Accumulation of Natural and Anthropogenic Radionuclides in Body Profiles of Bryidae, a Subgroup of Mosses

Environmental Science and Pollution Research (2019) 26:27872–27887 https://doi.org/10.1007/s11356-019-05993-3

RESEARCH ARTICLE

Accumulation of natural and anthropogenic radionuclides in body profiles of Bryidae, a subgroup of mosses

Qiangqiang Zhong1 & Jinzhou Du1 & Viena Puigcorbé2 & Jinlong Wang1 & Qiugui Wang3 & Binbin Deng1 & Fule Zhang1

Received: 15 March 2019 /Accepted: 16 July 2019 /Published online: 25 July 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019

Abstract Mosses can be used as biomonitors to monitor radionuclide deposition and heavy metal pollution in cities, forests, and grasslands. 210 210 210 210 The aims of this work were to determine the activity concentrations of natural ( Po, Pb or Pbex (excess Pb is defined as the activity of 210Pb minus the activity of 226Ra), 7Be, 40K, 226Ra, 238U, and 232Th) and anthropogenic radionuclides (137Cs) in moss body profiles and in situ underlying soils of moss samples and to assess/determine the distribution features and accumulation of these radionuclides. Activity concentrations of radionuclides in the samples were measured using a low-background gamma spectrometer and a low-background alpha spectrometer. Consistent with their source, the studied radionuclides in the moss samples and underlying 210 210 210 7 soils were divided according to the principal component analysis (PCA) results into an airborne group ( Po, Pb ( Pbex), Be, 137 40 238 226 232 210 210 and Cs) and a terrestrial group ( K, U, Ra, and Th). The activity concentrations of Po and Pbex in moss body profiles 210 210 were mainly concentrated in the stems–rhizoid parts, in which we measured some of the highest Po and Pbex levels compared to the results in the literature. 7Be mainly accumulated in the leaves–stem parts. Different positive correlations were observed between 210Po and 210Pb and between 7Be and 210Pb, which indicated that the uptake mechanisms of 210Po, 210Pb, and 7Be by moss plants were different, to some extent. 137Cs was detected only in some moss samples, and the fraction of 137Cs in the underlying soils was much lower than that in the moss, suggesting that mosses were protecting the underlying soils from further pollution. Except for 40K, the terrestrial radionuclide (238U, 226Ra, and 232Th) content in mosses was predominantly at low levels, which indicated not only the inability of mosses to use those elements for metabolic purposes but also the rather poor capability of mosses to directly mobilize, absorb, and transport elements (U, Ra, or Th) not dissolved in water.

Highlights 1. 210Po, 210Pb, 7Be, 137Cs, 40K, 226Ra, 238U, and 232Th activity concentrations in vertical moss profiles were measured. 2. PCA distinguished these radionuclides into airborne and terrestrial sources. 3. Extremely high levels of 210Po and 210Pb and the deficiency of 210Po relative to 210Pb were observed in moss bodies. 4. 7Be almost exclusively accumulated in the leaves–stem tissues of all moss samples. 5. Mosses taken from Svalbard showed very high 137Cs levels, indicating that mosses may accumulate 137Cs and protect soils from further pollution. 6. Low accumulation of terrestrial radionuclides (238U, 226Ra, and 232Th) was found in mosses, suggesting the inefficient uptake mechanisms of moss plants and their inability to use these elements. Responsible editor: Georg Steinhauser

* Jinlong Wang 2 School of Science, Centre for Marine Ecosystems Research, Edith [email protected] Cowan University, Joondalup, WA 6027, Australia

3 State Key Laboratory of Nuclear Resources and Environment, East 1 State Key Laboratory of Estuarine and Coastal Research, East China China University of Technology, Nanchang 330013, Jiangxi Normal University, Shanghai 200241, People’sRepublicofChina Province, People’s Republic of China Environ Sci Pollut Res (2019) 26:27872–27887 27873

Keywords Accumulation . Biomonitoring . Moss body profiles . 137Cs . 7Be . 210Po–210Pb disequilibrium . Terrestrial radionuclides

Introduction 7Be (half-life 53.3 days) is a cosmogenic radionuclide produced in the stratosphere and upper troposphere by the inter- Mosses are nonvascular plants that grow on various substrata actions of high-energy particles of cosmic rays with the nuclei and in various habitats, forming an important component of of the most abundant elements in the air (Du et al. 2015;Lal the terrestrial ecosystem of various climate zones. Mosses are et al. 1958). The amount of 7Be in the atmosphere depends on a highly diverse group, with more than 10,000 species record- the cosmic ray flux, proton flux from the sun during solar ed in the global dataset (Geffert et al. 2013). In contrast to activities, stratosphere–troposphere exchange, and meteoro- vascular plants, mosses have no root systems, and they lack logical conditions. After it is formed, 7Be attaches to aerosols a water-repellent cuticle on their body surface. In addition, because of its high affinity for particles. Thus, both radon mosses obtain most nutrients for growth directly from the air daughters (210Po, 210Pb) and 7Be follow all atmospheric pro- via precipitation or by dry deposition. Hence, their capacity cesses for the transport, scavenging, and deposition of aero- for accumulation of airborne elements is greater than that of sols (Chen et al. 2016). other terrestrial plants growing in the same environments Man-made radionuclides in terrestrial and marine environ- (Aleksiayenak et al. 2013; Ross and Wesley 2011). ments come from many different sources, including direct dis- Furthermore, their morphologies are not affected by seasons, charges from nuclear installations (fuel reprocessing facilities or leading to the retention and accumulation of pollutants nuclear power plants), thermonuclear bomb testing, geological throughout the year (Wattanavatee et al. 2017). Thus, these repository of high-level nuclear wastes, leakages from disposed properties make moss an ideal medium for monitoring heavy radioactive waste containers, and nuclear accidents (Hu et al. metal pollution and radionuclides in various environments, 2010; Kershaw and Baxter 1995; Steinhauser et al. 2014). such as in mining areas (Demková et al. 2017; Pettersson However, the artificial radionuclide 137Cs that has been released et al. 1988;Tsikritzis2005), coal-fired power plants into the atmosphere mostly originated from more than 400 at- ğ (Delfanti et al. 1999;Sertetal.2011;U ur et al. 2003), or mospheric nuclear weapon tests and nuclear accidents (e.g., the areas affected by nuclear accidents (Chernobyl: Celik et al. Chernobyl nuclear accident and Fukushima accident) (Krmar 2009; Dragović et al. 2010; Mitrović et al. 2016; et al. 2013). Globally, there were no significant 137Cs emissions Fukushima: Oguri and Deguchi 2018). after the Chernobyl accident; although the Fukushima accident Many studies that monitored radioactive substances taken up released 137Cs into the atmosphere, the effects were minor in by mosses have focused on one or several types of radionu- 137 clides (Boryłoetal.2017;Długosz-Lisiecka and Wróbel 2014; regions far from Japan (Betsou et al. 2018). Hence, Cs was Oguri and Deguchi 2018). To better understand the transfer and removed from the atmosphere through physical decay as well as uptake of radionuclides by wild moss species and to add to the wet and dry deposition, and subsequently, it reached aquatic and body of knowledge on the monitoring of the radionuclides re- terrestrial environments in sediments, soils, and biota leased into the environment as a whole, investigations on both (Aleksiayenak et al. 2013; Burger and Lichtscheidl 2018; natural (238U, 232Th, 226Ra, radon daughters, 40K, and 7Be) and Dragović et al. 2010). anthropogenic radionuclides (137Cs) are needed. In contrast to the airborne radionuclides, the terrestrial ra- 226Ra (half-life 1620 years) is a member of the 238U(half- dionuclides, 40K, 232Th, 238U, and 226Ra, originate from crust- life 4.47 × 109 years) decay chain. After the alpha decay of al materials in soil particles. These radionuclides can also be 226Ra in soil, the product 222Rn (half-life 3.8 days), as a nat- transported and removed from the atmosphere by the dry or ural radioactive gas, escapes from the ground and diffuses into wet deposition of dust particles, especially during dust storms. the air. 222Rn decay products include the long-lived 210Pb 40K (half-life 1.25 × 109 years) is an isotope of potassium. (half-life 22.4 years) and 210Po (half-life 138.4 days), which Although 40K is not abundant in nature, the element K is can be present as unattached radon particles and/or as attached important for the metabolism of all living cells. 238U, 232Th radon particles (Li et al. 2019) in the atmosphere. In addition, (half-life 1.40 × 1010 years), and 226Ra are ubiquitous through- 210Pb and 210Po can also be released from anthropogenic out the earth’s surface. The global average activities of 40K, sources, and their levels have increased in the environment 232Th, and 238U in soil are estimated to be 400, 35, and − as a result of human activities such as the operation of power 30 Bq kg 1, respectively (UNSCEAR 2000). plants that burn fossil fuels, agriculture, fertilizer industries, Krmar et al. (2007)measured7Be, 214Bi, and 210Pb activities and exhaust fumes from vehicles (Belivermiş et al. 2016; in moss samples collected in Serbia and suggested that terrestrial Boryłoetal.2013; Martínez-Aguirre et al. 1996;Sertetal. mosses are a possible medium for the detection of the atmo- 2011;Uğur et al. 2009). spheric deposition of 7Be over large areas. Długosz-Lisiecka 27874 Environ Sci Pollut Res (2019) 26:27872–27887 and Wróbel (2014) investigated the 210Po activity concentra- profiles), we sought moss samples growing in different geo- tions in 180 moss and lichen samples in central Poland and graphical situations and belonging to different species. On the mapped the 210Po-contaminated regions with higher 210Po con- whole, samples were collected in two different latitude zones: centrations in urban air. Oguri and Deguchi (2018) investigated polar and temperate. A list of the sampled moss species and the 134Cs and 137Cs activity concentrations in the moss species information about the sampling process are presented in Hypnum plumaeforme collected within a 100-km radius of the Table 1. Three samples of the moss Herpetineuron toccoae Fukushima Dai-ichi Nuclear Power Plant and found positive were collected in an area adjacent to the Arctic Yellow River correlations between the radiocesium activity concentration in Station on the Svalbard archipelago (BJ01, BJ16, and BJ17). moss plants and the air dose rate. Długosz-Lisiecka (2017)pro- Three moss samples were collected from a semiarid region of posed a first-order kinetic model to understand 210Po and 210Pb Xining City, Qinghai Province in northwest China, with moss transport between the three body components of mosses and QH-1 (Leptobryum pyriforme) collected in Xishan Park, moss applied it to the estimation of the 210Po activity concentration QH-2 (Ditrichum pallidum) collected in an area adjacent to in the air. Most previous studies focused more on the activity the Qinghai Institute of Salt Lakes, and moss QH-3 concentrations of radionuclides in the entire moss plant (Al- (Hypnodendron reinwardtii) collected from a tree near the Masri et al. 2005;Długosz-Lisiecka and Wróbel 2014; highway. Moss samples of Funaria hygrometrica from sites Dragović et al. 2010; Krmar et al. 2013; Oguri and Deguchi SHZB and FJ01 were collected on campuses of the East China 2018;Uğur et al. 2003; Wattanavatee et al. 2017) and ignored Normal University and Xiamen University, respectively, the accumulation features of radionuclides in different tissues of which may be affected by human activities and industrial the moss body. However, the accumulation characteristics of emissions. The sampling sites JX01–JX03, HN01, and radionuclides in the moss body profile can provide more infor- HN03 are located in cultivated areas and villages in Jiangxi mation to better understand the transfer and accumulation mech- and Hunan provinces in central China. anisms of radionuclides and heavy metal pollutants from ambi- The underlying soils and moss samples were collected ent substrates and to guide the use of moss plants as using simple tools such as a large knife or shovel. In the field, bioindicators for air pollution monitoring and soil remediation. after removing the moss carpets, the underlying soil (1 cm of The aim of the study was to determine the concentrations of the the soil on top) was collected into a plastic bag. These moss activities of natural and anthropogenic radionuclides in moss plant samples were then cleaned to remove grasses, stones, (i.e., Bryidae) body profiles and underlying soil samples. and dead branches and leaves and immediately placed into Based on the obtained results, this study improved our under- plastic bags. The moss species were identified by examining standing of the accumulation processes of airborne and terres- macroscopic and microscopic characters with a light micro- trial radionuclides and the important role of mosses in protecting scope and referencing the relevant literature. the soil from atmospheric radioactive pollutants. Sample preparation and radiometric analysis

Materials and methods In the laboratory, the soil attached to the stem–rhizoid parts was also mechanically separated from the moss plants after Sampling areas and species of moss drying and incorporated into the aforementioned underlying soils. Generally, the mass of the underlying soils could reach Based on our objective (to measure and understand the gen- 20 g (dry weight). After drying in an oven at 60 °C to a eral distribution characteristics of radionuclides in moss body constant weight, soil samples were sieved out from the

Table 1 Moss species, locations, and sampling date

Sample Species Longitude (° E) Latitude (° N) Location Sampling date

BJ01 Herpetineuron toccoae 12.29 78.91 Svalbard, Norway 2017 August 22 BJ16 Herpetineuron toccoae 12.34 78.96 Svalbard, Norway 2017 August 27 BJ17 Herpetineuron toccoae 12.17 78.95 Svalbard, Norway 2017 August 27 QHX Leptobryum pyriforme 101.68 36.92 Xining, China 2017 December 23 QHY Ditrichum pallidum 101.75 36.64 Xining, China 2017 December 23 QHT Hypnodendron reinwardtii 101.68 36.92 Xining, China 2017 December 23 SHZB Funaria hygrometrica 121.40 31.23 Shanghai, China 2017 December 21 JX01 Meteoriella solute 116.60 27.15 Nanfeng, China 2018 February 12 JX02 Ditrichum pallidum 116.60 27.15 Nanfeng, China 2018 February 20 JX03 Racomitrium anomodontoides 116.60 27.15 Nanfeng, China 2018 February 20 HN01 Syntrichia norvegica 111.48 27.26 Shaoyang, China 2018 February 24 HN03 Hypnum plumaeforme 111.48 27.26 Shaoyang, China 2018 February 24 FJ01 Funaria hygrometrica 118.07 24.45 Xiamen, China 2018 April 23 Environ Sci Pollut Res (2019) 26:27872–27887 27875 residual fragments of plant remnants and further crushed to Data analysis homogenize the particles. The fresh moss samples were indi- vidually carefully cut into “leaves–stem” (green parts) and Principal component analysis (PCA) can be used to distin- “stems–rhizoid” (brownish and black parts) portions with guish the sources of radionuclides (Gordo et al. 2015; scissors. Later, both the leaves–stem and stems–rhizoid parts Wattanavatee et al. 2017). PCAwas conducted using the com- of mosses were carefully cleaned several times using tap water mercial statistics software package SPSS 10.0 for Windows. to remove any small dust and soil particles from the moss body surface and then dried at 60 °C to a constant weight. Radionuclide accumulation and transfer Subsequently, the dry moss body parts were crushed and quantification passed through a 2-mm mesh sieve. Two subsamples were prepared for each moss body part and underlying soil for Knowledge on radionuclide bioaccumulation and transfer different radionuclide analyses. Finally, both the tiny soil par- could give the meaningful values of bioconcentration and ticles and the finely ground moss plant materials were translocation factors. Generally, the estimation of soil-to- weighed, sealed, and stored in 7-mL centrifuge tubes for at biota radionuclide bioaccumulation factor (BCF) was defined least 3 weeks to allow secular equilibrium between 226Ra and as the ratio of activity concentration in the whole biota and the its decay daughters. To obtain a similar geometry for sample activity concentration in soil. However, in this study, activity measurements, the sample height was controlled at 5 cm for concentration in the whole moss plant is not available; hence, unknown samples and standard samples. Generally, the concentration ratio (CR) was used for quantifying and ex- amount of soil samples sealed in the tubes ranged from 5 to pressing uptake of radionuclides by stems–rhizoid parts of 9 g dry, and the mass of the finely ground moss plants varied moss plants (Eq. (1)) (Dragović et al. 2010). And the moss from2to4gdry. translocation factor (TF) which expresses the transfer between All the sealed samples were analyzed for 210Pb, 7Be, 226Ra, different moss parts was defined as the ratio of the activity 40K, 238U, 232Th, and 137Cs using a well-type HPGe γ spec- concentration in the leaves–stems and the activity concentra- trometer (GWL-120-15-XLB-AWT, ORTEC-AMETEK, 35% tion in stems–rhizoids (Eq. (2)) (Szymańska et al. 2018). relative efficiency and 1.65 keV FWHM for 60Co at 1.33 MeV). – ðÞ= Full energy peak efficiencies were determined using the ¼ Activity concentation in stems rhizoids Bq kg ð Þ CR ðÞ= 1 Standard Reference Material for soil and moss–soil samples Activity concentration in soil Bq kg prepared by the International Atomic Energy Agency (IAEA- Activity concentration in leaves–stemsðÞ Bq=kg TF ¼ ð2Þ 375; IAEA-447). Decay corrections and background subtraction Activity concentration in stems–rhizoidsðÞ Bq=kg were performed for all soil and moss samples. The measuring times for samples varied from 30,000 to 86,400 s to reduce the statistical count errors. 7Be was determined from the intensity of the 477.6-keV gamma line. The peaks corresponding to the Results 46.5- and 662-keV gamma lines were used to analyze 210Pb and 137Cs, respectively. The activity concentration of 238Uwas Activity concentrations of radionuclides obtained from the weighted mean of the gamma-ray lines of in the leaves–stems, stems–rhizoids, and underlying 234Th (63.3 and 92.8 keV), the activity concentration of 226Ra soil was obtained from the gamma-ray lines of 214Bi (609.3 keV) and 214Pb (295.2 and 352.0 keV), and 232Th activity concentra- The results of the activity concentration measurements of tion was obtained from the gamma-ray lines of 228Ac at 338.4, 210Po, unsupported/excess 210Pb, 7Be, 137Cs, 40K, 238U, 911.1, and 968.9 keV. The activity of 40K was determined di- 226Ra, and 232Th in different moss body parts and underlying rectly from the intensity of the 1460-keV gamma peak. soils are presented in Table 2 and Fig. 1. The error in Table 2 210 210 210 Alpha spectrometry was used to analyze Po. Prior to the denotes the measurement uncertainty. Both Po and Pbex alpha analyses, each sample was placed in a Teflon beaker and were detected in all moss sample tissues and underlying soils 210 digested using a mixed acid (HF:HNO3:HClO4 =1:1:1).To (Table 2 and Fig. 1a, b). The activity concentrations of Po correct the trace potential losses during digestion and sample ranged from 38 to 1518 Bq/kg in the leaves–stems, from 118 processing, a 209Po isotope with known activity (No. 7299, to 3139 Bq/kg in the stems–rhizoids, and from 82 to 2235 Bq/ 210 Eckert & Ziegler Isotope Products) was added to each sample kg in underlying soils. Pbex was within the range of 47– as an internal standard. After digestion, 210Po and 209Po were 2897, 114–5815, and 50–3829 Bq/kg for the leaves–stems, separated from the solution by autodeposition on silver discs. stems–rhizoids, and underlying soils, respectively. The activities of 209Po and 210Po on Ag discs were determined In the leaves–stems and stems–rhizoids, the activity con- using an ultralow-background alpha spectrometer (Canberra, centrations of 7Be ranged from 19 to 1442 Bq/kg and from 28 7200, USA). to 1005 Bq/kg, respectively (Table 2 and Fig. 1c). Our 27876

Table 2 Activities of anthropogenic and natural radionuclides in different moss body parts and underlying soils

Station Moss species Sample type Activity (Bq/kg, dry weight)

210 226 210 210 7 40 238 232 137 Pb Ra Pbex Po Be K U Th Cs

BJ01 Herpetineuron toccoae Leaves–stems 47 ± 18 BDL 47 ± 18 38 ± 3 227 ± 34 235 ± 79 BDL BDL BDL Stems–rhizoids 136 ± 13 21 ± 2 114 ± 14 118 ± 7 28 ± 16 470 ± 38 31 ± 10 25 ± 6 BDL Underlying soil 74 ± 6 22 ± 1 52 ± 6 84 ± 4 25 ± 6 650 ± 23 37 ± 7 40 ± 4 2 ± 1 BJ16 Herpetineuron toccoae Leaves–stems 2138 ± 47 BDL 2138 ± 47 920 ± 35 674 ± 32 188 ± 64 BDL BDL 24 ± 4 Stems–rhizoids 1628 ± 45 BDL 1628 ± 45 987 ± 37 42 ± 27 226 ± 52 BDL BDL 44 ± 5 Underlying soil 703 ± 19 13 ± 2 690 ± 19 750 ± 33 BDL 251 ± 28 20 ± 11 11 ± 4 70 ± 3 BJ17 Herpetineuron toccoae Leaves–stems 655 ± 25 BDL 655 ± 25 703 ± 33 332 ± 21 26 ± 36 BDL BDL 38 ± 3 Stems–rhizoids 832 ± 27 7 ± 3 825 ± 27 814 ± 38 115 ± 15 61 ± 37 50 ± 21 BDL 144 ± 5 Underlying soil 77 ± 10 27 ± 2 50 ± 10 322 ± 16 BDL 673 ± 33 58 ± 18 34 ± 5 6 ± 2 QHX Leptobryum pyriforme Leaves–stems 179 ± 15 8 ± 3 171 ± 16 164 ± 11 223 ± 27 258 ± 45 BDL 7 ± 7 BDL Stems–rhizoids 361 ± 33 23 ± 5 339 ± 33 279 ± 15 178 ± 36 308 ± 92 BDL 31 ± 16 3 ± 6 Underlying soil 99 ± 11 31 ± 3 68 ± 31 86 ± 6 BDL 535 ± 39 36 ± 13 34 ± 6 6 ± 1 QHT Hypnodendron reinwardtii Whole plant 1209 ± 27 15 ± 2 1195 ± 27 805 ± 43 19 ± 11 458 ± 36 15 ± 11 7 ± 6 2 ± 1 QHY Ditrichum pallidum Leaves–stems 241 ± 18 BDL 241 ± 18 124 ± 9 578 ± 26 285 ± 36 BDL BDL BDL Stems–rhizoids 710 ± 73 11 ± 9 699 ± 73 508 ± 85 758 ± 90 295 ± 86 BDL 22 ± 26 5 ± 5 Underlying soil 209 ± 13 29 ± 2 180 ± 13 227 ± 14 17 ± 7 561 ± 32 39 ± 11 37 ± 6 2 ± 1 SHZB Funaria hygrometrica Leaves–stems 361 ± 26 BDL 361 ± 26 131 ± 8 1238 ± 44 125 ± 50 BDL BDL BDL Stems–rhizoids 433 ± 32 7 ± 4 426 ± 32 227 ± 11 770 ± 44 278 ± 69 30 ± 19 18 ± 18 BDL Underlying soil 77 ± 7 25 ± 1 52 ± 8 82 ± 5 13 ± 6 504 ± 21 42 ± 7 37 ± 3 BDL JX01 Meteoriella soluta Leaves–stems 618 ± 31 17 ± 4 602 ± 31 279 ± 17 365 ± 32 284 ± 68 BDL 31 ± 10 BDL Stems–rhizoids 731 ± 41 11 ± 4 720 ± 42 656 ± 44 127 ± 35 212 ± 66 33 ± 19 35 ± 11 BDL Underlying soil 158 ± 11 43 ± 2 115 ± 11 202 ± 14 12 ± 10 1245 ± 43 99 ± 12 68 ± 5 2 ± 1 JX02 Ditrichum pallidum Leaves–stems 1241 ± 50 5 ± 2 1236 ± 50 794 ± 35 811 ± 48 244 ± 76 BDL BDL BDL Stems–rhizoids 2569 ± 52 14 ± 3 2555 ± 52 1302 ± 85 120 ± 19 399 ± 55 24 ± 14 4 ± 7 BDL Underlying soil 2233 ± 44 7 ± 2 2226 ± 44 1622 ± 25 63 ± 14 631 ± 61 BDL 33 ± 7 BDL JX03 Racomitrium anomodontoides Leaves–stems 2903 ± 92 6 ± 5 2897 ± 92 1518 ± 80 1442 ± 74 140 ± 86 BDL BDL BDL Stems–rhizoids 5815 ± 201 BDL 5815 ± 201 3139 ± 69 1005 ± 118 205 ± 186 BDL BDL BDL Underlying soil 3848 ± 64 19 ± 3 3829 ± 64 2235 ± 78 231 ± 23 611 ± 54 35 ± 21 39 ± 8 BDL 26:27872 (2019) Res Pollut Sci Environ HN01 Syntrichia norvegica Leaves–stems 1373 ± 30 7 ± 3 1366 ± 30 1006 ± 91 642 ± 26 114 ± 32 BDL 9 ± 6 BDL Stems–rhizoids 1698 ± 44 16 ± 3 1681 ± 44 1098 ± 84 89 ± 14 116 ± 51 BDL 19 ± 13 BDL Underlying soil 759 ± 32 25 ± 3 735 ± 25 838 ± 54 16 ± 15 378 ± 38 69 ± 26 46 ± 8 BDL HN03 Hypnum plumaeforme Leaves–stems 1278 ± 71 14 ± 7 1264 ± 71 718 ± 39 913 ± 80 135 ± 73 BDL BDL BDL Stems–rhizoids 1719 ± 58 13 ± 5 1706 ± 58 1214 ± 70 243 ± 33 140 ± 63 BDL BDL BDL Underlying soil 897 ± 20 23 ± 2 874 ± 20 731 ± 57 40 ± 11 315 ± 26 45 ± 10 36 ± 5 2 ± 1 FJ01 Funaria hygrometrica Whole plant 545 ± 34 15 ± 5 530 ± 35 203 ± 12 258 ± 27 236 ± 50 BDL 238 ± 17 BDL Underlying soil 256 ± 19 24 ± 4 232 ± 19 92 ± 5 92 ± 17 526 ± 43 37 ± 19 174 ± 12 4 ± 3

BDL below detection level – 27887 Environ Sci Pollut Res (2019) 26:27872–27887 27877

3500 6000 (a) 210 (b) 210 Po Pbex 3000 Leaves-stems 5000

)t Stems-rhizoids

h 2500 Underlying soil giewyr 4000 2000 d

gk/qB(ytivitcA 3000 1500 2000 1000

1000 500

0 0 BJ01 BJ16 BJ17 QHX QHT QHY SH01 JX01 JX02 JX03 HN01 HN03 FJ01 BJ01 BJ16 BJ17 QHX QHT QHY SH01 JX01 JX02 JX03 HN01 HN03 FJ01 150 (d) 137 1500 (c) 7Be Cs 125

)thgiewyrdgk/qB(ytivitcA 1200 100

900 75

600 50

300 25

0 0 BJ01 BJ16 BJ17 QHX QHT QHY SH01 JX01 JX02 JX03 HN01 HN03 FJ01 BJ01 BJ16 BJ17 QHX QHT QHY SH01 JX01 JX02 JX03 HN01 HN03 FJ01 1400 150 (e) 40K (f) 238U 1200 125 )thgiewyrdgk/qB(ytivitcA 1000 100 800 75 600 50 400

25 200

0 0 BJ01 BJ16 BJ17 QHX QHT QHY SH01 JX01 JX02 JX03 HN01 HN03 FJ01 BJ01 BJ16 BJ17 QHX QHT QHY SH01 JX01 JX02 JX03 HN01 HN03 FJ01 50 250 (g) 226Ra (h) 232Th Moss species information: 40 BJ01, BJ16, BJ17: Herpetineuron toccoae

) 200 thg QHX: Leptobryum pyriforme iewy QHY, JX02: Ditrichum pallidum 30 150 QHT: Hypnodendron reinwardtii rdg SHZB, FJ-1: Funaria hygrometrica JX01: k Meteoriella soluta / q 20 JX03: Racomitrium anomodontoides B 100 ( HN01: yt Syntrichia norvegica iv HN03:

it Hypnum plumaeforme

cA 10 50

0 0 BJ01 BJ16 BJ17 QHX QHT QHY SH01 JX01 JX02 JX03 HN01 HN03 FJ01 BJ01 BJ16 BJ17 QHX QHT QHY SH01 JX01 JX02 JX03 HN01 HN03 FJ01 Sample Sample 210 210 7 137 40 238 226 232 Fig. 1 Activity concentrations of Po (a), Pbex (b), Be (c), Cs (d), K(e), U(f), Ra (g), and Th (h) in moss body profiles and underlying soils. Please note that sample FJ01 refers to the entire moss and the scale of the y-axis is different for all the panels measurements of 7Be were comparable with the values report- and at Kaiga, India (234–1061 Bq/kg, Karunakara et al. ed at Sellafield, England (100–900 Bq/kg, Sumerling 1984), 2003). Generally, 7Be can be detected in just several 27878 Environ Sci Pollut Res (2019) 26:27872–27887 millimeters of nondisturbed topsoil. However, 7Be was detect- Discussion ed in most underlying soils (from 12 to 231 Bq/kg) except for three samples (BJ16, BJ17, and QHX), although only the top Factors influencing activity concentrations 1-cm layer of the underlying soils was collected after remov- and distribution features of the radionuclides in moss ing the moss carpets. Anthropogenic 137Cs was detected only samples in some moss samples and underlying soils (Fig. 1d), with the highest activity concentration (144 ± 5 Bq/kg) in the stems– The accumulation processes of radionuclides in bryophytes rhizoids of moss (Herpetineuron toccoae)atlocationBJ17. are complicated and may be influenced by a number of factors The activity concentration of 40K was detected in all moss (moss species, topography, geology, meteorology, etc.). At samples and underlying soils (Table 2 and Fig. 1e). In the sites JX01, JX02, and JX03, we collected three different moss leaves–stems and stems–rhizoids, the activity concentration species, Meteoriella soluta, Ditrichum pallidum,and of 40K ranged from 26 ± 36 to 458 ± 36 Bq/kg and from 61 Racomitrium anomodontoides, respectively. Although they ±37to470±38Bq/kg,respectively.The40Kactivityinun- grew in a similar environment (in a small town in Nanfeng derlying soils ranged from 251 ± 28 to 1245 ± 42 Bq/kg, with County, a small county in Jiangxi Province, China), we found the highest value found at site JX01. that the activity concentrations of the analyzed radionuclides 238 226 232 210 210 7 The activity concentrations of U, Ra, and Th are ( Po, Pbex,and Be) varied significantly in these three presented in Table 2 and Fig. 1 f–h. The value of 238Uranged moss samples (Fig. 1). This variation indicates that the signif- from below detection level (BDL) to 15 ± 11 Bq/kg, from icant intrinsic factor may be the moss species (Sert et al. 2011; BDL to 50 ± 21 Bq/kg, and from BDL to 99 ± 12 Bq/kg in Boryłoetal.2017). Other intrinsic factors may pertain to the the leaves–stems, stems–rhizoids, and underlying soils, re- morphological structure of the bryophytes (especially the sur- spectively. The activity concentrations of 226Ra ranged be- face morphology of the leaves), different uptake mechanisms, tween BDL and 17 ± 4 Bq/kg, between BDL and 23 ± 5 Bq/ and the growth speed (some mosses grow faster than others). kg, and between 7 ± 2 and 43 ± 2 Bq/kg in the leaves–stems, Unfortunately, we lack sufficient evidence to further discuss stems–rhizoids, and underlying soils, respectively. 232Th was these effects. nearly undetectable in most moss samples except for the moss Other extrinsic factors that could affect the accumulation sample at location FJ01 (up to 238 ± 16 Bq/kg), and it was processes of radionuclides in the moss body include weather mainly detected in underlying soils for all samples, with a conditions (humidity, rainfall, etc.), artificial addition of radio- range of 11–174 Bq/kg. nuclides by human activity, geographical characteristics (whether it is easy to obtain water, whether it is easy to face the sun, etc.), competition for living space and nutrients Concentration ratio and translocation factor between bryophytes and higher plants, and the degree of of radionuclides local shelter provided by trees. For example, Kamar et al. (2017) found that the activities of 7Be in mosses collected The CRs calculated from the activity concentrations of radio- under trees were two times lower than those in mosses col- nuclides in soils and mosses are presented in Table 3. The CRs lected in open fields, and Boryłoetal.(2017) noted that some for 226Ra, 238U, 232Th, and 40Krangedfrom0.25to2.03(n = moss species growing in the lower parts of trees were 10), from 0.34 to 0.85 (n = 4), from 0.12 to 1.37 (n = 8), and protected from direct radioactive deposition. However, it is from 0.09 to 0.90 (n = 12), respectively. However, the concen- beyond the scope of this study to discuss all of these factors. 210 210 210 7 tration ratios of Pb (or Pbex), Po, and Be were higher Here, we focused on the sources of the radionuclides and the than unity for almost all of the moss samples (Table 3). The possible accumulation process during moss growth based on CRs of 137Cs were higher than unity for samples BJ17 (23.21) the existing data. and QHY (3.47) and lower than unity for samples BJ16 (0.62) PCA is one of the most widely used techniques to reduce and QHX (0.56). the dimensionality of a dataset in order to preserve most of the The TFs for these radionuclides are shown in Table 4.The information. In the present study, PCA was performed on the translocation factors of 238Uand232Th for all the moss sam- natural and anthropogenic radionuclide measured in the ples could not be calculated due to the undetectable activity leaves–stems, stems–rhizoids, and underlying soils to identify concentration in the moss leaves–stem parts. The TFs of 7Be the similarities and differences among these radionuclides. were higher than unity for almost all of the moss samples Figure 2 a–c show the score plot between the first two princi- 210 210 210 (0.76–16.25). The TFs for Pb (or Pbex)and Po ranged pal components (component 1 vs. component 2). The first two from 0.34 to 1.31 (n = 11) and from 0.24 to 0.93 (n = 11), principal components explained about 66.02, 67.10, and respectively. The TFs of 40K for all the moss plants changed 74.42% of the total variance for the leaves–stems, stems–rhi- from 0.42 to 1.34 (Table 4). The TFs of 226Ra and 137Cs could zoids, and underlying soils, respectively (Fig. 2a–c). The x- be calculated for only several moss samples (Table 4). axis represents component 1, while the y-axis represents nio c oltRs(09 26:27872 (2019) Res Pollut Sci Environ – 27887 Table 3 The values of radionuclide concentration ratios (CR) for the analyzed moss plants (note that CRs for sample QHT were not calculated)

Sample sites Moss species Concentration ratio (CR)

210 226 210 210 7 40 238 232 137 Pb Ra Pbex Po Be K U Th Cs

BJ01 Herpetineuron toccoae 1.83 ± 0.24 0.95 ± 0.12 2.21 ± 0.38 1.40 ± 0.10 1.12 ± 0.70 0.72 ± 0.06 0.84 ± 0.31 0.64 ± 0.16 – BJ16 Herpetineuron toccoae 2.32 ± 0.09 – 2.36 ± 0.09 1.32 ± 0.08 – 0.90 ± 0.23 ––0.62 ± 0.07 BJ17 Herpetineuron toccoae 10.86 ± 1.50 0.27 ± 0.11 16.53 ± 3.49 2.53 ± 0.17 – 0.09 ± 0.06 0.85 ± 0.45 – 23.21 ± 6.79 QHX Leptobryum pyriforme 3.65 ± 0.53 0.74 ± 0.17 4.96 ± 2.30 3.23 ± 0.28 – 0.58 ± 0.18 – 0.92 ± 0.49 0.56 ± 1.19 QHY Ditrichum pallidum 3.40 ± 0.41 0.37 ± 0.30 3.89 ± 0.28 2.24 ± 0.40 43.80 ± 17.98 0.52 ± 0.16 – 0.58 ± 0.70 3.47 ± 3.93 SHZB Funaria hygrometrica 5.59 ± 0.67 0.28 ± 0.16 8.12 ± 1.31 2.75 ± 0.21 57.43 ± 25.93 0.55 ± 0.14 0.72 ± 0.47 0.48 ± 0.48 – JX01 Meteoriella soluta 4.63 ± 0.42 0.25 ± 0.08 6.28 ± 0.72 3.25 ± 0.31 10.33 ± 8.86 0.17 ± 0.05 0.34 ± 0.20 0.51 ± 0.17 – JX02 Ditrichum pallidum 1.15 ± 0.03 2.03 ± 0.75 1.15 ± 0.03 0.80 ± 0.05 1.89 ± 0.52 0.63 ± 0.11 – 0.12 ± 0.20 – JX03 Racomitrium anomodontoides 1.51 ± 0.06 – 1.52 ± 0.06 1.40 ± 0.06 4.35 ± 0.67 0.17 ± 0.30 –– – HN01 Syntrichia norvegica 2.24 ± 0.11 0.66 ± 0.15 2.29 ± 0.10 1.31 ± 0.13 5.43 ± 5.10 0.31 ± 0.14 – 0.42 ± 0.30 – HN03 Hypnum plumaeforme 1.92 ± 0.08 0.56 ± 0.24 1.95 ± 0.08 1.66 ± 0.16 6.11 ± 1.91 0.44 ± 0.20 –– – FJ01* Funaria hygrometrica 2.13 ± 0.21 0.61 ± 0.24 2.29 ± 0.24 2.21 ± 0.18 2.81 ± 0.59 0.45 ± 0.10 – 1.37 ± 0.13 –

– not available *CR values of this sample were calculated from the whole moss plants and the underlying soil 27879 27880 Environ Sci Pollut Res (2019) 26:27872–27887

Table 4 The values of radionuclide translocation factors (TF) for the analyzed moss plants (note that TFs for samples QHT and FJ01 were not calculated)

Sample sites Moss species Translocation factor (TF)

210 226 210 210 7 40 238 232 137 Pb Ra Pbex Po Be K U Th Cs

BJ01 Herpetineuron toccoae 0.34 ± 0.14 – 0.41 ± 0.17 0.32 ± 0.03 8.22 ± 4.89 0.50 ± 0.17 –– – BJ16 Herpetineuron toccoae 1.31 ± 0.05 – 1.31 ± 0.05 0.93 ± 0.05 16.25 ± 10.48 0.83 ± 0.34 –– 0.55 ± 0.11 BJ17 Herpetineuron toccoae 0.79 ± 0.04 – 0.79 ± 0.04 0.86 ± 0.06 2.89 ± 0.42 0.42 ± 0.64 –– 0.27 ± 0.02 QHX Leptobryum pyriforme 0.50 ± 0.06 0.36 ± 0.15 0.51 ± 0.07 0.59 ± 0.05 1.25 ± 0.30 0.84 ± 0.29 –– – QHY Ditrichum pallidum 0.34 ± 0.04 – 0.34 ± 0.03 0.24 ± 0.04 0.76 ± 0.10 0.97 ± 0.31 –– – SHZB Funaria hygrometrica 0.83 ± 0.09 – 0.83 ± 0.09 0.58 ± 0.05 1.61 ± 0.11 0.45 ± 0.21 –– – JX01 Meteoriella soluta 0.85 ± 0.06 1.54 ± 0.62 0.85 ± 0.06 0.42 ± 0.04 2.88 ± 0.83 1.34 ± 0.53 –– – JX02 Ditrichum pallidum 0.48 ± 0.02 0.33 ± 0.18 0.48 ± 0.02 0.61 ± 0.05 6.77 ± 1.14 0.61 ± 0.21 –– – JX03 Racomitrium anomodontoides 0.50 ± 0.02 – 0.50 ± 0.02 0.48 ± 0.03 1.43 ± 0.18 1.33 ± 2.50 –– – HN01 Syntrichia norvegica 0.81 ± 0.03 0.40 ± 0.18 0.81 ± 0.03 0.92 ± 0.11 7.22 ± 1.18 0.98 ± 0.51 –– – HN03 Hypnum plumaeforme 0.74 ± 0.05 1.09 ± 0.70 0.74 ± 0.05 0.59 ± 0.05 3.75 ± 0.60 0.97 ± 0.68 –– –

− not available component 2, so points close to each axis are associated with calculated CRs and TFs are displayed in Tables 3 and 4.The 210 210 210 7 component 1 or component 2. The graphs (Fig. 2a–c) clearly CRs of Pb (or Pbex), Po, and Be were higher than indicate that there are two different groups of radionuclides. unity for almost all of the moss samples (Table 3) due to the Component 1 represented the group of radionuclides from higher activity concentration in moss tissues and the lower 210 210 210 7 137 7 atmospheric sources ( Po, Pb, Pbex, Be, and Cs), activity concentration in soils, especially in the case of Be. and component 2 represented the other group of radionuclides The activity concentrations of 7Be followed the order leaves– from terrestrial sources (40K, 226Ra, 238U, and 232Th). As stems > stems–rhizoids ≫ underlying soils, which caused the shown in Fig. 2 a, a plot of the leaves–stem parts of moss relatively higher TFs of 7Be (higher than unity) for almost all samples, the loading factors for 7Be and 137Cs were slightly of the moss samples (Table 4) and proved that 7Be mainly different from those for 210Po and 210Pb, but as shown in Fig. accumulated in the upper part of moss plants, especially in 2 b and c, both 7Be and 210Po–210Pb pairs have similar loading the leaves–stems. As mentioned before, 7Be is formed by a factors. These figures indicate that moss plants and underlying spallation reaction between cosmic rays and the nucleus of soils are not sensitive enough to distinguish the production oxygen and nitrogen in the atmosphere (Du et al. 2015;Lal and deposition differences in these airborne radionuclides et al. 1958); hence, 7Be exists in surface air and wet and dry (7Be, 210Po, and 210Pb), although 7Be mainly originates from deposition samples. Krmar et al. (2016) observed that the nuclear reactions in the stratosphere and upper troposphere, atmospheric depositional 7Be measured in mosses depended and 210Pb is generated from the decay of 222Rn in the atmo- on cumulative precipitation. As shown in our results (Fig. 1c), sphere. The reason for this is that 7Be and 210Pb (including 7Be mainly accumulated in the leaves–stem parts of moss daughter 210Po) follow very similar transport and deposition body profiles. One possible mechanism for this phenomenon processes of aerosols, and they have continuous and relatively may be related to the assumption that 7Be would not be mo- constant deposition fluxes from the atmosphere. Unlike 7Be bilized and transported in the moss body. In other words, 7Be and 210Po–210Pb pairs, 137Cs was sporadically discharged deposited on the leaves of the moss is mainly retained and from atmospheric weapon testing and the Chernobyl incident, stored in the upper segment of the plants and this captured and most of it had been deposited on the earth’s surface sev- 7Be will not be transferred down to the stems–rhizoid tissues. eral decades ago. These results imply that there are various In the next growth cycle, new 7Be will again be captured by atmospheric processes and accumulation mechanisms affect- the new moss leaves, but the old 7Be stored in the old leaves– ing radionuclide activity concentrations in moss samples. A stems will decay completely over time. The green parts of detailed discussion about the accumulation processes of radio- moss plants usually contain the last several years of annual nuclides in the moss body is given in the following growth segments. The half-life of 7Be is as short as 53 days; paragraphs. thus, the 7Be stored in the green parts (leaves–stems) of mosses probably represented about 1 year (~ 7 half-lives of 7 210 210 7 7 Accumulation of Be, Po, and Pbex Be) of accumulated Be fallout. Another completely different 210 210 7 and the disequilibrium of Po and Pbex in moss mechanism for Be distribution in moss plants may be related body to another assumption that moss plants may mistake Be for K and that they would probably actively transport 7Be toward Figure 1 cshowsthelevelsof7Be in moss tissues and under- the growing parts because mosses are able to translocate nu- lying soils. Based on these radionuclide activities, the trients from senescent parts (e.g., stems–rhizoids). Environ Sci Pollut Res (2019) 26:27872–27887 27881

short half-life of 7Be. However, the results in Table 2 show that in some cases, the differences were significantly lower; furthermore, in one example, the 7Be concentration was higher in the stems–rhizoids than in the leaves–stems (e.g., sample QHY). It is more likely that both parts of the moss can accept 7Be regardless of the purpose because in the case of dry deposition, if 7Be is almost completely stopped in the upper green part of the moss, during wet deposition, it is not possible to stop 7Be from reaching the lower part of the moss. Although we do not know which mechanism is the dominant one in reality, the results show that the activity concentrations of 7Be in the stems–rhizoids were generally at low levels or nearly BDL. Investigating the intrinsic mechanisms for metal accumulation in moss would benefit both environment monitoring application and our understanding of plant physiology. In addition, because of the covering by the moss carpet, 7Be in the underlying soils was also nearly undetectable. It was observed that most of the activity concentrations of 210 210 Po and Pbex were concentrated in the leaves–stems and stems–rhizoids (Fig. 1a, b) compared to those in underlying soils. And in the majority of the samples, the calculated CRs 210 210 210 for Pb (or Pbex)and Po were higher than 1 (Table 3). The TFs of 210Pb and 210Po were lower than 1 (Table 4)andthe analyzed moss stems–rhizoids contained more 210Po and 210Pb when compared with the leaves–stems. These CRs and TFs for airborne 210Po, 210Pb, and 7Be implied that the important source might be atmospheric fallout, while internal processes during moss growth played a minor role. Table 5 represents the results of 210Po and 210Pb reported in the literature for moss 210 210 plants. Most of the Po and Pbex activity concentrations from this study were higher than the values from around the worldfoundintheliterature.Moreover,asshowninTable5, 210Po is in disequilibrium with 210Pb, not just in this study, but also in other investigations. For underlying soils at some sites (BJ16, JX02, JX03, HN01, and HN03), 210Po (750–2235 Bq/ 210 kg) and Pbex levels (690–3829 Bq/kg) were higher than the average activity concentration levels of 210Po and 210Pb in various soils (20–240 Bq/kg, reviewed by Persson and Holm (2011)), which indicated that the elevated levels of 210Po and 210Pb in underlying soils may be attributed to the introduction of the detritus/fragments of moss plants. 210 210 210 210 210 7 The Po/ Pb activity ratios in moss plants and underly- Fig. 2 Component plot in a rotated space for Po, Pb, Pbex, Be, 210 137Cs, 40K, 238U, 226Ra, and 232Th the in leaves–stems (a), stems–rhizoids ing soils are presented in Table 6.Alowerlevelof Po relative (b), and underlying soils (c) to that of 210Pb in the leaves–stems and stems–rhizoids was observed for nearly all samples. In addition, the 210Po/210Pb Additionally, 7Be might also be adsorbed by ion exchange to disequilibrium was stronger in the leaves–stems than in the the cell walls of the leaves, and because the leaves represent stems–rhizoids. These results indicated that the source of most of the total surface, they would also help to accumulate 210Po and 210Pb in moss plants was mainly atmospheric. most of the 7Be that the plants may encounter. However, con- However, 210Po was nearly in equilibrium with 210Pb in the sidering that new green segments and old brown stems– underlying soils for most of the sites. 210Po/210Pb activity ratio rhizoid parts can be several years old, differences in 7Be con- was reported in the literature to be > 1 in many moss samples centrations between the leaves–stems and stems–rhizoid parts collected around coal-fired power plants (1.0–1.9, Uğur et al should be more than two orders of magnitude because of the 2003;1.0–1.8, Sert et al. 2011;1.1–2.0, Bakar et al. 2014). 27882

Table 5 Comparison of 210 Po and 210 Pb activity concentrations (Bq/kg dry weight) in moss samples in the literature

Location Plant type 210 Po 210 Pb Number of samples Moss species References

Svalbard archipelago, Norway Leaves–stems, moss 38–920 47–2138* 3 Herpetineuron toccoae This study Stems–rhizoids, moss 118–987 114–1628* China Leaves–stems, moss 124–1518 171–2897* 8 Leptobryum pyriforme, Ditrichum pallidum, Funaria Stems–rhizoids, moss 227–3139 339–5815* hygrometrica, Meteoriella soluta, Racomitrium anomodontoides,andHypnum plumaeforme Eastern Mediterranean Sea region Whole plant, moss 341–2119 165–2392 33 Lycopodium cernuum and Funaria hygrometrica Al-Masri et al. (2005) (Syrian coastal mountains series) Novi Sad, Serbia Green part of the moss – 556 ± 113 55 Hypnum cupressiforme Krmar et al. (2016) Peninsular Thailand Whole plant, moss – 135–1630 46 ** Wattanavatee et al. (2017) Lodz City, Poland Whole plant, moss 50–450 – 180 Pleurozium schreberi Długosz-Lisiecka and Wróbel (2014) Sobieszewo Island in northern Poland Whole plant, moss 133–501 – 70 Dicranum scoparium and Pleurozium schreberi Boryłoetal.(2017) Kaiga nuclear power plant site in South India Whole plant 2724 ± 13 – 2 Pterobryopsis tumida (Hook.) Dix. Karunakara et al. (2000) Coal-fired power plants in Soma and Whole plant, moss 124–1125 94–724 78 Tortella tortuosa, Homalothecium sericeum, Pterogonium Sert et al. (2011) Yatagan, western Turkey graciale, Isothecium alopecuroides, Didymodon acutus, Hypnum lacunosum, Hypnum cupressiforme Çan coal-fired power plant, Turkey Whole plant, moss 151–550 219–724 8 Hypnum cupressiforme Belivermiş et al. (2016) Thermal power plant and coal mine Whole plant, moss 107–721 – 4 Cylindrocolea rhizantha (Mont.) R.M. Schust. and Galhardi et al. (2017) area, southern Brazil Sematophyllum galipense (Müll. Hal.) Mitt. Uraniferous coal-fired power plant Whole plant, moss 256–1228 200–650 6 Grimmia pulvinata and Hypnum cupressiforme Uğur et al. (2003) in western Turkey South Shetland archipelago, Antarctic Whole plant, moss – 21–93 6 Polytrichum alpinum and Drepanoclatus uncinatus Godoy et al. (1998) Different Belarus regions Whole plant, moss – 141–575 63 Pleurozium schreberi Aleksiayenak et al. (2013) Slovakia Whole plant, moss – 330–1521 11 Hylocomium splendens

– not available 26:27872 (2019) Res Pollut Sci Environ 210 226 210 210 *Denotes Pbex activity concentration value. Due to the very low level of Ra in mosses, the Pbex value is nearly equal to the Pb value **This research investigated 17 moss species, which include Octoblepharum albidum Hedw., Himantocladium sp., Leucobryum aduncum Dozy & Molk., Thuidium sp.1, Barbella asp., Hyophila cf. involute (Hook. f.) A. Jaeger, Arthrocormus schimperi Dozy & Molk., Leucoloma sp., Pyrrhobryum spiniforme (Hedw.) Mitt., Thuidium sp.2, Mitthyridium sp., Aerobryopsis sp., Neckeropsis sp., Syrrhopodon cf. japonicus (Besch.) Broth, Leucobryum sanctum (Brid.) Hampe, Leucophanes glaucum (Schwaegr.) Mitt., and Hypnaceae sp. – 27887 Environ Sci Pollut Res (2019) 26:27872–27887 27883

Table 6 210Po/210Pb activity ratios in moss plants and underlying soils 210 210 There was a strong correlation between Pbex and Po 210 210 in moss samples and underlying soils (leaves–stems: r =0.94, Sample Po/ Pbex p < 0.05; stems–rhizoids: r =0.98, p < 0.05; underlying soil: Leaves– Stems– Underlying soil r = 0.98, p < 0.05, Fig. 3a), which indicates that the major stems rhizoids contributor of 210Po was 210Pb decay. The lower correlation between 7Be and 210Pb in moss and soil samples (Fig. 3b) BJ01 0.81 ± 0.32 0.87 ± 0.10 1.13 ± 0.10 ex indicated that the accumulation process of 7Be was to some BJ16 0.43 ± 0.02 0.60 ± 0.02 1.06 ± 0.05 extent different from that of 210Pb. BJ17 1.07 ± 0.06 0.97 ± 0.05 4.19 ± 0.60 QHX 0.91 ± 0.09 0.77 ± 0.08 0.87 ± 0.11 137 QHT 0.66 ± 0.03 ––Sources and accumulation of Cs QHY 0.51 ± 0.05 0.71 ± 0.14 1.08 ± 0.09 137 SH01 0.36 ± 0.03 0.52 ± 0.04 1.06 ± 0.11 Cs was detected only in some moss samples and soils col- JX01 0.45 ± 0.03 0.89 ± 0.07 1.27 ± 0.12 lected from Yellow River Station, the Svalbard archipelago in JX02 0.63 ± 0.03 0.50 ± 0.03 0.72 ± 0.01 Norway (sites BJ01, BJ16, and BJ17), and Xining, Qinghai Province in China (sites QHX and QHY) (Fig. 1d). The source JX03 0.52 ± 0.03 0.53 ± 0.01 0.58 ± 0.02 of 137Cs in the Svalbard archipelago is linked to the global HN01 0.73 ± 0.06 0.64 ± 0.05 1.10 ± 0.08 fallout from atmospheric weapons testing in the 1950s and HN03 0.56 ± 0.04 0.70 ± 0.04 0.81 ± 0.06 1960s, because Svalbard is considered to have been relatively FJ01 0.37 ± 0.03* – 0.35 ± 0.03 unaffected by fallout from the Chernobyl accident in 1986 137 – not available (Dowdall et al. 2005). The source of Cs in Xining may *This value is the 210 Po/210 Pbratiointhewholemossplant pertain to the global fallout and China’s nuclear weapon tests (Zeng et al. 2007;Wuetal.2011). In addition, an additional source of the 137Cs in mosses in Xining is related to the redis- 210 210 In contaminated sites, Po and Pb can diffuse via fly tribution of soil or dust during agricultural production and dust ash, in which the 210Po concentration is about two times higher than that of 210Pb (UNSCEAR 2000;Uğur et al. 2003). Moreover, the boiling point of 210Po (962 °C) is much lower than that of 210Pb (1749 °C) (Uğur et al. 2003), and there may be an additional input of 210Po around coal-fired power plants because the chimney gases carry the volatile 210Po. However, our sampling sites were not in the vicinity of any industrial pollution sources. As mentioned before, the PCA results indicated atmospheric sources of 210Po and 210Pb. The main source of 210Po and 210Pb entering the mosses is the exhaled radon gas from the surface layers of the earth’scrust into the atmosphere. In the atmosphere, 222Rn decays with the formation of the daughter radionuclides 210Pb and 210Po. Because of the short residence times of aerosols (several days to several weeks) in the troposphere and planetary boundary layer, the ratio of 210Po/210Pb in aerosols and rainwater samples is typically < 0.1–0.2 (Baskaran 2011). Hence, 210Po activity in these moss plants was composed of 210Po received from the atmosphere and produced by 210Pb decay in the moss bodies. Except for site BJ17 (210Po was nearly in equilibrium with 210Pb in the leaves–stems and stems–rhizoids), the 210Po/210Pb ratios ranged from 0.36 to 0.91 in the leaves– stem parts and from 0.50 to nearly unity in the stems– rhizoid parts (Table 6). These 210Po/210Pb ratios in moss bodies were much higher than those in aerosols or rainwater samples (from < 0.1 to 0.2, Baskaran 2011), which may indicate that 210Pb was retained in the moss plants for a long time and 210 that the ingrowth of Po caused the increase in the Fig. 3 The correlation plots of activity concentrations measured in 210 210 210 210 7 210 Po/ Pb ratio. mosses and soils for a Po– Pbex and b Be– Pbex 27884 Environ Sci Pollut Res (2019) 26:27872–27887 storms. The levels of 137Cs in moss bodies ranged from 24 to age of the moss plants at site BJ17 can be calculated to be 144 Bq/kg for samples in Svalbard, which are in good agree- more than 53 years old (2017–1964 = 53 years). Interestingly, ment with the levels reported by Dowdall et al. (2005)(11– themossbodydistributionof137Cs at site BJ16 was similar to 292 Bq/kg) and Aarkrog et al. (1984) (230 Bq/kg). At site that in moss at site BJ17, but the 137Cs activity concentrations BJ16, the levels of 137Cs followed the order of underlying soil in the soils were very different. The moss plants at site BJ16 > stems–rhizoids > leaves–stems, while at BJ17, 137Cs mainly might have started to grow after the first 137Cs global fallout accumulated in the leaves–stems and stems–rhizoids, and at events based on the activity concentrations of 137Cs measured BJ01, 137Cs was only detected in the soil. For samples collect- in the soil; thus, it can be deduced that the moss plants at BJ16 ed in Xining, the activity concentrations of 137Cs were low (< are younger (< 53 years) than the moss at BJ17. In addition, 6 Bq/kg) in the stems–rhizoids and soils and below detection we found that most of the 137Cs accumulated in the moss body level in the leaves–stem parts for all samples. Hence, the CRs (sites BJ16, BJ17), and consequently, the underlying soil of 137Cs were only calculated for several moss samples (BJ17, remained relatively unpolluted. In other words, without a QHY, BJ16, and QHX, see Table 3). However, the TFs of moss carpet covering the underlying soil, the 137Cs levels in 137Cs were available only for two moss samples (Table 4, the underlying soil would be higher than the current state BJ16 (0.55 ± 0.11) and BJ17 (0.27 ± 0.02)). because of the global fallout of 137Cs.However,incontrast, As mosses have no root system, the uptake of nutrients we detected fairly high levels of 137Cs in feces samples from from the substrate may be insignificant (Krmar et al. 2013). reindeer (26 ± 1 Bq/kg, unpublished data) and rabbits (40 ± However, this may be different for different moss species be- 1 Bq/kg, unpublished data) in Svalbard. The vegetation in the cause the leaves, stems, rhizoids, and paraphyllia can work region of the Yellow River Station on Svalbard is mainly together and absorb nutrient solutions from the soil to the mosses and lichens. It is speculated that mosses and lichens upper parts of the plants. The effectiveness of this type of are the major food sources for reindeer and rabbits. The 137Cs absorption depends on the specifics of the moss plant mor- in the reindeer and rabbit feces indicated that the animals can phology. Whether the plant has a short stem that is anchored to mobilize 137Cs in moss (or lichen) and transfer it to the soil or the soil by rhizoids (as in Funaria) or an elongated, creeping the ecosystem. Generally, it is recognized that radionuclides stem (as in Hypnum) that has virtually no direct contact with from mosses are not likely to be transferred to other parts of the soil can have a marked difference. Hence, in case of 137Cs, the ecosystem and that mosses are a secure sink for radionu- mosses would probably mistake it for K and try to absorb it clides because moss plants tend to decay very slowly. from soil solution in some specific or extreme situation. All However, herbivores (e.g., rabbits, reindeer, horses, insects, these features may contribute to the distribution of 137Cs in the etc.) can access this sink and induce the diffusion of 137Cs to moss body. Moreover, because of the absence of the cuticle in other parts of the ecosystem. Further studies are needed to the leaves, the uptake of 137Cs could occur through ion- determine the adverse effects of 137Cs and other radionuclides exchange processes directly from the atmosphere via wet on animals that feed on mosses. and dry deposition (Uğur et al. 2003). If the 137Cs that accumulated in a certain layer of the moss does not redistribute or Weak accumulation of terrestrial radionuclides transfer to the rest of the body, then the 137Cs peak recorded in in moss samples the moss body profile may correspond to 137Cs fallout events. Although, as with K and Na, there is a strong likelihood that The activity concentrations of 40K in moss samples were Cs will be redistributed inside the moss body, the 137Cs signal higher than the values for 238U, 226Ra, and 232Th (Fig. 1e– from Chernobyl or the 1963 global fallout events will still be h). In all cases, 40K activity concentrations were detected in stored in the moss body because of the relatively long “mem- the order of leaves–stems < stems–rhizoids < underlying soils ory” and long life of moss. Unfortunately, because of the dif- (Fig. 1e). The CRs of 40K ranged from 0.09 to 0.90, which ficulties in dividing the whole moss plant body profile into implied the existence of a weak 40K transfer from the soil to more segments, we only divided the moss body into two seg- the moss body. Lower 40K content in mosses compared to ments (leaves–stems and stems–rhizoids). Hence, we were not those in the underlying soil has been previously reported able to determine the vertical distribution of the 137Cs activity (Dowdall et al. 2005;Dragović et al. 2010;Eckletal.1986). concentration in moss body profiles with a higher resolution. Potassium is a necessary element for the metabolic processes Assuming that the 137Cs in moss samples from Svalbard of plants; thus, the source of 40K for moss plants may be dust was entirely from global fallout and not from the Chernobyl or tiny soil particles carried via dry deposition. The direct accident, then it is reasonable to speculate that the moss from uptake of 40K by moss plants from the underlying soil may BJ17 experienced and recorded the 137Cs fallout event. represent an alternative pathway because the 40Kactivitycon- Moreover, assuming that the 137Cs fallout event recorded by centration in the stems–rhizoid parts was slightly higher than the moss corresponded to the year 1964 although the atmo- that in the leaves–stem parts. In addition, the TFs of 40Kintwo spheric weapons testing occurred in the 1950s–1960s, then the moss samples were higher than unity (JX01, Meteoriella Environ Sci Pollut Res (2019) 26:27872–27887 27885

Table 7 Concentration ratios of radionuclides (mean ± SD) for different moss species

210 226 210 210 7 40 238 232 137 Moss species Pb Ra Pbex Po Be K U Th Cs

Herpetineuron toccoae 5.00 ± 5.08 0.61 ± 0.34 7.03 ± 6.72 1.75 ± 0.55 1.12 0.57 ± 0.35 0.845 ± 0.005 0.64 11.92 ± 11.30 Ditrichum pallidum 2.27 ± 1.13 1.20 ± 0.83 2.52 ± 1.37 1.52 ± 0.72 22.84 ± 20.96 0.57 ± 0.06 – 0.35 ± 0.23 3.47 Funaria hygrometrica 3.86 ± 1.73 0.45 ± 0.17 5.21 ± 2.92 2.48 ± 0.27 30.12 ± 27.31 0.50 ± 0.05 0.72 0.93 ± 0.45 – Leptobryum pyriforme 3.65 0.74 4.96 3.23 – 0.58 – 0.92 0.56 Meteoriella soluta 4.63 0.25 6.28 3.25 10.33 0.17 0.34 0.51 – Racomitrium 1.51 – 1.52 1.4 4.35 0.17 ––– anomodontoides Syntrichia norvegica 2.24 0.66 2.29 1.31 5.43 0.31 – 0.42 – Hypnum plumaeforme 1.92 0.56 1.95 1.66 6.11 0.44 –––

– not available soluta, 1.34 and JX03, Racomitrium anomodontoides,1.33), 232Th in mosses can occur by direct uptake from the substrate which indicated that 40K can be transferred and concentrated in certain circumstances. to the green parts of moss plants. 238 226 232 The U, Ra, and Th activity concentrations in the Comparison of CRs and TFs of radionuclides leaves–stems were generally below the level of detection, al- for different moss species though low levels of these nuclides were found in the stems– 238 rhizoids for some moss samples. Hence, the CRs of U, When CRs and TFs for the different moss species ana- 226 232 Ra, and Th for only several moss samples were calcu- lyzed here are compared, it can be obviously found that 238 232 lated, and the TFs of Uand Th were not calculated for all they are species-specific (Tables 7 and 8). All the moss of the moss samples. The nearly below detectable levels of species showed great ability in interception and retention these terrestrial radionuclides in moss samples indicate that of airborne radionuclides (e.g., CRs of 210Pb, 210Po, and they do not have metabolic use for growth. Mosses tend to 7Be > 1), although there are some interspecies differences. absorb nutrients via contact with water rather than from the The average CR for 7Be in Ditrichum pallidum and underlying substrate. However, one exception is the moss Funaria hygrometrica was up to 20-fold higher than that sample FJ01 (Funaria hygrometrica, Fig. 1h). At this site, for Herpetineuron toccoae andupto3-foldhigherthan the moss plants were taken from one big stone on the campus that for other species (Table 7). However, some moss of Xiamen University, and this stone was covered with a layer species showed undetectable accumulation abilities for of weathered rock detritus and some decaying branches and some terrestrial radionuclides (U, Th, and Ra 232 leaves. The activity concentration of Th (238 ± 17 Bq/kg) isotopes) because the CRs could not be calculated for in the whole plants was higher than that in the underlying some moss species or the calculated CRs were as low as substrate materials (weathered rock detritus) (174 ± 12 Bq/ 0.17 (Table 7). Although the average TFs for 7Be in all kg) and much higher than that in any other sample (Fig. 1h). the moss species were higher than unity, the interspecies These results may support the notion that the accumulation of differences of mosses were still significant. The TFs of

Table 8 Translocation factors of radionuclides (mean ± SD) for different moss species

210 226 210 210 7 40 238 232 137 Moss species Pb Ra Pbex Po Be K U Th Cs

Herpetineuron toccoae 0.81 ± 0.40 – 0.84 ± 0.37 0.70 ± 0.27 9.12 ± 5.49 0.58 ± 0.18 –– 0.41 ± 0.14 Ditrichum pallidum 0.41 ± 0.07 0.33 0.41 ± 0.07 0.43 ± 0.19 3.77 ± 3.01 0.79 ± 0.18 –– – Funaria hygrometrica 0.83 – 0.83 0.58 1.61 0.45 –– – Leptobryum pyriforme 0.5 0.36 0.51 0.59 1.25 0.84 –– – Meteoriella soluta 0.85 1.54 0.85 0.42 2.88 1.34 –– – Racomitrium anomodontoides 0.5 – 0.5 0.48 1.43 1.33 –– – Syntrichia norvegica 0.81 0.4 0.81 0.92 7.22 0.98 –– – Hypnum plumaeforme 0.74 1.09 0.74 0.59 3.75 0.97 –– –

– not available 27886 Environ Sci Pollut Res (2019) 26:27872–27887

7Be in Herpetineuron toccoae (9.12) and Syntrichia References norvegica (7.22) were up to three times higher than those for other species. Two moss species showed obvious Aarkrog A, Dahlgaard H, Holm E, Hallstadius L (1984) Evidence for – transfer and accumulation of 40Kfromthestems–rhizoid bismuth-207 in global fallout. J Environ Radioact 1:107 117 – Aleksiayenak YV,Frontasyeva MV,Florek M, Sykora I, Holy K, Masarik parts to the leaves stem parts based on the calculated TFs J, Brestakova L, Jeskovsky M, Steinnes E, Faanhof A, Ramatlhape (1.34 for Meteoriella soluta and1.33forRacomitrium KI (2013) Distributions of 137Cs and 210Pb in moss collected from anomodontoides)(Table8). However, the average TFs Belarus and Slovakia. J Environ Radioact 117:19–24 of 238Uand232Th for all the moss species (Table 8)could Al-Masri MS, Mamish S, Al-Haleem MA, Al-Shamali K (2005) Lycopodium cernuum and Funaria hygrometrica as deposition indi- not be calculated due to the undetectable activity in the cators for radionuclides and trace metals. J Radioanal Nucl Chem moss leaves–stem parts. It should be noted that in 266:49–55 assessing accumulation and transfer of radionuclides to Bakar NSA, Mahmood ZUYW, Saat A, Ishak AK (2014) Anthropogenic mosses, the effect of age differences and living conditions airborne depositions of Po-210, Pb-210 and Po-210/Pb-210 in the between moss plants was not taken into consideration. mosses and surface soils at the vicinity of a coal-fired power. J Sains Nukl Malays 26(1):9–17 Baskaran M (2011) Po-210 and Pb-210 as atmospheric tracers and global atmospheric Pb-210 fallout: a review. J Environ Radioact 102:500– 513 Conclusion Belivermiş M, KılıçÖ,ÇayırA,Coşkun M, Coşkun M (2016) Assessment of 210Po and 210Pb in lichen, moss and soil around Çan coal-fired power plant, Turkey. J Radioanal Nucl Chem 307: In this study, we measured the activity concentrations of – 210 210 210 7 137 40 238 226 523 531 Po, Pb ( Pbex), Be, Cs, K, U, Ra, and Betsou C, Tsakiri E, Kazakis N, Hansman J, Krmar M, Frontasyeva M, 232 Th in the leaves–stems and stems–rhizoid parts of moss Ioannidou A (2018) Heavy metals and radioactive nuclide concen- plants and underlying soils. The PCA results were used to trations in mosses in Greece. Radiat Eff Defects Solids 173(9–10): 851–856 divide the studied radionuclides into an airborne group 210 210 210 7 137 40 Boryło A, Olszewski G, Skwarzec B (2013) A study on lead ( Pb) and ( Po, Pb, Be, and Cs) and a terrestrial group ( K, 210 238 226 232 137 polonium ( Po) contamination from phosphogypsum in the envi- U, Ra, and Th). Cs was only detected in moss ronment of Wiślinka (northern Poland). Environ Sci Processes samples from two areas: the Yellow River Station on the Impacts 15(8):1622–1628 Svalbard archipelago and Xining, Qinghai Province. The BoryłoA,Romańczyk G, Skwarzec B (2017) Lichens and mosses as 137Cs activity concentrations in moss plants were much higher polonium and uranium biomonitors on Sobieszewo Island. J Radioanal Nucl Chem 311:859–869 than those in underlying soils, which indicated that mosses act Burger A, Lichtscheidl I (2018) Stable and radioactive cesium: a review as filters and prevent the deposition of radioactive fallout ma- about distribution in the environment, uptake and translocation in 210 210 terials in the underlying soil. Most of the Po and Pbex plants, plant reactions and plants' potential for bioremediation. Sci were concentrated in the stems–rhizoid parts, and we hypoth- Total Environ 618:1459–1485 esize that the dead and decaying moss plants could increase Celik N, Cevik U, Celik A, Koz B (2009) Natural and artificial radioac- 210 210 tivity measurements in eastern Black Sea region of Turkey. J Hazard the Po and Pb levels in the underlying soils. In addition, Mater 162:146–153 210 210 the strong disequilibrium between Po and Pb was found Chen J, Luo S, Huang Y (2016) Scavenging and fractionation of particle- in the leaves–stem parts. 7Be was mainly accumulated in the reactive radioisotopes 7Be, 210Pb and 210Po in the atmosphere. – leaves–stem parts of moss plants. Positive correlations were Geochim Cosmochim Acta 188:208 223 observed between 210Po and 210Pb,buttherewerelowercor- Delfanti R, Papucci C, Benco C (1999) Mosses as indicators of radioac- 7 210 tivity deposition around a coal-fired power station. Sci Total Environ relations between Be and Pb, which indicated that the 227:49–56 uptake mechanisms of these radionuclides were different, to Demková L, Bobul’ská L, Árvay J, Jezný T, Ducsay L (2017) some extent. Moreover, the activity concentrations of 40Kin Biomonitoring of heavy metals contamination by mosses and li- 238 chens around Slovinky tailing pond (Slovakia). J Environ Sci most moss samples were much higher than those of U, – 226 232 Health A Toxic/Hazard Subst Environ Eng 52(1):30 36 Ra, and Th because of the effective uptake and accumu- Długosz-Lisiecka M (2017) Kinetics of 210Po accumulation in moss body lation of potassium. profiles. Environ Sci Pollut Res 24(25):20254–20260 Długosz-Lisiecka M, Wróbel J (2014) Use of moss and lichen species to Acknowledgments We are grateful to Dr. Ruiliang Zhu, School of Life identify 210Po-contaminated regions. Environ Sci Processes Impacts Science, East China Normal University, for his advice and guidance in 16(12):2729–2733 moss species identification. We would like to thank the group members of Dowdall M, Gwynn JP, Moran C, O'Dea J, Davids C, Lind B (2005) the RIC team in East China Normal University for their help in sampling. Uptake of radionuclides by vegetation at a high Arctic location. We would also like to thank the in-depth reviews of two anonymous Environ Pollut 133:327–332 reviewers. Dragović S, Mihailović N, Gajić B (2010) Quantification of transfer of 238U, 226Ra, 232Th, 40Kand137Cs in mosses of a semi-natural eco- Funding information This study was partly supported by the Natural system. J Environ Radioact 101:159–164 Science Foundation of China (grants 41576083, 41706089, and Du J, Du J, Baskaran M, Bi Q, Huang D, Jiang Y (2015) Temporal 41706083). variations of atmospheric depositional fluxes of 7Be and 210Pb over Environ Sci Pollut Res (2019) 26:27872–27887 27887

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