Will global warming affect soil-to-plant transfer of radionuclides?

Journal of Environmental Radioactivity 99 (2008) 1736–1745

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Will global warming affect soil-to-plant transfer of radionuclides? M. Dowdall a, *, W. Standring b, G. Shaw c, P. Strand b a

Norwegian Radiation Protection Authority, Environmental Unit, Polar Environmental Centre, Hjalmer Johansens Gt., 9296 Tromsø, Norway Norwegian Radiation Protection Authority, PO Box 55, N-1332 Østerås, Norway c School of Biosciences, Faculty of Science, University of Nottingham, University Park, Nottingham NG7 2RD, UK b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 25 September 2007 Received in revised form 13 June 2008 Accepted 16 June 2008 Available online 3 August 2008

Recent assessments of global climate/environmental change are reaching a consensus that global climate change is occurring but there is significant uncertainty over the likely magnitude of this change and its impacts. There is little doubt that all aspects of the natural environment will be impacted to some degree. Soil-to-plant transfer of radionuclides has long been a significant topic in radioecology, both for the protection of humans and the environment from the effects of ionising radiation. Even after five decades of research considerable uncertainty exists as to the interplay of key environmental processes in controlling soil–plant transfer. As many of these processes are, to a lesser or greater extent, climatedependent, it can be argued that climate/environmental change will impact soil-to-plant transfer of radionuclides and subsequent transfers in specific environments. This discussion attempts to highlight the possible role of climatic and climate-dependent variables in soil-to-plant transfer processes within the overall predictions of climate/environmental change. The work is speculative, and intended to stimulate debate on a theme that radioecology has either ignored or avoided in recent years. Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: Climate change Environmental change Radionuclides Soil-to-plant transfer factors Terrestrial radioecology

1. Introduction The past decade has been a period of a concerted international scientific effort regarding changes in the global climate and its effects on all facets of life. The findings of scientific groups such as the Intergovernmental Panel on Climate Change (IPCC) and Arctic Climate Impact Assessment (ACIA) are beginning to reach consensus regarding climate/environmental change and probable future impacts. The nature and magnitude of the predicted changes and impacts are so wide ranging and fundamental that it appears that there are few aspects of the environment that will not be affected as a result of significant changes from global to microscopic scales. Radioecology is grounded in an understanding of fundamental environmental processes, specifically those controlling radionuclide behaviour in the environment. It is reasonable to conclude that any parameter controlled by these processes, in this case soilto-plant transfer, may also be affected. With this in mind, the intention of this discussion is to consider the possibilities regarding climate change effects on soil-to-plant transfer of radionuclides. As climate/environmental change will impact regions and ecosystems differently, a limited set of variables is discussed –

* Corresponding author. Tel.: þ47 77750167; fax: þ47 77750171. E-mail address: [email protected] (M. Dowdall). 0265-931X/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.jenvrad.2008.06.012

primarily temperature, precipitation and consequent changes in soil properties. Significant changes are also predicted in atmospheric CO2 levels and UV-B exposure, but as these are more relevant to physiological vegetation responses, discussion is limited. By focussing on temperature and precipitation we do not imply that these are the only variables of potential consequence to radioecology: factors such as radon flux, species assemblages, land use patterns and agricultural practices may also merit future consideration. This discussion does not aim to comprehensively review soil-to-plant transfer as excellent reviews already exist (see for example Coughtrey and Thorne, 1983; Ehlken and Kirchner, 2002), but confines itself to climate-vulnerable aspects of soil-to-plant transfer. A comprehensive overview of climate change predictions, their scientific basis and potential impacts can be found in IPCC (2001a,b), ACIA (2004) and Christensen et al. (2007). Fig. 1 shows global climate change predictions up to 2100 from Christensen et al. (2007), indicating that the probable type and magnitude of change are highly variable from one region to another. These changes are likely to affect soil properties which control soil-to-plant transfer of radionuclides. Assessing how soil–plant systems in specific ecosystems may be affected by such changes is extremely difficult but it is reasonable to consider individual soil properties and try to assess whether, individually, these could affect soil-to-plant transfer.

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Fig. 1. Regional climate change predictions for mean and extreme precipitation, drought and snow based upon Atmosphere–Ocean General Circulation Model (AOGCM) studies, Regional Climate Models, statistical downscaling and process understanding. The background map indicates degree of consistency between 21 simulations for the direction of precipitation changes. From Christensen et al. (2007). Scenario descriptions can be found in Nakicenovic et al. (2000). Figure reproduced from Christensen et al. (2007).

2. Climate/environmental change: potential impacts on the physicochemical properties of soils Soils are the product of their geological parent material and the climate under which they develop. A limited set of soil processes and constituents are found globally though their role varies with climatic region and ecosystem. The complexity of soil and the behaviour of some radionuclides make it difficult to predict soilto-plant transfer, as reflected by the wide ranges of transfer factors (TFs) reported in the literature. Soil-to-plant transfer depends on soil properties controlling bioavailability, as well as the radioelement (and chemical analogues) and specific physiological demands of the plant. Frissel et al. (1990), VanBergeijk et al. (1992) and others have collated databases of TFs from field and laboratory studies and identified key soil properties involved in soil-to-plant transfer of radionuclides: pH, soil organic matter (SOM), clay content and mineralogy, cation exchange capacity (CEC), moisture content, nutrient status (including concentrations of analogue elements such as Ca and K), the ionic nature of the soil solution and factors influencing radionuclide partitioning between liquid and solid

phases. The relative importance of these properties depends on the radionuclide considered and local conditions including temperature, precipitation and dominant plant species. 2.1. Influence of temperature and precipitation The two primary climate change variables are temperature and precipitation, both of which are significant to soil-to-plant transfer. Higher temperatures are predicted to result in increased cracking and fissure formation in temperate clay soils resulting in accelerated runoff and increased erosion (Armstrong et al., 1994; Flurry et al., 1994), reducing soils’ filtration capacity and increasing nutrient losses (Rounsevell et al., 1999). Seasonal increases in precipitation may not result in wetter soils on average since soils may also experience increased water loss by evapotranspiration at higher temperatures. Precipitation affects radionuclide transfer in several ways. Soil resuspension or rain splash can increase the soil-to-plant transfer of radionuclides depending on soil texture and rainfall intensity/ amount, both of which are vulnerable to climate change

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(Armstrong et al., 1994; Rounsevell et al., 1999). The extent of these effects is environment-specific but it is likely that this vulnerability may increase transfer in both arid/semi-arid environments and temperate regions. Resuspension of deposited radionuclides via rain splash is a significant process by which radionuclides can be transferred to plants’ surfaces and in combination with wind, it is probably the most important mechanism by which actinides and other radionuclides are transferred to plants in arid and semi-arid environments (see for example Hakonson, 2007). Resuspension has also been demonstrated as a transfer mechanism for more temperate regions and extensive literature on the matter exists since the early 1980s (see for example Dreicer et al., 1984). As soil texture and the intensity, duration and frequency of rain events play a role in resuspension and these four are predicted to undergo changes in the future, the potential exists for resuspension to increase in importance as a transfer mechanism and result in greater transfer for a number of environments. A subsequent section will discuss soil moisture content in relation to soil-to-plant transfer. A third mechanism related to precipitation is physical transport of radionuclides attached to soil particles out of the rooting zone. Evidence exists that temperature effects on soil–metal interaction/retention is not limiting for plant uptake, as some evidence of increased plant uptake of metals with temperature is available (Hooda and Alloway, 1994). Temperature can play a role in the amount and the rate of metal adsorption to soil particles (Barrow, 1992) and Almås et al. (2000) found that increased temperature increased the fixation of 109Cd and 65Zn tracers to soil, however, the addition of organic matter decreased this effect. 2.2. Soil organic matter (SOM) The IPCC (2001b) discusses the agricultural implications of climate scenarios for soil properties. Predicted precipitation/temperature changes will affect soil moisture and SOM with consequent effects on soil structure, redox potential, pH, nutrient levels, water retention capacity and cation exchange capacity (CEC). SOM contents depend upon a system of inputs from vegetation and outputs via decomposition by soil organisms. Inputs tend to increase with temperature and atmospheric CO2 levels (Loiseau et al., 1994) though increased decomposition under the same conditions may lead to an overall decrease in SOM (Berg et al., 1993; Kirschbaum, 1995; Kirschbaum et al., 1996). Post et al. (1982) and Kirschbaum (1995) suggest this is more relevant for the cooler regions of Europe. Among others, Peterjohn et al. (1994), Neff and Hooper (2002) and Katterer et al. (1998) have confirmed the roles of temperature and aeration in SOM decomposition rates, with increasing decomposition outstripping the return of carbon to soils via primary productivity. Increasing soil moisture contents and decreasing temperatures increase SOM contents (Robinson et al., 1995), although decomposition rates vary across soil carbon sinks (Parton et al., 1987). Reductions in precipitation can result in increases in the oxidative status of organic soils (Pregitzer and Atkinson, 1993). Short term enhanced productivity due to increased temperature or CO2 can be offset by changes in soil structure (cracking and accelerated runoff) which increases nutrient leaching (Rounsevell et al., 1999; Shaver et al., 1992; Bhattacharya and Geyer, 1993). Climate/environmental changes might also change the type of SOM present. SOM constituents (humic and fulvic acids) play a major role and are largely responsible for a soil’s CEC, structure, nutrient status and retention of heavy metal cations (Sholkovitz and Copeland, 1981). Whereas SOM was formerly characterised on the basis of humic, fulvic and humin fractions, now ‘‘pools’’ of carbon are defined (Reeves, 1997) which have specific properties and turnover rates within different soil types. Generally, these

include dissolved organic matter (DOM, <0.45 mm), particulate organic matter (POM: >53 mm plus ‘‘light’’ fraction by floatation), humus (non-humic and humic substances) and inert organic matter (IOM) comprising materials such as charcoal (e.g. Skjemstad et al., 1998). ‘‘Light’’ fractions and POM have turnover times in soil of several years whilst humified materials may remain unaltered for decades (Krull et al., 2003). Humified materials can be subdivided into humic materials that are physically or chemically protected against further breakdown and a non-protected group that experiences normal decomposition processes (e.g. Dalal and Chan, 2001). The different vulnerabilities of these two subgroups to temperature change has been debated: Knorr et al. (2005) hypothesised that non-labile SOM is most temperature sensitive while Fang et al. (2005) and Reichstein et al. (2005) disagree. The sensitivity of SOM temperature response can be affected by changes in microbial communities (Conant et al., 2004) and soil moisture (Waldrop and Firestone, 2004). Clearly, the ‘‘pool’’ in which any specific radionuclide resides will determine its behaviour in response to climate/environmental changes. A decrease in precipitation or an increase in temperature can increase the oxidation rate of organic materials and Kuntze (1993) has estimated 40% losses in total volume of agricultural peat soils under certain climate change scenarios (decreased precipitation and increased temperature). The pH of organic soils can be lowered by leaching of cations due to heavy precipitation (Brinkman, 1990). Varying amounts of information exist regarding SOM and the behaviour and transfer of specific radionuclides such as Sr, U, Pu, Ra, Th and Tc (e.g. Stevenson and Fitch, 1986; VanBergeijk et al., 1992; Szalay, 1958, 1964; Sheppard, 1980; Sheppard and Evenden, 1992, 1988; Vyas and Mistry, 1981; Bondietti, 1974; Stalmans et al., 1986; Yanagisawa and Muramatsu, 1995; Tagami and Uchida, 1997; Standring et al., 2002). The amount of SOM present has been shown to be one of the factors that can affect soil-to-plant transfer of a range of radionuclides, by directly or indirectly controlling their availability. Determining the vulnerability of an ecosystem to changes in the role of SOM resulting from climate changes would require information about the ecosystem, soil type, radionuclide contamination and the likely changes in SOM. The literature indicates varying vulnerabilities of SOM fractions to climate change and a relative lack of information about which specific SOM ‘‘pool’’ (if any) is most significant in soil-to-plant transfer for specific radionuclides. A reduction of 2% SOM might not be expected to affect transfer, but if that small fraction was primarily responsible for binding a specific radionuclide then the overall effect may be highly significant. Frissel et al. (1990), collating soil-to-plant transfer data and relationships between transfer and soil parameters, highlighted the difficulties in determining what effect climate driven changes in SOM would have. Plant uptake depends on a range of intrinsically linked factors in a complex system, which varies from one radionuclide to another. However, given that SOM interplays with many of these factors, climate driven changes in SOM could be expected to affect soil-to-plant transfer of radionuclides. Livens and Loveland (1988) list clay mineral contents, pH, SOM þ content as factors determining the biocontent, NHþ 4 and K availability of Cs. The role of SOM in Cs behaviour in soils has been much debated (e.g. Sheppard et al., 1980; Brouwer et al., 1983; DeJong et al., 1986; Fawaris and Johanson, 1995). Barber (1964) identified SOM as an important factor in the transfer of 137Cs to plants and several later studies have concluded that Cs uptake is relatively high in organic soils (Absalom et al., 1996; Sanchez et al., 1999). Cs interacts with both humic and clay substances (primarily illite and vermiculite) becoming firmly fixed (Tamura and Jacobs, 1960; Comans et al., 1991). Fixation processes have been described via binding of Cs to sites within or on the edge of mineral lattice particles which are specific for Csþ (DePreter, 1990; Valcke and

M. Dowdall et al. / Journal of Environmental Radioactivity 99 (2008) 1736–1745 þ þ Cremers, 1994). Ions such as Kþ, NHþ 4 and Rb compete with Cs for these sites. In a recent review, Rigol et al. (2002) concluded that only in soils with an excess of 95% organic material and insignificant clay content does Cs adsorb primarily to non-specific sites, that enhanced Cs transfer to plants is due to low clay contents, þ high NHþ 4 and low K soil solution concentrations and that, in soils with less organic matter, Cs sorption is controlled by clay minerals. However, Staunton et al. (2002) concluded that SOM can reduce the affinity of clay minerals for radiocesium and contribute to higher plant uptake. In general, SOM plays a variety of roles in soil-to-plant transfer, via mechanisms affecting the physicochemical nature of the soil such as CEC, pH, redox potential, moisture content and soil structure. Stevenson (1994) reported that SOM contributes between 25 and 90% of a soil’s CEC. Haynes and Naidu (1998) estimated this contribution to be 40–50% while Loveland and Webb (2003) estimated 30–60%. Moreover, the CEC of a soil is sensitive to slight changes in SOM as demonstrated by McGrath et al. (1988) and Eshetu et al. (2004). The intrinsic relationship between CEC, pH and soil buffering capacity is described as being partly dependent on SOM content, any change in SOM content is therefore likely to affect these parameters. The water holding capacity of a soil is of primary radioecological concern. Total plant-available water is the amount of water held by the soil between field capacity and the permanent wilting point and radionuclides in this water fraction are plantavailable. SOM increases plant-available water by affecting the soil’s bulk density and the nature of the soil aggregates (Khaleel et al., 1981; Haynes and Naidu, 1998; Emerson and McGarry, 2003). Many authors contend that increasing SOM content increases the water holding capacity of a soil, though the extent and reasons for this are debated (Danalatos et al., 1994; Loveland and Webb, 2003; Rawls et al., 2003). Changes in SOM content will most likely occur in combination with changes in precipitation and temperature. Thus, it is likely that soil moisture content may be one of the most obvious impacts of future climate scenarios. The impact of soil moisture on radionuclide uptake has been studied occasionally although conclusions are inconsistent. Pendleton and Uhler (1960) reported increased radionuclide accumulation by plants with increasing moisture. However, Kulikov et al. (1973) and Ehlken and Kirchner (1996) reported the opposite.

2.3. Climate change and dissolved organic carbon/matter (DOC/DOM) An increase in freshwater DOC in the UK was reported recently by Evans and Monteith (2001) and Evans et al. (2005), and it has been proposed that increased temperatures drive increased leaching of carbon from peat soils (Freeman et al., 2001; Worrall et al., 2003). Hejzlar et al. (2003) reported increased DOM in South Bohemian waterways while Schindler et al. (1997), Driscoll et al. (2003), Stoddard et al. (2003) and Skjelkvåle et al. (2005) have reported similar results from the Nordic countries and US. Increasing DOM in waterways indicates a loss of SOM from catchment soils. Insam (1990) has shown that microbial conversion of SOM to low molecular weight (LMW) DOM compounds is driven by temperature, hydrology and nutrient status. Eivazi and Tabatabai (1990) also demonstrated the role of pH, redox potential and certain inorganic species in this process while Pastor et al. (2003) concluded that increases in DOM cannot be explained solely by temperature increases. Testing the hypothesis that climate change alone accounted for DOM increases, Worrall et al. (2004) concluded that a reported temperature rise of 0.78  C could only account for some of the observed DOM increases although Bonnett et al. (2006) showed that 87% of seasonal variation in Welsh DOM concentrations was due to soil temperature. The authors believe that further increases in temperature and consequent changes in hydrology, pH,

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redox potential and nutrient status will influence DOM discharges, increasing DOM concentrations in runoff waters. Possible climate-induced increases in DOM leaching from soils are interesting from a radioecological point of view. Firstly, peat (upland and lowland) and organic soils constitute a significant sink for several natural and anthropogenic radionuclides. Secondly, DOM plays a major role in the mobility and availability of metals (Lawlor and Tipping, 2003) and increased organically associated Al and Fe have been observed at sites with increased DOM in soil waters (Evans et al., 2005). Bunzl et al. (1998) studied the association of Pu, Am and Cs with different molecular size fractions of DOM found in podsols and a peat soil within 10 km of the Chernobyl nuclear power plant. Pu and Am were observed in all DOM size fractions (between >2000 and 560 Da) in a well-decomposed soil (deep peat), while Cs was only observed in one LMW DOM fraction in a less humified soil. Agapkina (2002) reported on the occurrence of anthropogenic radionuclides in soil solutions demonstrating that association of radionuclides with different molecular weight fractions of DOM is radionuclide- and soil typedependent. Most 238Pu, 239þ240Pu and 241Am (72–98%) was bound with dissolved organic matter. In organic horizons, these radionuclides were selectively associated with high molecular mass fractions (Mw 2000). Sr radioisotopes were mostly present as inorganic compounds (19–100%) and in the low molecular mass organic matter fraction (Mw 350–500). 137Cs was not observed to interact selectively with specific organic molecular mass fractions, but was present in a wide range of ‘‘organic’’ fractions (34–97% in Mw 350 to 18,000) as well as in the inorganic fraction. Bednar et al. (2004) have also explained Th mobility in semi-arid soils by association with DOM. The fact that DOM plays a role in the mobility and bioavailability of many radionuclides and that climate-influenced changes appear to affect DOM runoff suggests a potentially significant link between climate change and the behaviour of some isotopes in the terrestrial environment. 2.4. Climate/environmental change: soil organisms and soil-to-plant transfer Wide optimal temperature ranges for the functioning of soil communities lead to uncertainties in assessments of climate/ environmental change effects (Tinker and Ineson, 1990; Smith et al., 1998). Rounsevell et al. (1996) and Swift et al. (1998) discuss changes that may occur in soil functional types when soil organisms are affected by changes in CO2 concentrations and moisture availability. The complex interaction between fine plant roots, the rhizosphere, microbial communities and soil fungi has received attention in relation to climate/environmental change but no clear picture of the potential impacts has emerged. Clemmensen et al. (2006) observed increased nitrogen/carbon cycling in ectomycorrhizal fungi responding to warmer conditions in arctic tundra. Yuste Curiel et al. (2003) monitored soil respiration in a moist temperate pine forest, identifying temperature as the controlling factor (soil respiration decreases in response to soil moisture were less than 15%). They concluded that, even in maritime climates, rainfall played a controlling role in carbon turnover by soil biomass indicating soil communities are vulnerable to climate change. The ‘‘Birch Effect’’ demonstrates soil biomass response to precipitation and temperature (Jarvis et al., 2007), where wetting of the soil after summer dry periods produces a burst of CO2 generation due to increased decomposition and mineralisation. Wet/dry cycles and their impacts on soil biomass are likely to increase under predicted climate changes, with more intense warm periods and increased precipitation. The role of mycorrhizae, soil bacteria and rhizospheric effects on soil-to-plant transfer has received some attention, particularly in studies undertaken after the Chernobyl accident. Olsen et al. (1990) discussed the important role of soil

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fungi and the symbiotic relationship between mycorrhizal fungi and plant roots as a means of transferring 137Cs from soil to plants. However, no clear role of mycorrhizae in the transfer of radiocesium was observed by Drissner et al. (1998) in a forest ecosystem. Stemmer et al. (2005) did, however, find evidence of microbial biomass playing a role in radiocesium transfer at higher altitude sites on an ascending altitude transect. Clint and Dighton (1992) and Berreck and Haselwandter (2001) studied the role of mycorrhizae on radiocesium uptake in heather and grass with conflicting results. Clint et al. (1989) studied 137Cs release patterns in two groups of litter samples, moist and wet/dry cycled. The latter had slower release of 137Cs and lower soil respiration, which is contrary to the ‘‘Birch Effect’’ though it is possible that laboratory conditions isolated the soil litter from communities present in the field. 3. Evidence for the influence of climate on soil-to-plant transfer Studies of direct climatic effects on plant uptake of radionuclides are rare. However, studies into seasonality, altitude and comparison of radionuclide uptake in different climatic zones can potentially be used to glean useful climate-related information. 3.1. Radionuclide uptake in vegetation: seasonal variations Seasonal variation of plant uptake has been studied, directly and indirectly, by a number of authors. Studies vary from long term (years) field trials to short term laboratory experiments and have examined variation in uptake with and within season to various plant parts. Sandalls and Bennett (1992) conducted a multi-year study on radiocesium uptake in grass species on upland soils (peat and brown earths), observing seasonal patterns and climatic conditions were noted as a possible influence though no specific controlling climate variable was identified. Rafferty et al. (1994a) performed a one-year study at three different sites in Ireland, reporting monthly concentration ratios for 40K and 137Cs in grasses. Highest transfer of 137Cs was observed in the winter months whereas the highest transfer of 40K was during spring–summer. Seasonal variability in the transfer of soil particles to vegetation surfaces (high transfer in winter due to short grass, high rainfall and high grazing intensity) was concluded to be the most likely explanation and was confirmed by further study (Rafferty et al., 1994b). Kirchner and Ehlken (1997) noted some weak general trends with temperature and precipitation and concluded that the interplay of variables with soil hydrological properties caused seasonal variations in uptake. Ehlken and Kirchner (1996) observed seasonal fluctuations in 137Cs, 134Cs, 90Sr and 40K transfers in North German soils in a multi-year field study, though no specific pattern was evident. Site-specific positive correlations between plant concentration of 137Cs and air temperature and rainfall were observed for some sites (based on soil type) but negative correlations at others. Sr-90 root uptake tended to be lower after heavy rainfall at some sites. Strebl et al. (2002) observed seasonal patterns for 40K and 137Cs uptake, with decreasing transfer through May and July rising to a peak in September for a variety of species and soil types. Salt and Mayes (1991) observed significant correlations between radiocesium uptake and air temperature. Marked seasonality in transfer observed in a Mediterranean ecosystem for a range of nuclides were discussed by Baeza et al. (1996, 2001) who concluded that variations were due to changing temperature and humidity over the season and not changes in availability of radionuclides in soil. Twining et al. (2004) studied soil–plant transfer in a tropical monsoon environment, concluding that redox shifts and changes in fungal populations could account for seasonality in transfer, highlighting the potential for enhanced uptake of a range of radionuclides. Salt et al. (2004) discussed the lack of a specific

seasonal pattern to uptake and two general patterns of seasonality with respect to radiocaesium were described by Salt (2007): (a) a rise in spring towards a peak in summer with decline through the autumn and a winter low or (b) a rise in the spring with decline over summer and autumn to a winter low. There is a general lack of data describing seasonality in uptake for other radionuclides, although Hartmann and Bachmann (1988), observing seasonality of Pu uptake in tree species, advocated that the role of meteorological (and hence climatic) variables requires more study. Whilst evidence exists that at least radiocaesium exhibits some seasonality in soil-to-plant transfer, it is the reasons for this that are of interest regarding climate change. Willey and Martin (1995) proposed soil moisture as the factor involved in seasonality of stable Cs uptake. Salt et al. (1996) observed different patterns in uptake of 137Cs and 40K where water stress was eliminated as a variable, concluding that declining 40K towards the end of the summer was related to diminishing plant growth. Kirchner and Ehlken (1997) provided what is possibly the best evidence for the impact of short term seasonal climatic changes on uptake of Cs and Sr and suggested the impact of variables such as precipitation, may be masked depending on the soil type studied, some soils having better water retention capacities than others. An added complexity is the physiological changes which plants undergo throughout the seasons, which are likely to affect uptake such that seasonality is a result of both physiological and climatic influences. 3.2. Radionuclide uptake in vegetation: altitude studies A few studies have been conducted in which altitude appears to function as a reasonable surrogate for climate differences. Echevarria et al. (2003) studied the uptake of 99Tc at two locations in France which were at different altitude but with similar geology and topography, in order to simulate the effect of climate on both the soil characteristics and uptake of 99Tc. They observed higher CRs under the warmer lowland regime than for the higher cooler regime. Lettner et al. (2006) demonstrated an increase in 137Cs TFs with altitude at an Austrian site, concluding that a combination of climatic variables, including temperature and precipitation, were responsible. 3.3. Comparisons of soil-to-plant transfer in climatic regions Comparative studies between different climatic regions may offer insights into possible effects of climate change. Studies conducted in extreme Arctic environments may not be applicable as such conditions are unlikely to apply to predicted climate change scenarios. A number of relevant studies do exist such as the IAEA coordinated research projects (CRP) ‘‘Transfer of Radionuclides from Air, Soil and Freshwater to the Foodchain of Man in Tropical and Subtropical Environments’’ and ‘‘Classification of Soil Systems on the Basis of Transfer Factors of Radionuclides from Soil to Reference Plants’’ (IAEA, 1997, 2006; Frissel et al., 2002). The former concluded that no systematic differences existed between TF values in temperate, subtropical and tropical ecosystems. However, some ecosystems exhibited TF values that differed from average values by over an order of magnitude, precipitating the second study which focussed on transfer in relation to soil type. A number of points can be made in relation to the second IAEA study and its finding that ‘‘there are no significant differences between soil-to-plant transfer factors in temperate, subtropical and tropical environments’’. First, it examined commercial crops grown in agricultural systems using local agricultural practices, hence possible climate effects could have been masked. Secondly, it is possible that soil–plant transfer in natural or semi-natural ecosystems is particularly sensitive to changes in climate regime. It is further possible that the CRP did not adequately consider specific climate driven processes that may

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affect transfer over periods longer than those studied or the effect of climate on transfer within as opposed to between climate regions. Uchida (2007) observed the largest deviation of TF values from the average for sub- and tropical environments. A review by Carini (2001) of soil-to-fruit transfer in temperate and (sub)-tropical regions concluded that Cs transfer was higher in (sub)-tropical regions while transfer factors for Sr, Pu and Am were lower for the same species (though this observation may have been influenced by other factors). High intensity weathering in tropical zones produces soils depleted in cations, where the dominant structural role is played by Fe and Al oxide/hydroxides and with lower quantities of minerals such as kaolinite present. Tropical soils exhibit high SOM turnover due to enhanced biological activity, although high inputs of organic matter compensate for rapid losses, decreasing the difference in SOM between temperate and tropical soils (see Parton et al., 1989; Theng et al., 1989). Loss of soil material can be substantial due to intense periods of heavy precipitation. Twining et al. (2006) reported changes in redox potential in Australian tropical soils over one growing season, concluding that these changes may affect redox sensitive radioelements, especially Tc and Pu. Li et al. (2006) concluded that annual variability in TF values may be due to climatic factors. Al-Oudat and Al-Asfary (2006) observed TF values in a cereal species in a semi-arid ecosystem at the lower end of the expected range (IAEA, 1994), concluding that climatic conditions may have reduced 137Cs uptake compared with temperate areas. Topcuog˘lu et al. (2006) observed higher 137Cs TF values for brassicas (cabbage family) and maize species grown under warm, sheltered conditions compared with exposed conditions, concluding that climatic conditions affected the biokinetics of 137 Cs in these plants. Jianguo et al. (1997) observed significantly

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lower uptake of a range of isotopes of Cs, U, Ra and Sr in a broad suite of agricultural crops for subtropical regions of China compared with those obtained in temperate zones. 4. Is climate/environmental change going to impact soil-to-plant transfer? The difficulty in trying to predict definite affects of climate or environmental change on soil-to-plant transfer from information currently available is probably best indicated by Kirchner and Ehlken (1997) who stated: ‘‘Of primary influence on the processes discussed (those governing soil-to-plant transfer) are climatic variables, in particular solar radiation, temperature and precipitation. Surprisingly, the potential influence of climatic variables on radionuclide concentrations in plants was studied only rarely and with conflicting results.’’ Little research on the specific effects of climatic variables on soil-to-plant transfer has been conducted to date and attempting to conduct analyses on the databases of TF values that exist is complicated by the variability of the data. The only useful information that could be obtained from such databases would be differences in soil-to-plant transfer between climatic zones which does not provide any information on how soil-to-plant transfers may change within any particular climatic zone. The potential for affects, however, is evident. Fig. 2 represents the dominant processes generally accepted to govern soil-to-plant transfer ofradionuclides. As can be seen, a significant proportion of these processes are vulnerable to changes in climatic variables such as temperature or precipitation. Although identifying vulnerable processes is relatively simple, predicting the effects of variations in these processes is not for two main reasons: the interplay and feedback mechanisms

Fig. 2. Schematic of processes involved in the transfer of radionuclides from soil to vegetation (after Schreckhise, 1980). Transfer processes outlined in red represent those vulnerable to climate change.

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Table 1 Potential for changes in soil-to-plant transfer of radionuclides for three generic soil types with respect to climate-vulnerable parameters Parameter

Possible change

Precipitation

Increase in total amount

Arid/dryland soil

Y Long term – loss of radionuclides via runoff/migration out of soil/rooting zone Increase in event freq./intensity [ Increased resuspension

Organic matter SOM loss CEC reduction Moisture reduction DOC discharge

[ Cs, Sr, U, Pu [ For Cs, Sr, U, Pu

Temperature

4 4

General increase Structural changes in soil

4

between these processes and the information that exists to date on their roles in the transfer of a range of nuclides. Nevertheless, Table 1 provides a necessarily general summary of possible scenarios in an attempt to tentatively describe how changes in climate could possibly affect transfer in a limited number of environments. Whatever the predictions as to climate/environmental change, it does not seem likely that such changes could result in a significant increase in the dose to man due to any possible increases in transfer. Seasonal variations such as those reported by Ehlken and Kirchner (1996) in 90Sr and 137Cs values do not exceed an order of magnitude throughout their study, those of Sandalls and Bennett (1992) also being of the order of 2 or 3. These studies, however, involve systems operating within the ranges of a normal seasonal cycle and cannot reflect a situation where a seasonal cycle is superimposed upon a long term shift in climatic parameters. The effects of such decadal scale climate and environmental changes can only be observed through the establishment of long term systematic monitoring strategies. Laboratory and field based studies may also further efforts to elucidate the potential of climate/environmental changes affecting the fundamental radioecological process of soil-to-plant transfer. The techniques for simulation of the type of warming likely to occur in coming years are well established and have been used in ecological studies for some years. A number of facilities exist designed for the type of studies necessary already are in operation, notably facilities such as the Artificial Climate Experiment Facility (ACEF) of the Institute for Environmental Sciences in Japan and the Risø Environmental Risk Assessment Facility (RERAF) in Denmark. 5. Conclusion There is little doubt that climate/environmental changes are now a probability rather than a possibility, despite the uncertainties related to the predictions being made by scientists. Of the range of processes and parameters related to the soil-to-plant transfer of radionuclides, it is plain that some of them are climate dependant to some degree. There is some evidence of the effect of climate parameters on radionuclide behaviour, derived from nonideal but relevant surrogate studies such as those into seasonal patterns of uptake, an aspect of the soil-to-plant transfer situation that has been much understudied. Certain soils, such as arid and organic soils, would appear to be potentially more vulnerable than others. As processes govern our understanding of the behaviour and ultimate fate of radionuclides in our environment, it could be considered a grave oversight not to devote some attention towards

Organic soil

Clay soil

4 Assuming water retention properties sufficient to reduce impact on runoff

Y Long term – migration out of rooting zone, increased runoff

4

[ Increased resuspension

[ For I, Y or 4 for Cs, Pu, Sr [ For Cs, Sr, U, Pu Y For Cs, Sr, I, Pu as pH increases [ For Cs, Sr, U, Pu due to colloidal increases Y For Cs, Sr, I, Pu long term due to inventory loss

[ For I, Y or 4 for Cs, Pu, Sr [ For Cs, Sr, U, Pu

Y Long term – loss of radionuclides via runoff/migration out of soil/rooting zone

Y Long term – migration out of rooting zone, increased runoff

[ For Cs, Sr, U, Pu due to colloidal increases Y For Cs, Sr, I, Pu long term due to inventory loss

establishing what climate/environmental change could mean for soil-to-plant transfer in particular and radioecology in general, for both the radionuclides we can find in the environment today and the radionuclides that may be in the environment as a result of future accidents or incidents. Acknowledgements The authors wish to acknowledge the helpful and thought provoking reviews provided by the two anonymous reviewers of this article. References Absalom, J.P., Crout, N.M.J., Young, S.D., 1996. Modeling radiocesium fixation in upland organic soils of Northwest England. Environmental Science and Technology 30, 2735–2741. ACIA (Arctic Climate Impact Assessment), 2004. Impacts of a Warming Arctic, Arctic Climate Impact Assessment. Cambridge University Press, Cambridge, United Kingdom, 139 pp. Agapkina, G.I., 2002. Organic forms of artificial radionuclide compounds in soil solutions from natural biogeocenosis. Radiatsionnaia Biologiia, Radioecologiia 42 (4), 404–411 (in Russian). Almås, Å.R., Salbu, B., Singh, B.R., 2000. Changes in partitioning of 109Cd and 65Zn in soil as affected by organic matter addition and temperature. Soil Science Society of America Journal 64, 1951–1958. Al-Oudat, M., Al-Asfary, F., 2006. Transfer of cesium-137, strontium-90 and polonium-210 from soil to maize and black cabbage crops. In: Classification of Soil Systems on the Basis of Transfer Factors of Radionuclides from Soil to Reference Plants. IAEA (International Atomic Energy Agency), Vienna, Austria, pp. 145–153. IAEA-TECDOC-1497. Armstrong, A.C., Mathews, A.M., Portwood, A.M., Addiscott, T.M., Leeds-Harrison, P. B., 1994. Modelling the effects of climate change on the hydrology and water quality of structured soils, NATO ASI Series 23. In: Rounsevell, M.D.A., Loveland, P.J. (Eds.), Soil Responses to Climate Change. Springer-Verlag, Germany, pp. 113–136. Baeza, A., Paniagua, J., Rufo, M., Barandica, J., 1996. Bio-availability and transfer of natural radionuclides in a Mediterranean ecosystem. Applied Radiation and Isotopes 47 (9/10), 939–945. Baeza, A., Paniagua, J., Rufo, M., Guillen, J., Sterling, A., 2001. Seasonal variations in radionuclide transfer in a Mediterranean grazing-land ecosystem. Journal of Environmental Radioactivity 55, 238–302. Barber, D.A., 1964. Influence of soil organic matter on the entry of cesium-137 into plants. Nature 204, 1326–1327. Barrow, N.J., 1992. A brief discussion on the effect of temperature on the reaction of inorganic ions with soil. European Journal of Soil Science 43, 37–45. Bednar, A.J., Gent, D.B., Gilmore, J.R., Sturgis, T.C., Larson, S.L., 2004. Mechanisms of thorium migration in a semiarid soil. Journal of Environmental Quality 33 (6), 2070–2077. Berg, B., Berg, M.P., Box, E., Bottner, P., Breymeyer, A., et al., 1993. Litter mass loss in pine forests of Europe: relationship with climate and litter quality. In: Breymeyer, A., Krawczyk, A., Kulikowski, B., Solon, R.J., Rosciszewski, M., Jaworska, B. (Eds.), Geography of Organic Matter Production and Decay. Polish Academy of Sciences, Warsaw, Poland, pp. 81–109.

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