Accumulation of natural and anthropogenic radionuclides in body … · 2019-12-30 · and Wróbel (2014) investigated the 210Po activity concentra- tions in 180 moss and lichen samples

RESEARCH ARTICLE

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

Qiangqiang Zhong1& Jinzhou Du1

& Viena Puigcorbé2& JinlongWang1

&QiuguiWang3& 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

AbstractMosses can be used as biomonitors to monitor radionuclide deposition and heavy metal pollution in cities, forests, and grasslands.The aims of this work were to determine the activity concentrations of natural (210Po, 210Pb or 210Pbex (excess

210Pb is defined as theactivity of 210Pbminus the activity of 226Ra), 7Be, 40K, 226Ra, 238U, and 232Th) and anthropogenic radionuclides (137Cs) inmoss bodyprofiles and in situ underlying soils of moss samples and to assess/determine the distribution features and accumulation of theseradionuclides. Activity concentrations of radionuclides in the samples were measured using a low-background gamma spectrometerand a low-background alpha spectrometer. Consistent with their source, the studied radionuclides in themoss samples and underlyingsoils were divided according to the principal component analysis (PCA) results into an airborne group (210Po, 210Pb (210Pbex),

7Be,and 137Cs) and a terrestrial group (40K, 238U, 226Ra, and 232Th). The activity concentrations of 210Po and 210Pbex inmoss body profilesweremainly concentrated in the stems–rhizoid parts, in which wemeasured some of the highest 210Po and 210Pbex levels compared tothe results in the literature. 7Be mainly accumulated in the leaves–stem parts. Different positive correlations were observed between210Po and 210Pb and between 7Be and 210Pb, which indicated that the uptake mechanisms of 210Po, 210Pb, and 7Be by moss plantswere different, to some extent. 137Cs was detected only in some moss samples, and the fraction of 137Cs in the underlying soils wasmuch 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 theinability 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.

Highlights1. 210Po, 210Pb, 7Be, 137Cs, 40K, 226Ra, 238U, and 232Th activityconcentrations in vertical moss profiles were measured.2. PCA distinguished these radionuclides into airborne and terrestrialsources.3. Extremely high levels of 210Po and 210Pb and the deficiency of 210Porelative to 210Pb were observed in moss bodies.4. 7Be almost exclusively accumulated in the leaves–stem tissues of allmoss samples.5. Mosses taken from Svalbard showed very high 137Cs levels, indicatingthat mosses may accumulate 137Cs and protect soils from further pollu-tion.6. Low accumulation of terrestrial radionuclides (238U, 226Ra, and 232Th)was found in mosses, suggesting the inefficient uptake mechanisms ofmoss plants and their inability to use these elements.

Responsible editor: Georg Steinhauser

* Jinlong [email protected]

1 State Key Laboratory of Estuarine and Coastal Research, East ChinaNormal University, Shanghai 200241, People’s Republic of China

2 School of Science, Centre for Marine Ecosystems Research, EdithCowan University, Joondalup, WA 6027, Australia

3 State Key Laboratory of Nuclear Resources and Environment, EastChina University of Technology, Nanchang 330013, JiangxiProvince, People’s Republic of China

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

http://crossmark.crossref.org/dialog/?doi=10.1007/s11356-019-05993-3&domain=pdf

http://orcid.org/0000-0003-1750-7580

mailto:[email protected]

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

Introduction

Mosses are nonvascular plants that grow on various substrataand in various habitats, forming an important component ofthe terrestrial ecosystem of various climate zones. Mosses area highly diverse group, with more than 10,000 species record-ed in the global dataset (Geffert et al. 2013). In contrast tovascular plants, mosses have no root systems, and they lacka water-repellent cuticle on their body surface. In addition,mosses obtain most nutrients for growth directly from the airvia precipitation or by dry deposition. Hence, their capacityfor accumulation of airborne elements is greater than that ofother terrestrial plants growing in the same environments(Aleksiayenak et al. 2013; Ross and Wesley 2011).Furthermore, their morphologies are not affected by seasons,leading to the retention and accumulation of pollutantsthroughout the year (Wattanavatee et al. 2017). Thus, theseproperties make moss an ideal medium for monitoring heavymetal pollution and radionuclides in various environments,such as in mining areas (Demková et al. 2017; Petterssonet al. 1988; Tsikritzis 2005), coal-fired power plants(Delfanti et al. 1999; Sert et al. 2011; Uğur et al. 2003), orareas affected by nuclear accidents (Chernobyl: Celik et al.2009; Dragović et al. 2010; Mitrović et al. 2016;Fukushima: Oguri and Deguchi 2018).

Many studies that monitored radioactive substances taken upby mosses have focused on one or several types of radionu-clides (Boryło et al. 2017; Długosz-Lisiecka and Wróbel 2014;Oguri and Deguchi 2018). To better understand the transfer anduptake of radionuclides by wild moss species and to add to thebody of knowledge on the monitoring of the radionuclides re-leased into the environment as a whole, investigations on bothnatural (238U, 232Th, 226Ra, radon daughters, 40K, and 7Be) andanthropogenic radionuclides (137Cs) are needed.

226Ra (half-life 1620 years) is a member of the 238U (half-life 4.47 × 109 years) decay chain. After the alpha decay of226Ra in soil, the product 222Rn (half-life 3.8 days), as a nat-ural radioactive gas, escapes from the ground and diffuses intothe air. 222Rn decay products include the long-lived 210Pb(half-life 22.4 years) and 210Po (half-life 138.4 days), whichcan be present as unattached radon particles and/or as attachedradon particles (Li et al. 2019) in the atmosphere. In addition,210Pb and 210Po can also be released from anthropogenicsources, and their levels have increased in the environmentas a result of human activities such as the operation of powerplants that burn fossil fuels, agriculture, fertilizer industries,and exhaust fumes from vehicles (Belivermiş et al. 2016;Boryło et al. 2013; Martínez-Aguirre et al. 1996; Sert et al.2011; Uğur et al. 2009).

7Be (half-life 53.3 days) is a cosmogenic radionuclide pro-duced in the stratosphere and upper troposphere by the inter-actions of high-energy particles of cosmic rays with the nucleiof the most abundant elements in the air (Du et al. 2015; Lalet al. 1958). The amount of 7Be in the atmosphere depends onthe cosmic ray flux, proton flux from the sun during solaractivities, stratosphere–troposphere exchange, and meteoro-logical conditions. After it is formed, 7Be attaches to aerosolsbecause of its high affinity for particles. Thus, both radondaughters (210Po, 210Pb) and 7Be follow all atmospheric pro-cesses for the transport, scavenging, and deposition of aero-sols (Chen et al. 2016).

Man-made radionuclides in terrestrial and marine environ-ments come from many different sources, including direct dis-charges from nuclear installations (fuel reprocessing facilities ornuclear power plants), thermonuclear bomb testing, geologicalrepository of high-level nuclear wastes, leakages from disposedradioactive waste containers, and nuclear accidents (Hu et al.2010; Kershaw and Baxter 1995; Steinhauser et al. 2014).However, the artificial radionuclide 137Cs that has been releasedinto the atmosphere mostly originated from more than 400 at-mospheric nuclear weapon tests and nuclear accidents (e.g., theChernobyl nuclear accident and Fukushima accident) (Krmaret al. 2013). Globally, there were no significant 137Cs emissionsafter the Chernobyl accident; although the Fukushima accidentreleased 137Cs into the atmosphere, the effects were minor inregions far from Japan (Betsou et al. 2018). Hence, 137Cs wasremoved from the atmosphere through physical decay as well aswet and dry deposition, and subsequently, it reached aquatic andterrestrial environments in sediments, soils, and biota(Aleksiayenak et al. 2013; Burger and Lichtscheidl 2018;Dragović et al. 2010).

In contrast to the airborne radionuclides, the terrestrial ra-dionuclides, 40K, 232Th, 238U, and 226Ra, originate from crust-al materials in soil particles. These radionuclides can also betransported and removed from the atmosphere by the dry orwet deposition of dust particles, especially during dust storms.40K (half-life 1.25 × 109 years) is an isotope of potassium.Although 40K is not abundant in nature, the element K isimportant for the metabolism of all living cells. 238U, 232Th(half-life 1.40 × 1010 years), and 226Ra are ubiquitous through-out the earth’s surface. The global average activities of 40K,232Th, and 238U in soil are estimated to be 400, 35, and30 Bq kg−1, respectively (UNSCEAR 2000).

Krmar et al. (2007) measured 7Be, 214Bi, and 210Pb activitiesinmoss samples collected in Serbia and suggested that terrestrialmosses are a possible medium for the detection of the atmo-spheric deposition of 7Be over large areas. Długosz-Lisiecka

Environ Sci Pollut Res (2019) 26:27872–27887 27873

and Wróbel (2014) investigated the 210Po activity concentra-tions in 180 moss and lichen samples in central Poland andmapped the 210Po-contaminated regions with higher 210Po con-centrations in urban air. Oguri and Deguchi (2018) investigatedthe 134Cs and 137Cs activity concentrations in the moss speciesHypnum plumaeforme collected within a 100-km radius of theFukushima Dai-ichi Nuclear Power Plant and found positivecorrelations between the radiocesium activity concentration inmoss plants and the air dose rate. Długosz-Lisiecka (2017) pro-posed a first-order kinetic model to understand 210Po and 210Pbtransport between the three body components of mosses andapplied it to the estimation of the 210Po activity concentrationin the air. Most previous studies focused more on the activityconcentrations of radionuclides in the entire moss plant (Al-Masri et al. 2005; Długosz-Lisiecka and Wróbel 2014;Dragović et al. 2010; Krmar et al. 2013; Oguri and Deguchi2018; Uğur et al. 2003; Wattanavatee et al. 2017) and ignoredthe accumulation features of radionuclides in different tissues ofthe moss body. However, the accumulation characteristics ofradionuclides in the moss body profile can provide more infor-mation to better understand the transfer and accumulationmech-anisms of radionuclides and heavy metal pollutants from ambi-ent substrates and to guide the use of moss plants asbioindicators for air pollution monitoring and soil remediation.The aim of the study was to determine the concentrations of theactivities of natural and anthropogenic radionuclides in moss(i.e., Bryidae) body profiles and underlying soil samples.Based on the obtained results, this study improved our under-standing of the accumulation processes of airborne and terres-trial radionuclides and the important role of mosses in protectingthe soil from atmospheric radioactive pollutants.

Materials and methods

Sampling areas and species of moss

Based on our objective (to measure and understand the gen-eral distribution characteristics of radionuclides in moss body

profiles), we sought moss samples growing in different geo-graphical situations and belonging to different species. On thewhole, samples were collected in two different latitude zones:polar and temperate. A list of the sampled moss species andinformation about the sampling process are presented inTable 1. Three samples of the moss Herpetineuron toccoaewere collected in an area adjacent to the Arctic Yellow RiverStation on the Svalbard archipelago (BJ01, BJ16, and BJ17).Three moss samples were collected from a semiarid region ofXining City, Qinghai Province in northwest China, with mossQH-1 (Leptobryum pyriforme) collected in Xishan Park, mossQH-2 (Ditrichum pallidum) collected in an area adjacent tothe Qinghai Institute of Salt Lakes, and moss QH-3(Hypnodendron reinwardtii) collected from a tree near thehighway. Moss samples of Funaria hygrometrica from sitesSHZB and FJ01 were collected on campuses of the East ChinaNormal University and Xiamen University, respectively,which may be affected by human activities and industrialemissions. The sampling sites JX01–JX03, HN01, andHN03 are located in cultivated areas and villages in Jiangxiand Hunan provinces in central China.

The underlying soils and moss samples were collectedusing simple tools such as a large knife or shovel. In the field,after removing the moss carpets, the underlying soil (1 cm ofthe soil on top) was collected into a plastic bag. These mossplant samples were then cleaned to remove grasses, stones,and dead branches and leaves and immediately placed intoplastic bags. The moss species were identified by examiningmacroscopic and microscopic characters with a light micro-scope and referencing the relevant literature.

Sample preparation and radiometric analysis

In the laboratory, the soil attached to the stem–rhizoid partswas also mechanically separated from the moss plants afterdrying and incorporated into the aforementioned underlyingsoils. Generally, the mass of the underlying soils could reach20 g (dry weight). After drying in an oven at 60 °C to aconstant 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 22BJ16 Herpetineuron toccoae 12.34 78.96 Svalbard, Norway 2017 August 27BJ17 Herpetineuron toccoae 12.17 78.95 Svalbard, Norway 2017 August 27QHX Leptobryum pyriforme 101.68 36.92 Xining, China 2017 December 23QHY Ditrichum pallidum 101.75 36.64 Xining, China 2017 December 23QHT Hypnodendron reinwardtii 101.68 36.92 Xining, China 2017 December 23SHZB Funaria hygrometrica 121.40 31.23 Shanghai, China 2017 December 21JX01 Meteoriella solute 116.60 27.15 Nanfeng, China 2018 February 12JX02 Ditrichum pallidum 116.60 27.15 Nanfeng, China 2018 February 20JX03 Racomitrium anomodontoides 116.60 27.15 Nanfeng, China 2018 February 20HN01 Syntrichia norvegica 111.48 27.26 Shaoyang, China 2018 February 24HN03 Hypnum plumaeforme 111.48 27.26 Shaoyang, China 2018 February 24FJ01 Funaria hygrometrica 118.07 24.45 Xiamen, China 2018 April 23

27874 Environ Sci Pollut Res (2019) 26:27872–27887

residual fragments of plant remnants and further crushed tohomogenize the particles. The fresh moss samples were indi-vidually carefully cut into “leaves–stem” (green parts) and“stems–rhizoid” (brownish and black parts) portions withscissors. Later, both the leaves–stem and stems–rhizoid partsof mosses were carefully cleaned several times using tap waterto remove any small dust and soil particles from the mossbody surface and then dried at 60 °C to a constant weight.Subsequently, the dry moss body parts were crushed andpassed through a 2-mm mesh sieve. Two subsamples wereprepared for each moss body part and underlying soil fordifferent radionuclide analyses. Finally, both the tiny soil par-ticles and the finely ground moss plant materials wereweighed, sealed, and stored in 7-mL centrifuge tubes for atleast 3 weeks to allow secular equilibrium between 226Ra andits decay daughters. To obtain a similar geometry for samplemeasurements, the sample height was controlled at 5 cm forunknown samples and standard samples. Generally, theamount of soil samples sealed in the tubes ranged from 5 to9 g dry, and the mass of the finely ground moss plants variedfrom 2 to 4 g dry.

All the sealed samples were analyzed for 210Pb, 7Be, 226Ra,40K, 238U, 232Th, and 137Cs using a well-type HPGe γ spec-trometer (GWL-120-15-XLB-AWT, ORTEC-AMETEK, 35%relative efficiency and 1.65 keV FWHM for 60Co at 1.33MeV).Full energy peak efficiencies were determined using theStandard Reference Material for soil and moss–soil samplesprepared by the International Atomic Energy Agency (IAEA-375; IAEA-447). Decay corrections and background subtractionwere performed for all soil and moss samples. The measuringtimes for samples varied from 30,000 to 86,400 s to reduce thestatistical count errors. 7Be was determined from the intensity ofthe 477.6-keV gamma line. The peaks corresponding to the46.5- and 662-keV gamma lines were used to analyze 210Pband 137Cs, respectively. The activity concentration of 238U wasobtained from the weighted mean of the gamma-ray lines of234Th (63.3 and 92.8 keV), the activity concentration of 226Rawas obtained from the gamma-ray lines of 214Bi (609.3 keV)and 214Pb (295.2 and 352.0 keV), and 232Th activity concentra-tion was obtained from the gamma-ray lines of 228Ac at 338.4,911.1, and 968.9 keV. The activity of 40K was determined di-rectly from the intensity of the 1460-keV gamma peak.

Alpha spectrometry was used to analyze 210Po. Prior to thealpha analyses, each sample was placed in a Teflon beaker anddigested using a mixed acid (HF:HNO3:HClO4 = 1:1:1). Tocorrect the trace potential losses during digestion and sampleprocessing, a 209Po isotope with known activity (No. 7299,Eckert & Ziegler Isotope Products) was added to each sampleas an internal standard. After digestion, 210Po and 209Po wereseparated from the solution by autodeposition on silver discs.The activities of 209Po and 210Po on Ag discs were determinedusing an ultralow-background alpha spectrometer (Canberra,7200, USA).

Data analysis

Principal component analysis (PCA) can be used to distin-guish the sources of radionuclides (Gordo et al. 2015;Wattanavatee et al. 2017). PCAwas conducted using the com-mercial statistics software package SPSS 10.0 for Windows.

Radionuclide accumulation and transferquantification

Knowledge on radionuclide bioaccumulation and transfercould give the meaningful values of bioconcentration andtranslocation factors. Generally, the estimation of soil-to-biota radionuclide bioaccumulation factor (BCF) was definedas the ratio of activity concentration in the whole biota and theactivity concentration in soil. However, in this study, activityconcentration in the whole moss plant is not available; hence,concentration ratio (CR) was used for quantifying and ex-pressing uptake of radionuclides by stems–rhizoid parts ofmoss plants (Eq. (1)) (Dragović et al. 2010). And the mosstranslocation factor (TF) which expresses the transfer betweendifferent moss parts was defined as the ratio of the activityconcentration in the leaves–stems and the activity concentra-tion in stems–rhizoids (Eq. (2)) (Szymańska et al. 2018).

CR ¼ Activity concentation in stems–rhizoids Bq=kgð ÞActivity concentration in soil Bq=kgð Þ ð1Þ

TF ¼ Activity concentration in leaves–stems Bq=kgð ÞActivity concentration in stems–rhizoids Bq=kgð Þ ð2Þ

Results

Activity concentrations of radionuclidesin the leaves–stems, stems–rhizoids, and underlyingsoil

The results of the activity concentration measurements of210Po, unsupported/excess 210Pb, 7Be, 137Cs, 40K, 238U,226Ra, and 232Th in different moss body parts and underlyingsoils are presented in Table 2 and Fig. 1. The error in Table 2denotes the measurement uncertainty. Both 210Po and 210Pbexwere detected in all moss sample tissues and underlying soils(Table 2 and Fig. 1a, b). The activity concentrations of 210Poranged from 38 to 1518 Bq/kg in the leaves–stems, from 118to 3139 Bq/kg in the stems–rhizoids, and from 82 to 2235 Bq/kg in underlying soils. 210Pbex was within the range of 47–2897, 114–5815, and 50–3829 Bq/kg for the leaves–stems,stems–rhizoids, and underlying soils, respectively.

In the leaves–stems and stems–rhizoids, the activity con-centrations of 7Be ranged from 19 to 1442 Bq/kg and from 28to 1005 Bq/kg, respectively (Table 2 and Fig. 1c). Our


Table2

Activities

ofanthropogenicandnaturalradionuclides

indifferentm

ossbody

partsandunderlying

soils

Station

Mossspecies

Sampletype

Activity

(Bq/kg,dry

weight)

210Pb

226Ra

210Pb e

x210Po

7Be

40K

238U

232Th

137Cs

BJ01

Herpetin

eurontoccoae

Leaves–stem

s47

±18

BDL

47±18

38±3

227±34

235±79

BDL

BDL

BDL

Stem

s–rhizoids

136±13

21±2

114±14

118±7

28±16

470±38

31±10

25±6

BDL

Underlyingsoil

74±6

22±1

52±6

84±4

25±6

650±23

37±7

40±4

2±1

BJ16

Herpetin

eurontoccoae

Leaves–stem

s2138

±47

BDL

2138

±47

920±35

674±32

188±64

BDL

BDL

24±4

Stem

s–rhizoids

1628

±45

BDL

1628

±45

987±37

42±27

226±52

BDL

BDL

44±5

Underlyingsoil

703±19

13±2

690±19

750±33

BDL

251±28

20±11

11±4

70±3

BJ17

Herpetin

eurontoccoae

Leaves–stem

s655±25

BDL

655±25

703±33

332±21

26±36

BDL

BDL

38±3

Stem

s–rhizoids

832±27

7±3

825±27

814±38

115±15

61±37

50±21

BDL

144±5

Underlyingsoil

77±10

27±2

50±10

322±16

BDL

673±33

58±18

34±5

6±2

QHX

Leptobryum

pyriform

eLeaves–stem

s179±15

8±3

171±16

164±11

223±27

258±45

BDL

7±7

BDL

Stem

s–rhizoids

361±33

23±5

339±33

279±15

178±36

308±92

BDL

31±16

3±6

Underlyingsoil

99±11

31±3

68±31

86±6

BDL

535±39

36±13

34±6

6±1

QHT

Hypnodendronreinwardtii

Wholeplant

1209

±27

15±2

1195

±27

805±43

19±11

458±36

15±11

7±6

2±1

QHY

Ditrichumpallidum

Leaves–stem

s241±18

BDL

241±18

124±9

578±26

285±36

BDL

BDL

BDL

Stem

s–rhizoids

710±73

11±9

699±73

508±85

758±90

295±86

BDL

22±26

5±5

Underlyingsoil

209±13

29±2

180±13

227±14

17±7

561±32

39±11

37±6

2±1

SHZB

Funaria

hygrom

etrica

Leaves–stem

s361±26

BDL

361±26

131±8

1238

±44

125±50

BDL

BDL

BDL

Stem

s–rhizoids

433±32

7±4

426±32

227±11

770±44

278±69

30±19

18±18

BDL

Underlyingsoil

77±7

25±1

52±8

82±5

13±6

504±21

42±7

37±3

BDL

JX01

Meteoriella

soluta

Leaves–stem

s618±31

17±4

602±31

279±17

365±32

284±68

BDL

31±10

BDL

Stem

s–rhizoids

731±41

11±4

720±42

656±44

127±35

212±66

33±19

35±11

BDL

Underlyingsoil

158±11

43±2

115±11

202±14

12±10

1245

±43

99±12

68±5

2±1

JX02

Ditrichumpallidum

Leaves–stem

s1241

±50

5±2

1236

±50

794±35

811±48

244±76

BDL

BDL

BDL

Stem

s–rhizoids

2569

±52

14±3

2555

±52

1302

±85

120±19

399±55

24±14

4±7

BDL

Underlyingsoil

2233

±44

7±2

2226

±44

1622

±25

63±14

631±61

BDL

33±7

BDL

JX03

Racom

itriumanom

odontoides

Leaves–stem

s2903

±92

6±5

2897

±92

1518

±80

1442

±74

140±86

BDL

BDL

BDL

Stem

s–rhizoids

5815

±201

BDL

5815

±201

3139

±69

1005

±118

205±186

BDL

BDL

BDL

Underlyingsoil

3848

±64

19±3

3829

±64

2235

±78

231±23

611±54

35±21

39±8

BDL

HN01

Syntrichia

norvegica

Leaves–stem

s1373

±30

7±3

1366

±30

1006

±91

642±26

114±32

BDL

9±6

BDL

Stem

s–rhizoids

1698

±44

16±3

1681

±44

1098

±84

89±14

116±51

BDL

19±13

BDL

Underlyingsoil

759±32

25±3

735±25

838±54

16±15

378±38

69±26

46±8

BDL

HN03

Hypnumplum

aeform

eLeaves–stem

s1278

±71

14±7

1264

±71

718±39

913±80

135±73

BDL

BDL

BDL

Stem

s–rhizoids

1719

±58

13±5

1706

±58

1214

±70

243±33

140±63

BDL

BDL

BDL

Underlyingsoil

897±20

23±2

874±20

731±57

40±11

315±26

45±10

36±5

2±1

FJ01

Funariahygrom

etrica

Wholeplant

545±34

15±5

530±35

203±12

258±27

236±50

BDL

238±17

BDL

Underlyingsoil

256±19

24±4

232±19

92±5

92±17

526±43

37±19

174±12

4±3

BDLbelowdetectionlevel


measurements of 7Be were comparable with the values report-ed at Sellafield, England (100–900 Bq/kg, Sumerling 1984),

and at Kaiga, India (234–1061 Bq/kg, Karunakara et al.2003). Generally, 7Be can be detected in just several

BJ01 BJ16 BJ17 QHX QHT QHY SH01 JX01 JX02 JX03 HN01 HN03 FJ010

500

1000

1500

2000

2500

3000

3500)thgie

wyrd

gk/qB(

ytivitcA

Leaves-stems Stems-rhizoids Underlying soil

210Po(a)


1000

2000

3000

4000

5000

6000(b) 210Pbex


300

600

900

1200

1500 (c)

)thgiew

yrdgk/q

B(ytivitc

A

7Be


25

50

75

100

125

150(d) 137Cs


200

400

600

800

1000

1200

1400(e)

)thgiew

yrdgk/q

B(ytivitc

A

40K


25

50

75

100

125

150(f) 238U


10

20

30

40

50(g)

)thgiew

yrdgk/q

B(ytivitc

A

Sample

226Ra


50

100

150

200

250 (h)

Sample

232Th

BJ01, BJ16, BJ17: Herpetineuron toccoaeQHX: Leptobryum pyriformeQHY, JX02: Ditrichum pallidumQHT: Hypnodendron reinwardtiiSHZB, FJ-1: Funaria hygrometricaJX01: Meteoriella solutaJX03: Racomitrium anomodontoidesHN01: Syntrichia norvegicaHN03: Hypnum plumaeforme

Moss species information:

Fig. 1 Activity concentrations of 210Po (a), 210Pbex (b),7Be (c), 137Cs (d), 40K (e), 238U (f), 226Ra (g), and 232Th (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


millimeters of nondisturbed topsoil. However, 7Be was detect-ed in most underlying soils (from 12 to 231 Bq/kg) except forthree samples (BJ16, BJ17, and QHX), although only the top1-cm layer of the underlying soils was collected after remov-ing the moss carpets. Anthropogenic 137Cs was detected onlyin some moss samples and underlying soils (Fig. 1d), with thehighest activity concentration (144 ± 5 Bq/kg) in the stems–rhizoids of moss (Herpetineuron toccoae) at location BJ17.

The activity concentration of 40K was detected in all mosssamples and underlying soils (Table 2 and Fig. 1e). In theleaves–stems and stems–rhizoids, the activity concentrationof 40K ranged from 26 ± 36 to 458 ± 36 Bq/kg and from 61± 37 to 470 ± 38 Bq/kg, respectively. The 40K activity in un-derlying soils ranged from 251 ± 28 to 1245 ± 42 Bq/kg, withthe highest value found at site JX01.

The activity concentrations of 238U, 226Ra, and 232Th arepresented in Table 2 and Fig. 1 f–h. The value of 238U rangedfrom below detection level (BDL) to 15 ± 11 Bq/kg, fromBDL to 50 ± 21 Bq/kg, and from BDL to 99 ± 12 Bq/kg inthe leaves–stems, stems–rhizoids, and underlying soils, re-spectively. The activity concentrations of 226Ra ranged be-tween BDL and 17 ± 4 Bq/kg, between BDL and 23 ± 5 Bq/kg, and between 7 ± 2 and 43 ± 2 Bq/kg in the leaves–stems,stems–rhizoids, and underlying soils, respectively. 232Th wasnearly undetectable in most moss samples except for the mosssample at location FJ01 (up to 238 ± 16 Bq/kg), and it wasmainly detected in underlying soils for all samples, with arange of 11–174 Bq/kg.

Concentration ratio and translocation factorof radionuclides

The CRs calculated from the activity concentrations of radio-nuclides in soils and mosses are presented in Table 3. The CRsfor 226Ra, 238U, 232Th, and 40K ranged from 0.25 to 2.03 (n =10), from 0.34 to 0.85 (n = 4), from 0.12 to 1.37 (n = 8), andfrom 0.09 to 0.90 (n = 12), respectively. However, the concen-tration ratios of 210Pb (or 210Pbex),

210Po, and 7Be were higherthan unity for almost all of the moss samples (Table 3). TheCRs of 137Cs were higher than unity for samples BJ17 (23.21)and QHY (3.47) and lower than unity for samples BJ16 (0.62)and QHX (0.56).

The TFs for these radionuclides are shown in Table 4. Thetranslocation factors of 238U and 232Th for all the moss sam-ples could not be calculated due to the undetectable activityconcentration in the moss leaves–stem parts. The TFs of 7Bewere higher than unity for almost all of the moss samples(0.76–16.25). The TFs for 210Pb (or 210Pbex) and

210Po rangedfrom 0.34 to 1.31 (n = 11) and from 0.24 to 0.93 (n = 11),respectively. The TFs of 40K for all the moss plants changedfrom 0.42 to 1.34 (Table 4). The TFs of 226Ra and 137Cs couldbe calculated for only several moss samples (Table 4).

Discussion

Factors influencing activity concentrationsand distribution features of the radionuclides in mosssamples

The accumulation processes of radionuclides in bryophytesare complicated and may be influenced by a number of factors(moss species, topography, geology, meteorology, etc.). Atsites JX01, JX02, and JX03, we collected three different mossspecies, Meteoriella soluta, Ditrichum pallidum, andRacomitrium anomodontoides, respectively. Although theygrew in a similar environment (in a small town in NanfengCounty, a small county in Jiangxi Province, China), we foundthat the activity concentrations of the analyzed radionuclides(210Po, 210Pbex, and

7Be) varied significantly in these threemoss samples (Fig. 1). This variation indicates that the signif-icant intrinsic factor may be the moss species (Sert et al. 2011;Boryło et al. 2017). Other intrinsic factors may pertain to themorphological structure of the bryophytes (especially the sur-face morphology of the leaves), different uptake mechanisms,and the growth speed (some mosses grow faster than others).Unfortunately, we lack sufficient evidence to further discussthese effects.

Other extrinsic factors that could affect the accumulationprocesses of radionuclides in the moss body include weatherconditions (humidity, rainfall, etc.), artificial addition of radio-nuclides by human activity, geographical characteristics(whether it is easy to obtain water, whether it is easy to facethe sun, etc.), competition for living space and nutrientsbetween bryophytes and higher plants, and the degree oflocal shelter provided by trees. For example, Kamar et al.(2017) found that the activities of 7Be in mosses collectedunder trees were two times lower than those in mosses col-lected in open fields, and Boryło et al. (2017) noted that somemoss species growing in the lower parts of trees wereprotected from direct radioactive deposition. However, it isbeyond the scope of this study to discuss all of these factors.Here, we focused on the sources of the radionuclides and thepossible accumulation process during moss growth based onthe existing data.

PCA is one of the most widely used techniques to reducethe dimensionality of a dataset in order to preserve most of theinformation. In the present study, PCAwas performed on thenatural and anthropogenic radionuclide measured in theleaves–stems, stems–rhizoids, and underlying soils to identifythe similarities and differences among these radionuclides.Figure 2 a–c show the score plot between the first two princi-pal components (component 1 vs. component 2). The first twoprincipal components explained about 66.02, 67.10, and74.42% of the total variance for the leaves–stems, stems–rhi-zoids, and underlying soils, respectively (Fig. 2a–c). The x-axis represents component 1, while the y-axis represents


Table3

The

values

ofradionuclid

econcentrationratio

s(CR)fortheanalyzed

mossplants(notethatCRsforsampleQHTwerenotcalculated)

Sam

plesites

Mossspecies

Concentratio

nratio

(CR)

210Pb

226Ra

210Pb

ex210Po

7Be

40K

238U

232Th

137Cs

BJ01

Herpetin

eurontoccoae

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

Herpetin

eurontoccoae

2.32

±0.09

–2.36

±0.09

1.32

±0.08

–0.90

±0.23

––

0.62

±0.07

BJ17

Herpetin

eurontoccoae

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

pyriform

e3.65

±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

Ditrichumpallidum

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

hygrom

etrica

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

Ditrichumpallidum

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

Racom

itriumanom

odontoides

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

Hypnumplum

aeform

e1.92

±0.08

0.56

±0.24

1.95

±0.08

1.66

±0.16

6.11

±1.91

0.44

±0.20

––

–

FJ01*

Funaria

hygrom

etrica

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

–

–notavailable

*CRvalues

ofthissamplewerecalculated

from

thewholemossplantsandtheunderlying

soil


component 2, so points close to each axis are associated withcomponent 1 or component 2. The graphs (Fig. 2a–c) clearlyindicate that there are two different groups of radionuclides.Component 1 represented the group of radionuclides fromatmospheric sources (210Po, 210Pb, 210Pbex,

7Be, and 137Cs),and component 2 represented the other group of radionuclidesfrom terrestrial sources (40K, 226Ra, 238U, and 232Th). Asshown in Fig. 2 a, a plot of the leaves–stem parts of mosssamples, the loading factors for 7Be and 137Cs were slightlydifferent from those for 210Po and 210Pb, but as shown in Fig.2 b and c, both 7Be and 210Po–210Pb pairs have similar loadingfactors. These figures indicate that moss plants and underlyingsoils are not sensitive enough to distinguish the productionand deposition differences in these airborne radionuclides(7Be, 210Po, and 210Pb), although 7Be mainly originates fromnuclear reactions in the stratosphere and upper troposphere,and 210Pb is generated from the decay of 222Rn in the atmo-sphere. The reason for this is that 7Be and 210Pb (includingdaughter 210Po) follow very similar transport and depositionprocesses of aerosols, and they have continuous and relativelyconstant deposition fluxes from the atmosphere. Unlike 7Beand 210Po–210Pb pairs, 137Cs was sporadically dischargedfrom atmospheric weapon testing and the Chernobyl incident,and most of it had been deposited on the earth’s surface sev-eral decades ago. These results imply that there are variousatmospheric processes and accumulation mechanisms affect-ing radionuclide activity concentrations in moss samples. Adetailed discussion about the accumulation processes of radio-nuclides in the moss body is given in the followingparagraphs.

Accumulation of 7Be, 210Po, and 210Pbexand the disequilibrium of 210Po and 210Pbex in mossbody

Figure 1 c shows the levels of 7Be in moss tissues and under-lying soils. Based on these radionuclide activities, the

calculated CRs and TFs are displayed in Tables 3 and 4. TheCRs of 210Pb (or 210Pbex),

210Po, and 7Be were higher thanunity for almost all of the moss samples (Table 3) due to thehigher activity concentration in moss tissues and the loweractivity concentration in soils, especially in the case of 7Be.The activity concentrations of 7Be followed the order leaves–stems > stems–rhizoids ≫ underlying soils, which caused therelatively higher TFs of 7Be (higher than unity) for almost allof the moss samples (Table 4) and proved that 7Be mainlyaccumulated in the upper part of moss plants, especially inthe leaves–stems. As mentioned before, 7Be is formed by aspallation reaction between cosmic rays and the nucleus ofoxygen and nitrogen in the atmosphere (Du et al. 2015; Lalet al. 1958); hence, 7Be exists in surface air and wet and drydeposition samples. Krmar et al. (2016) observed that theatmospheric depositional 7Be measured in mosses dependedon cumulative precipitation. As shown in our results (Fig. 1c),7Be mainly accumulated in the leaves–stem parts of mossbody profiles. One possible mechanism for this phenomenonmay be related to the assumption that 7Be would not be mo-bilized and transported in the moss body. In other words, 7Bedeposited on the leaves of the moss is mainly retained andstored in the upper segment of the plants and this captured7Be will not be transferred down to the stems–rhizoid tissues.In the next growth cycle, new 7Be will again be captured bythe new moss leaves, but the old 7Be stored in the old leaves–stems will decay completely over time. The green parts ofmoss plants usually contain the last several years of annualgrowth segments. The half-life of 7Be is as short as 53 days;thus, the 7Be stored in the green parts (leaves–stems) ofmosses probably represented about 1 year (~ 7 half-lives of7Be) of accumulated 7Be fallout. Another completely differentmechanism for 7Be distribution in moss plants may be relatedto another assumption that moss plants may mistake Be for Kand that they would probably actively transport 7Be towardthe growing parts because mosses are able to translocate nu-trients from senescent parts (e.g., stems–rhizoids).

Table 4 The values of radionuclide translocation factors (TF) for the analyzed moss plants (note that TFs for samples QHT and FJ01 were notcalculated)

Sample sites Moss species Translocation factor (TF)

210Pb 226Ra 210Pbex210Po 7Be 40K 238U 232Th 137Cs

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 ± 0.11BJ17 Herpetineuron toccoae 0.79 ± 0.04 – 0.79 ± 0.04 0.86 ± 0.06 2.89 ± 0.42 0.42 ± 0.64 – – 0.27 ± 0.02QHX 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


Additionally, 7Be might also be adsorbed by ion exchange tothe cell walls of the leaves, and because the leaves representmost of the total surface, they would also help to accumulatemost of the 7Be that the plants may encounter. However, con-sidering that new green segments and old brown stems–rhizoid parts can be several years old, differences in 7Be con-centrations between the leaves–stems and stems–rhizoid partsshould be more than two orders of magnitude because of the

short half-life of 7Be. However, the results in Table 2 showthat in some cases, the differences were significantly lower;furthermore, in one example, the 7Be concentration washigher in the stems–rhizoids than in the leaves–stems (e.g.,sample QHY). It is more likely that both parts of the mosscan accept 7Be regardless of the purpose because in the case ofdry deposition, if 7Be is almost completely stopped in theupper green part of the moss, during wet deposition, it is notpossible to stop 7Be from reaching the lower part of the moss.Although we do not know which mechanism is the dominantone in reality, the results show that the activity concentrationsof 7Be in the stems–rhizoids were generally at low levels ornearly BDL. Investigating the intrinsic mechanisms for metalaccumulation in moss would benefit both environment mon-itoring application and our understanding of plant physiology.In addition, because of the covering by the moss carpet, 7Be inthe underlying soils was also nearly undetectable.

It was observed that most of the activity concentrations of210Po and 210Pbex were concentrated in the leaves–stems andstems–rhizoids (Fig. 1a, b) compared to those in underlyingsoils. And in the majority of the samples, the calculated CRsfor 210Pb (or 210Pbex) and

210Po were higher than 1 (Table 3).The TFs of 210Pb and 210Po were lower than 1 (Table 4) and theanalyzed moss stems–rhizoids contained more 210Po and 210Pbwhen compared with the leaves–stems. These CRs and TFs forairborne 210Po, 210Pb, and 7Be implied that the importantsource might be atmospheric fallout, while internal processesduring moss growth played a minor role. Table 5 represents theresults of 210Po and 210Pb reported in the literature for mossplants. Most of the 210Po and 210Pbex activity concentrationsfrom this study were higher than the values from around theworld found in the literature. Moreover, as shown in Table 5,210Po is in disequilibrium with 210Pb, not just in this study, butalso in other investigations. For underlying soils at some sites(BJ16, JX02, JX03, HN01, and HN03), 210Po (750–2235 Bq/kg) and 210Pbex levels (690–3829 Bq/kg) were higher than theaverage activity concentration levels of 210Po and 210Pb in var-ious soils (20–240 Bq/kg, reviewed by Persson and Holm(2011)), which indicated that the elevated levels of 210Po and210Pb in underlying soils may be attributed to the introductionof the detritus/fragments of moss plants.

The 210Po/210Pb activity ratios in moss plants and underly-ing soils are presented in Table 6. A lower level of 210Po relativeto that of 210Pb in the leaves–stems and stems–rhizoids wasobserved for nearly all samples. In addition, the 210Po/210Pbdisequilibrium was stronger in the leaves–stems than in thestems–rhizoids. These results indicated that the source of210Po and 210Pb in moss plants was mainly atmospheric.However, 210Po was nearly in equilibrium with 210Pb in theunderlying soils for most of the sites. 210Po/210Pb activity ratiowas reported in the literature to be > 1 in many moss samplescollected around coal-fired power plants (1.0–1.9, Uğur et al2003; 1.0–1.8, Sert et al. 2011; 1.1–2.0, Bakar et al. 2014).

Fig. 2 Component plot in a rotated space for 210Po, 210Pb, 210Pbex,7Be,

137Cs, 40K, 238U, 226Ra, and 232Th the in leaves–stems (a), stems–rhizoids(b), and underlying soils (c)


Table5

Com

parisonof

210Poand

210Pbactiv

ityconcentrations

(Bq/kg

dryweight)in

mosssamples

intheliterature

Location

Plant

type

210Po

210Pb

Num

berof

samples

Mossspecies

References

Svalbard

archipelago,Norway

Leaves–stem

s,moss

38–920

47–2138*

3Herpetin

eurontoccoae

Thisstudy

Stem

s–rhizoids,m

oss

118–987

114–1628*

China

Leaves–stem

s,moss

124–1518

171–2897*

8Leptobryum

pyriform

e,Ditrichumpallidum,F

unaria

hygrom

etrica,M

eteoriella

soluta,R

acom

itrium

anom

odontoides,and

Hypnumplum

aeform

eStem

s–rhizoids,m

oss

227–3139

339–5815*

Eastern

MediterraneanSearegion

(Syriancoastalm

ountains

series)

Wholeplant,moss

341–2119

165–2392

33Lycopodium

cernuumandFunaria

hygrom

etrica

Al-Masrietal.(2005)

NoviS

ad,S

erbia

Green

partof

themoss

–556±113

55Hypnumcupressiform

eKrm

aretal.(2016)

Peninsular

Thailand

Wholeplant,moss

–135–1630

46**

Wattanavateeetal.(2017)

LodzCity,P

oland

Wholeplant,moss

50–450

–180

Pleuroziumschreberi

Długosz-LisieckaandWróbel(2014)

SobieszewoIsland

innorthern

Poland

Wholeplant,moss

133–501

–70

DicranumscopariumandPleuroziumschreberi

Boryłoetal.(2017)

Kaiga

nuclearpower

plantsite

inSo

uthIndia

Wholeplant

2724

±13

–2

Pterobryopsistumida(H

ook.)Dix.

Karunakaraetal.(2000)

Coal-firedpower

plantsin

Som

aand

Yatagan,w

estern

Turkey

Wholeplant,moss

124–1125

94–724

78Tortella

tortuosa,H

omalothecium

sericeum

,Pterogonium

graciale,Isotheciumalopecuroides,Didym

odon

acutus,

Hypnumlacunosum,H

ypnumcupressiform

e

Sertetal.(2011)

Çan

coal-fired

power

plant,Turkey

Wholeplant,moss

151–550

219–724

8Hypnumcupressiform

eBelivermişetal.(2016)

Therm

alpower

plantand

coalmine

area,southernBrazil

Wholeplant,moss

107–721

–4

Cylindrocolea

rhizantha(M

ont.)

R.M

.Schust.and

Sematophyllu

mgalip

ense

(Müll.Hal.)Mitt.

Galhardietal.(2017)

Uraniferous

coal-fired

power

plant

inwestern

Turkey

Wholeplant,moss

256–1228

200–650

6Grimmia

pulvinataandHypnumcupressiform

eUğuretal.(2003)

SouthSh

etland

archipelago,Antarctic

Wholeplant,moss

–21–93

6Polytrichum

alpinumandDrepanoclatus

uncinatus

Godoy

etal.(1998)

Different

Belarus

regions

Wholeplant,moss

–141–575

63Pleuroziumschreberi

Aleksiayenaketal.(2013)

Slovakia

Wholeplant,moss

–330–1521

11Hylocom

iumsplendens

–notavailable

*Denotes

210Pb

exactiv

ityconcentrationvalue.Due

tothevery

lowlevelo

f226Rain

mosses,the210Pb e

xvalueisnearly

equaltothe210Pbvalue

**Thisresearch

investigated

17mossspecies,which

includeOctoblepharum

albidum

Hedw.,Himantocladium

sp.,Leucobryum

aduncum

Dozy&

Molk.,Th

uidium

sp.1,Barbella

asp.,Hyophila

cf.

involute

(Hook.

f.)A.Jaeger,Arthrocormus

schimperiDozy&

Molk.,Leucolom

asp.,Pyrrhobryum

spinifo

rme(H

edw.)Mitt.,Th

uidium

sp.2,Mitthyridium

sp.,Aerobryopsissp.,Neckeropsissp.,

Syrrhopodoncf.japonicus

(Besch.)Broth,L

eucobryumsanctum(Brid.)Ham

pe,L

eucophanes

glaucum(Schwaegr.)Mitt.,andHypnaceae

sp.


In contaminated sites, 210Po and 210Pb can diffuse via flyash, in which the 210Po concentration is about two timeshigher than that of 210Pb (UNSCEAR 2000; Uğur et al.2003). Moreover, the boiling point of 210Po (962 °C) is muchlower than that of 210Pb (1749 °C) (Uğur et al. 2003), andthere may be an additional input of 210Po around coal-firedpower plants because the chimney gases carry the volatile210Po. However, our sampling sites were not in the vicinityof any industrial pollution sources. As mentioned before, thePCA results indicated atmospheric sources of 210Po and 210Pb.The main source of 210Po and 210Pb entering the mosses is theexhaled radon gas from the surface layers of the earth’s crustinto the atmosphere. In the atmosphere, 222Rn decays with theformation of the daughter radionuclides 210Pb and 210Po.Because of the short residence times of aerosols (several daysto several weeks) in the troposphere and planetary boundarylayer, the ratio of 210Po/210Pb in aerosols and rainwater sam-ples is typically < 0.1–0.2 (Baskaran 2011). Hence, 210Po ac-tivity in these moss plants was composed of 210Po receivedfrom the atmosphere and produced by 210Pb decay in the mossbodies. Except for site BJ17 (210Po was nearly in equilibriumwith 210Pb in the leaves–stems and stems–rhizoids), the210Po/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 bod-ies were much higher than those in aerosols or rainwater sam-ples (from < 0.1 to 0.2, Baskaran 2011), which may indicatethat 210Pb was retained in the moss plants for a long time andthat the ingrowth of 210Po caused the increase in the210Po/210Pb ratio.

There was a strong correlation between 210Pbex and210Po

in moss samples and underlying soils (leaves–stems: r = 0.94,p < 0.05; stems–rhizoids: r = 0.98, p < 0.05; underlying soil:r = 0.98, p < 0.05, Fig. 3a), which indicates that the majorcontributor of 210Po was 210Pb decay. The lower correlationbetween 7Be and 210Pbex in moss and soil samples (Fig. 3b)indicated that the accumulation process of 7Be was to someextent different from that of 210Pb.

Sources and accumulation of 137Cs

137Cs was detected only in some moss samples and soils col-lected from Yellow River Station, the Svalbard archipelago inNorway (sites BJ01, BJ16, and BJ17), and Xining, QinghaiProvince in China (sites QHX and QHY) (Fig. 1d). The sourceof 137Cs in the Svalbard archipelago is linked to the globalfallout from atmospheric weapons testing in the 1950s and1960s, because Svalbard is considered to have been relativelyunaffected by fallout from the Chernobyl accident in 1986(Dowdall et al. 2005). The source of 137Cs in Xining maypertain to the global fallout and China’s nuclear weapon tests(Zeng et al. 2007; Wu et al. 2011). In addition, an additionalsource of the 137Cs in mosses in Xining is related to the redis-tribution of soil or dust during agricultural production and dust

Fig. 3 The correlation plots of activity concentrations measured inmosses and soils for a 210Po–210Pbex and b 7Be–210Pbex

Table 6 210Po/210Pb activity ratios in moss plants and underlying soils

Sample 210Po/210Pbex

Leaves–stems

Stems–rhizoids

Underlying soil

BJ01 0.81 ± 0.32 0.87 ± 0.10 1.13 ± 0.10

BJ16 0.43 ± 0.02 0.60 ± 0.02 1.06 ± 0.05

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

QHT 0.66 ± 0.03 – –

QHY 0.51 ± 0.05 0.71 ± 0.14 1.08 ± 0.09

SH01 0.36 ± 0.03 0.52 ± 0.04 1.06 ± 0.11

JX01 0.45 ± 0.03 0.89 ± 0.07 1.27 ± 0.12

JX02 0.63 ± 0.03 0.50 ± 0.03 0.72 ± 0.01

JX03 0.52 ± 0.03 0.53 ± 0.01 0.58 ± 0.02

HN01 0.73 ± 0.06 0.64 ± 0.05 1.10 ± 0.08

HN03 0.56 ± 0.04 0.70 ± 0.04 0.81 ± 0.06

FJ01 0.37 ± 0.03* – 0.35 ± 0.03

– not available

*This value is the 210 Po/210 Pb ratio in the whole moss plant


storms. The levels of 137Cs in moss bodies ranged from 24 to144 Bq/kg for samples in Svalbard, which are in good agree-ment with the levels reported by Dowdall et al. (2005) (11–292 Bq/kg) and Aarkrog et al. (1984) (230 Bq/kg). At siteBJ16, the levels of 137Cs followed the order of underlying soil> stems–rhizoids > leaves–stems, while at BJ17, 137Cs mainlyaccumulated in the leaves–stems and stems–rhizoids, and atBJ01, 137Cs was only detected in the soil. For samples collect-ed in Xining, the activity concentrations of 137Cs were low (<6 Bq/kg) in the stems–rhizoids and soils and below detectionlevel in the leaves–stem parts for all samples. Hence, the CRsof 137Cs were only calculated for several moss samples (BJ17,QHY, BJ16, and QHX, see Table 3). However, the TFs of137Cs were available only for two moss samples (Table 4,BJ16 (0.55 ± 0.11) and BJ17 (0.27 ± 0.02)).

As mosses have no root system, the uptake of nutrientsfrom the substrate may be insignificant (Krmar et al. 2013).However, this may be different for different moss species be-cause the leaves, stems, rhizoids, and paraphyllia can worktogether and absorb nutrient solutions from the soil to theupper parts of the plants. The effectiveness of this type ofabsorption depends on the specifics of the moss plant mor-phology.Whether the plant has a short stem that is anchored tothe soil by rhizoids (as in Funaria) or an elongated, creepingstem (as in Hypnum) that has virtually no direct contact withthe soil can have a marked difference. Hence, in case of 137Cs,mosses would probably mistake it for K and try to absorb itfrom soil solution in some specific or extreme situation. Allthese features may contribute to the distribution of 137Cs in themoss body. Moreover, because of the absence of the cuticle inthe leaves, the uptake of 137Cs could occur through ion-exchange processes directly from the atmosphere via wetand dry deposition (Uğur et al. 2003). If the 137Cs that accu-mulated in a certain layer of the moss does not redistribute ortransfer to the rest of the body, then the 137Cs peak recorded inthe moss body profile may correspond to 137Cs fallout events.Although, as with K and Na, there is a strong likelihood thatCs will be redistributed inside the moss body, the 137Cs signalfrom Chernobyl or the 1963 global fallout events will still bestored in the moss body because of the relatively long “mem-ory” and long life of moss. Unfortunately, because of the dif-ficulties in dividing the whole moss plant body profile intomore segments, we only divided the moss body into two seg-ments (leaves–stems and stems–rhizoids). Hence, we were notable to determine the vertical distribution of the 137Cs activityconcentration in moss body profiles with a higher resolution.

Assuming that the 137Cs in moss samples from Svalbardwas entirely from global fallout and not from the Chernobylaccident, then it is reasonable to speculate that the moss fromBJ17 experienced and recorded the 137Cs fallout event.Moreover, assuming that the 137Cs fallout event recorded bythe moss corresponded to the year 1964 although the atmo-spheric weapons testing occurred in the 1950s–1960s, then the

age of the moss plants at site BJ17 can be calculated to bemore than 53 years old (2017–1964 = 53 years). Interestingly,the moss body distribution of 137Cs at site BJ16 was similar tothat in moss at site BJ17, but the 137Cs activity concentrationsin the soils were very different. The moss plants at site BJ16might have started to grow after the first 137Cs global falloutevents based on the activity concentrations of 137Cs measuredin the soil; thus, it can be deduced that the moss plants at BJ16are younger (< 53 years) than the moss at BJ17. In addition,we found that most of the 137Cs accumulated in the moss body(sites BJ16, BJ17), and consequently, the underlying soilremained relatively unpolluted. In other words, without amoss carpet covering the underlying soil, the 137Cs levels inthe underlying soil would be higher than the current statebecause of the global fallout of 137Cs. However, in contrast,we detected fairly high levels of 137Cs in feces samples fromreindeer (26 ± 1 Bq/kg, unpublished data) and rabbits (40 ±1 Bq/kg, unpublished data) in Svalbard. The vegetation in theregion of the Yellow River Station on Svalbard is mainlymosses and lichens. It is speculated that mosses and lichensare the major food sources for reindeer and rabbits. The 137Csin the reindeer and rabbit feces indicated that the animals canmobilize 137Cs in moss (or lichen) and transfer it to the soil orthe ecosystem. Generally, it is recognized that radionuclidesfrom mosses are not likely to be transferred to other parts ofthe ecosystem and that mosses are a secure sink for radionu-clides because moss plants tend to decay very slowly.However, herbivores (e.g., rabbits, reindeer, horses, insects,etc.) can access this sink and induce the diffusion of 137Cs toother parts of the ecosystem. Further studies are needed todetermine the adverse effects of 137Cs and other radionuclideson animals that feed on mosses.

Weak accumulation of terrestrial radionuclidesin moss samples

The activity concentrations of 40K in moss samples werehigher than the values for 238U, 226Ra, and 232Th (Fig. 1e–h). In all cases, 40K activity concentrations were detected inthe order of leaves–stems < stems–rhizoids < underlying soils(Fig. 1e). The CRs of 40K ranged from 0.09 to 0.90, whichimplied the existence of a weak 40K transfer from the soil tothe moss body. Lower 40K content in mosses compared tothose in the underlying soil has been previously reported(Dowdall et al. 2005; Dragović et al. 2010; Eckl et al. 1986).Potassium is a necessary element for the metabolic processesof plants; thus, the source of 40K for moss plants may be dustor tiny soil particles carried via dry deposition. The directuptake of 40K by moss plants from the underlying soil mayrepresent an alternative pathway because the 40K activity con-centration in the stems–rhizoid parts was slightly higher thanthat in the leaves–stem parts. In addition, the TFs of 40K in twomoss samples were higher than unity (JX01, Meteoriella


soluta, 1.34 and JX03, Racomitrium anomodontoides, 1.33),which indicated that 40K can be transferred and concentratedto the green parts of moss plants.

The 238U, 226Ra, and 232Th activity concentrations in theleaves–stems were generally below the level of detection, al-though low levels of these nuclides were found in the stems–rhizoids for some moss samples. Hence, the CRs of 238U,226Ra, and 232Th for only several moss samples were calcu-lated, and the TFs of 238U and 232Th were not calculated for allof the moss samples. The nearly below detectable levels ofthese terrestrial radionuclides in moss samples indicate thatthey do not have metabolic use for growth. Mosses tend toabsorb nutrients via contact with water rather than from theunderlying substrate. However, one exception is the mosssample FJ01 (Funaria hygrometrica, Fig. 1h). At this site,the moss plants were taken from one big stone on the campusof Xiamen University, and this stone was covered with a layerof weathered rock detritus and some decaying branches andleaves. The activity concentration of 232Th (238 ± 17 Bq/kg)in the whole plants was higher than that in the underlyingsubstrate materials (weathered rock detritus) (174 ± 12 Bq/kg) and much higher than that in any other sample (Fig. 1h).These results may support the notion that the accumulation of

232Th in mosses can occur by direct uptake from the substratein certain circumstances.

Comparison of CRs and TFs of radionuclidesfor different moss species

When CRs and TFs for the different moss species ana-lyzed here are compared, it can be obviously found thatthey are species-specific (Tables 7 and 8). All the mossspecies showed great ability in interception and retentionof airborne radionuclides (e.g., CRs of 210Pb, 210Po, and7Be > 1), although there are some interspecies differences.The average CR for 7Be in Ditrichum pallidum andFunaria hygrometrica was up to 20-fold higher than thatfor Herpetineuron toccoae and up to 3-fold higher thanthat for other species (Table 7). However, some mossspecies showed undetectable accumulation abilities forsome te r res t r i a l rad ionuc l ides (U, Th , and Raisotopes) because the CRs could not be calculated forsome moss species or the calculated CRs were as low as0.17 (Table 7). Although the average TFs for 7Be in allthe moss species were higher than unity, the interspeciesdifferences of mosses were still significant. The TFs of

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

Moss species 210Pb 226Ra 210Pbex210Po 7Be 40K 238U 232Th 137Cs

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 –

Racomitriumanomodontoides

1.51 – 1.52 1.4 4.35 0.17 – – –

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

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

Moss species 210Pb 226Ra 210Pbex210Po 7Be 40K 238U 232Th 137Cs

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


7Be in Herpetineuron toccoae (9.12) and Syntrichianorvegica (7.22) were up to three times higher than thosefor other species. Two moss species showed obvioustransfer and accumulation of 40K from the stems–rhizoidparts to the leaves–stem parts based on the calculated TFs(1.34 for Meteoriella soluta and 1.33 for Racomitriumanomodontoides) (Table 8). However, the average TFsof 238U and 232Th for all the moss species (Table 8) couldnot be calculated due to the undetectable activity in themoss leaves–stem parts. It should be noted that inassessing accumulation and transfer of radionuclides tomosses, the effect of age differences and living conditionsbetween moss plants was not taken into consideration.

Conclusion

In this study, we measured the activity concentrations of210Po, 210Pb (210Pbex),

7Be, 137Cs, 40K, 238U, 226Ra, and232Th in the leaves–stems and stems–rhizoid parts of mossplants and underlying soils. The PCA results were used todivide the studied radionuclides into an airborne group(210Po, 210Pb, 7Be, and 137Cs) and a terrestrial group (40K,238U, 226Ra, and 232Th). 137Cs was only detected in mosssamples from two areas: the Yellow River Station on theSvalbard archipelago and Xining, Qinghai Province. The137Cs activity concentrations in moss plants were much higherthan those in underlying soils, which indicated that mosses actas filters and prevent the deposition of radioactive fallout ma-terials in the underlying soil. Most of the 210Po and 210Pbexwere concentrated in the stems–rhizoid parts, and we hypoth-esize that the dead and decaying moss plants could increasethe 210Po and 210Pb levels in the underlying soils. In addition,the strong disequilibrium between 210Po and 210Pb was foundin the leaves–stem parts. 7Be was mainly accumulated in theleaves–stem parts of moss plants. Positive correlations wereobserved between 210Po and 210Pb, but there were lower cor-relations between 7Be and 210Pb, which indicated that theuptake mechanisms of these radionuclides were different, tosome extent. Moreover, the activity concentrations of 40K inmost moss samples were much higher than those of 238U,226Ra, and 232Th because of the effective uptake and accumu-lation of potassium.

Acknowledgments We are grateful to Dr. Ruiliang Zhu, School of LifeScience, East China Normal University, for his advice and guidance inmoss species identification.We would like to thank the group members ofthe RIC team in East China Normal University for their help in sampling.We would also like to thank the in-depth reviews of two anonymousreviewers.

Funding information This study was partly supported by the NaturalScience Foundation of China (grants 41576083, 41706089, and41706083).

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Accumulation of natural and anthropogenic radionuclides in body … · 2019-12-30 · and Wróbel (2014) investigated the 210Po activity concentra- tions in 180 moss and lichen samples