137Cs in fungal sporocarps in relation to vegetation in a bog, pine swamp and forest along a transect

Chemosphere 90 (2013) 713–720

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137

Cs in fungal sporocarps in relation to vegetation in a bog, pine swamp and forest along a transect M. Vinichuk a,b,⇑, K. Rosén a, A. Dahlberg c a

Department of Soil and Environment, Swedish University of Agricultural Sciences, SLU, Box 7014, SE-75007 Uppsala, Sweden Department of Ecology, Zhytomyr State Technological University, 103 Chernyakhovsky Str., 10005 Zhytomyr, Ukraine c Department of Forest Mycology and Pathology, Swedish University of Agricultural Sciences, SLU, Box 7014, SE-75007 Uppsala, Sweden b

h i g h l i g h t s 137 Cs in fungal sporocarps in terrestrial ecosystems. Cs activity in fungi was highest among other aboveground vegetation. 137 " Ectomycorrhizal sporocarps have higher Cs values than saprotrophic. 137 " Fungal sporocarps comprised negligible amount of total Cs activity.

" We estimated the amount of "

137

a r t i c l e

i n f o

Article history: Received 25 June 2012 Received in revised form 21 August 2012 Accepted 18 September 2012 Available online 24 October 2012 Keywords: Cesium Forest Forested peatland Fungi Peatland

a b s t r a c t In this study, we estimated the relative importance of vegetation and fungi for radiocesium uptake and biological retention in adjacent bog, pine swamp, and forest. The measurements for 137Cs activity concentration in sporocarps (i.e. fruitbodies of fungi) and vegetation along a bog to forest transect were combined with complementary published data to calculate estimates. Aboveground vegetation comprised 17.7% of the total fallout-derived radiocesium in the system in bog, 16.5% in pine swamp, and 40.6% in forest. In fungal sporocarps grown along a gradient, 137Cs activity comprised <0.001% of the total radiocesium for peat bog, <0.02% for pine swamp, and 0.11% for forest. Total 137Cs activity in sporocarps increased along the gradient due to increased production of sporocarps in the presence of trees from 0.006 (bog), 0.097 (pine swamp) and 0.67 (forest) g dwt m2. Based on calculation of the total vegetation biomass and through relationships between fungal biomass in sporocarps and as mycelia in soil, the total 137 Cs activity located in fungi was estimated as 0.1% in bog, 2% in pine swamp, and 11% in forest. An analysis of the time-dependency of 137Cs in the sporocarps in forest between 1990 and 2011 suggested an ecological half-life for 137Cs between 8 and 13 years. Although fungi comprised a relatively small fraction of the total radiocesium in the systems, its activity decreased slowly with time, and ecological residence time for 137Cs in sporocarps of fungi was long, suggesting they will continue to contribute to the accumulation and cycling of this radionuclide in forest. Ó 2012 Elsevier Ltd. All rights reserved.

1. Introduction Fungi are fundamentally important for the cycling of nutrient and carbon in terrestrial ecosystems. Since the Chernobyl accident in 1986 (Steiner et al., 2002), fungi have attracted large interest, as they are essential in the uptake and retention of 137Cs within organic soil systems (Parekh et al., 2008), particularly in nutrient-poor forest soils (Olsen et al., 1990). Both saprotrophic and mycorrhizal fungi take up cesium from soil more efficiently than ⇑ Corresponding author at: Department of Soil and Environment, Swedish University of Agricultural Sciences, SLU, Box 7014, SE-75007 Uppsala, Sweden. Tel.: +46 18 67 14 42; fax: +46 18 67 28 95. E-mail address: [email protected] (M. Vinichuk). 0045-6535/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.chemosphere.2012.09.054

vascular plants (Calmon et al., 2009; Vinichuk et al., 2010a). Fungi in semi-natural ecosystems have long ecological half-lives for radiocesium (Strandberg, 2004; Zibold and Klemt, 2005), i.e. the time required to reduce the contaminant burden by 50% after first coming into steady-state with contaminant levels in other parts of the environment, which contributes to the high radioecological sensitivity of these ecosystems. Long ecological half-life, even though much shorter than physical half-life (the time required for the decay of half the atoms in a given amount of a radioactive substance) and high 137Cs activity in forest food products derived from forest ecosystems can result in high time-integrated intake of 137Cs by humans through local consumption of fungi (Fesenko et al., 2000).

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However, sporocarps only constitute a small percentage of the total fungal biomass, with the biomass of mycelia in soil constituting the major part of the total fungal biomass (Horton and Bruns, 2001). The majority of fungal biomass in soil is located in the upper soil horizon below the soil surface (Bååth, 1980), and in soil from boreal forest ecosystems, the fungal biomass is estimated to comprise between 30% (Olsen et al., 1990) and 50% (Vinichuk and Johanson, 2003) of the total radiocesium in soil. Sporocarps of ectomycorrhizal fungi typically have higher 137Cs levels than sporocarps of saprotrophic fungi (Smith et al., 1993), and the level varies among species (Gillet and Crout, 2000). The relationships between fungal biomass allocated as sporocarps and mycelium are poorly known, although some data are available (Olsen et al., 1990). Besides, the relation between mycelia in soil and in sporocarps differs by species (O‘Dell et al., 1998). The distribution of Chernobyl fallout in a Swedish forest indicates fungi, forest-floor vegetation, and ruminant populations collectively contain about 1% of the total radiocesium fallout (McGee et al., 2000). Aboveground fungal biomass in forest accumulates between 0.01% and 0.1% of the total cesium during different years (Nikolova et al., 1997), depending on the variable production of fungal sporocarps (Krivtsov et al., 2003). In grassland environments, the quantity of 137Cs stored in the fungal biomass is relatively small. For example, in meadow soils with high amounts of fungal biomass, microbially stored 137Cs comprises 1.2–2.7% of the total 137Cs soil inventory (Stemmer et al., 2005). However, there is limited data on 137Cs stored by fungi in bog and the radioecological functions of fungi in peatlands (Rosén et al., 2009). Water-covered lands, mostly peatlands (i.e., bogs and fens), comprise about 30% of the total area of the world’s boreal forest biome (Benoy et al., 2007a). In Sweden, the area covered by natural or near natural mires comprises about 4.9 million ha or 11% of total land area (Rydin et al., 1999). It has been shown that 137Cs activity may be correlated with the mushroom season in sheep grazing on heather-dominated peatland (McGee et al., 1993) and in roe deer living in spruce forest and peat bog (Zibold et al., 2001). Although 137Cs distribution in peat soil profiles, in plants of various species (Rosén et al., 2009), and distribution of 137Cs, K, Rb and Cs within individual Sphagnum plants (Vinichuk et al., 2010b) on a peatland in eastern central Sweden have been investigated, the radioecological importance of fungi to 137Cs cycling in peatlands is unclear. However, there is a difference in microbial communities in peatland and forest; in surface peat soils of northern peatlands, bacterial activity dominates over fungal activity, whereas fungal activity dominates over bacterial activity in coniferous forest soils (Winsborough and Basiliko, 2010). Another major difference is that ectomycorrhizal fungi are not present in peat bogs due to their dependence on living trees, their symbiotic partners. Hence, ectomycorrhizal activity is typically absent in peat bogs, low in pine swamp peatland, and high in forests (Wurzburger et al., 2004). The objective of this study was to estimate the relative importance of vegetation and fungi in radiocesium uptake and biological retention in adjacent bog, pine swamp, and forest. Measurements of 137 Cs activity concentration in above and belowground vegetation and sporocarps were analyzed/synthesized and complemented with estimates of sporocarp production, and relation between sporocarps and fungal biomass in soil/peat. Data from a chronosequence of sporocarp measurements from the same location between 1990 and 2011 were analyzed to determine whether 137Cs activity concentration in fungal sporocarps after the Chernobyl fallout correlated with the expected decay of 137Cs activity concentration. Fungi are major contributors to accumulation and cycling of radionuclides in forest ecosystems, thus, part of the aim was to determine how long fungi contributed to the accumulation and cycling of radiocesium. That is, if 137 Cs activity concentration in fungal sporocarps correlated directly with the availability of 137 Cs in

soil, or if the uptake and retention of 137Cs by and within fungal mycelia resulted in successively higher 137Cs activity concentrations in fungal tissue. 2. Material and methods 2.1. Study area The study area was located on a small peatland (Pålsjömossen) (ca. 2 ha) within a coniferous forest in Heby municipality in eastern central Sweden, about 35 km NW of Uppsala (60°030 4000 N, 17°070 4700 E). This area has been well monitored, as it was affected by the Chernobyl (about 1300 km away) fallout (Rosén et al., 2009; Vinichuk et al., 2010b). The ecotone from peatland to surrounding forest (within about 1 km2) was investigated. Based on the vegetation, the peatland was divided into two subareas, peat bog and pine swamp peatland. The forest surrounding the peatland is located on mineral soil. The peat bog site lacked trees and the vegetation was dominated by Sphagnum species sparsely covered by dwarf-shrubs such as bog-rosemary (Andromeda polifolia L.), heather (Calluna vulgaris L.), black crowberry (Empetrum nigrum L.), and cranberry (Vaccinium oxycoccus L.). The field layer i.e. the herb and small shrub layer of a plant community on the pine swamp peatland was dominated by vascular plants such as cloudberry (Rubus chamaemorus L.), heather (Calluna vulgaris L.), cranberry (Vaccinium oxycoccus L. and Vaccinium macrocarpon Ait.), and slow growing Scots pine. The forest on mineral soil consisted of Scots pine coniferous forest (Picea abies (L.) H.Karst. and Pinus sylvestris L.) with an intermixture of birch (Betula spp.). In the field layer, heather was the predominant dwarf shrub intermixed with bilberry (Vaccinium myrtillus L.) and lingon berry (Vaccinium vitis-idaea L.). The study site is displayed in Fig. 1: a detailed description of the site is provided by Vinichuk et al. (2010a). In 2005, the ground deposition of 137Cs on peatland was about 23 kBq m2 (Rosén et al., 2009). The forest surrounding Pålsjömossen peatland has similar ground deposition of 137Cs to the nearby Harbo area (SGAB, 1986). 2.2. Sampling and treatment Fungal sporocarps Sporocarps were collected once to several times per year through extensive searching and collection of all frequently occurring species during the peak of the fruiting period, August to September. The aim was to obtain representative measurements of radiocesium activity concentration in sporocarps of predominant fungal species. The bog and pine swamp were sampled annually between 2006 and 2011. In the forests, sporocarp collections were initiated in 1990 and samples taken most years until 2011. No sporocarps of saprotrophic fungi were collected from the forest due to their minor contribution to the total production of sporocarp biomass. Sporocarps were identified to species level according to fungal taxonomy (Knudsen and Vesterholt, 2008). The sporocarps were carefully cleaned of extraneous fragments, dried at 40 °C to constant weight, and then milled to obtain a homogeneous material for measuring 137Cs activity concentration. Plants Aboveground plant biomass was estimated on peat bog and pine swamp peatland sites in September 2010. From each sampling site, aboveground parts of vascular plants and Sphagnum (upper 3–8 cm long, mostly green parts) were clipped (0.5  0.5 m frame) at six randomly selected sampling areas about 20 m apart. All vegetation was sorted to species level and dried at 40 °C to constant weight. The dry weight (dwt) of each species per unit area was calculated. On the pine swamp peatland site, aboveground biomass of separately standing pine trees were estimated by measuring the

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3 2

1

Fig. 1. 137Cs deposition over Sweden (kBq m–2), adapted from the Swedish National Atlas, 2012, and study sites: open bog (1, foreground), pine swamp and forest (2 and 3, background). Location of study site is indicated by the arrow.

diameter at breast height and the total height of trees, standard forestry charts were then used to convert the measurements into total tree biomass (Sampson, 2002). Standing biomass of trees, understorey, and bryophyte biomass in surrounding forest was adapted from McGee et al. (2000), as the sampling site in their study was located in nearby spruce forest and their data on aboveground biomass and mushroom biomass were based on more sampling than was done in this study. The available data on aboveground biomass in coniferous forest were adapted and compiled from Rieley et al. (1979), Havas and Kubin (1983), Sawidis (1988), and Wardle et al. (1997). Data on aboveground biomass on peat bog were adapted and compiled from Backèus (1985), Wallén (1987, 1986), Sjörs (1991), and Benoy et al. (2007b), and data on 137Cs activity in trees were adapted and compiled from McGee et al. (2000). Published measurements of annual average biomass production of fungal sporocarps for peat bog, pine swamp peatland, and forest were used to estimate the amount of 137Cs activity concentration in sporocarps per unit area (Salonen and Saari, 1990; Ohenoja, 1993). 2.3. Measurements and data treatment The activity concentration (Bq kg1) of 137Cs in samples of plants and fungal sporocarps was determined with calibrated HPGe detectors in laboratories at former Department of Radioecology and present Department of Soil and Environment (SLU). Both laboratories participated in intercomparison studies organized by the Swedish Radiation Protection Authority. Plant and fungi material were measured filled-up in different geometries, except for a few fungal sporocarp samples collected at the peatland site that contained about 0.2 g of dry material. Due to the random process of decay, the measuring time (8–24 h) was chosen to obtain a statistical error ranging between 5% and 10%. All 137Cs activity concentrations were recalculated to the sampling date and expressed on a dry mass basis. 137Cs activity data in plants published in previous work on the contamination of raised bog in central Sweden after the Chernobyl fallout (Rosén et al., 2009; Vinichuk et al., 2010b) were updated and used. The 137Cs activity concentration in sporocarps of three ectomycorrhizal fungal species, Cortinarius semisanguineus, Russula paludosa and Suillus variegatus, that had been repeatedly collected between 1990 and 2011 in forests were

compared through regression analyses with the calculated expected physical decay of 137Cs. 3. Results 3.1.

137

Cs in fungi

Activity concentration of 137Cs was analyzed in 441 sporocarp samples from 50 taxa (species or subgenera) (Table 1). Fungal sporocarps occurring on open Sphagnum-dominated peat bog were small and sparse and ectomycorrhizal fungi were absent. Only a few species were recorded from both the peatland and the forsest. No ectomycorrhizal fungi were found at the bog, due to lack of ectomycorrhizal host trees. The 137Cs activity concentration in sporocarps increased from bog via pine swamp to forest, with sporocarps from ectomycorrhizal fungi typically having 1.5–2.0 times higher 137Cs activity concentration than sporocarps from saprotrophic fungi (Table 1). The difference between 137Cs activity concentration levels in sporocarps was not statistically significant among either saprotrophic species on bog and pine swamp or among mycorrhizal on pine swamp and forest. In individual saprotrophs growing at the peat bog site, 137Cs activity concentration varied between 68.3 kBq kg1 (Hypholoma spp.) and 8.2 kBq kg1(Omphalina spp.) (Table 1). Among species growing on pine swamp, the highest 137Cs activity (70.9– 82.7 kBq kg1) was in mycorrhizal Cortinarius spp. and the lowest in saprotroph Omphalina spp. (4.9–9.7 kBq kg1). The highest 137Cs activity concentration in sporocarps collected in forest was in Cortinarius spp. (122.5–186.7 kBq kg1), whereas, activity in Albatrellus spp., Boletus edulis Bull., and Leccinum scabrum (Bull.) Gray was relatively low (5.3–11.6 kBq kg1). Fungal sporocarps had the highest 137 Cs activity among other components of the systems, however, the percentage of the total 137Cs activity within the system that was allocated within fungi was small (0.1%: Tables 2–4). 3.2.

137

Cs in vegetation

The portion of 137Cs fallout allocated within aboveground vegetation varied depending on the ecosystem. On bog, 137Cs fallout was mainly found in Sphagnum mosses (Table 2), with vascular plants comprising a small part of the total 137Cs activity in the

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Table 1 137 Cs in fungal sporocarps (kBq kg1) collected from a bog, pine swamp, and in forest. Mean ± standard error (number of samples), when only one collection no parentheses. All 137 Cs activity concentrations were recalculated to the sampling date and expressed on a dry mass basis.

a

Species

Mode of nutritiona

Albatrellus confluens Albatrellus ovinus Ascoryne turficola Boletus edulis Cantharellus cibarius Cortinarius acutus Cortinarius armillatus Cortinarius brunneus Cortinarius caperatus Cortinarius collinitus Cortinarius tegérrimus Cortinarius obtusus Cortinarius semisanguineus Cortinarius spp. Cortinarius subgenera Dermocybe Cortinarius subgenera Telamonia spp. Cantharellus tubaeformis Entoloma cetratum Galerina sphagnorum Galerina stagnina Galerina spp. Gomphidius glutinosus Hygrocybe miniata Hypholoma elongatum Hypholoma polytrichi Hypholoma spp. Hebeloma bryogenes Laccaria laccata Laccaria spp. Lactarius helvus Lactarius trivialis Lactarius vietus Leccinum scabrum Mycena floridula Mycena rosella Mycena spp. Omphalina grossula Omphalina oniscus Omphalina philonotis Omphalina spp. Paxillus involutus Russula betulorum Russula decolorans Russula emetica Russula obscura Russula paludosa Sarcodon imbricatus Suillus variegatus Tephrocybe palustre Mean, all species Mean, ectomycorrhizal Mean, saprotrophic

EM EM S EM EM EM EM EM EM EM EM EM EM EM EM EM EM S S S S EM S S S S EM EM EM EM EM EM EM S S S S S S S EM EM EM EM EM EM EM EM S

Bog (2006–2011)

Pine swamp (2006–2010)

Forest (1990–2011) 5.3 ± 0.8 (14) 6.9 ± 0.9 (29)

23.0 9.3 ± 1.9 (3) 68.1 ± 1.9 (21) 28.5 ± 13.0 (3) 117.5 ± 19.8 (14) 36.8 ± 10.3 (2) 59.9 ± 9.5 (6) 186.7 ± 40.9 (14) 64.0 ± 13.5 (4) 59.1 82.7 80.8 ± 29.1 (4) 70.9 47.8 ± 7.8 (6) 28.6 ± 7.2 (3) 38.3 ± 4.4 (9) 61.7 37.9 ± 1.8 (35) 7.5 39.3 ± 5.1 (7) 59.2 68.3

101.6 ± 12.7 (30)

60.7 ± 14.9 (5) 28.7 ± 2.6 (30)

32.2 ± 21.0 (2) 5.1

69.2 61.4 ± 38.2 (3) 99.2 ± 11.6 (2) 20.9 23.9 ± 2.6 (8)

30.1 26.6 33.7 38.8 ± 18.3 (2) 8.2 ± 0.7 (2) 21.3 ± 2.9 (3) 21.2 ± 5.9 (6)

43.9 ± 19.2 (4) 50.2 ± 34.3 (4) 11.6 ± 2.5 (2)

71.3 9.7

4.9 76.6 ± 10.4 (19) 25.5 29.9 ± 3.6 (28) 43.8 ± 20.3 (4) 49.4 ± 1.3 (2) 58.9 ± 8.4 (3)

13.7 34.8 ± 1.7 (78) 34.8 ± 1.7 (78)

41.1 ± 4.0 (51) 43.0 ± 4.3 (46) 19.8 ± 11.2 (5)

39.7 ± 7.8 24.9 ± 2.9 43.8 ± 6.9 62.7 ± 4.9

(3) (36) (2) (47)

53.9 ± 3.3 (351) 53.9 ± 3.3 (351)

Ectomycorrhizal (EM), saprotrophic (S).

system. Generally, aboveground vegetation contained 19.0% of the total 137Cs activity. On pine swamp, 137Cs fallout was mainly in Sphagnum mosses, slow growing pine trees, and heather. The portion of the total 137Cs activity located in aboveground vegetation on pine swamp was similar to that in bog and was estimated as 18.0% (Table 3). In forest on mineral soil, the portion of 137Cs activity allocated within the aboveground vegetation and fungal sporocarps was estimated to be about 41%, mainly in bryophytes, trees, and understory vegetation (Table 4). In forest on mineral soil calculation is based on the ground deposition of 137Cs 33 kBq m2 (SGAB, 1986). The majority of 137Cs in all three ecosystems was in belowground soil or peat (Tables 2–4). 3.3. Time series of

137

Cs activity concentration in fungal sporocarps

The 137Cs activity levels in the sporocarps deviated from the calculated physical 137Cs decay, and the ecological half-lives for 137Cs

i.e. the time for half the cesium to disappear from the sporocarps, ranged between 8 and 13 years (Fig. 2a–c, and Table 5). 4. Discussion Even 25 years after Chernobyl fallout, 137Cs activity concentration in fungal sporocarps in all three ecosystems appeared to remain about one order of magnitude higher than in any other component of aboveground vegetation. However, this relation appeared to have decreased since the 1990s, when radiocesium activity in fungal fruit bodies of many mycorrhizal species in forest ecosystems in the Nordic countries was about 50 times higher than in plants sampled in the same forest (Olsen, 1994). The 137Cs levels in fungal sporocarps obtained in this study were orders of magnitude higher than maximum permissible limits of contamination, which should not exceed 600 Bq kg1 according to EU legislation (Council Regulation, 2000).

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Table 2 Data compilation from bog: 137Cs activity concentration (mean values, kBq kg1 ± standard error), biomass (mean values ± standard error or range, g dwt m2), total 137Cs in aboveground vegetation and fungi (Bq m2) and 137Cs as percentage of the total 137Cs activity in various aboveground vegetation components and fungi (%). The data adapted from published sources are indicated by numbered superscripts1,2,3,4,5. All 137Cs activity concentrations were recalculated to the sampling date and expressed on a dry mass basis. kBq kg1

Species, compartment a

Andromeda polifolia (n = 4) Calluna vulgaris (n = 4)a Carex rostrata infructescence (n = 9)b Drosera rotundifoliac Empetrum nigrum (n = 2)a Eriophorum vaginatumb Menyanthes trifoliataa Phragmites communisa Vaccinium oxycoccos (n = 7)a Sphagnum spp. (n = 195)d Fungal sporocarps (n = 75)e Total in aboveground vegetation and fungi Total in soilf Total inventory

0.96 ± 0.04 7.6 ± 2.21 4.0 ± 1.31 4.71 0.62 ± 0.09 1.91 2.61 0.31 1.6 ± 0.3 3.2 ± 0.251 34.8 ± 1.7

1

g dwt m2

Bq m2

%

10.3 ± 2.2 81.6 ± 41.2 12.3 ± 6.5 0.082 31.1 ± 17.1 29.0 (5.0–50.0)2,3 38.5 (35.0–52.4)4 5.1 24.9 ± 8.6 1102 ± 330 6  103 (4  103–1.4  103)5

9.9 616 49.2 0.38 19.3 55.1 100 1.6 39.8 3471 0.2 4363 18 637 23 000

<0.1 2.7 0.2 <0.1 <0.1 0.2 0.4 <0.1 0.2 15.1 <0.001 19.0 81.0 100.0

a

Above ground biomass. Above ground biomass green and brown, senescent leaves. c Whole plant. d Upper 3–8 cm green part (S. magellanicum, S. fuscum). e Predominantly Galerina, Hypholoma, Omphalina. f Estimated as a difference between measured ground deposition (Rosén et al., 2009) and 137Cs in aboveground vegetation and fungal sporocarps. 1 Updated 137Cs activity data originates from previous work (2008) on the contamination of Sphagnum-dominated peatland in central Sweden (Vinichuk et al., 2010a); 2 Skattlösberg Stormosse in the SW part of the province of Dalarna central Sweden (Backèus, 1985). 3 Stordalen ombrotrophic mire, 10 km E of Abisko (68°220 N, 19°030 E), N Sweden (Wallén, 1987, 1986). 4 Stordalen ombrotrophic mire, 10 km E of Abisko (68°220 N, 19°030 E), N Sweden (Benoy et al., 2007b); Small moderately rich fen ‘‘Torsängsmyren’’ along the creek Enån, 3 km E of Orsa, central Sweden (Sjörs, 1991). 5 Salonen and Saari (1990), data from sporocarp measurements over three years at a treeless mire. b

Table 3 Data compilation from pine swamp: 137Cs activity concentration (mean values, kBq kg1 ± standard error), biomass (mean values ± standard error or range, g dwt m2), total 137Cs in aboveground vegetation and fungi (Bq m2) and 137Cs as percentage of the total 137Cs activity in various aboveground vegetation components and fungi (%). The data adapted from published sources are indicated by numbered superscripts1,2. All 137Cs activity concentrations were recalculated to the sampling date and expressed on a dry mass basis. Species, compartment a

Andromeda polifolia Calluna vulgaris (n = 4)a Carex rostrata infructescenceb Empetrum nigrum (n = 4)a Eriophorum vaginatum (n = 5)b Ledum palustre (n = 5)a Lichensc Vaccinium oxycoccus (n = 6)a Vaccinium uliginosum (n = 2)a Sphagnum spp. (n = 6)d Fungal sporocarps (n = 48)e Pinus sylvestrisa Total in aboveground vegetation and fungi Total in soilf Total inventory a b c d e f 1 2

137

Biomass (g dwt m2)

137

0.76 6.72 ± 1.46 1.39 1.39 ± 0.41 1.37 ± 0.29 1.18 ± 0.18 0.54 1.26 ± 0.40 0.75 ± 0.09 3.68 ± 0.98 41.1 ± 4.0 0.37

4.38 112 ± 38 1.96 2.28 ± 0.93 27.7 ± 9.56 96.9 ± 37.8 10.8 8.2 ± 2.89 54.3 ± 34.1 544 ± 73.4 0.097 (0.02–0.14)1 3000 (3000–10 286)2

3.3 753 2.7 3.2 37.9 114 5.8 10.3 40.7 2001 4.0 1110 4134 18 866 23 000

Cs (kBq kg1)

Cs (Bq m2)

% <0.1 3.3 <0.1 <0.1 0.2 0.5 <0.1 0.1 0.2 8.7 <0.02 4.8 18.0 82.0 100.0

Above ground biomass. Above ground biomass green and brown, senescent leaves. Total biomass. Upper 3–8 cm green part. Predominantly (Cortinarius, Lactarius, Russula). Estimated as a difference between measured ground deposition (Rosén et al., 2009) and 137Cs in aboveground vegetation and fungal sporocarps. Salonen and Saari (1990), data from sporocarp measurements over three years at a Sphagnum fuscum mire with Scots pine. Spruce forest in central Sweden (60°300 N, 17°100 E) (McGee et al., 2000).

In sporocarps, 137Cs activity levels increased along a gradient from bog via pine swamp to forest. The percentage of 137Cs activity accumulated in sporocarps of fungi as portion of the total cesium inventory in bogs was negligible and varied between <0.001% and <0.02% in pine swamp and 0.11% in forest, due to low sporocarp biomass, however it is concentrated on a mass basis. Estimates obtained for peat bog were lower than reported by Nikolova et al. (1997); aboveground fungal biomass in forest can only accumulate between 0.01% and 0.1% of the total cesium inventory. Even if radiocesium activity in fungi is high, the negligible

aboveground fungal biomass in forest limits radionuclide accumulation. The estimated percentages of 137Cs activity accumulated in sporocarps in forest soil (ca. 0.11%) were slightly lower than reported by McGee et al. (2000) in the same forest (0.46%). This discrepancy might be due to different time scales used; McGee et al. (2000) use a single year with a good mushroom season whereas in this study, an estimate of an average annual sporocarp production over eight years was used (an average value of 40 habitats with a moderate or well-balanced supply of moisture mature coniferous forests adapted from Ohenoja, 1993). Assuming

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Table 4 Data compilation for forests; 137Cs activity concentration (mean values, kBq kg1 ± standard error), biomass (mean values ± standard error or range, g dwt m2), total 137Cs in aboveground vegetation and fungi (Bq m2) and 137Cs as percentage of the total 137Cs activity in various aboveground vegetation and fungi (%). The data adapted from published sources are indicated by numbered superscripts1-5. All 137Cs activity concentrations were recalculated to the sampling date and expressed on a dry mass basis. Species, compartment a

Trees Understorey vegetationa Bryophytesb Fungal sporocarps (n = 318)c Total in aboveground vegetation and fungi Total in soild Total inventory

137

Cs (kBq kg1)

Biomass (g dwt m2)

1

2

0.48 (0.3–0.78) 10.5 (0.96–20.0)1 6.9 (0.96–20.0)3 53.9 ± 3.3 – – –

7443 (3000–10 286) 360 (332–365)2 758 (272–1563)4 0.67 (0.5  105–3.1)5 – – –

137

Cs (Bq m2)

4391 3780 5230 36 13 437 19 563 33 000

% 13.3 11.5 15.8 0.11 40.7 59.3 100.00

a

Above ground biomass. Bryophytes layer, herb layer, litter. c Predominantly Cortinarius, Suillus, Russula. d Estimated as a difference between measured ground deposition (Rosén et al., 2009) and 137Cs in aboveground vegetation and fungal sporocarps. 1 Spruce forest in central Sweden (60°300 N, 17°100 E) (McGee et al., 2000). 2 An old spruce forest in northern Finland (Havas and Kubin 1983); Island archipelago, northern boreal forest zone of Sweden (65°550 –66°090 N; 17°430 –17°550 E) (Wardle et al., 1997). 3 North Greece (Sawidis, 1988); Spruce forest, C. Sweden (60°300 N, 17°100 E) (McGee et al., 2000). 4 Oakwood area (Rieley et al., 1979); Island archipelago, northern boreal forest zone of Sweden (65°550 –66°090 N; 17°430 –17°550 E) (Wardle et al., 1997). 5 An average value of 40 mesic mature coniferous forests in Finland, studied 1976–1988 (Ohenoja, 1993). b

sporocarps constitute less than 1% (0.5%) of the total fungal biomass (Wallander et al., 2004) the total fungal biomass could be 20–100 times higher than sporocarp biomass. Supposing 137Cs levels in sporocarps are similar to mycelium (Olsen et al., 1990), the total 137Cs activity accumulated in soil mycelia could be 20–100 times higher, which is between 2.2% and 11% (0.11  20 and 0.11  100) of the total radiocesium in soil i.e. ground deposition of 137Cs in forest. This estimate supported earlier results (Vinichuk and Johanson, 2003), as the percentage of the total soil-inventory of 137Cs held in fungal mycelium ranged from 0.1% to 50%, with a mean value of 15%. This may explain long residence of 137Cs in fungal sporocarps over years in forests, since extensive fungal mycelium counteracts the downward transport of 137Cs and results in very slow net downward transport of 137Cs in the soil profile. On pine swamp, fungal sporocarps comprised 0.02% of the total 137Cs activity in the system. These estimates might be significant as sporocarp biomass in pine swamp is an order of magnitude lower due to lower productivity and less tree growth than in forest. In mycorrhizal species, growing in pine swamp, 137Cs activity concentration levels were also generally lower than 137Cs activity concentration of mycorrhizal species occurring in forest. This might be due to higher vertical leakage of Cs to deeper layers due to significantly less dense mycelial top soil network as a consequence of lower production of trees/unit area in pine swamp compared to forests. Generally, the abundance and 137Cs activity of mycorrhizal species is directly related to the abundance and growth of trees and environmental conditions. The transfer of radiocesium from soil to sporocarps is greater for mycorrhizal than for saprotrophic species (Rühm et al., 1997; Barnett et al., 1999) and mycorrhizal species had higher 137Cs activity concentration than saprotrophic species (Römmelt et al., 1990). In the humus layer and deeper ectomycorrhizal species replace saprotrophic fungi (Lindahl et al., 2007), and in boreal forest soils mycelium of mycorrhizal fungi contribute substantially to the total microbial biomass (Högberg and Högberg 2002). Accordingly, mycorrhizal species generally have higher transfer of radiocesium from soil to sporocarps than saprotrophic species (Rühm et al., 1998; Gillet and Crout 2000). The transfer of radiocesium from soil to sporocarps is expressed as the radionuclide concentration in fungal fruit bodies divided by the radionuclide concentration in soil. Thus, the combination of >100 times higher sporocarp biomass and the high 137Cs activity concentration in forest results in a higher content of total radiocesium fallout accumulating in fungi in forest than in fungi in peat bog.

The fungal community in the bog consisted of a low number of saprotrophic species, and ectomycorrhizal species with more fleshy sporocarps were completely absent, except occasionally near the rare occurrence of small trees. This ecosystem is extremely nutrient-poor, ombrotrophic, and almost entirely rain-fed, especially in wetter parts of open peatlands where water logging reduces the oxygen level and redox potential. The amount of vascular plant roots and mycelia in the upper soil layer is lower in the bog than in the forest due to the lack of trees and hence lack of ectomycorrhizal fungi. Hence, a lower share of the deposited Cs is taken up and recirculated and a larger portion leak into deeper soil horizons. In addition, the mycelia of sporocarp producing fungi on bogs grow superficially and its mass expected to fluctuate more than mycelia in the forest floor, which should result in a higher leakage of Cs. As saprotrophic fungi grow on decomposing materials above or within the surface layers of a peat, the transfer of 137Cs will subsequently decrease due to the radionuclide effectively gets buried deep enough over time that it no longer cycles. Thus, sporocarps grown on peatland have a negligible amount of 137Cs fallout. A majority of the total fallout-derived radiocesium in aboveground vegetation in forest was in bryophytes, biomass-dominated trees, and understory vegetation. In the bog and pine swamp ecotypes, radiocesium was mainly associated with peat mosses, pine trees, and heather. A Sphagnum-dominated peat bog is an extremely nutrient-poor ecosystem, in which Sphagnum selectively absorbs mineral ions from the surrounding water, including Cs (Vinichuk et al., 2010b). Heather also accumulates radiocesium and has consistently high 137Cs activity concentration on both peat bog and pine swamp peatland (Rosén et al., 2009). A plausible explanation for the enhanced uptake of cesium is the lateral root distribution of heather, mostly within the top 10 cm of soil (Messier and Kimmins, 1991) and the presence of ericoid mycorrhizal fungi: fungi-forming ericoid mycorrhiza were not considered in this study, as they are microfungi and typically lack sporocarps. On both bog and pine swamp sites, heather had the highest 137Cs activity concentration among vascular plants and the highest biomass (after Sphagnum). Other vascular plant species forming ericoid mycorrhizae (e.g. Andromeda polifolia L., Empetrum nigrum L., Vaccinium spp.) had less total 137Cs activity in aboveground biomass due to lower biomass and lower (up to one order of magnitude) levels of 137Cs activity concentration. Regression analyses of the time-dependency of 137Cs activity concentration in fungal sporocarps revealed a decrease in activity over time (Fig. 2). Thus, the hypothesis that the uptake and retention of 137Cs by and within fungal mycelia resulted in successively

M. Vinichuk et al. / Chemosphere 90 (2013) 713–720

a 300

137Cs,

kBq kg -1

250 200 150 100 50 0 1990

1995

2000

2005

2010

b 300

137Cs,

kBq kg -1

250 200

5. Conclusions 100

0 1990

1995

2000

2005

2010

c 300 250

kBk kg -1

over time differed from a time-series study from the same area, in which 137Cs uptake did not decrease during the period 1986 to 2007 in S. variegatus but increased in Cantharellus spp. (Mascanzoni, 2009). This may be due to the variability of 137Cs transfer to fungi, (Gillet and Crout, 2000), as fungal growth is influenced by precipitation and temperature, resulting in differences in uptake of 137Cs from year to year. The variation in long-term 137Cs activity concentration in analyzed species of fungi can be due to the complexity of interactions between fungi and environment (Dahlberg et al., 1997). The uptake 137Cs by fungi and consequently half-life length of the radionuclide in fungal sporocarps are influenced by continuous and complicated interplay that occurs between surrounding ecosystem and fungi. Among others, the different half-lives possibly relate to depth of soil exploration by fungi. The longer half-life can be expected with greater mycelia depth in soil profile; although 137Cs migration in forest soils is slowly, it moves down with time and gets accessible for deeper located mycelium. 137Cs half-life in fungal sporocarps may be related to the age of mycelia i.e. longer half-life can be due to longer retention of 137Cs in mycelium.

150

50

137Cs,

719

200 150

The percentage of 137Cs activity accumulated in sporocarps of fungi as portion of the total cesium inventory in adjacent bog, pine swamp, and forest is relatively small and varied between <0.001% and 0.11%. Assuming sporocarps constitute less than 1% (0.5%) of the total fungal biomass, the total 137Cs activity accumulated in soil mycelia could be up to two orders of magnitude higher. A majority of the total fallout-derived radiocesium in aboveground vegetation in forest was in bryophytes, biomass-dominated trees, and understory vegetation. On bog and pine swamp, radiocesium was mainly associated with peat mosses, pine trees, and heather. 137Cs activity concentration in fungal sporocarps growing in forest decreases over time and the estimated ecological 137Cs half-life ranged from 8 to 13 years.

100

Acknowledgements

50 0 1990

1995

2000

2005

2010

Fig. 2. The dynamics of 137Cs activity concentration in fungal sporocarps collected in forest (1990–2011): (a) Cortinarius semisanguineus, (b) Russula paludosa, (c) Suillus variegatus. Solid black line represents the regression line; black dotted lines are the upper and lower 95% confidence intervals; solid red line is the physical decay of 137Cs. Activity concentration values are expressed on a dry mass basis. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Table 5 Estimates of half-life decay for

137

Cs for fungal sporocarps collected in forest.

Species

Half-lives (years)

95% Confidence interval

Suillus variegatus Cortinarius semisanguineus Russula paludosa

12.7 10.6 7.8

9–19 7–17 6–11

higher 137Cs activity concentrations over time cannot be supported. The estimated ecological half-life of 137Cs in fungal sporocarps growing in our forest plots ranged from 8 to 13 years, agreeing with results reported by Zibold and Klemt (2005) for 137 Cs in Xerocomus badius, but was higher than reported by Rühm et al. (1998) in Bavarian forest (2.8 and 7.7 years). The changes in the 137Cs activity concentration in fungal sporocarps

The authors would like to thank Professor Emeritus K.J. Johanson from the Department of Mycology and Forest Pathology, SLU, for valuable suggestions and comments on the manuscript. This work was supported by the Swedish University of Agricultural Sciences (SLU), References Bååth, E., 1980. Soil fungal biomass after clear-cutting of a pine forest in Central Sweden. Soil Biol. Biochem. 12, 495–500. Backèus, I., 1985. Aboveground production and growth dynamics of vascular bog plants in Central Sweden. Acta Phytogeogr. Suec. 74, 98. Barnett, C., Beresford, N.A., Self, P.L., Howard, B.J., Frankland, J.C., Fulker, M.J., Dodd, B.A., Marriott, J.V.R., 1999. Radiocaesium activity concentrations in the fruitbodies of macrofungi in Great Britain and an assessment of dietary intake habits. Sci. Total Environ. 231, 67–83. Benoy, G., Cash, K., McCauley, E., Wrona, F., 2007a. Antecedent snow conditions affect water levels and plants biomass of a fen in the southern boreal forest: results from an experiment using mesocosms. Boreal Environ. Res. 12, 501–513. Benoy, G., Cash, K., McCauley, E., Wrona, F., 2007b. Carbon dynamics in lakes of the boreal forest under a changing climate. Environ. Rev. 15, 175–189. Calmon, P., Thiry, Y., Zibold, G., Rantavaara, A., Fesenko, S., 2009. Transfer parameter values in temperate forest ecosystems: a review. J. Environ. Radioact. 100, 757– 776. Council Regulation (EC) No. 616/2000 and Council Regulation (EEC) No. 737/90. 2000. Official Journal of the European Communities 24.3.2000, L.75/1, Brussels. Dahlberg, A., Nikolova, I., Johanson, K., 1997. Intraspecific variation in 137Cs activity concentration in sporocarps of Suillus variegatus in seven Swedish populations. Mycol. Res. 101, 545–551. Fesenko, S., Voigt, G., Spiridonov, S.I., Sanzharova, N.I., Gontarenko, I.A., Belli, M., Sansone, U., 2000. Analysis of the contribution of forest pathways to the

720

M. Vinichuk et al. / Chemosphere 90 (2013) 713–720

radiation exposure of different population groups in the Bryansk region of Russia. Radiat. Environ. Biophys. 39, 291–300. Gillet, A., Crout, N., 2000. A review of 137Cs transfer to fungi and consequences for modeling environmental transfer. J. Environ. Radioactiv. 48, 95–121. Havas, P., Kubin, E., 1983. Structure, growth and organic matter content in the vegetation cover of an old spruce forest in northern Finland. Annu. Bot. Fenn. 20, 115–149. Högberg, M.N., Högberg, P., 2002. Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol. 154, 791–795. Horton, T., Bruns, T., 2001. The molecular revolution in ectomycorrhizal ecology: peeking into the black-box. Mol. Ecol. 10, 1855–1871. Knudsen, H., Vesterholt, J., 2008. Funga Nordica. Nordsvamp, Kopenhagen. Krivtsov, V., Watling, R., Walker, S.J.J., Knot, D., Palfreyman, J.W., Staines, H.J., 2003. Analysis of fungal fruiting patterns at the Dawyck Botanic Garden. Ecol. Model. 170, 393–406. Lindahl, B.D., Ihrmark, K., Boberg, J., Trumbore, S.E., Hogberg, P., Stenlid, J., Finlay, R., 2007. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol. 173, 611–620. Mascanzoni, D., 2009. Long-term transfer of 137Cs from soil to mushrooms in a semi-natural environment. J. Radioanal. Nucl. Chem. 282, 427–431. McGee, E., Synnott, H.J., Johanson, K.J., Fawaris, B.H., Nielsen, S.P., Horrill, A.D., Kennedy, V.H., Barbayiannis, N., Veresoglou, D.S., Dawson, D.E., Colgan, P.A., McGarry, A.T., 2000. Chernobyl fallout in a Swedish spruce forest ecosystem. J. Environ. Radioact. 48, 59–78. McGee, E., Synnott, H.J., Keatinge, M., Colgan, P.A., 1993. Persistence and prediction of radiocaesium levels in animals grazing semi- natural environments. Sci. Total Environ. 138, 91–99. Messier, C., Kimmins, J., 1991. Above- and below-ground vegetation recovery in recently clearcut & burned sites dominated by Gaultheria shallon in coastal British Columbia. Forest Ecol. Manag. 46, 275–294. Nikolova, I., Johanson, K., Dahlberg, A., 1997. Radiocaesium in fruitbodies and mycorrhizae in ectomycorrhizal fungi. J. Environ. Radioact. 37, 115–125. O‘Dell, T., Smith, J.E., Castellano, M., Luoma, D., 1998. Diversity and conservation of forest fungi. In: Pilz, D., Molina, R. (Eds.), Managing Forest Ecosystems to Conserve Fungus Diversity and Sustain Wild Mushroom Harvest. DIANE Publishing, Nature, pp. 5–18. Ohenoja, E., 1993. Effect of weather conditions on the larger fungi at different forest sites in northern Finland in 1976–1988. Acta. Univ. Oulun. Ser. A. 243, 1–69. Olsen, R., 1994. The transfer of radiocaesium from soil to plants and fungi in seminatural ecosystems. In: Dahlgaard, H. (Ed.), Nordic Radioecology. Elsevier, Amsterdam, pp. 265–301. Olsen, R., Joner, E., Bakken, L.R., 1990. Soil fungi and the fate of radiocaesium in the soil ecosystem – a discussion of possible mechanisms involved in the radiocaesium accumulation in fungi, and the role of fungi as a Cs-sink in the soil. In: Desmet, G., Nassimbeni, P., Belli, M. (Eds.), Transfer of Radionuclides in Natural and Semi-natural Environment. Luxemburg, Elsevier Applied Science, pp. 657–663. Parekh, N.R., Poskitt, J.M., Dodd, B.A., Potter, E.D., Sanchez, A., 2008. Soil microorganisms determine the sorption of radionuclides within organic soil systems. J. Environ. Radioact. 99, 841–852. Rieley, J., Richards, P., Bebbington, A., 1979. The ecological role of bryophytes in a North Wales Woodland. J. Ecol. 67, 497–527. Römmelt, R., Hiersche, L., Schaller, G., Wirth, E., 1990. Influence of soil fungi (basidiomycetes) on the migration of Cs134+137 and Sr 90 in coniferous forest soils. In: Desmet, G., Nassimbeni, P., Belli, M. (Eds.), Transfer of Radionuclides in Natural and Semi-natural Environments. Elsevier Applied Science, London, New York, pp. 152–160.

Rosén, K., Vinichuk, M., Johanson, K., 2009. 137Cs in a raised bog in central Sweden. J. Environ. Radioact. 100, 534–539. Rühm, W., Steiner, M., Kammerer, L., Hiersche, L., Wirth, E., 1998. Estimating future radiocaesium contamination of fungi on the basis of behaviour patterns derived from past instances of contamination. J. Environ. Radioact. 39, 129–147. 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, 129–148. Rydin, H., Sjörs, J., Löfroth, M., 1999. Mires. Acta Phytogeogr Suec. 84, 91–112. Salonen, V., Saari, V., 1990. Generic composition of macrofungal communities on virgin mire types in central Finland. Ann. Bot. Fenn. 27, 33–38. Sampson, N. 2002. Monitoring and Measuring Wood Carbon. Colorado SWCS Conference on Carbon as a Potential Commodity, Denver. . Sawidis, T., 1988. Uptake of radionuclides by plants after the chernobyl accident. Environ. Pollut. 50, 317–324. SGAB. 1986. 137Cs Ground Deposition Map Over Sweden. Swedish Geological Co., Uppsala. Sjörs, H., 1991. Phyto- and necromass above and below ground in a fen. Holarctic Ecol. 14, 208–218. Smith, M., Taylor, H., Sharma, H., 1993. Comparison of the post-Chernobyl 137Cs contamination of mushrooms from Eastern Europe, Sweden, and North America. Appl. Environ. Microb. 59, 134–139. Steiner, M., Linkov, I., Yosida, S., 2002. The role of fungi in the transfer and cycling of radionuclides in forest ecosystems. J. Environ. Radioact. 58, 217–241. Stemmer, M., Hromatka, A., Lettner, H., Strebl, F., 2005. Radiocesium storage in soil microbial biomass of undisturbed alpine meadow soils and its relation to 137Cs soil-plant transfer. J. Environ. Radioact. 79, 107–118. Strandberg, M., 2004. Long-term trends in the uptake of radiocesium in Rozites caperatus. Sci. Total Environ. 327, 315–321. Vinichuk, M., Johanson, K.J., Rydin, H., Rosén, K., 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, 2543–2548. Vinichuk, M., Taylor, A.F.S., Rosén, K., Johanson, K.J., 2010b. The distribution of 137Cs, K, Rb and Cs in plants in a Sphagnum-dominated peatland in eastern central Sweden. J. Environ. Radioactiv. 101, 170–176. Vinichuk, M., Johanson, K., 2003. Accumulation of 137Cs by fungal mycelium in forest ecosystems of Ukraine. J. Environ. Radioact. 64, 27–43. Wallander, H., Göransson, H., Rosengren, U., 2004. Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia 139, 89–97. Wallén, B., 1987. Growth pattern and distribution of biomass Calluna vulgaris on an ombrotrophic peat bog. Holarctic Ecol. 10, 73–79. Wallén, B., 1986. Above and below ground dry mass of the three main vascular plants on hummocks on a subarctic peat bog. Oikos 46, 51–56. Wardle, D., Zackrisson, O., Hörnberg, G., Gallet, C., 1997. The influence of Island area on ecosystem properties. Science 277, 1296–1299. Winsborough, C., Basiliko, N., 2010. Fungal and bacterial activity in Northern peatlands. Geomicrobiol. J. 27, 315–320. Wurzburger, N., Hartshorn, A., Hendrick, R., 2004. Ectomycorrhizal fungal community structure across a bog-forest ecotone in southeastern Alaska. Mycorrhiza 14, 383–389. Zibold, G., Drissner, J., Kaminski, S., Klemt, E., Miller, R., 2001. Time-dependence of the radiocaesium contamination of roe deer: measurement and modelling. J. Environ. Radioactiv. 55, 5–27. Zibold, G., Klemt, E., 2005. Ecological half-times of 137Cs and 90Sr in forest and freshwater ecosystems. Radioprotection Suppl. 1 (40), 497–502.