types of radiation (a-, b- and g-radiation) have different conse- quences for plants, animals and humans. That is especially evident for a-emitting radionuclides. For example, under contamination with radionuclides of 235U decay chains, the soil biota species receive doses 480 times greater than a human (Spirin et al., 2013).

Radiation damage to herbaceous communities in the Eastern Urals Radioactive Trace (EURT) was evident as early as in the first post-accident growing season of 1958 (Smirnov, 1993). Herbaceous communities within the EURT showed high heterogeneity in spe- cies composition (above 100 species), and their radiosensitivity reaches 100 fold differences. Biological effects in different plant species during the acute period of the accident depended on location of the most radiosensitive organs relative to the soil sur- face as the main source of external b- and g-exposure. Reproductive organs located on the soil surface were the most affected, while the least affected were located within the soil. In the first vegetation period after the accident contamination density of 37 MBq/m2 for 90Sr was achieved, and changes in the structure of the plant com- munity occurred. Plants with winter seeds disappeared, and there was an initial decline in the cumulative stock of the above-ground biomass by 30% (Smirnov, 1993). Up to 5e6 years after the accident, there was a considerable decline in the fraction of plant cover with buds on the soil surface (the obvious result of damage to repro- ductive organs), and an increase in the proportion of plants with buds within the soil. In the following 5e6 years a slow recovery of the plant community was noticed, although it failed to achieve the pre-accidental state.

The strong effects of extremely high dose rates of radiation to plants and animals at the early period of severe radiation accidents are clear. On the other hand, although 30 years have passed since the Chernobyl accident, the radioecology community has yet to

reach a consensus on the effects of long-term chronic low dose irradiation on organisms occupying high trophic levels within the Chernobyl ecosystem. Using snow track surveys Møller and Mousseau (2013) have shown significant declines in population of larger mammals with increasing radioactive contamination. In contrast, a study used the same method, however, covering a much larger area and time of observations suggests that populations of several large mammal species increased within the Chernobyl zone during the first decade after the accident, and found no relation between radioactive contamination density and mammal abun- dances (Deryabina et al., 2015). Similarly, the results of the first remote-camera scent-station survey suggest (Webster et al., 2016) that radioactive contamination within the Chernobyl Exclusion Zone has no discernible impact on the current distribution of four mammalian species (gray wolf (Canis lupus L.), raccoon dog (Nyc- tereutes procyonoides Gray), Eurasian boar (Sus scrofa L.), and red fox (Vulpes vulpes L.)).

Finally, large-scale radioecological studies performed in the areas affected by severe radiation accidents have made it possible to obtain unique information on responses of living organisms at different levels of biological organization under conditions of wide- ranging and heterogeneous radioactive contamination. Unique ecosystems have developed within the zones affected by heavy radiation, where humans are absent, and representatives of numerous taxonomic groups are reproducing against the back- ground of drastic changes in the range of ecological factors.

4. Indirect effects of radiation exposure

In radiation-impacted ecosystems two groups of effects are identified. In the first period after an accident, when the short-lived radionuclides are the main contributors to the dose, direct effects appear. This type of effects depends on radiosensitivity of species that an ecosystem comprises. Direct effects depending on dose can vary from slight inhibition of growth to death or even changes in community structure. The ranges of lethal doses for major groups of organisms are extremely wide and cover several orders of magni- tude (Whicker and Schultz, 1982). The lethal dose ranges for different groups of organisms only partially overlap. Therefore, a part of radiosensitive species die after irradiation with high doses, while in some other species vital functions are suppressed. For radioresistant species the same dose is harmless or even stimu- lating. This creates a background for formation of indirect effects in exposed ecosystems.

Each ecological community is a structured, self-sustaining sys- tem in which a variety of ecological interactions contribute to sta- bility. Irradiation can result in disruption of ecological interactions between components of ecosystems. Such effects may act as a trigger of perturbation and lead to consequences that may differ from those expected from direct effects observed at the organismal level. Some typical examples of indirect radiation effects are given below.

Suppression of radiosensitive species and intensive development of radioresistant ones. Radioactive contamination can significantly affect the composition of soil microbiological community. For example, the total number of bacteria and actinomycete strains declines, while the percentage of radioresistant strains grows with increasing radioactive contamination of soil in the range of 100e10,000 Bq/kg in northwest China affected as a result of nuclear weapons tests (Gu et al., 2014).

In radiation-impacted forests around the Chernobyl NPP, coniferous trees died completely because of their high radiosensi- tivity. Destruction of the pine canopy greatly changed the micro- environment of the stand, rendering it similar to that of an open field. Since 1988, the Red Forest has been undergoing a community

S.A. Geras’kin / Journal of Environmental Radioactivity 162-163 (2016) 347e357 351

shift that has gradually been replaced by grasses, shrubs, and young deciduous trees. In this radioecological situation radioresistant species were actively developing due to an improvement of light, temperature and nutrition conditions. Changes in microclimate and structure of grass communities within the area of died pine stands and severely affected birch stands led to a 3e5-fold increase in biomass of grass (Geras’kin et al., 2008). In meadow plant com- munities near Chernobyl NPP for the same reasons relative con- tributions of the radioresistant species increased significantly, while the total number of plants and species diversity decreased sharply with the level of radiation exposure (Fig. 1). These changes arises from intrinsic species differences in radiosensitivity and variable ability of different species to exploit altered environmental conditions. Similarly, within the Fukushima area, although bird species on average declined in abundance with increasing ambient levels, several species increased in abundance due to changes in land-use and/or to competitive release (Moller et al., 2015).

Production Association (PA) Mayak was the first plant in Russia for weapon-grade plutonium production. It is located in the Che- lyabinsk Region and was put into operation in 1948. Radiochemical processing resulted in huge volumes of liquid radioactive waste of different specific activities. To store this waste, water reservoirs located in the PA Mayak protection area were used. Up to now, these water bodies are heavily contaminated with radionuclides. The current excess of radionuclide content in water at the storage reservoirs is nine orders of magnitude for 90Sr and 137Cs, and six orders of magnitude for a-emitting radionuclides (Pryakhin et al., 2016). To the best of our knowledge, some of these reservoirs, namely the Old Swamp and Lake Karachai, are the most radioac- tively contaminated water bodies in the world. In these reservoirs phytoplankton, zooplankton and zoobenthos species diversity is reduced due to a loss of sensitive species, which leads to destruc- tion of interspecific interactions, weakening competition and causing active development of the most resistant forms (Pryakhin et al., 2016).

Disruption of trophic relations in ecologically connected groups of organisms. The next example is a survey of gypsy moth (Lymantria dispar dispar L.) populations and their parasite tahinid flies (Tach- inid sp.) inhabiting birch forest in the South Urals contaminated with 90Sr. Radioactive contamination can have both positive and

Fig. 1. Radiation effects in meadow plant communities Yanov, near the Chernobyl NPP, 1987 (Smirnov and Suvorova, 1996). ▫ e total number of plants per m2; -£- number of Agrostis syreistschikowii per m2; -▵- number of Calamagrostis epigeios per m2; -◊- number of plant species per 100 m2. D þ 15 e dose rates were measured on 15th day after the accident.

negative effects on the consecutive trophic levels (Fig. 2). Infesta- tion of caterpillars with parasites decreased, while their survival rate increased with level of radioactive contamination (Krivolutsky et al., 1988). These effects become evident at levels of radioactive contamination exceeding 1 MBq/m2. The observed paradoxical ef- fect, which is not expected from conventional radiobiology studies based on a single-species approach, is connected to the ecology of related species as well as with patterns of radionuclide distribution among components of the forest ecosystem. Caterpillars and pupae of gypsy moth inhabited the upper tiers of the forest, where radi- ation doses from 90Sr located in the litter were negligible. In contrast, pupae of tahinid flies occupied the litter, where dose reached up to 70 Gy. Thus, the observed indirect effect, i.e. the increased survival of caterpillars and butterflies with increasing level of radioactive contamination, caused due to the decrease in the number of parasites affected by radiation. In a similar way, population-level impacts of pesticide-induced chronic effects on field vole (Microtus agrestis L.) depend more on ecology than toxi- cology (Dalkvist et al., 2009).

Animals are assumed to play an important role in ecosystem functioning through their influence on seed set, seed consumption, seed dispersal, and maintenance of plant communities. A severe reduction in the abundance of pollinating insects in the most contaminated areas around Chernobyl have shown to be negatively related to fruit production by bushes and trees (Moller et al., 2012). The abundance of frugivorous birds decreased with decreasing abundance of fruit. Thus, negative cascading effects of irradiation have shown (Moller et al., 2012) from pollinating insects over fruit set and frugivory to recruitment of fruit-producing plants.

A large amount of organic residues leads to an increase in the number of insect pests. In the South Urals a sharp increase in the number of bark beetles was found in an irradiated forest (Alexakhin et al., 2004). In a similar way, in the 30-km ChNPP zone forest and fruit trees were seriously injured by pests (Krivolutsky, 2000). Thus, a large amount of organic residues and loss of immunity in sur- viving plants has led to an outbreak of pests.

A loss of immunity and novel infectious diseases. Radiation exposure can have substantial effects on host-pathogen relation- ships (Morley, 2012). These effects are predominantly associated with the serious damage to the immune system of hosts caused by ionizing radiation. In addition, chronic radiation exposure can act

Fig. 2. Effect of radioactive contamination on gypsy moth populations and their parasite tahinid flies (Krivolutsky et al., 1988). : e survival rate of gypsy moth cat- erpillars, relative units; D e infestation of gypsy moth caterpillars by tahinid flies, relative units.

S.A. Geras’kin / Journal of Environmental Radioactivity 162-163 (2016) 347e357352

as a mutagen that leads to the emergence of new clones in pop- ulations of pathogenic microorganisms. A loss of immunity in plants and animals has activated many infectious diseases such as tularemia, encephalitis and fungal pathogens. Indeed, within the 30-km ChNPP zone a decrease in plants resistance to disease and accelerated development of new phytopathogenic forms and races with enhanced virulence were revealed (Dmitriev et al., 2011). These pathogens could be easily exported out of the contaminated areas. Therefore, the 30-km ChNPP zone may be an environmental hazard and the ecological processes within the zone need to be monitored. In contrast, in a large area on the border between Belarus and Russia the higher the contamination with 137Cs, the lower the number of cases of rabies in wild Canidae observed, with no rabid animals in regions which are contaminated by 740e1480 kBq/m2 137Cs or higher (Adamovich, 1998). Although it is unclear which factors impact disease epidemiology, it seems likely that radiation either directly affects viral viability, or more likely indirectly, through a reduction in the number of animals acting as a source of infection. Indeed, in this region the number of wolf litters shows a significant negative correlation with the density of su- perficial soil contamination (Adamovich, 1998).

The examples reported above illustrate the difficulty of making general statements about the effects of radiation exposure that may propagate from individual to population and ecosystem levels. The type and the magnitude of indirect effects of radionuclides are depend on ecosystem composition, and many ecological factors other than radiation can be more important. Overall, the distur- bance of ecological interrelations are induced by the following factors: (1) changes in microclimatic and edaphic conditions (Alexakhin et al., 2004); (2) disturbance in the synchrony of sea- sonal phases in development of ecologically connected groups of organisms (Krivolutsky et al., 1988); (3) an imbalance in relation- ships between consumers and producers (Krivolutsky et al., 1988); (4) changes in competition as a result of species differences in radioresistance (Smirnov and Suvorova, 1996); and (5) a loss of immunity and accelerated development of new pathogenic forms with elevated virulence (Dmitriev et al., 2011). In addition, radiation-induced alterations in ecosystems may open ecological niches for immigration of new species. These indirect effects cannot be deduced solely from the effects on individuals. Therefore, the use of ecological knowledge is essential for understanding re- sponses of populations and ecosystems to radiation.

5. Radioadaptation

Severe radiation accidents dramatically changed the conditions of existence of plants and animals inhabiting contaminated areas. Hence, there is every reason to expect evolution of resistance to radiation in natural populations occupied these areas for a long time. The possibility and the rate of adaptation in natural pop- ulations to increased levels of radioactive contamination depend on two categories of factors:

- species flexibility (ecological range, intra-population variability, radiosensitivity, physiological status, mode of reproduction, structure and functional organisation of the genome);

- type and level of environmental contamination (the biophysical properties of radiation (the relative biological effectiveness, LET (the linear energy transfer), dose rates), absorbed doses from external and internal sources, biological availability of radio- nuclides and their distribution within a body, additional ecological factors that can modify radiation effects).

An extreme environmental change, like Chernobyl accident, can greatly accelerate phenotypic evolution and adaptation. Birds have

the capacity to adapt to chronic exposure to low-dose ionizing ra- diation, although this capacity varies among species and is partic- ularly reduced in species that produce larger amounts of pheomelanin and that show plastic responses to glutathione (GSH) levels (Galv�an et al., 2014). Analysis of the concentrations of the most important intracellular antioxidant e glutathione (i.e. GSH), its redox status, the DNA damage and body condition in 16 species of birds exposed to radiation in Chernobyl showed that GSH levels and body condition increased, while levels of oxidative stress and the DNA damage decreased with increasing of background radia- tion levels (Galv�an et al., 2014). Thus, some species of birds have physiologically adapted to current levels of chronic radiation exposure in Chernobyl.

In aquatic habitats, bottom deposits are characterized by the highest radionuclide concentrations leading to higher irradiation of benthic organisms. Tsytsugina and Polikarpov (2003), when studying the oligochaeta (Dero obtuse Undekem, Nais pseudobtusa Piguet, and Nais pardalis Piguet) reproduction in a reservoir of the Chernobyl affected zone near the settlement of Yanov (dose rate on the surface of bottom sediments was 0.34 mGy/day), evidenced a statistically significant relationship between the severity of cyto- genetic damage in the worm population and the number of in- dividuals switching to sexual reproduction. Similarly, increased proportion of reproduced sexually plants and, accordingly, reduced role of the apomixis was found in populations of perforate St John’s-wort (Hypericum perforatum L.) inhabiting the Chernobyl exclusion zone (Grodzinsky, 2013). It is known that sexless repro- duction, while maintaining valuable heterozygous types and thereby ensuring a high vitality, restricts the capacities of genetic variability and reduces potencies of populations in the changing environment. New gene combinations, arising from genetic recombination, can enhance the population’s tolerance to radiation exposure. Therefore, adverse environmental conditions activate the sexual mode of reproduction which is associated with the increase of adaptive possibilities of the populations.

Chronic radiation exposure can lead to switches in alternative types of ontogeny in populations of small rodents. Due to differ- ences in metabolism, individuals of different ontogenetic types show different radioresistance (Grigorkina et al., 2015). Populations of pigmy wood mice (Sylvaemus uralensis Pall.) within the EURT have more males with higher fecundity, whereas embryonic mor- tality and the proportion of females with embryonic losses were significantly lower in comparison with uncontaminated areas (Grigorkina and Olenev, 2011). A significant increase in fertility, fecundity and maturation rate in comparison with control animals were revealed in root vole (Microtus oeconomus Pall.) populations from sites with elevated levels of natural radioactivity in Komi Republic (Taskaev et al., 2010). Therefore, stability of a population in radioactively contamination environments may be linked to intensification of metabolism and reproduction activity.

In uncontaminated sites populations of northern rockjasmine (Androsace septentrionalis L.) consist of a mix of annual and biennial forms. However, under radioactive contamination much more radioresistant biennial forms get an advantage. Indeed, in chroni- cally irradiated populations within the EURT the proportion of biennial plants significantly exceeds the proportion for annual ones (Shevchenko et al., 1992).

When a population is exposed to radiation over multiple gen- erations, natural selection may favor more radioresistant genotypes and, thereby, gradually increase the mean tolerance of the popu- lation. Adaptation to ionizing radiation can arise either from an increase in the frequency of alleles that were already present before the accident or occur de novo from mutations. A comparison of radiosensitivity of populations among sites can thus provide evi- dence of adaptation, if individuals from a contaminated site display

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elevated resistance, and if differences in resistance among pop- ulations have a genetic basis. For example, all strains of the fila- mentous fungus Alternaria alternata Keissl. collected from the destroyed and highly contaminated 4th Chernobyl NPP reactor possessed high radioresistance, while strains from uncontaminated areas showed much less radioresistance (Mironenko et al., 2000). Radioresistant strains were genetically adapted to high levels of radiation exposure by means of selection, which increased the ploidy level and the number of nuclei. In addition, the diversity of microorganisms forming biofilms on concrete pillars and walls naturally exposed to sunlight in sites with different levels of ionizing radiation in the Chernobyl area (0.35e25 mGy/h) are comparable to non-irradiated samples in terms of general diversity patterns (Ragon et al., 2011). This does not mean that radiation does not affect these microbial communities, since the study of mutation frequencies in samples from non-irradiated and Chernobyl sites showed a positive correlation between increased radiation and mutation rates (Ragon et al., 2011). Therefore, biofilm communities growing in sunlight exposed substrates are capable of coping with increased mutation rates and appear pre-adapted to levels of ionizing radiation in Chernobyl due to their natural adaptation to periodical desiccation and ambient UV radiation.

The analysis of the progeny of a bull and three cows found in the 30-km Chernobyl zone one year and a half after the accident and later kept on an experimental farm located 10 km from the sarcophagus in the area with a contamination density of 7400 kBq/ m2 for 137Cs has shown significant deviations in the transmission of allele variants of some genes from parents to offsprings (Glazko, 2001). The prevailing allele variants were not typical for highly specialized Holstein breed but for a more primitive, however more tolerant to unfavorable conditions, breeds such as Gray Ukrainian. That means that radiation exposure manifested itself as a selection factor causing changes in the frequency of occurrence of non- mutant genes rather than by the induction of new mutations. Thus, one of the most harmful biological consequences of chronic radiation exposure is related to the “erosion” (van Straalen and Timmermans, 2002) of genetic diversity of natural population as a result of the directed selection against radiosensitive organisms. This also entails the elimination of rare alleles that could be ad- vantageous when environment is changed.

Laboratory studies of repair inhibition, dose-effect relationships for low- and high-LET radiation, measurements of unscheduled DNA synthesis and efficacy of single strand break recovery in Chlorella vulgaris Beyerink populations, which were collected from differently radioactive contaminated sites within the EURT, suggest that divergence of populations in terms of radioresistance is based on selection for increased effectiveness of the DNA repair systems (Shevchenko et al., 1992). Another study of the possible mecha- nisms of adaptation to radioactive contamination (Kovalchuk et al., 2004) showed extremely low (more than 10-fold) recombination level and a higher level of genome methylation in chronically irradiated plants that may have prevented extensive genome rearrangements.

Additional g-irradiation (20 Gy) of cornflower grungy (Centaurea scabiosa L.) seeds, which were collected on the EURT sites with radioactive contamination from 37 to 140 MBq/m2 for 90Sr, indicated an increase in the fraction of radioresistant plants and the appearance of a highly radioresistant fraction, which was absent in control (at the contamination density of 37 MBq/m2 an average rate of chromosome aberrations in seedlings was 30.4%, at 140 MBq/m2 e 19.7%, in the control e 42.9%). These findings were confirmed in a similar experiment with additional g-treatment of crepis roof (Crepis tectorum L.) seeds (Shevchenko et al., 1992). Similarly, the radioresistance of bank voles (Clethrionomys glareolus Schreber) that were reproducing at the Chernobyl NPP zone during

1987e1992 increased with the number of generations (Fig. 3a). In these populations a decrease in the fraction of radiosensitive ani- mals and an increase in the proportion of resistant to radiation voles were found. Resistant animals were absent in the initial population and appear only in the 6e10 generations. By the 12th generation the fraction of radioresistant animals was reached 20% (Ilyenko and Krapivko, 1998).

From Fig. 3b is evident that the manifestation of radioadaptation depends on the level of radioactive contamination: the higher the dose at the contaminated plot, the higher the radioresistance of Scots pine (Pinus sylvestris L.) seeds. Interestingly, the level of ra- diation exposure at the contaminated plots varied in the range of 1e20 Gy, while radioresistance of seeds increased only by 1.7 times. Similarly, populations of common vole and bank vole inhabiting severely contaminated plots (18500 and 37000 kBq/m2 for 137Cs) in the ChNPP Exclusion Zone mainly consisted of animals in which frequency of occurrence of cytogenetic disturbances did not exceed the control level (Glazko et al., 2006). Intensity of selection for radioresistance depended on the contamination level and was not observed in populations inhabiting sites with the contamination density below 7400 kBq/m2 for 137Cs. An increased numbers of radioresistant animals were first found only in 1999, i.e. in the 26th generation of voles survived in the Chernobyl accident. Hence, adaptation to low levels of radiation is unlikely because selection for resistance is likely to be lower.

Evolutionary adaptation can be rapid (Hendry et al., 2008; Levinton et al., 2003) and potentially result in resistance to stressful conditions. Contrary to the increased radioresistance of seeds from plant populations that inhabit radioactively contami- nated areas (Fedotov et al., 2006; Shevchenko et al., 1992), there was no significant and reproducible in time difference in resistance to subsequent g-ray exposure (Fig. 4a) between seeds collected from reference and exposed Scots pine populations from the Bryansk Region, which was affected by the Chernobyl accident. Similarly, seeds from crested hairgrass (Koeleria gracilis Pers.) populations from the Semipalatinsk Test Site that have experienced radiation exposure for more than half a century, and that have experienced high levels of cytogenetic abnormalities did not show an increase in resistance to additional g-ray exposure (Fig. 4b). A considerable shift in the dose rate of acute irradiation (more than 70 times, from 2970 Gy/h to 39 Gy/h) did not change this conclusion.

The absence of adaptation to chronic radiation exposure, which is documented in some natural populations, raises question about the conditions when radioadaptation might be expected. Which factors might constrain or promote adaptive responses? If they occur, will these responses be sufficient to keep up under the radioactive contamination?

Adaptation to radioactive contamination is equivalent to an in- crease in fitness under chronic exposure of radionuclides. However, fitness of an adapted population may decrease under normal con- ditions (Diaz-Ravina and Baath, 2001; Eranen, 2008; Hickey and McNeilly, 1975; Levinton et al., 2003). Furthermore, adaptation to one set of environmental stressors may increase vulnerability to other environmental stressors (Salice et al., 2010). With such a negative correlation between resistance and fitness, selection for increased resistance automatically decreases fitness. This addi- tional cost of increased radioresistance may be a consequence of antagonistic pleiotropy (Shirley and Sibly, 1999), or it may arise at the physiological level since metabolic energy has to be used to produce the adaptive trait even when it is not required (Levinton et al., 2003). As a result, there are situations when resistance to environmental changes does not evolve or does not persist. Moreover, adaptation is often observed in one species, but not in others, despite equivalent opportunity and exposure conditions

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(Bradshaw, 1991). Indeed, within the EURT, radioresistance increased 3e4 times in radiosensitive plants, but remained prac- tically unchanged in radioresistant species inhabiting the same place (Shevchenko et al., 1992). Consequently, other things being equal, in populations of radiosensitive species selection for radio- resistance is more intense than in populations of radioresistant species. Half a century after the accident, estimation of mutability based on the frequency of morphosis occurrence showed that mutation in plant species within the EURTarea is more intense than in background populations. However, radioadaptation in plant populations is rare and unstable (Molchanova et al., 2011).

It is important that the EURT has the specific configuration that looks like a prolonged and narrow area with a rapidly decreasing gradient of radioactive contamination. The current levels of soil contamination near the epicenter of the accident reach 30 � 103 kBq/m2 for 90Sr and 1 � 103 kBq/m2 for 137Cs. Contami- nation levels are reduced, in accordance with a power function, with the increasing distance from the accident site and at a distance of 100 km from the epicenter reaching close to background values (Molchanova et al., 2011). Small rodents can move considerable distances when searching for a partner or for better habitats. As a result, migratory activity of wood mice (Apodemus (Sylvaemus) uralensis Pall.), field mice (Apodemus agrarius Pall.) and red-backed voles (Clethrionomys rutilus Pall.) from the EURT prevents devel- opment of radioadaptation. In contrast, long-term residence by subterranean borrowing rodents (common mole-voles (Ellobius talpinus Pall.)) with low migratory activity in the epicenter of the EURT leads to development of adaptation to chronic radiation exposure (Grigorkina and Olenev, 2009).

The response of populations to radiation exposure depends on many factors: type of organism and its niche, radioresistance level and the mode of reproduction as well as biophysical properties of radiation (relative biological effectiveness, linear energy transfer, dose rates). Improved DNA repair capacity and an ability to germinate under abiotic stress (salinity and accelerated ageing) were shown in embryos of evening primrose (Oenothera biennis L.) growing near the Chernobyl NPP on sites contaminated with g- and b-emitters, while in seeds from the a-, b- and g-contaminated site such adaptation was not found (Boubriak et al., 2008). This is similar to findings for successful adaptation of wild vetch (Vicia cracca L.) populations on sites highly contaminated with b-, but not with a-emitters (Syomov et al., 1992).

Fig. 3. Examples of radioadaptation in natural populations. (a) Changes in life expectancy (da levels of radioactive contamination sites within the Chernobyl NPP zone (Ilyenko and Krap contrasting levels of radioactive contamination within the Chernobyl NPP zone, 1997 (Fedo

Finally, if we examine radioadaptation in nature, we find as much evidence of its existence, as of its absence. Consequently, there are good theoretical and practical reasons for more attention being paid to the mechanisms by which populations become radioresistant, and to situations where radioadaptation does not appear.

6. Discussion

The current approach to environmental protection from radia- tion relies on organismal-level endpoints (Environmental Protection …, 2008), and this approach is not matched by the stated protection goals of the international agencies: preserving life sustainability through protection of ecosystem structure and functioning (Bradshaw et al., 2014). Ignoring of population- or higher-level effects and focusing only on individual-level endpoints can lead to inaccurate risk estimates and errors in environmental management decisions. It may potentially lead to an over- estimation of risk, but in some cases to underestimation (Moe et al., 2013). Hence, currently there is little possibility for regulatory au- thorities to increase ecological realism and understand risk at the population and ecosystem levels. In addition, exposure to radio- nuclides can trigger non-linear changes in the structure and func- tion of an ecosystem that cannot be predicted from effects on individual organisms. Such impacts may not be manifested as the results of direct radiobiological effects on individual organisms, but rather the consequence of indirect effects, which result from dif- ferences in sensitivity of species and potentially lead to changes in habitat structure or alteration of trophic relationships. Although radioecologists discovered the potential importance of indirect ef- fects long time ago (Brechignac and Doi, 2009; Woodwell, 1967), these effects have remained understudied and not thoroughly included in radioecological risk assessment. For example, keystone species that govern resource dynamics, trophic structure, and disturbance modes have the greatest potential to affect ecosystem processes. Thus, protection of these species is essential for ecosystem preservation. If an ecologically important species be- longs to those most sensitive to radiation exposure, like conifers, its elimination has disproportional effects on ecosystem functioning (Alexakhin et al., 2004; Geras’kin et al., 2008). Methods for man- aging indirect effects and for detecting adverse changes in eco- systems before they become severely affected have been developed

ys after irradiation) of irradiated (14 Gy) bank voles which inhabit the contrasted in the ivko, 1998); (b). Radioresistance of pine seeds from populations inhabiting sites with tov et al., 2006).

Fig. 4. Frequency of aberrant cells in seedling meristems after the acute g-exposure of seeds collected from chronically exposed plant populations: (a) a root meristem of Scots pine seedlings, the Bryansk Region, 15 Gy (Geras’kin et al., 2011); (b) a coleoptile of crested hairgrass, the Semipalatinsk Test Site, 69 Gy at 2970 Gy/h in 2005 and 2006, 50 Gy at 39 Gy/h in 2007 (Geras’kin et al., 2012). In legends estimated dose rates at the sites are given in mGy/h. * e difference from the reference population is statistically significant at p < 0.05.

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(Clements and Rohr, 2009; Knights et al., 2013; Scheffer et al., 2009).

Biological systems are well-adapted to their native environment and usually tolerate to clines in environmental factors without obvious signs of stress. Indeed, there seem to be no visible harmful ecosystem-level effects that can be attributed to radiation under conditions of normal operation of nuclear facilities. However, in- direct responses at population and ecosystem levels are routinely observed at dose rates that occur in case of severe radiation acci- dents (Alexakhin et al., 2004; Geras’kin et al., 2008) as well as in some storage reservoirs of liquid radioactive waste (Pryakhin et al., 2016). In general, the complexity and non-linearity of ecosystem structure and functioning could lead to unexpected consequences of stressor effects that would otherwise appear harmless if assessed within a narrow context of traditional organism-based approach. Regulatory structures and approaches to protecting the environ- ment from ionizing radiation still have relied on outcomes that cannot completely cover the risks prevalent in real ecosystems.

The role of micro-evolutionary processes in responses of pop- ulations to low-level chronic exposure is still poorly understood. Natural populations can respond to radioactive contamination not only by common genetic alterations, but also by radioadaptation, which implies physiological acclimation or changes in sexual, age or genetic structure of populations. As a result, man-made contamination may increase resistance to pollution. However, every adaptation bears its costs associated with the loss of genetic diversity (van Straalen and Timmermans, 2002). This, in turn, leads to diminish the adaptive potential towards other stresses. On the other hand, there are radioecological situations in which enhanced radioresistance does not evolve or does not persist (Geras’kin et al., 2013). Therefore, a clear understanding of exposure history has fundamental importance for predicting how populations and eco- systems recover from radiation exposure.

Since radioadaptation plays an important role in response of populations to radiation exposure under natural setting, this in- formation is directly applicable for predicting impacts of radionu- clides at the population level and for ecological risk assessment. This process needs to be considered within the framework of developing management programmes, which are designed to minimize biodiversity loss under conditions of chronic exposure to radionuclides. However, with few exceptions, the importance of evolution tends to be ignored both in a broader discussion about radiation protection criteria for the environment and in develop- ment of new approaches for environmental risk assessment.

We are currently facing environmental uncertainty about

ecosystems response to inevitable increases in human habitat use. Human activity has resulted in simplified ecosystems that rapidly respond to external influences in an unpredictable fashion (Folke et al., 2004). Nowadays any release of radionuclides or a radiation accident, like at the Fukushima NPP, takes place at the time when many natural ecosystems have already been under pressure by habitat destruction, invasive species, and the chemical pollution. In such a situation the effects of radiation exposure may become more harmful and lead to emergence of adverse effects at the lower levels of radioactive contamination.

An integration of basic ecological principles into the design and implementation of radio-ecological research is essential for pre- dicting effects of radiation within the context of rapidly changing environmental conditions. The impact of environmental factors on the effects of radionuclides (although it is not considered in most cases) could be very important at all biological levels of complexity (Fischer et al., 2013; Noyes et al., 2009). Interactions of rapid climate change and radioactive contamination could compromise homeo- stasis and physiological responses, and potentially impair fitness, reproduction, and development (Noyes et al., 2009). Even without any change in levels of radiation exposure, climatic changes may affect sensitivity of organisms. Long-term radiation exposure can result in acquired tolerance at the population or community levels (Geras’kin et al., 2013), but an associated cost of tolerance may be the reduced potential for tolerance to subsequent climatic stress, or vice versa (Moe et al., 2013). Radiation exposure may further hinder the ability of organisms to acclimate and make them more sus- ceptible to infectious and vector-borne diseases (Dmitriev et al., 2011; Morley, 2012). In addition, species with short generation times, such as pathogenic microorganisms and insects, may adapt much faster to radioactive contamination than species with long generation times. Responses to such multiple stressor effects at different biological levels and temporal scales are not considered in current risk assessment practices and still need to be evaluated.

When disturbances are moderate, many populations and eco- systems may be able to persist through phenotypic plasticity or genetic change. As anthropogenic influences intensify, plasticity and genetic adaptation may be pushed to their limits. As a result, a loss of natural resistance, which is caused by long-term chronic exposure, may trigger a threshold response and shift the ecosystem to an alternative state (Scheffer et al., 2001). In a world of ever- more-pervasive anthropogenic impacts on natural communities, coupled with the increasing certainty of global change, such “ecological surprises” will become more common (Paine et al., 1998). In addition, abrupt changes to alternative stable states

S.A. Geras’kin / Journal of Environmental Radioactivity 162-163 (2016) 347e357356

more likely occur in contaminated ecosystems that are simulta- neously subject to effects of global change (Clements and Rohr, 2009; Moe et al., 2013). Therefore, efforts to reduce the risk of undesired shifts between ecosystem states should address gradual changes that affect resilience rather than focus all efforts on trying to control disturbance and fluctuations. If a state shift occurs after a threshold is exceeded, recovery may not take place until radionu- clide concentrations are reduced significantly below levels that triggered the initial shift. In light of the possibility of such changes and their implications for human well-being, the capacities for self- repair of ecosystems can no longer be taken for granted. Societies and scientists should begin to prepare themselves for novel and unanticipated consequences of previously well-understood phe- nomena. Active adaptive management will be required to help sustain or to create desired states of ecosystems.

Acknowledgements

The presented work was supported by the Russian Scientific Foundation (grant 14-14-00666). The author is very grateful to Dr. A. Møller, Universite Paris-Sud, France, for critical reading of the manuscript and help in improving the English of the paper. This article also benefited from the comments of three anonymous reviewers.

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