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Radiocaesium accumulation in stemwood: Integrated approach at the scale of forest stands for contaminated Scots pine in Belarus
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Journal of Environmental Management 85 (2007) 129–136 www.elsevier.com/locate/jenvman
Radiocaesium accumulation in stemwood: Integrated approach at the scale of forest stands for contaminated Scots pine in Belarus Franc- ois Goora,, Yves Thirya, Bruno Delvauxb a
Centre d’Etude de l’Energie nucle´aire (SCKCEN) Boeretang, 200 B-2400 Mol, Belgium Unite´ de Sciences du sol (UCL/AGRO/MILA) Croix du Sud, 2/10 B-1348 Louvain-la-Neuve, Belgium
b
Received 5 December 2005; received in revised form 16 August 2006; accepted 21 August 2006 Available online 9 October 2006
Abstract Twenty years after the Chernobyl accident, root uptake from the surface layers of contaminated forest soils plays a major role in radiocaesium (137Cs) transfer to the trees and accumulation in perennial compartments, including stemwood. Trustworthy long-term predictions (modelling) of stemwood contamination with 137Cs should accordingly be based on a reliable picture of this source–sink relationship. Considering the complexity of the processes involved in 137Cs cycling in forest stands, elementary ratios like transfer factors (TF) were shown to be not very relevant for that purpose. At the tree level, alternatives like the wood immobilisation potential (WIP) have therefore been proposed in order to quantify the current net 137Cs accumulation in stemwood. Our objective was here to compare WIP values determined for a series of contaminated forest stands in Belarus with the corresponding pools of 137Cs available in the soil for root uptake. The comparison reveals that both indices are quite proportional, whatever the forest ecosystem features. This corroborates the relevancy of WIP as an indicator of the current 137Cs root uptake by the trees, which could accordingly help to improve the existing models of 137Cs cycling and the long-term management of contaminated forest ecosystems. r 2006 Elsevier Ltd. All rights reserved. Keywords: Radiocaesium; Forest ecosystem; Modelling; Root uptake
1. Introduction Following the Chernobyl accident in April 1986, large territories have been contaminated with radionuclides fallout in former USSR countries, and to a lower extent Western Europe, causing the main ecological and socioeconomical disaster in the history of civil nuclear power. In semi-natural ecosystems, the contamination of forest stands with radiocaesium (137Cs, T1/2 ¼ 30.2 years) is particularly worrying due to large-scale (Izrael et al., 1996) and long-term radiation exposure risks for local populations and forest workers, but also in terms of loss of economic return for the wood industry (Shaw et al., 2001) because of sanitary restrictions applied to contaminated wood use (Tikhomirov et al., 1993; Davydchuk, 1999). Corresponding author. 130/02 Avenue F. Roosevelt, 50 B-1050 Bruxelles, Belgium. Tel.: +32 2 650 2684; fax: +32 2 650 4312. E-mail addresses: [email protected] (F. Goor), [email protected] (Y. Thiry), [email protected] (B. Delvaux).
0301-4797/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jenvman.2006.08.008
Accordingly, significant efforts have been carried out, during the last two decades, to understand the fate of 137Cs in contaminated forests, and particularly its accumulation in perennial tree components like stemwood (Ipatyev et al., 1999). Up to now, the assessment of 137Cs content in contaminated forest stands has largely been based on elementary ratios, the transfer factors (TF, (Bq kg1)/ (Bq m2)), comparing the 137Cs concentration in a given tree component (Bq kg1) to the total 137Cs deposition onto the soil (Bq m2) (Nimis, 1996). TF determined for a range of forest and soil types have been widely used to assess the redistribution of 137Cs in forest ecosystems (Ipatyev et al., 1999) and to elaborate maps of trees contamination from 137Cs deposition inventories (Goor et al., 2003; van der Perk et al., 2004). The use of TF was, however, shown to be not very relevant in a longterm perspective (Thiry et al., 2002; Thiessen et al., 1999), particularly if perennial tree compartments are considered. TF-based modelling approaches fail notably
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to satisfactorily predict the 137Cs root uptake and accumulation in various tree compartments, including stemwood, as revealed for example by a statistical comparison of predictions from the main existing models of 137Cs redistribution in trees for a Chernobyl-like contamination scenario (Goor and Avila, 2003). TF provide indeed only a static picture of the 137Cs redistribution in forests, derived from the total 137Cs content in soil and tree compartments at the time of TF measurement. Conceptually, the TF approach also supposes that the whole 137Cs content in trees originates from the soil, through root uptake. Conversely, 137Cs proved to be highly mobile and recycled within trees and between trees and soil, through similar patterns as potassium, a major plant nutrient (Strebl et al., 1999; Melin et al., 1994; Myttenaere et al., 1993). Retranslocation processes can in particular account for a significant fraction of the ‘‘apparent’’ 137Cs accumulation rate in stemwood, as shown by Goor and Thiry (2004) for a chronosequence of Scots pine stands in Belarus. Similar conclusions were presented by Thiry et al. (2002), whose observations in mature contaminated Scots pine stands suggest that TF-based approaches largely overestimate the current 137Cs accumulation rate in stemwood. According to these authors, this is at least partly due to an inaccurate consideration of the consequences of canopy interception and incorporation processes, in the early period following 137Cs fallout, on the total 137Cs content in stemwood. A new approach to determine the current 137Cs accumulation rate in stemwood was therefore recently proposed: the wood immobilisation potential (WIP) (Thiry et al., 2002). Contrary to static TF, the WIP definition is based on the actual radial redistribution of 137Cs in stemwood, closely connected with the production of biomass (the WIP corresponds to the additional 137Cs per volume of new woody biomass, calculated on an annual basis). Accordingly, the WIP may be considered as reflecting the current 137Cs net accumulation rate in stemwood. Considering besides that twenty years after the Chernobyl accident, the surface layers of forest soils constitute the major source of 137Cs for the trees (Thiry and Myttenaere, 1993; Shcheglov, 1999; Plamboeck et al., 2000), the WIP likely provides a good picture of 137Cs root uptake. Clear empirical evidence of the relationship between 137Cs availability in soil for root uptake and 137Cs accumulation in stemwood, calculated using the WIP approach, is however still missing. In a long-term perspective, such a relationship has been identified as a key step for the improvement of the existing models of 137 Cs cycling in contaminated forest stands (Goor and Avila, 2003). In this context, the objective of the present study is to evaluate the relevancy of the WIP approach at the scale of forest stands by comparing WIP values with the pools of 137 Cs available from the soil, for various forest ecosystems conditions. Practically, a methodology adapted from the literature will be implemented in order to assess the pool of
137
Cs potentially available for root uptake in multilayered forest soils, and applied to a series of contaminated Scots pine stands of the Chernobyl area, covering various tree ages and types of soil. WIP values will be determined for the same stands. The paired values will then be compared, in a standardized way, in order to highlight similarities in the 137Cs accumulation (tree)–availability (soil) relationship. On this basis, the relevancy of the WIP as an indicator of the current 137Cs root uptake will be discussed. Perspectives for the improvement of the existing models of 137Cs cycling in forests as well as for the management of contaminated stands will also be discussed. 2. Material and methods 2.1. Environmental setting The sampling site is a vast Scots pine (Pinus sylvestris L.) woodland located close to Vetka (52137.80 N, 31113.10 E, 159 m above sea level) in the Gomel district, in Belarus. Following the Chernobyl accident, the Gomel area was severely affected by 137Cs fallout (Izrael et al., 1996). The climate is continental and sub-boreal. The average annual temperature is 6.5 1C, but seasonal variations are important. The average precipitation is 550 mm y1. The vegetative period lasts about 6 months, from April to October. The landscape consists of slightly sloping plateaus, intersected by a network of rivers and swampy areas. The soils derive from glaciofluvial deposits of the Quaternary age. The dominant particle size fraction is sand (85–90%). In forest areas, the soil features are closely linked to the relief and the hydrological regime (Sorokina, 1996): on the plateaus, the soil development is not determined by lateral water drainage nor by variations of the water table level (automorphic1 soils, dry conditions), whereas in the bottoms of valleys and local depressions, the soil features are largely influenced by humid conditions (hydromorphic soils). 2.2. Site sampling Forest vegetation and soils were sampled in February 2001 in five neighbouring Scots pine stands. The stands I, II and III (17-, 37- and 57-year-old trees) were established on similar former-tilled automorphic soils, and can be classified as Pinetum cladinosum (Goskom, 1984). The other stands, established on automorphic (65-year-old trees, stand IV) and hydromorphic (95-year-old trees, stand V) soils, can be classified as Pinetum sphagnosum. The total 137Cs deposition varies between 9.9 and 17.7 GBq ha1. The trees were sampled as described in Goor and Thiry (2004). Briefly, three representative average trees were chosen in each stand, on the basis of the trunk 1 ‘‘Automorphic’’ and ‘‘hydromorphic’’ refer to the local soil classification, based on edaphotopes (Sorokina, 1996).
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circumference at 1.30 m, and felled. Wood discs that were 2 cm thick, were then sampled from the trunks at 1.30 m, 6 m (5 m for the 17-year-old stand) and then every 6 m up to the top of the trees. Undisturbed soil samples (five replicates per stand, randomly distributed) were also collected from the topsoil (0–15 cm), using little plastic boxes (15 cm wide and 3 cm thick). To avoid any physical or chemical alteration, wood and soil samples were immediately put into individual polyethylene bags and stored at 4 1C until analysis. 2.3. Laboratory analyses In the laboratory, the sampled wood discs were analysed to allow WIP calculation. The surface of each disc was polished, in order to reveal the annual wood increments. This operation was limited to the surface of the wood discs, to a depth not exceeding 2 mm, which was less than 4% of the total discs volumes. The discs were scanned for further measurement of radial growth. The wood increments were then separated with a chisel, in 3-years groups, dried out and weighed. The separation of annual wood rings was realised very carefully, on fresh wood discs in order to avoid any 137Cs radial redistribution during wood drying. After burning at 550 1C in a furnace, the ashes were solubilized in 10 ml HNO3 (2 N). On the other hand, the organic (O), transition (OA) and organo-mineral (A) horizons were identified on undisturbed soil samples before analysis, and the average thickness of each horizon was measured. The different horizons were then carefully separated, air dried for 5 days at 20 1C, and weighted. The O horizons were sieved at 2 mm. The main soil properties (weight loss after ignition at 450 1C, total exchangeable cations content, cation exchange capacity (CEC) (NH4OAc 1 M pH 7) and pH (5 g:25 ml of H2O) were determined from soil aliquots using well-known procedures (Page et al., 1982). The 137Cs content in wood and soil samples was determined by gamma spectrometry (NaI detector— Minaxi g 5000 series). The value of the counter background was 30 disintegrations min1, and the lower limit of detection was 3.8 Bq. The counter efficiency (13%) was determined using reference samples, calibrated using a high-resolution gamma spectrometer. The counting time was adjusted in order to reduce the counting error below 3%. The 137Cs activities were decaycorrected back to April 26, 1986.
mobilisation (RM) (Delvaux et al., 2000). Compared to chemical 137Cs extractions, the advantages of the RM test are that the quantification of 137Cs availability is based on plant root uptake, and that previous results from a range of soil types have linked RM results with key soil properties regarding 137Cs availability, notably for contaminated forest soils (Kruyts et al., 2004; Kruyts and Delvaux, 2002; Thiry et al., 2000). It is important to note that the 137 Cs availability measured with rye-grass plantlets is not quantitatively representative of the total 137Cs uptake by trees in contaminated forest stands. The values of the pool of 137Cs available, obtained in standardised conditions using the RM test will therefore be discussed in relative terms. The RM test was carried out as described in Delvaux et al. (2000). Briefly, seeds of rye-grass (Lolium multiflorum) were first germinated on a water-saturated net for 7 days. The root mat was then placed in contact with the contaminated soil samples for 4 days (five repetitions for each soil layer). The rye-grass plantlets were finally harvested and g-counted. The 137Cs-RM is the proportion (%) of 137Cs transferred to rye-grass plantlets (whole plants, including roots) during the experiment. The total pool of 137Cs available for root uptake was then calculated as follows: Total pool of 137 Cs available in the soil ðSAÞ ½Bq cm2 ¼ Si ðThi ½Csi RMi Þ, ð1Þ with i is the soil layer (O, OA or A layer), Thi the thickness of the layer i (cm), [Cs]i the 137Cs concentration of the layer i (Bq cm3) and RMi the 137Cs RM of the layer i [%] 3.2. Current
137
Cs accumulation rate in stemwood
The current 137Cs accumulation rate in stemwood was assessed using the WIP (Thiry et al., 2002). Conceptually, the WIP was developed in order to take into account the tree age- and time-dependent radial redistribution of 137Cs in stemwood, which influences the value of the current 137 Cs accumulation rate in stemwood. Accordingly, as illustrated in Fig. 1, the WIP (Bq cm3) was defined as the
3. Theory and calculation 3.1. Total pool of
137
Cs available in the soil for root uptake
Considering the complexity of measuring the 137Cs uptake by trees in situ in undisturbed soil conditions, the pool of 137Cs available in the soil was assessed using a standardised approach of 137Cs soil-to-plant transfer, based on miniaturised experiments: the rhizospheric
131
Fig. 1. The WIP concept (adapted from Thiry et al., 2002).
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tangency (first derivative) of the [cumulated 137Cs activity ¼ f(cumulated stemwood volume)] curve, at point 0 (current year). Forest production tables (Goskom, 1984) were used to express the WIP on a surface basis (Bq cm2), in order to allow the comparison with the pool of 137Cs available in the soil for root uptake. 4. Results
feature of dry forest soils (Thiry and Myttenaere, 1993; Shcheglov, 1999; Fesenko et al., 2001). The peak value decreases rapidly with the thickness of the O layer, as a function of tree age. In stands IV and V, the very thick O layer shows the highest 137Cs concentration compared to the mineral horizons. Due to the humus thickness, the contribution of the organic soil horizons to the total 137Cs storage increases with tree age and soil moisture, from stand I to stand V (Fig. 3).
4.1. Soil characteristics
4.3.
Major soil characteristics are presented in Table 1. The soils are acid to strongly acid and exhibit a very low base saturation (o10% in A horizons). These features are typical of forest soils of the Chernobyl area (Shcheglov et al., 2001). The soils of stands I–IV may be classified as Dystric Cambisols (dry conditions) (ISSS, 1998). The thickness of the organic horizons increases with tree age (from stand I to IV). The soil of stand V, developed in humid conditions, shows podzolisation features (AE horizon). The O and OA horizons are also particularly thick; the organic matter accumulates notably because of poor drainage.
Results of the RM experiment are presented in Table 2. The variability between replicates for the same soil layer was lower than 5%. In the organic layers, the RM is lower in stands I–III (Dystric Cambisols), compared to stands IV and V which exhibit a lower content of total exchangeable cations (Table 1). The proportion of monovalent cations (K and Na) is also significantly lower in stands II and III, where the 137Cs uptake by the plants from organic layers was the lowest. A similar inverse proportionality between 137Cs availability and total exchangeable cations in soil was previously highlighted in a series of contaminated forests of the Chernobyl area (Shcheglov et al., 2001). In the mineral soil layers, the RM is higher compared to the O and OA horizons of the different stands, the eluvial AE horizon of stand V showing the highest value.
4.2.
137
Cs redistribution in the soil layers
The patterns of 137Cs redistribution in the soil layers are presented in Fig. 2. The very low 137Cs concentration below 5 cm in the mineral soil layers of all stands confirms the low 137 Cs vertical migration usually observed in contaminated forest soils (Bunzl et al., 1995; Mamikhin, 1995). In stands I–III, the 137Cs peak observed in the OA layer is a common
4.4.
137
137
Cs availability from the upper soil layers
Cs transfer and incorporation in trees
The pools of 137Cs available in soil for root uptake (SA), calculated according to the Eq. (1), and the results of WIP
Table 1 Major soil characteristics in the forest stands Stand no. I
II
III
IV
V
Tree age (years) 17
37
57
65
95
Soil type AU
AU
AU
AU
HY
Layer
Depth (cm)
Bulk density (g cm3)
pH H2O
CEC (cmolc kg1)
Exchangeable elements (cmolc kg1) K
Ca
Mg
Na
(Na+K)/TRB (%)
Total C (%)
O OA A
0.6 0.6 10.0
0.2 0.9 1.4
4.2 4.5
52.8 6.7 3.1
1.55 0.18 0.05
11.25 0.35 0.06
1.29 0.09 0.02
0.22 0.07 0.04
12.4 35.6 52.8
85.9 24.9 3.2
O OA A
1.4 1.3 10.0
0.1 0.6 1.4
4.1 4.3
51.8 8.7 4.1
0.66 0.12 0.05
12.46 0.95 0.16
1.54 0.15 0.03
0.10 0.08 0.05
5.2 15.1 34.0
85.6 23.3 3.8
O OA A
2.6 1.0 10.0
0.1 0.7 1.3
3.2 3.6
68.5 15.5 5.1
0.95 0.23 0.04
13.29 2.12 0.31
1.68 0.28 0.04
0.15 0.03 0.05
6.8 10.0 21.1
86.5 29.3 3.5
O OA A
3.6 1.0 10.0
0.1 0.4 1.3
2.8 3.2
76.1 12.5 3.7
0.82 0.13 0.03
7.07 0.44 0.11
1.13 0.13 0.03
0.22 0.05 0.06
11.2 24.3 39.0
84.3 28.7 3.0
OF OH OA AE
4.6 3.8 3.6 5.0
0.2 0.3 0.6 1.0
2.9 3.1
85.1 61.3 13.5 4.0
1.27 0.66 0.10 0.04
7.11 1.66 0.25 0.06
1.69 0.63 0.10 0.02
0.11 0.11 0.05 n.d.
13.6 25.2 29.7 n.d.
88.4 54.4 13.2 3.4
AU, automorphic (dry conditions); HY, hydromorphic (humid conditions); TRB, total reserve in bases ¼ (K+Ca+Ma+Na); n.d., not determined.
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Stand II
Stand I 10 Soil depth (cm)
Soil depth (cm)
10 5 0 -5 0
25
50 137Cs
75 100 (Bq cm-3)
125
75 100 (Bq cm-3)
125
125
150
125
150
5 0 -5
150
0
25
50 137Cs
75 100 (Bq cm-3)
Stand V
10 Soil depth (cm)
75 100 (Bq cm-3)
Stand IV Soil depth (cm)
137Cs
50
10
-5 50
25
137Cs
0
25
0
0
5
0
5
-5
150
Stand III
10 Soil depth (cm)
133
5 0 -5 0
25
50 137Cs
Fig. 2.
125
150
137
Cs redistribution in the soil layers.
100% % of the total 137Cs content in soil located in the organic layers
75 100 (Bq cm-3)
Table 2 Rhizospheric mobilisation experiment: proportion of 137Cs in the ryegrass plantlets (%)
75%
Stand
50%
Proportion of Horizon
137
Cs in rye-grass plantlets O OA
I II III IV
25%
Horizon
0% I
II
III Stand
IV
V
Fig. 3. Contribution of the organic soil horizons to the total 137Cs content in soil.
calculation are synthesised in Table 3 for the five stands. In each stand, the radial gradients of 137Cs in annual wood rings obtained for the three sampled trees were similar and comparable to other results from the literature. The values of TF to wood are also presented, as a matter of comparison.
V
A
24.5% 11.1% 7.1% 25.3%
14.3% 8.3% 11.9% 26.0%
27.3% 23.6% 15.2% 38.7%
OF
OH
OA
AE
29.3%
29.5%
59.2%
82.0%
A geometrical comparison between SA and WIP is presented in Fig. 4, as statistical inference. The relationship between both indices is tested through the dispersion of paired values (SA, WIP) compared to a linear regression crossing the axes at their origin. Fig. 4 reveals a quite constant relationship between the two indices (r2 ¼ 0.87). The slope of the linear regression corresponds to an optimised value of the proportionality factor. From a statistical viewpoint, no representative error bars could be
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Table 3 137 Cs transfer and incorporation in trees Stand
I II III IV V
Total pool of 137 Cs available in soil for root uptake (SA) (Bq cm2) 43.0 19.7 6.9 28.0 11.7
Potential of 137 Cs immobilisation in wood (WIP) (Bq cm2)
Total Cs content in soil (SC) (Bq cm2)
Transfer factor (TF) (wood) (m2 kg1)
0.26 0.14 0.09 0.15 0.06
174.6 152.1 98.9 177.4 105.6
0.00238 0.00120 0.00172 0.00147 0.00221
137
0.30
WIP (Bq/cm2)
0.25 0.20 0.15 0.10 0.05
y = 0.006x R2 = 0.874
0.00 0
Fig. 4.
10
20 30 SA (Bq/cm2)
40
50
137
Cs transfer and incorporation in trees: comparative analysis.
determined, considering the complex calculation process for both WIP and SA indices and the limited number of replicates (n ¼ 3 for stemwood samples; n ¼ 5 for soil samples). 5. Discussion Attempts to describe the fate of 137Cs in contaminated forest ecosystems are not recent. The work dedicated to this topic was yet considerably amplified after the Chernobyl accident. Most of the existing studies focus nevertheless either on the soil or the tree level, leaving the interface between those compartments largely misunderstood. This has notably contributed to a wide use of integrated approaches based on parameters like TF to model the 137Cs redistribution in trees, with nevertheless some unsatisfactory outcomes, particularly for predictions of the evolution of 137Cs content in stemwood. The problem notably arises from the difficulty to localise precisely the 137Cs uptake from multilayered forest soils. The root fraction o2 mm (fine roots) is usually considered as responsible for the uptake of nutrients (Kalela, 1949; Persson, 1983) and 137Cs (Fesenko et al., 2001). These roots proliferate mostly in the surface soil layers, which contain nutrients from litter decomposition (Eissenstat and Van
Rees, 1994) and 137Cs. However, the distribution of active fine roots is variable and depends on the season, the age of the trees and the soil features (Persson, 1980; Makkonen and Helmisaari, 1999). The rapid turnover of fine roots (Fogel, 1983) also complicates the assessment of the current root biomass actually involved in nutrients uptake (Makkonen and Helmisaari, 1999). A consistent picture of the distribution of active fine roots in soil layers would consequently be difficult to determine. Our results suggest nevertheless that similarities in the 137 Cs accumulation (tree)–availability (soil) relationship may be highlighted between different tree ages and soil types, through an approach valorising as far as possible the existing knowledge about the 137Cs fate in forest ecosystems. Compared to TF values, which vary by a factor 2 between the forest stands sampled (cf. Table 3), the relative stability of the ratio WIP/SA may be at least partly connected with a more reliable and precise representation of the 137Cs distribution in key soil and tree compartments, as well as with a dynamic description of the 137Cs soil-towood transfer largely based on the existing literature (see above, Section 3). Indeed, in this ratio, the WIP (numerator) combines the effect of radial 137Cs gradient and stemwood biomass growth rate for the quantification of 137Cs accumulation in stemwood, while the SA (denominator), as calculated, takes into account the 137Cs migration between soil layers and the pool of 137Cs available for plant uptake. By comparison, TF corresponds to the ratio of an average 137Cs content in whole stemwood and an average 137Cs deposition onto the soil surface, integrating this way, without particular discrimination, numerous processes ruling the 137Cs fate in soil and redistribution in trees. At the soil level, the total pool of 137Cs available for root uptake (Eq. (1)) takes into account the specificities of the upper soil layers in terms of 137Cs migration and availability for root uptake. The upper soil layers features are closely connected with the age of trees and the soil type, which drive 137Cs redistribution. The 137Cs migration profiles (Fig. 2) reveal in particular that the O and OA layers, acting as a geochemical barrier, contribute to limit the 137Cs migration into the deep soil and therefore to store 137 Cs in the topsoil, where the radionuclide remains accessible for root uptake (Krasnov, 1999; Kruyts and Delvaux, 2002). The tendency of 137Cs concentration to decrease in the O layer with tree age and soil moisture may also be connected with the dilution of 137Cs in a thicker humus layer (Shcheglov et al., 2001). This effect is particularly marked in stand V. Organic layers are known to play a key role as 137Cs reservoir for the trees, particularly in mature stands (Tikhomirov and Shcheglov, 1994; Fesenko et al., 2001; Shcheglov et al., 2001). On the other hand, processes governing the 137Cs availability in soils (Table 2) have been investigated for a while. Results from the literature have notably shown that the 137Cs availability from forest soils is largely driven by specific fixation sites born by weathered micaceous clay minerals,
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namely the frayed edge sites (FES) (Sawhney, 1972; Cremers et al., 1990; Sweeck et al., 1990). The inverse relationship between concentration of FES and 137Cs availability has been illustrated for a large collection of soil types (Delvaux et al., 2000). In particular, the accumulation of organic matter on topsoils can exert a dilution of FES-bearing minerals, and consequently contribute to increase the 137Cs soil-to-plant transfer from the organic layers (Kruyts and Delvaux, 2002), as observed in stands IV and V. The lower RM in the Dystric Cambisols may tentatively be connected with a higher biological activity, which favours the mixing of organic compounds with clay minerals originating from the underlying mineral soil layers (Kruyts et al., 2004; Tyler et al., 2001). At the tree level, the advantages of the WIP approach compared to TF have already been discussed (Thiry et al., 2002). Our results confirm that WIP and TF values are in some cases contradictory. In the forest stands investigated, the divergences may be explained by discrepancies in the evaluation of 137Cs availability in soil (between stands III and IV) or stemwood production (between stands IV and V) (Table 3), which both are not satisfactorily described in the TF approach (Goor and Thiry, 2004). At the scale of forest stands, the proportionality observed between soil (SA) and tree (WIP) indices (Fig. 4) corroborates the relevancy of WIP as an indicator of the current 137Cs root uptake by the trees, even though a limited number of forest stands was investigated, which also limits the possibilities to extrapolate this relationship to other tree ages and types of soil. These results open, nevertheless, perspectives for the improvement of existing models of 137Cs cycling and accumulation in trees, notably through the possibility to deduce WIP values directly from SA calculations using the proportionality coefficient derived from Fig. 4, and inversely. For the near future, the WIP values, as proxy of the current 137Cs root uptake by trees, may also be combined with local forest production tables (Goskom, 1984) to estimate the evolution of the 137Cs content in stemwood, the additional 137Cs activity in whole stemwood between two successive growing seasons being obtained by multiplying the WIP by the relative wood volume increase, as discussed in Goor (2003). For longer time scales, the WIP of a given forest stand will nevertheless evolve as a function of tree ageing and changes in the upper soil layers features. In this case, new WIP values may be derived from Fig. 4 and Eq. (1) combined with 137Cs migration models in forest soils, considering a dynamic evolution of the soil profile depending on the edaphotope and the age of the trees. This solution, which could be conceptualised in a model, constitutes also a sound basis to rank contaminated forest ecosystems in terms of vulnerability to stemwood contamination with 137Cs. 6. Conclusion Twenty years after the Chernobyl accident, root uptake from the surface layers of contaminated forest soils plays a
135
major role in the 137Cs transfer and incorporation in trees. Considering the complexity and the extended lifetime of forest ecosystems, the adequacy of integrated parameters like the commonly used static TF to characterize the source-sink relationship between soil and trees is questionable, particularly in the perspective of modelling the evolution of 137Cs content in perennial tree components in the long term. An alternative approach was therefore proposed: the WIP for stemwood. Up to now, the relevancy of this parameter as an indicator of the current 137 Cs root uptake by trees was nevertheless not evaluated at the scale of the whole forest ecosystem. In this context, the main objective of the present paper was to compare WIP values with the pool of 137Cs available for root uptake, the latter being defined in order to integrate as far as possible the key parameters driving the fate of 137Cs in forest soils. Practically, the comparative analysis of five contaminated forests differing in tree ages and soil types revealed significant similarities in the 137Cs accumulation (stemwood)—availability (soil) relationship for the tree ages and soil types investigated, confirming the WIP as a relevant indicator of current 137Cs root uptake by trees. As the indicator of 137Cs availability was developed in view of the current knowledge to 137Cs fate in forest soils, this relationship also constitutes a sound basis for a common approach of 137Cs soil-to-stemwood transfer studies, whatever the characteristics of forests ecosystems, as well as for the improvement of predictions from the existing models of 137Cs cycling in contaminated forests. More mechanistic and dynamic descriptions of the processes involved in the 137Cs transfer are indeed required in order to provide reliable predictions for the long-term management of contaminated forest ecosystems. Acknowledgements The authors wish to thank P. Bogaert (UCL—ENGE) for his help in the interpretation of the datasets used in this study, and V. Brahy (ULB—IGEAT) for his relevant comments on the manuscript. References Bunzl, K., Kracke, W., Schimmack, W., 1995. Migration of Fallout 239+240 Pu, 241Am and 137Cs in the various horizons of a forest soil under pine. Journal of Environmental Radioactivity 28 (1), 17–34. Cremers, A., Elsen, A., Valcke, E., Wauters, J., Sandalls, F., Gaudern, S., 1990. Quantitative analysis of radiocaesium retention in soils. Nature 335, 247–249. Davydchuk, V., 1999. Radioactively contaminated forests: GIS application for the remedial policy development and environmental risk assessment. In: Linkov, I., Schell, W.R. (Eds.), Contaminated forests: recent developments in risk identification and future perspectives. Kluwer Academic, Kiev, pp. 369–376. Delvaux, B., Kruyts, N., Cremers, A., 2000. Rhizospheric mobilization of radiocesium in soils. Environmental Science and Technology 34, 1489–1493.
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Eissenstat, D.M., Van Rees, K.C.J., 1994. The growth and function of pine roots. Ecological Bulletins 43, 76–91. Fesenko, S.V., Soukhova, N.V., Sanzharova, N.I., Avila, R., Spiridonov, S.I., Klein, D., Lucot, E., Badot, P.M., 2001. Identification of processes governing long-term accumulation of 137Cs by forest trees following the Chernobyl accident. Radiation and Environmental Biophysics 40, 105–113. Fogel, R., 1983. Root turnover and productivity of coniferous forests. Plant and Soil 71, 75–85. Goor, F., 2003. Processes and dynamics of radiocaesium cycling in Chernobyl-contaminated pine forests: a multi-scale approach. Faculte´ d’inge´nie´rie biologique, agronomique et environnementale, UCL, Louvain-la-Neuve, Belgium. Goor, F., Avila, R., 2003. Quantitative comparison of models of 137Cs cycling in forest ecosystems. Environmental Modelling and Software 18, 273–279. Goor, F., Thiry, Y., 2004. Processes, dynamics and modelling of radiocaesium cycling in a chronosequence of Chernobyl-contaminated Scots pine (Pinus sylvestris L.) plantations. Science of the Total Environment 325, 163–180. Goor, F., Davydchuk, V., Vandenhove, H., 2003. GIS-based methodology for Chernobyl contaminated land management through biomass conversion into energy—a case study for Polessie, Ukraine. Biomass and Bioenergy 25, 409–421. Goskom, 1984. Normative material for forest taxation in Belarus. USSR Forest Management Committee, Moscow, Russia (in Russian). Ipatyev, V., Bulavik, I., Baginsky, V., Goncharenko, G., Dvornik, A., 1999. Forest and Chernobyl: forest ecosystems after the Chernobyl nuclear power plant accident: 1986–1994. Journal of Environmental Radioactivity 42, 9–38. ISSS, 1998. World Reference Base for Soil Resources: Keys to Reference Soil Groups of the World. World Soil Resource Report No 84, FAO, Rome, Italy Izrael, Y.A., De Cort, M., Jones, A.R., Nazarov, I.M., Fridman, S.D., Kvasnikova, E.V., Stukin, E.D., Kelly, J.N., Matveenko, I., Pokumeiko, Y.M., Tabatchnyi, L.Y., Tsaturov, Y., 1996. The atlas of 137Cs contamination of Europe after the Chernobyl accident. In: Karaoglou, G.D.A., Kelly, G.N., Menzel, H.G. (Eds.), The Radiological Consequences of the Chernobyl Accident. EUR 16544 EN, Brussels, Belgium Kalela, E.K., 1949. On the horizontal roots in pine and spruce stand I. Acta Forestalia Fennica 57 (2). Krasnov, V.P., 1999. The direction and intensity of 137Cs fluxes in forest ecosystems. In: Linkov, I., Schell, W.R. (Eds.), Contaminated forests: recent developments in risk identification and future perspectives. Kluwer Academic, Kiev, pp. 71–76. Kruyts, N., Delvaux, B., 2002. Soil organic horizons as a major source for radiocesium biorecycling in forest ecosystems. Journal of Environmental Radioactivity 58, 175–190. Kruyts, N., Titeux, H., Delvaux, B., 2004. Mobility of radiocesium in three distinct forest floors. The Science of the Total Environment 319, 241–252. Makkonen, K., Helmisaari, H.S., 1999. Assessing fine-root biomass and production in a Scots pine stand—comparison of soil core and root ingrowth core methods. Plant and Soil 210, 43–50. Mamikhin, S.V., 1995. Mathematical model of 137Cs vertical migration in a forest soil. Journal of Environmental Radioactivity 28 (2), 161–170. Melin, J., Wallberg, L., Suomela, J., 1994. Distribution and retention of cesium and strontium in Swedish boreal forest ecosystems. The Science of the Total Environment 157, 93–105. Myttenaere, C., Schell, W.R., Thiry, Y., Sombre, L., Ronneau, C., van der Stegen de Schrieck, J., 1993. Modeling of 137Cs cycling in forests: recent developments and research needed. The Science of Total Environment 136, 77–91.
Nimis, P.L., 1996. Radiocaesium in plants of forest ecosystems. Studia Geobotanica 15, 3–49. Page, A.L., Miller, R.H., Keeney, D.R., 1982. Methods of Soil Analysis: Part 2: Chemical and Microbiological Properties, second ed. American Society of Agronomy and Soil Science Society of America, Madison, WI, USA. Persson, H., 1980. Fine-root dynamics in a Scots pine stand with and without near-optimum nutrient and water regimes. Acta Phytogeographica Suecica 68, 101–110. Persson, H., 1983. The distribution and productivity of fine roots in boreal forests. Plant and Soil 71, 87–101. Plamboeck, A.H., Nylen, T., Grip, H., 2000. Uptake of cations under two different water regimes in a boreal Scots pine forest. The Science of the Total Environment 256, 175–183. Sawhney, B.L., 1972. Selective sorption and fixation of cations by clay minerals: a review. Clays and Clay Minerals 20, 93–100. Shaw, G., Robinson, C., Holm, E., Frissel, M.J., Crick, M., 2001. A costbenefit analysis of long-term management options for forests following contamination with 137Cs. Journal of Environmental Radioactivity 56, 185–208. Shcheglov, A.I., 1999. Dynamics of radionuclide redistribution and pathways in forest environments: long-term field research in different landscapes. In: Linkov, I., Schell, W.R. (Eds.), Contaminated Forests: Recent Developments in Risk Identification and Future Perspectives. Kluwer Academic, Kiev, pp. 23–39. Shcheglov, A.I., Tsvetnova, O.B., Klyashtorin, A.L., 2001. Biogeochemical Migration of Technogenic Radionuclides in Forest Ecosystems. Moscow Nauka, Moscow, Russia. Sorokina, L.Y., 1996. Accumulation of 137Cs by phytocomponents of forest ecosystem depending on edaphic conditions. Ukrainian Geographical Journal 1, 44–48. Strebl, F., Gerzabek, M.H., Bossew, P., Kienzl, K., 1999. Distribution of radiocaesium in an Austrian forest stand. The Science of the Total Environment 226, 75–83. Sweeck, L., Wauters, J., Valcke, E., Cremers, A., 1990. The specific interception potential of soils for radiocaesium. Transfer of radionuclides in natural and semi-natural environments. Elsevier Applied Science, London, UK. Thiessen, K.M., Thorne, M.C., Maul, P.R., Pro¨hl, G., Wheater, H.S., 1999. Modelling radionuclide distribution and transport in the environment. Environmental Pollution 100, 151–177. Thiry, Y., Myttenaere, C., 1993. Behavior of radiocaesium in forest multilayered soils. Journal of Environmental Radioactivity 18, 247–257. Thiry, Y., Kruyts, N., Delvaux, B., 2000. Respective horizon contributions to cesium-137 soil-to-plant transfer: a pot experiment approach. Journal of Environmental Quality 29, 1194–1199. Thiry, Y., Goor, F., Riesen, T., 2002. The true distribution and accumulation of radiocaesium in stem of Scots pine (Pinus sylvestris L.). Journal of Environmental Radioactivity 58, 243–259. Tikhomirov, F.A., Shcheglov, A.I., 1994. Main investigation results on the forest radioecology in the Kyshtym and Chernobyl accident zones. The Science of the Total Environment 157, 45–57. Tikhomirov, F.A., Shcheglov, A.I., Sidorov, V.P., 1993. Forest and forestry: radiation protection measures with special reference to the Chernobyl accident zone. The Science of the Total Environment 137, 289–305. Tyler, A.N., Carter, S., Davidson, D.A., Long, D.J., Tipping, R., 2001. The extent and significance of bioturbation on 137Cs distributions in upland soils. Catena 43, 81–99. van der Perk, M., Burema, J., Vandenhove, H., Goor, F., Timofeyev, S., 2004. Spatial assessment of the economic feasibility of short rotation coppice on radioactively contaminated land in Belarus, Ukraine, and Russia. I. Model description and scenario analysis. Journal of Environmental Management 72, 217–232.
Journal of Environmental Management 85 (2007) 129–136 www.elsevier.com/locate/jenvman
Radiocaesium accumulation in stemwood: Integrated approach at the scale of forest stands for contaminated Scots pine in Belarus Franc- ois Goora,, Yves Thirya, Bruno Delvauxb a
Centre d’Etude de l’Energie nucle´aire (SCKCEN) Boeretang, 200 B-2400 Mol, Belgium Unite´ de Sciences du sol (UCL/AGRO/MILA) Croix du Sud, 2/10 B-1348 Louvain-la-Neuve, Belgium
b
Received 5 December 2005; received in revised form 16 August 2006; accepted 21 August 2006 Available online 9 October 2006
Abstract Twenty years after the Chernobyl accident, root uptake from the surface layers of contaminated forest soils plays a major role in radiocaesium (137Cs) transfer to the trees and accumulation in perennial compartments, including stemwood. Trustworthy long-term predictions (modelling) of stemwood contamination with 137Cs should accordingly be based on a reliable picture of this source–sink relationship. Considering the complexity of the processes involved in 137Cs cycling in forest stands, elementary ratios like transfer factors (TF) were shown to be not very relevant for that purpose. At the tree level, alternatives like the wood immobilisation potential (WIP) have therefore been proposed in order to quantify the current net 137Cs accumulation in stemwood. Our objective was here to compare WIP values determined for a series of contaminated forest stands in Belarus with the corresponding pools of 137Cs available in the soil for root uptake. The comparison reveals that both indices are quite proportional, whatever the forest ecosystem features. This corroborates the relevancy of WIP as an indicator of the current 137Cs root uptake by the trees, which could accordingly help to improve the existing models of 137Cs cycling and the long-term management of contaminated forest ecosystems. r 2006 Elsevier Ltd. All rights reserved. Keywords: Radiocaesium; Forest ecosystem; Modelling; Root uptake
1. Introduction Following the Chernobyl accident in April 1986, large territories have been contaminated with radionuclides fallout in former USSR countries, and to a lower extent Western Europe, causing the main ecological and socioeconomical disaster in the history of civil nuclear power. In semi-natural ecosystems, the contamination of forest stands with radiocaesium (137Cs, T1/2 ¼ 30.2 years) is particularly worrying due to large-scale (Izrael et al., 1996) and long-term radiation exposure risks for local populations and forest workers, but also in terms of loss of economic return for the wood industry (Shaw et al., 2001) because of sanitary restrictions applied to contaminated wood use (Tikhomirov et al., 1993; Davydchuk, 1999). Corresponding author. 130/02 Avenue F. Roosevelt, 50 B-1050 Bruxelles, Belgium. Tel.: +32 2 650 2684; fax: +32 2 650 4312. E-mail addresses: [email protected] (F. Goor), [email protected] (Y. Thiry), [email protected] (B. Delvaux).
0301-4797/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jenvman.2006.08.008
Accordingly, significant efforts have been carried out, during the last two decades, to understand the fate of 137Cs in contaminated forests, and particularly its accumulation in perennial tree components like stemwood (Ipatyev et al., 1999). Up to now, the assessment of 137Cs content in contaminated forest stands has largely been based on elementary ratios, the transfer factors (TF, (Bq kg1)/ (Bq m2)), comparing the 137Cs concentration in a given tree component (Bq kg1) to the total 137Cs deposition onto the soil (Bq m2) (Nimis, 1996). TF determined for a range of forest and soil types have been widely used to assess the redistribution of 137Cs in forest ecosystems (Ipatyev et al., 1999) and to elaborate maps of trees contamination from 137Cs deposition inventories (Goor et al., 2003; van der Perk et al., 2004). The use of TF was, however, shown to be not very relevant in a longterm perspective (Thiry et al., 2002; Thiessen et al., 1999), particularly if perennial tree compartments are considered. TF-based modelling approaches fail notably
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to satisfactorily predict the 137Cs root uptake and accumulation in various tree compartments, including stemwood, as revealed for example by a statistical comparison of predictions from the main existing models of 137Cs redistribution in trees for a Chernobyl-like contamination scenario (Goor and Avila, 2003). TF provide indeed only a static picture of the 137Cs redistribution in forests, derived from the total 137Cs content in soil and tree compartments at the time of TF measurement. Conceptually, the TF approach also supposes that the whole 137Cs content in trees originates from the soil, through root uptake. Conversely, 137Cs proved to be highly mobile and recycled within trees and between trees and soil, through similar patterns as potassium, a major plant nutrient (Strebl et al., 1999; Melin et al., 1994; Myttenaere et al., 1993). Retranslocation processes can in particular account for a significant fraction of the ‘‘apparent’’ 137Cs accumulation rate in stemwood, as shown by Goor and Thiry (2004) for a chronosequence of Scots pine stands in Belarus. Similar conclusions were presented by Thiry et al. (2002), whose observations in mature contaminated Scots pine stands suggest that TF-based approaches largely overestimate the current 137Cs accumulation rate in stemwood. According to these authors, this is at least partly due to an inaccurate consideration of the consequences of canopy interception and incorporation processes, in the early period following 137Cs fallout, on the total 137Cs content in stemwood. A new approach to determine the current 137Cs accumulation rate in stemwood was therefore recently proposed: the wood immobilisation potential (WIP) (Thiry et al., 2002). Contrary to static TF, the WIP definition is based on the actual radial redistribution of 137Cs in stemwood, closely connected with the production of biomass (the WIP corresponds to the additional 137Cs per volume of new woody biomass, calculated on an annual basis). Accordingly, the WIP may be considered as reflecting the current 137Cs net accumulation rate in stemwood. Considering besides that twenty years after the Chernobyl accident, the surface layers of forest soils constitute the major source of 137Cs for the trees (Thiry and Myttenaere, 1993; Shcheglov, 1999; Plamboeck et al., 2000), the WIP likely provides a good picture of 137Cs root uptake. Clear empirical evidence of the relationship between 137Cs availability in soil for root uptake and 137Cs accumulation in stemwood, calculated using the WIP approach, is however still missing. In a long-term perspective, such a relationship has been identified as a key step for the improvement of the existing models of 137 Cs cycling in contaminated forest stands (Goor and Avila, 2003). In this context, the objective of the present study is to evaluate the relevancy of the WIP approach at the scale of forest stands by comparing WIP values with the pools of 137 Cs available from the soil, for various forest ecosystems conditions. Practically, a methodology adapted from the literature will be implemented in order to assess the pool of
137
Cs potentially available for root uptake in multilayered forest soils, and applied to a series of contaminated Scots pine stands of the Chernobyl area, covering various tree ages and types of soil. WIP values will be determined for the same stands. The paired values will then be compared, in a standardized way, in order to highlight similarities in the 137Cs accumulation (tree)–availability (soil) relationship. On this basis, the relevancy of the WIP as an indicator of the current 137Cs root uptake will be discussed. Perspectives for the improvement of the existing models of 137Cs cycling in forests as well as for the management of contaminated stands will also be discussed. 2. Material and methods 2.1. Environmental setting The sampling site is a vast Scots pine (Pinus sylvestris L.) woodland located close to Vetka (52137.80 N, 31113.10 E, 159 m above sea level) in the Gomel district, in Belarus. Following the Chernobyl accident, the Gomel area was severely affected by 137Cs fallout (Izrael et al., 1996). The climate is continental and sub-boreal. The average annual temperature is 6.5 1C, but seasonal variations are important. The average precipitation is 550 mm y1. The vegetative period lasts about 6 months, from April to October. The landscape consists of slightly sloping plateaus, intersected by a network of rivers and swampy areas. The soils derive from glaciofluvial deposits of the Quaternary age. The dominant particle size fraction is sand (85–90%). In forest areas, the soil features are closely linked to the relief and the hydrological regime (Sorokina, 1996): on the plateaus, the soil development is not determined by lateral water drainage nor by variations of the water table level (automorphic1 soils, dry conditions), whereas in the bottoms of valleys and local depressions, the soil features are largely influenced by humid conditions (hydromorphic soils). 2.2. Site sampling Forest vegetation and soils were sampled in February 2001 in five neighbouring Scots pine stands. The stands I, II and III (17-, 37- and 57-year-old trees) were established on similar former-tilled automorphic soils, and can be classified as Pinetum cladinosum (Goskom, 1984). The other stands, established on automorphic (65-year-old trees, stand IV) and hydromorphic (95-year-old trees, stand V) soils, can be classified as Pinetum sphagnosum. The total 137Cs deposition varies between 9.9 and 17.7 GBq ha1. The trees were sampled as described in Goor and Thiry (2004). Briefly, three representative average trees were chosen in each stand, on the basis of the trunk 1 ‘‘Automorphic’’ and ‘‘hydromorphic’’ refer to the local soil classification, based on edaphotopes (Sorokina, 1996).
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circumference at 1.30 m, and felled. Wood discs that were 2 cm thick, were then sampled from the trunks at 1.30 m, 6 m (5 m for the 17-year-old stand) and then every 6 m up to the top of the trees. Undisturbed soil samples (five replicates per stand, randomly distributed) were also collected from the topsoil (0–15 cm), using little plastic boxes (15 cm wide and 3 cm thick). To avoid any physical or chemical alteration, wood and soil samples were immediately put into individual polyethylene bags and stored at 4 1C until analysis. 2.3. Laboratory analyses In the laboratory, the sampled wood discs were analysed to allow WIP calculation. The surface of each disc was polished, in order to reveal the annual wood increments. This operation was limited to the surface of the wood discs, to a depth not exceeding 2 mm, which was less than 4% of the total discs volumes. The discs were scanned for further measurement of radial growth. The wood increments were then separated with a chisel, in 3-years groups, dried out and weighed. The separation of annual wood rings was realised very carefully, on fresh wood discs in order to avoid any 137Cs radial redistribution during wood drying. After burning at 550 1C in a furnace, the ashes were solubilized in 10 ml HNO3 (2 N). On the other hand, the organic (O), transition (OA) and organo-mineral (A) horizons were identified on undisturbed soil samples before analysis, and the average thickness of each horizon was measured. The different horizons were then carefully separated, air dried for 5 days at 20 1C, and weighted. The O horizons were sieved at 2 mm. The main soil properties (weight loss after ignition at 450 1C, total exchangeable cations content, cation exchange capacity (CEC) (NH4OAc 1 M pH 7) and pH (5 g:25 ml of H2O) were determined from soil aliquots using well-known procedures (Page et al., 1982). The 137Cs content in wood and soil samples was determined by gamma spectrometry (NaI detector— Minaxi g 5000 series). The value of the counter background was 30 disintegrations min1, and the lower limit of detection was 3.8 Bq. The counter efficiency (13%) was determined using reference samples, calibrated using a high-resolution gamma spectrometer. The counting time was adjusted in order to reduce the counting error below 3%. The 137Cs activities were decaycorrected back to April 26, 1986.
mobilisation (RM) (Delvaux et al., 2000). Compared to chemical 137Cs extractions, the advantages of the RM test are that the quantification of 137Cs availability is based on plant root uptake, and that previous results from a range of soil types have linked RM results with key soil properties regarding 137Cs availability, notably for contaminated forest soils (Kruyts et al., 2004; Kruyts and Delvaux, 2002; Thiry et al., 2000). It is important to note that the 137 Cs availability measured with rye-grass plantlets is not quantitatively representative of the total 137Cs uptake by trees in contaminated forest stands. The values of the pool of 137Cs available, obtained in standardised conditions using the RM test will therefore be discussed in relative terms. The RM test was carried out as described in Delvaux et al. (2000). Briefly, seeds of rye-grass (Lolium multiflorum) were first germinated on a water-saturated net for 7 days. The root mat was then placed in contact with the contaminated soil samples for 4 days (five repetitions for each soil layer). The rye-grass plantlets were finally harvested and g-counted. The 137Cs-RM is the proportion (%) of 137Cs transferred to rye-grass plantlets (whole plants, including roots) during the experiment. The total pool of 137Cs available for root uptake was then calculated as follows: Total pool of 137 Cs available in the soil ðSAÞ ½Bq cm2 ¼ Si ðThi ½Csi RMi Þ, ð1Þ with i is the soil layer (O, OA or A layer), Thi the thickness of the layer i (cm), [Cs]i the 137Cs concentration of the layer i (Bq cm3) and RMi the 137Cs RM of the layer i [%] 3.2. Current
137
Cs accumulation rate in stemwood
The current 137Cs accumulation rate in stemwood was assessed using the WIP (Thiry et al., 2002). Conceptually, the WIP was developed in order to take into account the tree age- and time-dependent radial redistribution of 137Cs in stemwood, which influences the value of the current 137 Cs accumulation rate in stemwood. Accordingly, as illustrated in Fig. 1, the WIP (Bq cm3) was defined as the
3. Theory and calculation 3.1. Total pool of
137
Cs available in the soil for root uptake
Considering the complexity of measuring the 137Cs uptake by trees in situ in undisturbed soil conditions, the pool of 137Cs available in the soil was assessed using a standardised approach of 137Cs soil-to-plant transfer, based on miniaturised experiments: the rhizospheric
131
Fig. 1. The WIP concept (adapted from Thiry et al., 2002).
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132
tangency (first derivative) of the [cumulated 137Cs activity ¼ f(cumulated stemwood volume)] curve, at point 0 (current year). Forest production tables (Goskom, 1984) were used to express the WIP on a surface basis (Bq cm2), in order to allow the comparison with the pool of 137Cs available in the soil for root uptake. 4. Results
feature of dry forest soils (Thiry and Myttenaere, 1993; Shcheglov, 1999; Fesenko et al., 2001). The peak value decreases rapidly with the thickness of the O layer, as a function of tree age. In stands IV and V, the very thick O layer shows the highest 137Cs concentration compared to the mineral horizons. Due to the humus thickness, the contribution of the organic soil horizons to the total 137Cs storage increases with tree age and soil moisture, from stand I to stand V (Fig. 3).
4.1. Soil characteristics
4.3.
Major soil characteristics are presented in Table 1. The soils are acid to strongly acid and exhibit a very low base saturation (o10% in A horizons). These features are typical of forest soils of the Chernobyl area (Shcheglov et al., 2001). The soils of stands I–IV may be classified as Dystric Cambisols (dry conditions) (ISSS, 1998). The thickness of the organic horizons increases with tree age (from stand I to IV). The soil of stand V, developed in humid conditions, shows podzolisation features (AE horizon). The O and OA horizons are also particularly thick; the organic matter accumulates notably because of poor drainage.
Results of the RM experiment are presented in Table 2. The variability between replicates for the same soil layer was lower than 5%. In the organic layers, the RM is lower in stands I–III (Dystric Cambisols), compared to stands IV and V which exhibit a lower content of total exchangeable cations (Table 1). The proportion of monovalent cations (K and Na) is also significantly lower in stands II and III, where the 137Cs uptake by the plants from organic layers was the lowest. A similar inverse proportionality between 137Cs availability and total exchangeable cations in soil was previously highlighted in a series of contaminated forests of the Chernobyl area (Shcheglov et al., 2001). In the mineral soil layers, the RM is higher compared to the O and OA horizons of the different stands, the eluvial AE horizon of stand V showing the highest value.
4.2.
137
Cs redistribution in the soil layers
The patterns of 137Cs redistribution in the soil layers are presented in Fig. 2. The very low 137Cs concentration below 5 cm in the mineral soil layers of all stands confirms the low 137 Cs vertical migration usually observed in contaminated forest soils (Bunzl et al., 1995; Mamikhin, 1995). In stands I–III, the 137Cs peak observed in the OA layer is a common
4.4.
137
137
Cs availability from the upper soil layers
Cs transfer and incorporation in trees
The pools of 137Cs available in soil for root uptake (SA), calculated according to the Eq. (1), and the results of WIP
Table 1 Major soil characteristics in the forest stands Stand no. I
II
III
IV
V
Tree age (years) 17
37
57
65
95
Soil type AU
AU
AU
AU
HY
Layer
Depth (cm)
Bulk density (g cm3)
pH H2O
CEC (cmolc kg1)
Exchangeable elements (cmolc kg1) K
Ca
Mg
Na
(Na+K)/TRB (%)
Total C (%)
O OA A
0.6 0.6 10.0
0.2 0.9 1.4
4.2 4.5
52.8 6.7 3.1
1.55 0.18 0.05
11.25 0.35 0.06
1.29 0.09 0.02
0.22 0.07 0.04
12.4 35.6 52.8
85.9 24.9 3.2
O OA A
1.4 1.3 10.0
0.1 0.6 1.4
4.1 4.3
51.8 8.7 4.1
0.66 0.12 0.05
12.46 0.95 0.16
1.54 0.15 0.03
0.10 0.08 0.05
5.2 15.1 34.0
85.6 23.3 3.8
O OA A
2.6 1.0 10.0
0.1 0.7 1.3
3.2 3.6
68.5 15.5 5.1
0.95 0.23 0.04
13.29 2.12 0.31
1.68 0.28 0.04
0.15 0.03 0.05
6.8 10.0 21.1
86.5 29.3 3.5
O OA A
3.6 1.0 10.0
0.1 0.4 1.3
2.8 3.2
76.1 12.5 3.7
0.82 0.13 0.03
7.07 0.44 0.11
1.13 0.13 0.03
0.22 0.05 0.06
11.2 24.3 39.0
84.3 28.7 3.0
OF OH OA AE
4.6 3.8 3.6 5.0
0.2 0.3 0.6 1.0
2.9 3.1
85.1 61.3 13.5 4.0
1.27 0.66 0.10 0.04
7.11 1.66 0.25 0.06
1.69 0.63 0.10 0.02
0.11 0.11 0.05 n.d.
13.6 25.2 29.7 n.d.
88.4 54.4 13.2 3.4
AU, automorphic (dry conditions); HY, hydromorphic (humid conditions); TRB, total reserve in bases ¼ (K+Ca+Ma+Na); n.d., not determined.
ARTICLE IN PRESS F. Goor et al. / Journal of Environmental Management 85 (2007) 129–136
Stand II
Stand I 10 Soil depth (cm)
Soil depth (cm)
10 5 0 -5 0
25
50 137Cs
75 100 (Bq cm-3)
125
75 100 (Bq cm-3)
125
125
150
125
150
5 0 -5
150
0
25
50 137Cs
75 100 (Bq cm-3)
Stand V
10 Soil depth (cm)
75 100 (Bq cm-3)
Stand IV Soil depth (cm)
137Cs
50
10
-5 50
25
137Cs
0
25
0
0
5
0
5
-5
150
Stand III
10 Soil depth (cm)
133
5 0 -5 0
25
50 137Cs
Fig. 2.
125
150
137
Cs redistribution in the soil layers.
100% % of the total 137Cs content in soil located in the organic layers
75 100 (Bq cm-3)
Table 2 Rhizospheric mobilisation experiment: proportion of 137Cs in the ryegrass plantlets (%)
75%
Stand
50%
Proportion of Horizon
137
Cs in rye-grass plantlets O OA
I II III IV
25%
Horizon
0% I
II
III Stand
IV
V
Fig. 3. Contribution of the organic soil horizons to the total 137Cs content in soil.
calculation are synthesised in Table 3 for the five stands. In each stand, the radial gradients of 137Cs in annual wood rings obtained for the three sampled trees were similar and comparable to other results from the literature. The values of TF to wood are also presented, as a matter of comparison.
V
A
24.5% 11.1% 7.1% 25.3%
14.3% 8.3% 11.9% 26.0%
27.3% 23.6% 15.2% 38.7%
OF
OH
OA
AE
29.3%
29.5%
59.2%
82.0%
A geometrical comparison between SA and WIP is presented in Fig. 4, as statistical inference. The relationship between both indices is tested through the dispersion of paired values (SA, WIP) compared to a linear regression crossing the axes at their origin. Fig. 4 reveals a quite constant relationship between the two indices (r2 ¼ 0.87). The slope of the linear regression corresponds to an optimised value of the proportionality factor. From a statistical viewpoint, no representative error bars could be
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134
Table 3 137 Cs transfer and incorporation in trees Stand
I II III IV V
Total pool of 137 Cs available in soil for root uptake (SA) (Bq cm2) 43.0 19.7 6.9 28.0 11.7
Potential of 137 Cs immobilisation in wood (WIP) (Bq cm2)
Total Cs content in soil (SC) (Bq cm2)
Transfer factor (TF) (wood) (m2 kg1)
0.26 0.14 0.09 0.15 0.06
174.6 152.1 98.9 177.4 105.6
0.00238 0.00120 0.00172 0.00147 0.00221
137
0.30
WIP (Bq/cm2)
0.25 0.20 0.15 0.10 0.05
y = 0.006x R2 = 0.874
0.00 0
Fig. 4.
10
20 30 SA (Bq/cm2)
40
50
137
Cs transfer and incorporation in trees: comparative analysis.
determined, considering the complex calculation process for both WIP and SA indices and the limited number of replicates (n ¼ 3 for stemwood samples; n ¼ 5 for soil samples). 5. Discussion Attempts to describe the fate of 137Cs in contaminated forest ecosystems are not recent. The work dedicated to this topic was yet considerably amplified after the Chernobyl accident. Most of the existing studies focus nevertheless either on the soil or the tree level, leaving the interface between those compartments largely misunderstood. This has notably contributed to a wide use of integrated approaches based on parameters like TF to model the 137Cs redistribution in trees, with nevertheless some unsatisfactory outcomes, particularly for predictions of the evolution of 137Cs content in stemwood. The problem notably arises from the difficulty to localise precisely the 137Cs uptake from multilayered forest soils. The root fraction o2 mm (fine roots) is usually considered as responsible for the uptake of nutrients (Kalela, 1949; Persson, 1983) and 137Cs (Fesenko et al., 2001). These roots proliferate mostly in the surface soil layers, which contain nutrients from litter decomposition (Eissenstat and Van
Rees, 1994) and 137Cs. However, the distribution of active fine roots is variable and depends on the season, the age of the trees and the soil features (Persson, 1980; Makkonen and Helmisaari, 1999). The rapid turnover of fine roots (Fogel, 1983) also complicates the assessment of the current root biomass actually involved in nutrients uptake (Makkonen and Helmisaari, 1999). A consistent picture of the distribution of active fine roots in soil layers would consequently be difficult to determine. Our results suggest nevertheless that similarities in the 137 Cs accumulation (tree)–availability (soil) relationship may be highlighted between different tree ages and soil types, through an approach valorising as far as possible the existing knowledge about the 137Cs fate in forest ecosystems. Compared to TF values, which vary by a factor 2 between the forest stands sampled (cf. Table 3), the relative stability of the ratio WIP/SA may be at least partly connected with a more reliable and precise representation of the 137Cs distribution in key soil and tree compartments, as well as with a dynamic description of the 137Cs soil-towood transfer largely based on the existing literature (see above, Section 3). Indeed, in this ratio, the WIP (numerator) combines the effect of radial 137Cs gradient and stemwood biomass growth rate for the quantification of 137Cs accumulation in stemwood, while the SA (denominator), as calculated, takes into account the 137Cs migration between soil layers and the pool of 137Cs available for plant uptake. By comparison, TF corresponds to the ratio of an average 137Cs content in whole stemwood and an average 137Cs deposition onto the soil surface, integrating this way, without particular discrimination, numerous processes ruling the 137Cs fate in soil and redistribution in trees. At the soil level, the total pool of 137Cs available for root uptake (Eq. (1)) takes into account the specificities of the upper soil layers in terms of 137Cs migration and availability for root uptake. The upper soil layers features are closely connected with the age of trees and the soil type, which drive 137Cs redistribution. The 137Cs migration profiles (Fig. 2) reveal in particular that the O and OA layers, acting as a geochemical barrier, contribute to limit the 137Cs migration into the deep soil and therefore to store 137 Cs in the topsoil, where the radionuclide remains accessible for root uptake (Krasnov, 1999; Kruyts and Delvaux, 2002). The tendency of 137Cs concentration to decrease in the O layer with tree age and soil moisture may also be connected with the dilution of 137Cs in a thicker humus layer (Shcheglov et al., 2001). This effect is particularly marked in stand V. Organic layers are known to play a key role as 137Cs reservoir for the trees, particularly in mature stands (Tikhomirov and Shcheglov, 1994; Fesenko et al., 2001; Shcheglov et al., 2001). On the other hand, processes governing the 137Cs availability in soils (Table 2) have been investigated for a while. Results from the literature have notably shown that the 137Cs availability from forest soils is largely driven by specific fixation sites born by weathered micaceous clay minerals,
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namely the frayed edge sites (FES) (Sawhney, 1972; Cremers et al., 1990; Sweeck et al., 1990). The inverse relationship between concentration of FES and 137Cs availability has been illustrated for a large collection of soil types (Delvaux et al., 2000). In particular, the accumulation of organic matter on topsoils can exert a dilution of FES-bearing minerals, and consequently contribute to increase the 137Cs soil-to-plant transfer from the organic layers (Kruyts and Delvaux, 2002), as observed in stands IV and V. The lower RM in the Dystric Cambisols may tentatively be connected with a higher biological activity, which favours the mixing of organic compounds with clay minerals originating from the underlying mineral soil layers (Kruyts et al., 2004; Tyler et al., 2001). At the tree level, the advantages of the WIP approach compared to TF have already been discussed (Thiry et al., 2002). Our results confirm that WIP and TF values are in some cases contradictory. In the forest stands investigated, the divergences may be explained by discrepancies in the evaluation of 137Cs availability in soil (between stands III and IV) or stemwood production (between stands IV and V) (Table 3), which both are not satisfactorily described in the TF approach (Goor and Thiry, 2004). At the scale of forest stands, the proportionality observed between soil (SA) and tree (WIP) indices (Fig. 4) corroborates the relevancy of WIP as an indicator of the current 137Cs root uptake by the trees, even though a limited number of forest stands was investigated, which also limits the possibilities to extrapolate this relationship to other tree ages and types of soil. These results open, nevertheless, perspectives for the improvement of existing models of 137Cs cycling and accumulation in trees, notably through the possibility to deduce WIP values directly from SA calculations using the proportionality coefficient derived from Fig. 4, and inversely. For the near future, the WIP values, as proxy of the current 137Cs root uptake by trees, may also be combined with local forest production tables (Goskom, 1984) to estimate the evolution of the 137Cs content in stemwood, the additional 137Cs activity in whole stemwood between two successive growing seasons being obtained by multiplying the WIP by the relative wood volume increase, as discussed in Goor (2003). For longer time scales, the WIP of a given forest stand will nevertheless evolve as a function of tree ageing and changes in the upper soil layers features. In this case, new WIP values may be derived from Fig. 4 and Eq. (1) combined with 137Cs migration models in forest soils, considering a dynamic evolution of the soil profile depending on the edaphotope and the age of the trees. This solution, which could be conceptualised in a model, constitutes also a sound basis to rank contaminated forest ecosystems in terms of vulnerability to stemwood contamination with 137Cs. 6. Conclusion Twenty years after the Chernobyl accident, root uptake from the surface layers of contaminated forest soils plays a
135
major role in the 137Cs transfer and incorporation in trees. Considering the complexity and the extended lifetime of forest ecosystems, the adequacy of integrated parameters like the commonly used static TF to characterize the source-sink relationship between soil and trees is questionable, particularly in the perspective of modelling the evolution of 137Cs content in perennial tree components in the long term. An alternative approach was therefore proposed: the WIP for stemwood. Up to now, the relevancy of this parameter as an indicator of the current 137 Cs root uptake by trees was nevertheless not evaluated at the scale of the whole forest ecosystem. In this context, the main objective of the present paper was to compare WIP values with the pool of 137Cs available for root uptake, the latter being defined in order to integrate as far as possible the key parameters driving the fate of 137Cs in forest soils. Practically, the comparative analysis of five contaminated forests differing in tree ages and soil types revealed significant similarities in the 137Cs accumulation (stemwood)—availability (soil) relationship for the tree ages and soil types investigated, confirming the WIP as a relevant indicator of current 137Cs root uptake by trees. As the indicator of 137Cs availability was developed in view of the current knowledge to 137Cs fate in forest soils, this relationship also constitutes a sound basis for a common approach of 137Cs soil-to-stemwood transfer studies, whatever the characteristics of forests ecosystems, as well as for the improvement of predictions from the existing models of 137Cs cycling in contaminated forests. More mechanistic and dynamic descriptions of the processes involved in the 137Cs transfer are indeed required in order to provide reliable predictions for the long-term management of contaminated forest ecosystems. Acknowledgements The authors wish to thank P. Bogaert (UCL—ENGE) for his help in the interpretation of the datasets used in this study, and V. Brahy (ULB—IGEAT) for his relevant comments on the manuscript. References Bunzl, K., Kracke, W., Schimmack, W., 1995. Migration of Fallout 239+240 Pu, 241Am and 137Cs in the various horizons of a forest soil under pine. Journal of Environmental Radioactivity 28 (1), 17–34. Cremers, A., Elsen, A., Valcke, E., Wauters, J., Sandalls, F., Gaudern, S., 1990. Quantitative analysis of radiocaesium retention in soils. Nature 335, 247–249. Davydchuk, V., 1999. Radioactively contaminated forests: GIS application for the remedial policy development and environmental risk assessment. In: Linkov, I., Schell, W.R. (Eds.), Contaminated forests: recent developments in risk identification and future perspectives. Kluwer Academic, Kiev, pp. 369–376. Delvaux, B., Kruyts, N., Cremers, A., 2000. Rhizospheric mobilization of radiocesium in soils. Environmental Science and Technology 34, 1489–1493.
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