Journal of Environmental Radioactivity 102 (2011) 386e392
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Correlations between potassium, rubidium and cesium (133Cs and sporocarps of Suillus variegatus in a Swedish boreal forest
137
Cs) in
M. Vinichuk a, c, *, K. Rosén a, K.J. Johanson a, A. Dahlberg b a
Department of Soil and Environment, Swedish University of Agricultural Sciences, P.O. Box 7014, SE-750 07 Uppsala, Sweden Department of Forest Mycology and Pathology, Swedish University of Agricultural Sciences, P.O. Box 7026, 750 07 Uppsala, Sweden c Department of Ecology, Zhytomyr State Technological University, 103 Cherniakhovsky Str., 10005 Zhytomyr, Ukraine b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 October 2010 Received in revised form 1 February 2011 Accepted 13 February 2011 Available online 8 March 2011
An analysis of sporocarps of ectomycorrhizal fungi Suillus variegatus assessed whether cesium (133Cs and 137 Cs) uptake was correlated with potassium (K) or rubidium (Rb) uptake. The question was whether intraspecific correlations of Rb, K and 133Cs mass concentrations with 137Cs activity concentrations in sporocarps were higher within, rather than among, different fungal species, and if genotypic origin of sporocarps within a population affected uptake and correlation. Sporocarps (n ¼ 51) from a Swedish forest population affected by the fallout after the Chernobyl accident were studied. The concentrations were 31.9 6.79 g kg1 for K (mean SD, dwt), 0.40 0.09 g kg1 for Rb, 8.7 4.36 mg kg1 for 133Cs and 63.7 24.2 kBq kg1 for 137Cs. The mass concentrations of 133Cs correlated with 137Cs activity concentrations (r ¼ 0.61). There was correlation between both 133Cs concentrations (r ¼ 0.75) and 137Cs activity concentrations (r ¼ 0.44) and Rb, but the 137Cs/133Cs isotopic ratio negatively correlated with Rb concentration. Concentrations of K and Rb were weakly correlated (r ¼ 0.51). The 133Cs mass concentrations, 137Cs activity concentrations and 137Cs/133Cs isotopic ratios did not correlate with K concentrations. No differences between, within or, among genotypes in S. variegatus were found. This suggested the relationships between K, Rb, 133Cs and 137Cs in sporocarps of S. variegatus is similar to other fungal species. Ó 2011 Elsevier Ltd. All rights reserved.
1. Introduction Radiocesium released after the Chernobyl accident in 1986 is still a critical fission product in the environment in Sweden because of its long half-life of 30 years. The behavior of 137Cs in forest ecosystems differs substantially from other ecosystems, foremost due to the abundance of fungi, which contribute to the persistence of Chernobyl radiocesium in the upper horizons of forest soils (Vinichuk and Johanson, 2003). Saprotrophic and mycorrhizal fungi have key roles in nutrient and carbon cycling processes in forest soils (Dighton, 2003). Although fungal biomass is relatively low (Dighton et al., 1991; Rafferty et al., 1997), many fungal species accumulate more 137Cs than vascular plants do (Rosén et al., 2009; Vinichuk et al., 2010b); hence, the contribution of fungi to 137Cs cycling in forest systems is substantial. Fungal
* Corresponding author. Department of Soil and Environment, Swedish University of Agricultural Sciences, P.O. Box 7014, SE-750 07 Uppsala, Sweden. Tel.: þ46 18 67 14 42; fax: þ46 18 67 28 95. E-mail addresses:
[email protected],
[email protected] (M. Vinichuk). 0265-931X/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jenvrad.2011.02.007
sporocarps may only account for about 0.5% (McGee et al., 2000), sometimes 0.01e0.1% (Nikolova et al., 1997), of the total radiocesium within a forest ecosystem; however, due to the high levels of 137Cs in sporocarps, their contribution to the internal dose in man may be high through consumption of edible mushrooms (Skuterud et al., 1997; Kalac, 2001). Fungi are important for 137Cs uptake and migration in forest systems and since the Chernobyl accident, fungal species may contain high concentrations of radiocesium; however, the reasons and mechanisms for the magnitude higher concentration of radiocesium in fungi than in plants is unclear (Yoshida and Muramatsu, 1998; Kuwahara et al., 1998; Bystrzejewska-Piotrowska and Bazala, 2008). Fungi accumulate rubidium (Rb) and stable cesium (133Cs) effectively (Gaso et al., 2000), and concentrations of 137Cs, 133Cs and Rb in fungal sporocarps can be one order of magnitude higher than those in plants growing in the same forest (Vinichuk et al., 2010a). However, the chemical behavior of the alkali metals, K, Rb and 133 Cs, is expected to be similar to 137Cs, due to similarities in their physicochemical properties (Enghag, 2000). The concentrations of K, Rb and 133Cs have been analyzed in fungal sporocarps (Tyler, 1980; Horyna and Zanda, 1988; Yoshida ˇ
Keywords: Ectomycorrhizal fungi K Rb 133 Cs 137 Cs
M. Vinichuk et al. / Journal of Environmental Radioactivity 102 (2011) 386e392
and Muramatsu, 1998; Baeza et al., 2005; Vinichuk et al., 2010a). Cesium uptake in fungi is affected by the presence of K and Rb, and the presence of 133Cs affects K uptake (Terada et al., 1998; Gyuricza et al., 2010). However, in sporocarps, the relationships between these alkali metals and 137Cs and their underlying mechanisms are insufficiently understood. The correlations between 137Cs and these alkali metals suggest the mechanism of fungal uptake of 133Cs and 137 Cs is different from that of K (Yoshida and Muramatsu, 1998): Rb has intermediate behavior between K and 133Cs (Yoshida and Muramatsu, 1998). This interpretation is based on sporocarp analysis of -different ectomycorrhizal and saprotrophic fungal species, although with few sporocarps from each species. Fungal accumulation of 133Cs is reported as species-dependent but there are few detailed studies of individual species (Gillett and Crout, 2000). However, the variation in 137Cs levels within the same genotype of fungal sporocarps can be as large as the variation among different genotypes (Dahlberg et al., 1997). The isotopic (atom) ratio 137 Cs/133Cs can also be used to interpret and understand the uptake and relations between 137Cs and 133Cs and K and Rb metals in fungi. Chemically 133Cs and 137Cs are the same, but the atom abundance and isotopic disequilibrium differ greatly. The attainment equilibrium between stable 133Cs and 137Cs in the bioavailable fraction of soils within forest ecosystems is reported (Rühm et al., 1999; Karadeniz and Yaprak, 2007). Sporocarps of ectomycorrhizal fungi Suillus variegatus from a single forest were analyzed to determine whether i) Cs (133Cs and 137Cs) uptake was correlated with K uptake, ii) intraspecific correlation of these alkali metals and 137Cs activity concentrations in sporocarps was higher within, rather than among, different fungal species; and iii) genotypic origin of sporocarps affected uptake and correlation. 2. Materials and methods 2.1. Sampling area The forest study area was located in Harbo (Heby county), about 40 km north-west of Uppsala in central Sweden (N 60 080 ; E 17100 ). The forest is located on moraine and is dominated by Scots pine (Pinus sylvestris) and Norway spruce (Picea abies), with inserts of deciduous trees, primarily birch (Betula pendula and Betula pubescens). The field layer consisted mainly of the dwarf shrub bilberry (Vaccinium myrtillus - L.), lingonberry (Vaccinium vitisidaea - L.) and, heather (Calluna vulgaris - L.). Sampling sites were generally located on superficial bedrock overlaid with a thin layer of soil: for further details about the area and sampling, see Dahlberg et al. (1997). The ground deposition of 137Cs within the Harbo area in 1986 was 35e40 kBq m2, according to aircraft measurements (SGAB, 1986) and, 33 10 kBq m2 in 1992, according to measurements on soil samples (Johanson and Bergström, 1994). 2.2. Samples of Suillus variegatus sporocarps A selection of dried sporocarps of S. variegatus (n ¼ 51) kept from the study on the relationship between 137Cs activity concentrations and genotype identification by Dahlberg et al. (1997) was used. The sporocarps were collected from five sampling sites (100e1600 m2 in size), within an area of about 1 km2, once a week during sporocarp season, from the end of August through September, 1994. Eight genotypes with 2e8 sporocarps each was tested (in total 32 sporocarps) and are referred to here as individual genotypes. Sporocarps within genotypes were spatially separated up to 10e12 m. All genotypes were used in the estimation of correlation coefficients, but only genotypes with at least four sporocarps were included in the alkali metal analysis. In addition, 19 individual sporocarps with unknown genotype (i.e. not tested
387
for genotype identity) were included: these sporocarps consisted of both the same and different genotypes. The combined set of sporocarps refers to all sporocarps: for further details about the sampling and identification of genotypes, see Dahlberg et al. (1997). 2.3. Chemical analyses and radiometry For purpose of this study, dry material from 51 individual sporocarps from the previous study (Dahlberg et al., 1997) was used. The 137Cs activity concentration values corrected to sampling date and expressed as kBq kg1 dry weight (d.w.) for each sporocarp, as reported by Dahlberg et al. (1997), were used. For element analyses (K, Rb and 133Cs), an aliquot of about 0.3 g of each sample was mixed with 5 mL HNO3 þ 0.5 ml 30% hydrogen peroxide and digested in a microwave oven. Then, the mixture was diluted with MQ water and analyzed by an inductively coupled plasma technique at the laboratories of ALS Scandinavia (a company within the ALS Laboratory Group, Luleå, Sweden). The analyses were accompanied by rigorous quality control. Accuracy assessment was with plant certified reference material, peach leaves NIST 1547 (NST, Gaithenburg, USA), which has a matrix close to fungal material: the recoveries were 97e101% for K; 97.5e99.4% for Rb and, 93.7e102.5% for 133Cs. For detailed measurement procedures, see Rodushkin et al. (2008). Element concentrations are reported as mg kg1 d.w. and the isotopic ratio of 137Cs/133Cs was calculated with Equations (1) and (2) (Chao et al., 2008): 137 Cs 133 Cs
¼
A a 103 C lN
(1)
where “A” is the 137Cs radioactivity (Bq kg1); “l” is the disintegration rate of 137Cs 7.25 1010 s1; “a” is the atomic weight of cesium (132.9); “N” is the Avogadro number, which is 6.02 1023; and “133C” and “C” are the 133Cs concentration (mg g1). Eq. (1) can be simplified as Eq. (2): 137 Cs 133 Cs
¼ 3:05 1010
A C
(2)
: where “A” is the 137Cs activity concentration in Bq kg1 and 133C is the 133Cs concentration in mg kg1. Thus, the units of the isotope ratio are dimensionless. 2.4. Statistical analyses Relationships between K, Rb, 133Cs and 137Cs concentrations in different fractions were identified by Pearson correlation coefficients. Correlation coefficients were analyzed in five separate sets of samples: in four sets, all samples had known genotype identity and, in the last set, there was a combined set of samples containing both genotypes that had been tested by somatic incompatibility sporocarps and geneotypes that had non been tested. Correlation analyses for genotypes with three or less sporocarps were omitted. All statistical analyses were run with MinitabÒ 15.1.1.0. (Ó 2007 Minitab Inc.) software, with level of significance of 5% (0.05), 1% (0.01) and 0.1% (0.001). 3. Results The concentrations of K (range 22.2e52.1 g kg1) and Rb (range 0.22e0.65 g kg1) in sporocarps of S. variegatus varied in relatively narrow ranges, whereas, the mass concentration of 133Cs had a range of 2.16e21.5 mg kg1 and the activity concentration of 137Cs from 15.8 to 150.9 kBq kg1. Both 133Cs and 137Cs had wider ranges than K or Rb within sporocarps from the same genotype or across
388
M. Vinichuk et al. / Journal of Environmental Radioactivity 102 (2011) 386e392
Table 1 Potassium, rubidium and cesium (133Cs) mass concentrations and 137Cs activity concentrations in sporocarps of S. variegatus (d.w.) from identified and unknown genotypes, where n ¼ number of sporocarps analyzed, M ¼ mean, SE ¼ standard deviation, CV ¼ coefficient of variation. Site-genotypea
n
K g kg1 M
SD
%
g kg1
CV
M
Sporocarps with identified genotypes 2-1 8 30.6 8.1 26 2-2 6 28.0 7.0 25 4-3 4 28.5 2.1 7.5 4-4 3 33.6 8.6 e 4-5 2 38.9 2.4 e 4-6 2 35.2 8.8 e 7-7 5 33.7 5.8 17 6-8 2 25.4 1.3 e Sporocarps with unknown genotypes 19 33.4 6.7 20 Combined set of sporocarps (identified and unknown genotypes) 51 31.9 6.8 21 a
133
Rb
137
Cs
%
mg kg1
SD
CV
M
0.47 0.50 0.39 0.30 0.36 0.37 0.34 0.31
0.12 0.07 0.16 0.04 0.02 0.11 0.06 0.03
25 14 4.0 e e e 18 e
0.38
0.08
0.40
0.09
Cs
%
kBq kg1
SD
CV
M
SD
CV
12.1 16.6 6.6 3.0 3.8 3.7 6.7 8.7
4.2 2.2 0.44 0.60 0.04 2.2 0.80 2.2
35 13 6.7 e e e 12 e
67 76 6.9 39.1 35.7 26.8 71.4 63.3
35 23 12 9.4 28 8.5 9.3 18
52 31 17 e e e 13 e
20
7.7
2.0
26
66
21
32
24
8.7
4.4
50
64
24
38
%
Site numbering according to Dahlberg et al. (1997), the second figure is a running number of the study’s different genotypes.
the combined set of sporocarps (Table 1). The mean 137Cs/Cs isotopic ratio in the combined set of sporocarps was 2.5 107 (range 8.3 108 and 4.4 107). The 137Cs/Cs isotopic ratios from identified genotypes were site-genotype dependent: the ratio values of genotypes at site 4 were about two times higher than the ratios of genotypes at site 2 (Table 2). The concentrations of K in sporocarps of S. variegatus were not related to the concentrations of 137Cs (r ¼ 0.10) or 133Cs (r ¼ 0.07) in the combined data set (Fig. 1: c2, b2). In contrast, the concentrations of K and Rb were significantly correlated in the combined data set (r ¼ 0.51, Fig. 1: a2). Rubidium was strongly correlated with stable 133Cs (r ¼ 0.75) and moderately correlated with 137Cs (r ¼ 0.44) and K (r ¼ 0.51) (Fig. 1: d2, e2, a2). Both 133Cs and 137Cs were significantly correlated in the combined set of data (Fig. 1: f2). The 137Cs/Cs isotopic ratio in the combined data set was not correlated to K concentration, but correlated moderately and negatively with both 133Cs (r ¼ 0.64) and Rb (r ¼ 0.50) concentrations (Fig. 2: a, c, b). Potassium, 133Cs and 137Cs within the four genotypes were not correlated, with one genotype exception (Table 3, Fig. 1: b1, c1). However, the exception was conditional due to a one single value. Three of four analyzed sporocarp genotypes had high correlation between K and Rb: the forth was only moderately correlated (Table 3; Fig. 1: a1). However, the correlations between 137Cs and K and, Rb and 133Cs in the four genotypes were inconsistent (Table 3; Fig. 1: c1, e1, f1). Potassium, Rb, 133Cs and 137Cs were correlated in genotype 2-1 (due to one single value), whereas, no or negative correlations were found between the same elements/isotopes for the other three genotypes. In two of four genotypes, the 137Cs/Cs isotopic ratio was not correlated with either 133Cs or K and Rb; however, there was a negative correlation with Rb in one genotype (2-2) and positive correlation with 133Cs in another (4-3) (Table 3).
4. Discussion The study of S. variegatus revealed no significant correlations between 133Cs mass concentration or 137Cs activity concentration and the concentration of K in sporocarps, either within the whole population or among the genotypes. The concentration of K in sporocarps appeared independent of the 137Cs/Cs isotopic ratio in both the whole population and among the genotypes, with one exception. This supported results from an earlier study (Ismail, 1994) suggesting 133Cs and K are not correlated in mushrooms. Ismail’s study, however, was based on sporocarps from many fungal species (28e72 species), but only a single or few sporocarps from each species. Based on a similar analyses of sporocarps from many fungal species, Yoshida and Muramatsu (1998) conclude the uptake mechanism for 137Cs differs from the uptake mechanism for K. Correlation analysis may be a useful, although not definitive, approach for elucidating similarities or differences in uptake mechanisms of cesium (137Cs and 133Cs) and K. The concentration of K, mass concentration of 133Cs and, activity concentration of 137Cs is usually higher in fungal sporocarps then in mycelium: ratios between concentrations (activity concentrations) in sporocarps and mycelium are reported to be 15 for K, 7 for 133Cs (Vinichuk et al., 2010a), about 10 for 137Cs (Vinichuk and Johanson, 2003). The absence of any relation between 137C (or 133Cs) and K in fungi may be because the incorporation of K is self-regulated by the nutritional requirements of the fungus, whereas, incorporation of 137Cs is not self-regulated by the fungus (Baeza et al., 2004). Although K and cesium (133Cs and 137Cs) concentrations did not correlate within S. variegatus, both Kþ and Csþ ions may compete for uptake by fungi. In experiments under controlled conditions and with sterile medium, the competition between Csþ and Kþ depends on Csþ concentration in the growth medium and on the path of Csþ uptake (Bystrzejewska-Piotrowska and Bazala, 2008). In
Table 2 137 Cs/133Cs isotopic (atom) ratios in sporocarps of S. variegatus from identified genotypes, with unknown genetic belonging and the two groupings combined, 107. M ¼ mean, CV ¼ coefficient of variation. Site-genotypea
M CV, % a
Identified genotypes 2-1
2-2
4-3
4-4
4-5
4-6
7-7
6-8
1.67 97
1.43 36
3.16 10
3.95 5.1
2.86 78
2.43 30
3.27 9.2
2.24 3.9
Unidentified genotypes
Combined set of sporocarps
2.62 20
2.50 35
Site numbering according to Dahlberg et al. (1997), the second figure is a running number of the study’s different genotypes.
M. Vinichuk et al. / Journal of Environmental Radioactivity 102 (2011) 386e392
a1
50
K:Rb
45
45
40
40
35
35
K, g kg-1
K, g kg-1
50
30 2-1
25
30
20
4-3
15
K:Rb
a2
25
2-2
20
15
7-7
10
y = 36.7x + 17.4; r = 0.505***
10 0.2
0.4
0.6
0.8
0.2
0.3
Rb, g kg-1
b1
50
K:133Cs
45
45
40
40
35
35
K, g kg-1
K, g kg-1
50
30 2-1
25
0.4 0.5 Rb g kg-1
0.6
0.7
K:133Cs
b2
30 25
2-2
20
20
4-3
15
y = -0.1x + 32.8; r = -0.066
15
7-7
10
10 5
10
15 133Cs,
50
20
0
25
5
mg kg-1
10 133Cs,
50
K:137Cs
c1
45 40
40
35
35
15
20
25
mg kg-1
K:137Cs
c2
45
K, g kg-1
K, g kg-1
389
30
30
2-1
25
2-2
25
20
4-3
20
15
7-7
15
y = 0.03x + 30.10; r = 0.103
10
10 0
50
100 137Cs,
kBq
150
0
200
50
100 137Cs,
kg-1
150
200
kBq kg-1
Fig. 1. Relationship between 137Cs and K, Rb and Cs concentrations in sporocarps from four genotypes (a1ef1) and in the combined set of all S. variegatus sporocarps (a2ef2). K:Rb (a1, a2); K:Cs (b1, b2); K:137Cs (c1, c2); Rb:Cs (d1, d2); Rb:137Cs (e1, e2); and, Cs:137Cs (f1, f2). The figures in a) refer to site number and running genotype number (see Table 1). ***p < 0.001.
addition, radiocesium transport by arbuscular mycorrhizal (AM) fungi decreases if there is increased K concentration in a compartment accessible only to AM (Gyuricza et al., 2010) and, a higher Cs:K ratio in the nutrient solution increases uptake of Cs by ectomycorrhizal seedlings (Brunner et al., 1996). A noticeable (20e60%) and long-lasting (at least 17 years) reduction in 133Cs activity concentration in fungal sporocarps due to a single K fertilization of 100 kg ha1 in a Scots pine forest is reported by Rosén et al. (2011). The relation between 137Cs and K and, Rb and 133Cs within S. variegatus was similar to an earlier report on different species of fungi (Yoshida and Muramatsu, 1998). Rubidium concentration in sporocarps was positively correlated with 133Cs and 137Cs, but negatively correlated with 137Cs/133Cs isotopic ratio, i.e. a lower
137
Cs/133Cs ratio in sporocarps resulted in a higher Rb uptake by fungi. This ratio may reflect the soil layers explored by the mycelia (Rühm et al., 1997). Fungi have a higher affinity for Rb than for K and cesium (Ban-Nai et al., 1997; Yoshida and Muramatsu, 1998), and Rb concentrations in sporocarps can be more than one order of magnitude greater than in mycelium extracted, as fungal sporocarps, from soil of the same plots (Vinichuk et al., 2010a). However, soil mycelia always consist of numerous fungal species and intraspecific relationships between soil mycelia and sporocarps is difficult and has not yet been estimated. Mass concentration of 133Cs and activity concentration of 137Cs have different relations in fungal sporocarps: in two of four genotypes there was a high and significant correlation, one showed high correlation
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Rb:133Cs
d1
0.8
0.7
0.7
0.6
0.6
Rb g kg-1
Rb, g kg-1
0.8
0.5 2-1
0.4
4-3
0.3
7-7
y = 0.02x + 0.26; r = 0.746***
0.2
0.2 5
10
15 133Cs,
0.8
20
25
0
10 133Cs,
Rb:137Cs
e1
5
mg kg-1 0.8
0.7
0.7
0.6
0.6
0.5 2-1
0.4
Rb, g kg-1
Rb, g kg-1
0.5 0.4
2-2
0.3
Rb:133Cs
d2
4-3
0.5
0.3 y = 0.002x + 0.287; r = 0.440***
0.2
0.2 50
100 137Cs,
23
150
0
200
50
kBq kg-1
100 137Cs,
133Cs:137Cs
f1
25
Rb:137Cs
e2
7-7
0
20
0.4
2-2
0.3
15
mg kg-1
25
kBq
150
200
kg-1
133Cs:137Cs
f2
21
15 13
2-1
11
mg kg-1
mg kg-1 133Cs,
17
15
133Cs,
20
19
10
2-2
9
5
4-3
7
y = 0.11x + 1.75; r = 0.605***
7-7
0
5 0
50
100 137Cs,
150 kBq kg-1
0
200
50 137Cs,
100 kBq kg-1
150
200
Fig. 1. (continued).
and one had no correlation, whereas, correlation between 137Cs and 133Cs within the whole population was only moderate. In terms of 133Cs and 137Cs behavior, there would be no biochemical differentiation, but there could be differences in atom abundance and isotopic disequilibrium within the system. Fungi have large spatiotemporal variation in 133Cs and 137Cs content in sporocarps of the same species and different species (de Meijer et al., 1988). The variation in K, Rb, 133Cs and 137Cs concentrations within a single genotype appeared similar, or lower, than the variation within all genotypes. The results for 137Cs and alkali elements in a set of samples of S. variegatus, collected during the same season and consisting of sporocarps from both different and the same genotype, indicated the variability in concentrations was similar to different fungal species collected in Japan over three years (Yoshida and Muramatsu, 1998).
The relatively narrow range in K and Rb variation and the higher Cs and 137Cs variations might be due to different mechanisms being involved. Baeza et al. (2004) suggest the incorporation of K is selfregulated by nutritional requirements of the fungus, whereas, the incorporation of 137Cs is not. The differences in correlation coefficients between 137Cs and the alkali metals varied among and within the genotypes of S. variegatus, suggesting both interspecific and intrapopulation variation in the uptake of K, Rb, stable 133Cs and, 137Cs and, their relationships could be explained by factors other than genotype identity. The variability in 137Cs transfer depends on the sampling location of fungal sporocarps (Smith et al., 1993; Gillett and Crout, 2000). For S. variegatus, these interaction factors might include the spatial pattern of soil chemical parameters, heterogeneity of 137Cs fallout, mycelia location and, heterogeneity, due to abiotic and biotic interactions, may have increased over time (Dahlberg et al., 1997). 133
M. Vinichuk et al. / Journal of Environmental Radioactivity 102 (2011) 386e392
a
5.E-07
b
137Cs/133Cs:K
5.E-07
4.E-07
4.E-07 137Cs/133Cs
137Cs/133Cs
391
3.E-07 2.E-07
3.E-07 2.E-07
1.E-07
1.E-07 y = 2E-09x + 2E-07; r = 0.181
y = -5E-07x + 4E-07; r = -0.500***
0.E+00
0.E+00 10
30 K, g kg-1
c
50
70
5.E-07
0.4 Rb, g kg-1
0.6
137Cs/Cs:133Cs
y = -1E-08x + 4E-07; r = -0.636***
4.E-07 137Cs/133Cs
0.2
3.E-07 2.E-07 1.E-07 0.E+00 0
5
10 133Cs,
Fig. 2. Relationship between the 137Cs/133Cs isotopic (atom) ratios and K, Rb and 137 Cs/133Cs:Rb; and, (c) 137Cs/133Cs:133Cs. ***p < 0.001.
Table 3 Correlation coefficients between concentrations of potassium, rubidium and cesium (133Cs and 137Cs) in genotypes of S. variegatus with more than four sporocarps analyzed. Cs
Genotype 2-1 (8 sporocarps) K 0.50 Rb 0.63* 133 Cs 0.91** 137 Cs/133Cs Genotype 2-2 (6 sporocarps) K 0.47 Rb 0.66 133 Cs 0.26 137 Cs/133Cs Genotype 4-3 (4 sporocarps) K 0.53 Rb 0.18 133 Cs 0.98* 137 133 Cs/ Cs Genotype 7-7(5sporocarps) K 0.56 Rb 0.47 133 Cs 0.70 137 Cs/133Cs *p < 0.05; **p < 0.01; ***p < 0.001.
133
K
Rb
0.97*** 0.75* 0.17
0.84** 0.058
0.93** 0.14 0.35
0.16 0.61
0.59
0.18 0.16
0.93
0.70 0.57 0.49
0.99** 0.53 0.12
Cs
0.24
20
133
Within the combined set of sporocarps the concentration of Rb and 137Cs activity concentration in S. variegatus sporocarps were normally distributed but the frequency distribution of 133Cs and K was not. Asymmetry of 137Cs frequency distributions is reported in other fungal species (Ismail, 1994; Gaso et al., 1998; Baeza et al.,
137
15 mg kg-1
25
Cs concentrations in the combined set of S. variegatus sporocarps, (a)
137
Cs/133Cs:K; (b)
2004). According to Gillett and Crout (2000), the frequency distribution of 137Cs appears species-dependent: high accumulating species tend to be normally distributed and low accumulating species tend to be log-normally distributed. However, lognormal distribution is almost the default for concentration of radionuclides and is unlikely to be a species-specific phenomenon, as it also occurs in soil concentrations; implying normal distribution would not be expected even if large set of samples were analyzed. 5. Conclusions The study of S. variegatus sporocarps sampled within 1 km2 forest area with high 137Cs fallout from the Chernobyl accident confirms 133Cs and 137Cs uptake is not correlated with uptake of K, whereas, the uptake of Rb is closely related to the uptake of 133Cs. The hypothesis of intraspecific correlations of alkali metals and 137 Cs activity concentrations in sporocarps being higher within, rather than among, different genotypes is not supported. Furthermore, the variability in 137Cs and alkali metals (K, Rb and 133Cs) within S. variegatus appears similar among different species. Finally, the variations in concentrations of K, Rb and 133Cs and, 137Cs activity concentration in sporocarps of S. variegatus appear to be influenced by factors other than genetic differences among fungal genotypes. Acknowledgments
0.40 0.16
0.35
The authors gratefully acknowledge the Swedish University of Agricultural Sciences (SLU), Sweden, for supporting the project.
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References Baeza, A., Guillén, J., Hernández, S., Salas, A., Bernedo, M., Manjón, J.L., Moreno, G., 2005. Influence of the nutritional mechanism of fungi (mycorrhize/saprophyte) on the uptake of radionuclides by mycelium. Radiochim. Acta 93 (4), 233e238. doi:10.1524/ract.93.4.233.64074. Baeza, A., Hernández, S., Guillén, F.J., Moreno, J., Manjón, J.L., Pascual, R., 2004. Radiocaesium and natural gamma emitters in mushrooms collected in Spain. Sci. Total Environ. 318 (1e3), 59e71. doi:10.1016/S0048-9697(03)00363-2. Ban-Nai, T., Muramatsu, Y., Yoshida, S., Uchida, S., Shibata, S., et al., 1997. Multitracer studies on the accumulation of radionuclides in mushrooms. J. Radiat. Res. 38 (4), 213e218. Brunner, I., Frey, B., Riesen, T.K., 1996. Influence of ectomycorrhization and cesium/ potassium ratio on uptake and localization of cesium in Norway spruce seedlings. Tree Physiol. 16, 705e711. Bystrzejewska-Piotrowska, G., Bazala, M.A., 2008. A study of mechanisms responsible for incorporation of cesium and radiocaesium into fruitbodies of king oyster mushroom (Pleurotus eryngii). J. Environ. Radioact. 99, 1185e1191. Chao, J.H., Chiu, C.Y., Lee, H.P., 2008. Distribution and uptake of 137Cs in relation to alkali metals in a perhumid montane forest ecosystem. Appl. Radiat. Isot. 66, 1287e1294. Dahlberg, A., Nikolova, I., Johanson, K.J., 1997. Intraspecific variation in 137Cs activity concentration in sporocarps of Suillus variegatus in seven Swedish populations. Mycol. Res. 101, 545e551. de Meijer, R.J., Aldenkamp, F.J., Jansen, A.E., 1988. Resorption of cesium radionuclides by various fungi. Oecologia 77, 268e272. Dighton, J., 2003. Fungi in Ecosystem Processes. Marcel Dekker, New York. Dighton, J., Clint, G., Poskitt, J., 1991. Uptake and accumulation of radiocaesium by upland grassland soil fungi: a potential pool of Cs immobilization. Mycol. Res. 95, 1052e1065. Enghag, P., 2000. Jordens Grundämnen Och Deras Upptäckt. Industrrilitteratur, Stockholm. Gaso, M.I., Segovia, N., Herrera, T., Perez-Silva, E., Cervantes, M.L., Quintero, EM.I., Palacios, J., Acosta, E., 1998. Radiocesium accumulation in edible wild mushrooms from coniferous forests around the Nuclear Centre of Mexico. Sci. Total Environ. 223, 119e129. Gaso, M.I., Segovia, N., Morton, O., Cervantes, M.L., Godinez, L., Peña, P., Acosta, E., 2000. 137Cs and relationships with major and trace elements in edible mushrooms from Mexico. Sci. Total Environ. 262 (1e2), 73e89. Gillett, A.G., Crout, N.M.J., 2000. A review of 137Cs transfer to fungi and consequences for modeling environmental transfer. J. Environ. Radioact. 48, 95e121. Gyuricza, V., Dupré de Boulois, H., Declerck, S., 2010. Effect of potassium and phosphorus on the transport of radiocaesium by arbuscular mycorrhizal fungi. J. Environ. Radioact. 101, 482e487. Horyna, J., Zanda, Z., 1988. Uptake of radiocesium and alkali metals by mushrooms. J. Radioanal. Nucl. Chem. 172 (2), 107e120. doi:10.1007/BF02164600. Ismail, S.S., 1994. Distribution of Na, K, Rb, Cs, and 137Cs in some Austrian higher fungi. Biol. Trace Elem. Res., 43e45. 707e714. Johanson, K.J., Bergström, R., 1994. Radiocaesium transfer to man from moose and roe deer in Sweden. Sci. Total Environ. 157, 309e316. Kalac, P., 2001. A review of edible mushroom radioactivity. Food Chem. 75, 29e35.
Karadeniz, Ö, Yaprak, G., 2007. Dynamic equilibrium of radiocesium with stable cesium within the soilemushroom system in Turkish pine forest. Environ. Pollut. 148 (1), 316e324. Kuwahara, C., Watanuki, T., Matsushita, K., Nishina, M., Sugiyama, H., 1998. Studies on uptake of cesium by mycelium of the mushroom (Pleurotus ostreatus) by 133 Cs-NMR. J. Radioan. Nucl. Chem. 235 (1e2), 191e194. McGee, E.J., Synnott, H.J., Johanson, K.J., Fawaris, B.H., Nielsen, S.P., Horrill, A.D., et al., 2000. Chernobyl fallout in a Swedish spruce forest ecosystem. J. Environ. Radioact. 48, 59e78. Nikolova, I., Johanson, K.J., Dahlberg, A., 1997. Radiocesium in fruitbodies and Mycorrhizae in ectomycorrhizal fungi. J. Environ. Radioact. 37, 115e125. Rafferty, B., Dawson, D., Kliashtorin, A., 1997. Decomposition in two pine forests: the mobilization of 137Cs and K from forest litter. Soil Biol. Biochem. 29 (11/12), 1673e1681. Rodushkin, I., Engström, E., Sörlin, D., Baxter, D., 2008. Levels of inorganic constituents in raw nuts and seeds on the Swedish market. Sci. Total Environ. 392, 290e304. Rosén, K., Vinichuk, M., Nikolova, I., Johanson, K., 2011. Long-term effects of single potassium fertilization on 137Cs levels in plants and fungi in a boreal forest ecosystem. J. Environ. Radioact. 102 (2), 178e184. Rosén, K., Vinichuk, M., Johanson, K.J., 2009. 137Cs in a raised bog in central Sweden. J. Environ. Radioact. 100, 534e539. Rühm, W., Yoshida, S., Muramatsu, Y., Steiner, M., Wirth, E., 1999. Distribution patterns for stable 133Cs and their implications with respect to the long-term fate of radioactive 134Cs and 137Cs in a semi-natural ecosystem. J. Environ. Radioact. 45 (3), 253e270. Rühm, W., Kammerer, L., Hiersche, L., Wirth, E., 1997. The 137Cs/134Cs ratio in fungi as an indicator of the major mycelium location in forest soil. J. Environ. Radioact. 35 (2), 129e148. SGAB, 1986. Cs-137 Ground Deposition Map over Sweden. Swedish Geological Co., Uppsala. Skuterud, L., Travnikova, I.G., Balonov, M.I., Strand, P., Howard, B.J., 1997. Contribution of fungi to radiocaesium intake by rural populations in Russia. Sci. Total Environ. 193, 237e242. Smith, M.L., Taylor, H.W., Sharma, H.D., 1993. Comparison of the post-chernobyl 137 Cs contamination of mushrooms from Eastern Europe, Sweden, and North America. Appl. Environ. Microbiol. 59 (1), 134e139. Terada, H., Shibata, H., Kato, F., Sugiyama, H., 1998. Influence of alkali elements on the accumulation of radiocesium by mushrooms. J. Radioanal. Nucl. Chem. 235 (1e2), 195e200. Tyler, G.,1980. Metals in sporophores of basidiomycetes. Trans. Br. Mycol. Soc. 74, 41e49. Vinichuk, M., Taylor, A.F.S., Rosén, K., Johanson, K.J., 2010a. Accumulation of potassium, rubidium and caesium (133Cs and 137Cs) in various fractions of soil and fungi in a Swedish forest. Sci. Total Environ. 408, 2543e2548. Vinichuk, M., Johanson, K.J., Rydin, H., Rosén, K., 2010b. The distribution of 137Cs, K, Rb and Cs in plants in a Sphagnum-dominated peatland in eastern central Sweden. J. Environ. Radioact 101, 170e176. Vinichuk, M.M., Johanson, K.J., 2003. Accumulation of 137Cs by fungal mycelium in forest ecosystems of Ukraine. J. Environ. Radioact. 64, 27e43. Yoshida, S., Muramatsu, Y., 1998. Concentration of alkali and alkaline earth elements in mushrooms and plants collected in a Japanese pine forest, and their relationship with 137Cs. J. Environ. Radioact 41 (2), 183e205.
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