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Identifying the origin of atmospheric inputs of trace elements in the Prades Mountains (Catalonia) with bryophytes, lichens, and soil monitoring Ander Achotegui-Castells, Jordi Sardans, Àngela Ribas & Josep Peñuelas

Environmental Monitoring and Assessment An International Journal Devoted to Progress in the Use of Monitoring Data in Assessing Environmental Risks to Man and the Environment ISSN 0167-6369 Volume 185 Number 1 Environ Monit Assess (2013) 185:615-629 DOI 10.1007/s10661-012-2579-z

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Author's personal copy Environ Monit Assess (2013) 185:615–629 DOI 10.1007/s10661-012-2579-z

Identifying the origin of atmospheric inputs of trace elements in the Prades Mountains (Catalonia) with bryophytes, lichens, and soil monitoring Ander Achotegui-Castells & Jordi Sardans & Àngela Ribas & Josep Peñuelas

Received: 6 September 2011 / Accepted: 17 February 2012 / Published online: 11 April 2012 # Springer Science+Business Media B.V. 2012

Abstract The biomonitors Hypnum cupressiforme and Xanthoria parietina were used to assess the deposition of trace elements and their possible origin in the Prades Mountains, a protected Mediterranean forest area of NE Spain with several pollution sources nearby. Al, As, Cd, Co, Cu, Cr, Ni, Pb, Sb, Ti, V, and Zn were determined in 16 locations within this protected area. Soil trace element concentrations were also ascertained to calculate enrichment factors (EF) and use them to distinguish airborne from soilborne trace element inputs. In addition, lichen richness was measured to further assess atmospheric pollution. EF demonstrated to be useful not only for the moss but also for the lichen. Cd, Cr, Cu, Ni, and Zn presented values higher than three in both biomonitors. These trace elements were also the main ones emitted by the potential sources of pollutants. The distance between sampling locations and potential pollution sources was correlated with the concentrations of Cu, Sb, and Zn in Electronic supplementary material The online version of this article (doi:10.1007/s10661-012-2579-z) contains supplementary material, which is available to authorized users. A. Achotegui-Castells : J. Sardans (*) : J. Peñuelas Global Ecology Unit CREAF-CEAB-CSIC, Edifici C. Universitat Autònoma de Barcelona, Bellaterra 08193 Barcelona, Spain e-mail: [email protected] À. Ribas Centre Tecnològic Forestal de Catalunya, 25280 Solsona, Spain

the moss and with Cr, Ni, and Sb in the lichen. Lichen richness was negatively correlated with lichen Cu, Pb, and V concentrations on dry weight basis. The study reflected the remarkable influence that the pollution sources have on the presence of trace elements and on lichen species community composition in this natural area. The study highlights the value of combining the use of biomonitors, enrichment factors, and lichen diversity for pollution assessment to reach a better overview of both trace elements’ impact and the localization of their sources. Keywords Biomonitors . Enrichment factor . Heavy metals . Hypnum cupressiforme . Species richness . Xanthoria parietina

Introduction The trace element inputs into the environment due to human activities have increased in the last decades (Nriagu and Pacyna 1988; Nriagu 1996; Peñuelas and Filella 2002). Since their accumulation may have unforeseeable biological effects, including chronic damage to ecosystems, effective large-scale monitoring networks for trace elements need to be developed (Bargagli et al. 2002; Gerdol and Bragazza 2006). However, monitoring anthropogenic air pollution is a very complex problem due to a variety of reasons: the great number of potentially dangerous substances, the difficulty in estimating bioavailability, the large spatial

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and temporal variation of pollution phenomena, the high costs of the recording instruments and hence the low sampling density of a purely instrumental approach (Nimis et al. 2000; Wolterbeek 2002). Lichens and mosses have been used as effective biomonitors of trace element atmospheric deposition since the 1960s, with a considerable number of papers being published during recent decades (Herpin et al. 1997; Carballeira et al. 2002; Spagnuolo et al. 2009; Sardans et al. 2010). The high surface/volume ratio of both lichens and mosses and their lack of welldeveloped cuticle and roots confer them with a high cation-exchange capacity (Bargagli 1998) and make them rely largely on atmospheric deposition for nourishment. They do not shed plant parts as readily as higher plants and accumulate persistent atmospheric pollutants to levels far greater than those found in air (Bargagli et al. 2002). These biomonitors can be used in two ways since they can reflect the deposition of airborne elements as well as its biological impact in organisms and soils. Bioaccumulation in tissues provides information on the uptake, the behavior, and the potential deleterious effects of trace elements on living organisms and in this way, their impact in trophic webs (Sardans and Peñuelas 2005). Bioaccumulation data also permits the study of possible synergism among different pollutants (Scerbo et al. 1999). Lichens, in addition to being useful as accumulating organisms, are the species of choice as bioindicators of air pollution, due to their high sensitivity to polluted environments (Nimis et al. 1990; Di Lella et al. 2004). In order to evaluate the impact of airborne pollutants using biomonitors, it is necessary to distinguish the soilborne and airborne origin of trace elements uptake and accumulation and their relative importance. With this aim, several enrichment factor (EF) approaches have been used to evaluate trace element concentrations in mosses (Sardans and Peñuelas 2006). When several methods have been compared in the same study, the equation employing the soil available forms of the elements analyzed has proved to be the most sensitive in determining the trace element enrichments from atmospheric inputs (Sardans and Peñuelas 2006, 2007; Sardans et al. 2008). In the case of lichen studies, it is considered that there is no need to use EF equations because the thalli are usually taken from 1 to 1.5 m above ground to prevent soil enrichment (Bargagli 1998; Brunialti and Frati 2007).

Environ Monit Assess (2013) 185:615–629

But as wind and animal activities can influence lichen uptake by carrying soilborne material, we hypothesized that the use of EF could be useful also in lichens to evaluate the influence of soilborne particles. The trace element pollution in remote natural areas that are within or near large urban and industrial regions deserves special attention. The most wellconserved areas of Europe are frequently near or surrounded by industrial areas and therefore they can be affected by trace element pollution (Sakalys et al. 2009; González-Miqueo et al. 2010). On a global scale, the most well-conserved and remote areas are increasingly more scarce and submitted to isolation in the middle of human-transformed territories. Our study was conducted in the Natural Park of Prades Mountains, a mountainous area surrounded by humanized plains in Catalonia. We focused on a quite small territory ca. 400 km2 and performed highdensity sampling to detect very detailed effects and to try to identify the pollution source. We aimed to: (1) determine the trace element accumulation in two of the most widespread biomonitors, the moss Hypnum cupressiforme and the lichen Xanthoria parietina in the Prades Mountains in order to assess air quality and the level of trace element impact on this forest ecosystem, (2) compare the behavior and sensibility of each biomonitor, (3) test different enrichment factor methods and possible improvements in their sensitivity with respect to plant concentrations, and (4) investigate the correlations of trace element concentrations, enrichment factors, and lichen richness with the distance from the potential sources of pollutants to assess the origins of trace element inputs.

Materials and methods Study area The study area is about 400 km2 coinciding mostly with the national protected area of Poblet forest and the future natural park of Prades Mountains (Catalonia, NE Spain). The zone is a Mediterranean mountainous area with an altitude above sea level from 250 to 1,200 m with the highest location at Turó de la Baltassana (1,201 m). There are a few little villages inside the park with no industrial activity, but this area is surrounded by significant pollution sources, mainly from the chemical industry such as petrochemical

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plants, and paper and glass industries. In the neighboring area, there is also a relatively big urban zone, Tarragona Metropolitan area, that includes the nearby city of Reus, and that gathers a population of 456,042 inhabitants (Fig. 1). Species studied The species chosen to carry out this study were the moss H. cupressiforme and the lichen X. parietina. These two species are widely distributed and abundant all across southern Europe (Nimis et al. 2001) and several studies have used them to determine trace element pollution (Scerbo et al. 1999; Brunialti and Frati 2007). Some such studies have been in Spain (Fernandez et al. 2000; Sardans and Peñuelas 2005), which allows comparison with previous works in order to make a precise assessment of pollution in the area. For more details of the species studied, see Electronic supplementary material (ESM).

Experimental design Sixteen sampling locations were homogeneously spread within the study area (Fig. 1) trying to capture the orography of the zone and to achieve the maximum homogenization of altitudes. The potential pollution sources were also taken into account, and the sampling locations were placed at different distances from local sources (Fig. 1). Sampling was conducted in April 2008 according to the protocol adopted within the European Heavy metal Survey (Rühling 1994). The sampling locations were at least 300 m away from highways and main roads and at least 100 m from any roads or houses in an area with slopes between 0% and 20%. The sampling location characteristics are listed in Table 1. Each sampling location included three subsample areas which measured 50×50 m each. In each one of these sub-areas, we sampled several thalli of the moss H. cupressiforme, six to ten thalli of the lichen X. parietina, a sample of soil, and determined the

Fig. 1 Map of the study zone. Red triangles the pollution foci, white squares sampling locations, gray scale altitudinal gradient, and letters meteorological station were the wind information was taken from (details in ESM Table S3). The scheme going out from Alforja illustrates how the sub-areas where organized within each sampling location

Pollution sources Sampling locations a-h Meteorological stations

344713 4579189

Rojalons

Montblanc 345850 4580903

340006 4583395

328564 4579576

Vilanova

Poblet

332904 4574803

Prades

339897 4580863

364

334307 4577238

Perrot

678

467

749

1004

1130

666

Abandoned field of Prunus dulcis and Olea europaea Abandoned field of Prunus dulcis and Olea europaea

Evergreen Quercus ilex forest

Field of Prunus dulcis and Olea europaea

Abandoned field of Corylus avellana


Pinus sylvestris and Quercus pyrenaica forest


Abandoned field of Prunus dulcis and Olea europaea Evergreen Quercus ilex forest

8,861 a (2,181) 6,657 a (208) 1,750 b (511) 3,280 a,b (184)

Hypnum cupressiforme Xanthoria patietina Hypnum cupressiforme Xanthoria patietina

Xanthoria patietina

0.032 b (0.005)

1.10 a,b (0.084)

1.31 a (0.363)

1.72 a (0.398)

0.161 b (0.009)

0.549 b (0.047)

0.359 b (0.114)

0.653 b (0.127)

5,070 a,b (341)

0.240 b (0.048)

2,053 b 0.810 a,b (153) (0.105)

2,891 b (83.9)

Xanthoria patietina

Hypnum cupressiforme

640 b (334)

4,222 a,b (269)

Xanthoria patietina Hypnum cupressiforme

2,372 b (782)


1.15 (0.666)

0.460 b (0.055)

0.160 (0.104)

2.25 a (0.706)

0.503 (0.259)

0.584 b (0.091)

0.622 (0.203)

1.00 a,b (0.549)

0.641 (0.362)

0.286 b (0.038)

0.538 (0.213)

0.550 b (0.260)

0.542 (0.045)

0.249 (0.107)

2.67 a (0.131)

0.459 (0.364)

0.050 b 0.824 a,b (0.002) (0.051)

0.158 b (0.019)

0.116 b (0.020)

0.132 b (0.007)

0.430 a 0.935 a,b (0.096) (0.206)

0.309 a (0.035)

0.116 b (0.008)

0.094 b (0.009)

0.052 b (0.002)

0.084 b (0.014)

0.114 b (0.052)

Xanthoria patietina

4,225 a,b 0.623 a,b (172) (0.137)

0.088 b (0.011)

Hypnum 6,355 a,b 0.740 a,b cupressiforme (598) (0.070)

0.246 b (0.084)

0.083 b (0.020)

0.113 b (0.004)

2,532 b (96.5)

Xanthoria patietina

0.419 b (0.040)

0.205 b (0.008)

0.067 b (0.011)

0.092 b (0.020)

0.364 b (0.046) 0.533 b (0.100)

0.084 b (0.004)

0.452 b (0.111)

0.490 b (0.003)

0.319 b (0.075)

3,100 b (284)

2,642 b (141)


1,439 b (371)

2,589 b (228)


3,254 b (1,642)


4,893 a,b (124)

0.838 (0.489)

Co

0.074 b 0.971 a,b (0.009) (0.284)

Cd

Xanthoria patietina

As

0.100 b (0.003)

Al

Hypnum 6,594 a,b 0.894 a,b cupressiforme (2,124) (0.069)

Species

27.4 b (7.75)

6.89 (0.515)

24.6 b (5.34)

2.84 (0.303)

25.7 b (11.9)

20.3 (8.87)

13.1 b (6.20)

9.15 (3.08)

4.37 (0.706)

11.4 b (1.31)

10.0 (1.56)

8.89 b (0.400)

8.60 (1.41)

8.04 b (0.759)

5.03 (0.331)

9.87 b (0.490)

4.21 (0.986)

8.75 b (2.00)

15.3 (8.31) 132 a (44.8)

7.36 (1.07)

6.03 b (0.113)

5.39 (0.271)

6.20 b (0.846)

3.76 (0.866)

4.44 b (0.505)

5.63 (0.093)

6.93 b (1.15)

7.40 (0.380)

9.38 b (1.11)

Cu

14.3 a,b (4.82)

11.9 (4.17)

14.1 b (3.42)

24.3 (14.5)

1.24 b (0.458)

24.9 (10.7)

21.9 b (14.9)

10.1 (3.00)

28.6 a,b (15.2)

9.57 (3.53)

Cr

15.2 b (3.81)

3.63 (0.681)

15.5 b (2.84)

3.47 (0.457)

14.2 b (6.41)

13.4 (5.62)

7.79 b (2.96)

6.20 (2.40)

69.8 a (23.3)

9.00 (4.34)

8.28 b (2.57)

8.03 (1.79)

7.74 b (1.79)

13.4 (7.01)

1.27 b (0.262)

13.1 (5.30)

12.1 b (2.11)

8.98 (1.05)

16.0 b (2.57)

6.43 (1.96)

Ni

1.24 b (0.318)

0.029 (0.011)

0.032 (0.015)

1.87 b (0.714) 6.08 a (1.71)

0.023 (0.007)

0.047 (0.020)

0.012 (0.007)

0.043 (0.023)

0.018 (0.010)

0.039 (0.008)

0.035 (0.014)

0.010 (0.006)

0.057 (0.028)

0.015 (0.008)

0.037 (0.014)

0.043 (0.019)

0.036 (0.014)

0.026 (0.015)

Sb

5.08 a,b (0.730)

8.92 a (1.75)

6.31 a (0.649)

1.23 b (0.058)

2.52 b (0.157)

1.99 b (0.624)

3.16 b (0.735)

2.57 b (0.210)

3.93 b (0.286)

3.52 a,b (0.589)

1.89 b (0.229)

1.37 b (0.366)

3.18 b (0.673)

3.12 b (0.098)

2.24 b (0.455)

3.55 a,b (0.854)

4.62 b (0.318)

Pb

5.68 a (1.93)

34.0 b (8.68)

9.02 b (1.42)

32.7 b (4.25)

8.93 b (4.14)

61.5 a (7.39)

87.8 a,b (24.8)

19.9 b (1.88)

4.0 b (2.24)

27.1 b (4.21)

11.0 b (1.80)

27.4 b (3.31)

4.46 a,b (0.893)

1.79 b (0.145)

5.81 a (0.403)

1.78 b (0.343)

4.73 a,b (0.658)

6.34 a (1.50)

2.52 a,b (0.175)

1.39 b (0.032)

3.33 a,b (0.768)

1.79 b (0.339)

3.08 a,b (0.247)

3.97 a,b (0.185)

1.91 b (0.170)

3.02 a,b (0.201)

17.5 b (0.832) 19.4 b (1.30)

1.93 b (0.317)

1.43 b (0.314)

1.93 b (0.538)

3.42 a,b (0.053)

3.92 a,b (0.367)

V

18.9 b (3.43)

7.99 b (3.58)

19.1 b (4.89)

20.5 b (0.191)

51.7 a (3.47)

118 a (59.1)

25.2 a,b (3.31)

Ti

30.4 a,b (4.05)

18.7 b (4.35)

37.8 a (3.25)

27.3 a,b (7.13)

41.3 a (4.06)

48.5 a (4.27)

21.8 b (0.300)

19.6 b (1.92)

29.8 a,b (3.22)

20.2 b (5.95)

26.8 b (1.82)

29.4 a,b (2.30)

38.1 a (1.95)

28.1 a,b (1.71)

20.0 b (1.09)

14.9 b (4.94)

26.1 b (3.16)

21.5 b (1.51)

31.5 a,b (2.20)

32.1 a,b (1.04)

Zn

618

Pena

854

327189 4569839

Siurana

772

333021 4571834

362

Altitude Vegetation (m) cover

Febró

Y (UTM)

333095 4564449

X (UTM)

Alforja

Sampling location

Table 1 Sample plots location (X, Y, UTM), altitude above sea level (meter) and vegetation cover

Author's personal copy Environ Monit Assess (2013) 185:615–629

344853 4571453

341113 4572585

343591 4575400

348004 4575630

Gomis

Montral

Pinetell

La Riba

306

604

810

546

293

972

Abandoned field of Prunus dulcis and Olea europaea Field of Prunus dulcis and Olea europaea

Abandoned field of Corylus avellana

Abandoned field of Prunus dulcis and Olea europaea Abandoned field of Corylus avellana


Altitude Vegetation (m) cover

0.313 b (0.114)

1,805 b (106)

Xanthoria patietina

0.493 b (0.063)

0.427 b (0.070)

0.348 b (0.144)

0.565 b (0.061)

0.273 b (0.104)

0.429 b (0.006)

Hypnum 2,176 0.989 a,b (0.293) cupressiforme Xanthoria 4,998 a,b 0.520 patietina (429)

2,782 b (597)

2,931 b (76.2)


3,357 b (893)

1,748 b (18.7)


2,147 b (320)

0.308 b (0.122)

3,262 a,b (76.0)


0.709 b (0.038)

1,776 b (417)


5,407 a (174)

Xanthoria patietina

As

0.644 b (0.053)

Al

Hypnum 6,594 a,b cupressiforme (2,124)

Species

0.399 (0.151)

0.411 b (0.171)

0.372 (0.100)

1.35 a,b (0.274)

1.13 (1.14)

0.662 b (0.193)

0.357 (0.041)

Co

36.2 a,b (18.1)

11.7

0.140 b 0.459 (0.015) 0.232 0.997 a,b (0.379)

28.3 (7.60) 31.1 b (15.6)

0.437 (0.335)

42.9 a,b (5.38)

5.95 (2.01)

17.0 b (0.229)

9.40 (1.48)

73.9 a,b (15.4)

65.7 (41.9)

24.8 b (13.1)

9.07 (6.13)

Cr

0.104 b 0.628 a,b (0.016) (0.280)

0.095 b (0.007)

0.074 b 0.816 a,b (0.008) (0.098)

0.132 b (0.005)

0.203 b (0.026)

0.095 b (0.005)

0.123 b (0.026)

0.147 b (0.013)

0.121 b (0.011)

0.128 b (0.010)

Cd

65.6 a (34.4) 16.0

6.24 (0.926)

4.49 b (0.357)

6.37 (0.755)

7.22 b (0.600)

7.43 (0.300)

5.31 b (0.487)

7.50 (1.18)

12.7 b (5.47)

6.55 (0.569)

7.80 b (0.436)

Cu

20.7 b (9.15)

7.70

17.5 b (9.40)

10.9 (4.87)

23.4 b (2.48)

5.48 (1.56)

9.67 b (0.124)

6.67 (0.863)

39.3 a,b (8.73)

35.5 (21.5)

13.2 b (6.05)

6.66 (4.19)

Ni

6.89 a (1.82) 2.72

2.04 b (0.396)

1.92 b (0.166)

2.53 b (0.297)

3.01 b (0.102)

2.64 b (0.189)

2.41 b (0.068)

2.15 b (0.359)

3.70 b (0.098)

1.92 b (0.312)

2.98 b (0.452)

Pb

0.021 (0.012) 0.064

0.047 (0.003)

0.025 (0.015)

0.059 (0.022)

33.4 b (9.03)

11.2

12.6 b (1.83)

10.8 b (2.82)

19.8 b (1.17)

14.7 b (4.11)

0.022 (0.013)

11.0 b (2.43)

22.2 b (1.13)

9.44 b (2.81)

21.2 b (1.12)

11.0 b (3.14)

12.1 b (0.802)

Ti

0.054 (0.012)

0.004 (0.002)

0.047 (0.004)

0.049 (0.028)

0.051 (0.015)

0.012 (0.013)

Sb

29.9 a,b (4.06)

Zn

5.45 a (1.67)

3.28

1.57 a,b (0.247)

2.48 a,b (0.381)

2.95 a,b (0.309)

3.37 a,b (0.505)

1.68 b (0.052)

3.55 a,b (0.463)

3.29 a,b (0.140)

3.12 a,b (0.581)

44.8 a (4.81)

35.9

29.3 a,b (5.69)

31.3 a,b (2.70)

31.8 a,b (3.98)

29.0 a,b (2.66)

17.7 b (0.484)

37.8 a,b (6.00)

28.1 a,b (1.17)

35.9 a,b (2.67)

2.48 b b29.7 a,b (0.263) (1.54)

2.41 a,b (0.343)

V

Trace element concentrations (microgram per gram) of Hypnum cupressiforme and Xanthoria parietina. SE between brackets. The letters indicate statistically significant differences among the sampling locations (pZn>Ni>Cr>Cu>Pb>V>Co>As, whereas for X. parietina the order was: Cr>Ni>Cd>Zn>Cu> Pb>Co>V>As. Relationship of trace elemental concentrations and enrichment factors with local pollution sources The concentration of Cu, Sb, and Zn in moss was significantly higher in the locations closer to several local emission sources (ESM Table S2). The concentration of Cr, Ni, and Sb in lichen was also significantly higher in the locations closer to several local emission sources (ESM Table S2). We conducted two-factor analyses (one per biomonitor) of all the trace element concentrations in biomass as variables and the sampling locations as cases. For the moss, the scores of the two-factor analysis variables did not show statistically significant correlations with the distance to any local sources (ESM Table S3). For the lichen, the two-factor analysis variables accounted for 71.9% of the total variability (53.8% for factor 1 and 18.1% for factor 2). The values of factor 2, in contrast to the results for moss, showed significant correlations with the distances from almost all the local pollution sources with the exception of Montblanc (ESM Fig. S2, Table S3; from R0−0.78, P