Effects of nitrogen oxides on ground vegetation, Pleurozium schreberi and the soil beneath it in urban forests

Ecological Indicators 24 (2013) 485–493

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Effects of nitrogen oxides on ground vegetation, Pleurozium schreberi and the soil beneath it in urban forests Sirkku Manninen a,∗ , Minna-Kristiina Sassi b , Katja Lovén b a b

Department of Environmental Sciences, University of Helsinki, P.O. Box 56, 00014 Helsinki, Finland Finnish Meteorological Institute, P.O. Box 503, 00101 Helsinki, Finland

a r t i c l e

i n f o

Article history: Received 18 August 2011 Received in revised form 8 August 2012 Accepted 9 August 2012 Keywords: Bryophyte Nitrogen Carbon Biomass Shoot length Tree canopy cover Plant functional groups

a b s t r a c t Nitrogen oxides (NOx ) are among the key phytotoxic components in many urban areas and contribute to acidification and eutrophication of ecosystems. This study looked at the composition of ground layer vegetation, dry biomass and shoot length of Pleurozium schreberi ((Brid.) Mitt.), and moss and soil total carbon (C) and nitrogen (N) concentrations and ratios in relation to modelled NO, NO2 and NOx concentrations in the Helsinki Metropolitan Area, southern Finland, in September 2010. The aim was to assess the use of P. schreberi as a bioindicator of atmospheric NOx concentrations and N deposition. The modelled annual mean of NO and NO2 concentrations, and consequently NOx concentrations, were 1–20, 8–27, and 9–48 ␮g m−3 , respectively, at the sites in the Helsinki Metropolitan Area. Samples from Kevo in Finnish Lapland, where the measured annual mean NO2 concentration was 0.8 ␮g m−3 , were used as references for moss C and N. The results indicate NOx -related decreases in moss shoot length, moss total C concentration, and soil C:N ratio. The moss total N concentration of 1.23 ± 0.13% and the soil C:N ratio of 21 ± 4 suggest N saturation in urban forests. The composition of ground layer vegetation varied depending on the relative sensitivity of functional groups and species to total N deposition, which was estimated to range from 0.8 to 1.5 g m−2 a−1 . P. schreberi seems to acclimatise well to open and dry urban sites by forming a more dense carpet. The results challenge the use of total N concentration of P. schreberi as a bioindicator of NOx deposition. © 2012 Elsevier Ltd. All rights reserved.

1. Introduction The main emission sources of nitrogen oxides (NOx ) are fossil fuel combustion processes in power plants, industry and transport (Levy et al., 1999). Concurrently with the decline in the NOx emissions from heavy industries such as steel and coal production, emissions from vehicle exhausts have become a major problem in busy city centres (Pearson et al., 2000). Most of vehicle exhausts are emitted as nitric oxide (NO) which reacts especially with ozone (O3 ) within a few minutes to form NO2 (Clapp and Jenkin, 2001; Cape et al., 2004). Hence atmospheric nitrogen (N) inputs close to large industrial conurbations and in urban areas occur mainly as dry deposition of NO2 (Pearson et al., 2000), while the proportion of wet-deposited N increases in background areas (Hicks et al., 2000). In addition to NO and NO2 , the main oxidised N compounds in atmospheric deposition comprise their reaction products, i.e. nitric acid (HNO3 ), particulate nitrate (NO3 − ), and nitrate (NO3 − ) in rain (Pitcairn et al., 2006).

∗ Corresponding author. Tel.: +358 9 19159101; fax: +358 9 19159262. E-mail addresses: sirkku.manninen@helsinki.fi (S. Manninen), kristiina.sassi@fmi.fi (M.-K. Sassi), katja.loven@fmi.fi (K. Lovén). 1470-160X/$ – see front matter © 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ecolind.2012.08.008

The emissions of reduced N compounds, especially dry deposition of ammonia (NH3 ), dominate in areas of intensive agriculture (Pearson and Stewart, 1993; Asman et al., 1998; Galloway et al., 2008), although the increasing use of three-way catalysts in cars has also lead to increasing emissions of NH3 from vehicle exhausts (Cape et al., 2004). The main reduced N compounds in atmospheric deposition comprise, in addition to NH3 , particulate ammonium (NH4 + ), and ammonium (NH4 + ) and organic N in rain (Pitcairn et al., 2006). Like NO and NO2 , NH3 is absorbed through plant stomata. It is also readily deposited on moist leaf surfaces, where it is reduced to NH4 + (Cape et al., 2004). Ectohydric bryophytes are particularly vulnerable to excess N supply as they are largely dependent on the atmosphere for nutrients and cannot regulate N uptake directly, i.e. they lack stomata and take up dissolved N through their whole surface (Jones et al., 2002). This is why total N concentration in mosses can generally be used as a surrogate to estimate total N deposition and identify areas with high N deposition, especially on a large scale (≥50 km × 50 km) (Harmens et al., 2008, 2011; and references therein). On a local scale, however, changes in moss total N concentration often relate particularly to local sources of NH3 in terms of livestock farming, and agriculture in general (Fowler et al., 1998; Sutton et al., 1998; Solga et al., 2006; Pesch et al., 2008). This is because mosses take

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up NH4 + more efficiently than NO3 − (Weber and van Cleve, 1981; Nordin et al., 2006; Pitcairn et al., 2006; Solga and Frahm, 2006). Once in the plant, NO3 − derived from NO2 is reduced to NH4 + via an intermediate product nitrite (NO2 − ) by nitrate and nitrite reductases, respectively. The conversion process is enhanced by the same environmental factors that enhance photosynthesis – high light levels and warm temperatures (Salisbury and Ross, 1978). N additions resulting in increased tissue N levels have been shown, for example, to reduce Sphagnum shoot extension, with the effect of NO3 − being potentially more harmful than that of NH4 + (Carfrae et al., 2007; Kivimäki, 2011). However, the direct effects of N deposition on bryophytes may be masked by indirect effects due to increased shading by grasses whose growth is enhanced by NO3 − (van Dobben et al., 1999; van der Wal et al., 2005; Nordin et al., 2006). Nevertheless, the negative effects of N deposition on mosses largely depend on water availability, because it regulates the uptake of nutrients by bryophytes (Bates, 1987) as well as their growth (Busby et al., 1978). When there is no water, there is no uptake of N, but neither is there any growth dilution of the N already absorbed, given that other nutrients are not limiting growth. Conversely, elevated N deposition may increase moss water stress. Solga et al. (2005) reported decreasing biomass in Pleurozium schreberi ((Brid.) Mitt.) per area with increasing N deposition, due to a reduction in stem density, which may decrease the boundary layer resistance and hence increase evaporation rate of individual shoots (Proctor, 1984; Rice et al., 2001). The effects of N deposition on the structure of the moss carpet may be confounded by microclimate though. The results of Bonnett et al. (2010) and Manninen et al. (2011) show that Sphagnum capillifolium ((Ehrh.) Hedw.) acclimates morphologically to its environment, with the moss carpet having higher biomass under open rather than shaded and probably more moist conditions. Background bulk N deposition was about 0.8 g m−2 a−1 , with a NO3 − :NH4 + ratio of 1:1, in the Helsinki Metropolitan Area in 1999–2003 (Jussi Vuorenmaa/Finnish Environment Institute, personal communication). However, the proportion of oxidised N forms in deposition is considered to exceed that of reduced N forms in the most urbanised parts of the Helsinki Metropolitan Area, where there are large coal-powered energy plants and heavy traffic, including aircraft and large container and passenger ships, but little agricultural activity (Lappi et al., 2008). The municipal and regional environmental authorities do not monitor ambient NH3 concentrations nor total N deposition, while NOx are measured continuously at nine air quality monitoring stations. Moreover, NOx emissions from the high power plant stacks are dispersed and diluted over a large area (Lappi et al., 2008), whereas vehicle exhaust emissions of NO and NO2 are considered to affect vegetation and ecosystems on a more local scale (Bernhardt-Römermann et al., 2006; Larsen et al., 2007; Bell et al., 2011). Earlier studies performed in the area have shown increased tree foliar and soil N concentrations in urban forests and meadows (Manninen et al., 2010; Nikula et al., 2010). Therefore we performed a study with special aims (i) to examine the relationship between modelled NOx concentrations in the air and total N concentration of P. schreberi, and (ii) to assess the use of moss total N concentration as bioindicator of N deposition. P. schreberi is the most common moss on Earth (Kuc, 1997) and the most prevalent feather moss in the boreal forest region accounting for between 50 and 80% of ground cover in boreal forests (Mälkönen, 1974; Foster, 1985; Oechel and Van Cleve, 1986; DeLuca et al., 2002). This is why it was chosen as the study species. In addition to total N concentration, we measured total carbon (C) concentration along with the C:N ratios in green P. schreberi shoots and the surface soil beneath it to assess the effects of N deposition on ecosystem C:N status in urban forests. Dry biomass and length of moss shoots were measured to show potential negative effects

of NOx on moss vitality (Solga et al., 2005; van der Wal et al., 2005; Nordin et al., 2006) and productivity (Glime, 2007, and references therein). In other words, we expected to find a positive relationship between the total N concentrations in green moss shoots and modelled NO2 concentration due to the large range in NO2 concentrations in the study area. This was partly because we expected the highest NOx levels to lead to accumulation of toxic cellular levels of N compounds and consequently decrease moss growth and/or biomass. It was also hypothesised that there would be changes in ground vegetation composition, as the annual mean NOx concentration exceeded the critical level of 30 ␮g m−3 a−1 (WHO, 2000) at some of the sites.

2. Materials and methods 2.1. Air quality and climatic conditions in the study areas The study was performed at 41 sites located 2–30 km away from the Helsinki city centre (60◦ 1 N, 24◦ 57 E), on the southern coast of Finland, in September 2010 (Fig. 1 and Table 1). The urban forests in the area are heterogeneous and the study sites were rocky Cladina- or Calluna-type patches within an urban green infrastructure or a Vaccinium-type forest matrix with mature Scots pine (Pinus sylvestris L.) as the dominant tree species. P. schreberi collected from three sites in Scots pine-mountain birch (Betula pubescens Ehrh. ssp. cherepanovii) forests in the Kevo National Park (69◦ 45 N, 27◦ 01 E), northern Finland, in early September 2007 served as reference material for moss chemistry. In addition, samples of Hylocomium splendens ((Hedw.) B.S.G.) were collected for total C and N analyses from 14 of the sites in the Helsinki Metropolitan Area. The sites were chosen based on the distribution of modelled annual mean NOx concentration at ground level for the year of 2005 (Lappi et al., 2008), so that there were gradients from highly urban areas and those in close proximity to heavily trafficked roads, to the local background area. The model calculations were performed by using local scale Gaussian dispersion models CAR-FMI (traffic model) (Härkönen et al., 1996) and UDM-FMI (urban dispersion model) (Karppinen et al., 1998, 2000a,b) developed at the Finnish Meteorological Institute (FMI) to study the dispersion of exhaust gases from power plants, industry and traffic. NOx concentrations were modelled for 20,000 points within an area of 35 km × 35 km. In 2005, the major source of NOx emissions (NO + NO2 expressed as NO2 ) in the area was energy production with 6756 tonnes, which comprised 50% of the total NO2 emissions. Second came road traffic (5015 tonnes, 36%) and third harbours and ships (1741 tonnes, 13%) (Lappi et al., 2008). Contrary to the coal-powered Hanasaari and Salmisaari plants, coal plays only a minor role compared to natural gas as an energy source in the Vuosaari power plants. The modelled annual mean NO concentrations were between 1 and 20 ␮g m−3 , NO2 concentrations 8 and 27 ␮g m−3 and NOx concentrations 9 and 48 ␮g m−3 at the sites. The modelled NO and NOx concentrations were the highest at site 3 approximately 300 m away from the Hanasaari coal power plant, and 2.5 km downwind of the city centre, and also therefore affected by NOx emissions from both road traffic and ships. The highest NO2 concentration was modelled for site 26, ≤100 m from a motorway with around 47,500 cars per day, and 8 km northeast of the city centre. As a comparison, measurements made in 2010 found the highest NO, NO2 and NOx concentrations were 75, 53, and 85 ␮g m−3 a−1 in the city centre, and 1, 8 and 9 ␮g m−3 a−1 , respectively, at the local background air quality monitoring station in Luukki, which is approximately 20 km northwest of the city centre (Maria Myllynen/Helsinki Region Environmental Services Authority, personal communication). The annual mean NO2 concentration measured at the Sammaltunturi GAW (Global Atmosphere Watch) station in

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Fig. 1. Location of the study sites (purple quadrats) in relation to major emission sources and modelled annual mean NOx concentration in the Helsinki Metropolitan Area. Site 13 was outside the map area about 30 km northwest from the city centre.

Finnish Lapland (67◦ N58 E, 24◦ 07 E) was 0.8 ␮g m−3 in 2007, and the deposition of NO3 + –N in precipitation was 0.04 g m−2 and that of NH4 + –N 0.01 g m−2 in Kevo (Finnish Meteorological Institute, 2011). The weather in 2009–2010 was normal as compared to longterm averages (1971–2000) in terms of annual total precipitation (662 cf. 642 mm) and mean temperature (5.6 cf. 5.6 ◦ C) in the city centre of Helsinki, but slightly drier (585 cf. 650 mm) and clearly warmer (5.0 cf. 2.9 ◦ C) in the vicinity of Helsinki-Vantaa airport, 15 km north of the city centre. The annual total precipitation was approximately 150 mm lower in Kevo (410 mm in 2007) in very north of Finland than in very south of Finland. The annual mean temperature in Kevo is around −1 ◦ C (Finnish Meteorological Institute, 2011). 2.2. Vegetation and soil studies At each site, the total cover of grasses, forbs, mosses, lichens, dwarf shrubs, litter, bare soil and rock/stone were scored as one layer on a scale of 0–100% in three 1 m2 quadrats. The most abundant forb, grass, moss and lichen species at each site were also listed. The quadrats were positioned so that it was possible to detach a monospecific 10 cm × 10 cm P. schreberi cushion from the middle. The moss samples were detached by hand from the substrate, after which a soil sample was taken from each 100 cm2 quadrat, except at two sites where the humus or soil

layer was too thin. Depending on the vegetation, i.e. the ratio of grasses to mosses and lichens which affected the depth of humus layer and soil type, the soil samples represented the 0–5 cm surface soil. The 1 m2 quadrats were located at least 1 m away from each other and the moss samples were taken at least 1 m away from the canopy drip zone of the nearest tree. Tree canopy cover was scored as follows: 0, 1–10, 11–30%, and it was used as a environmental variable describing microclimatic conditions at the sites. Total shoot length and the length of green apical sections and brown basal sections were measured from three randomly chosen points within the 100 cm2 cushion. After that, dead material and litter were removed from moss samples and the green shoot sections representing the last 2 years’ growth were separated from the brown ones, dried for 48 h (60 ◦ C) and weighed for dry weight prior to preparation for total C and N analyses. Plant roots and small sand particles were removed from air dried soil samples before grinding them in a mortar. The total C and N concentrations were analysed using high-temperature combustion (Vario MAX CN analyzer, Elementar Analysesysteme GmbH, Germany) at the Department of Forest Sciences, University of Helsinki. The ratio of total shoot dry biomass (per 100 cm2 ): total shoot length and that of green shoot sections were also calculated to assess potential differences and changes in moss shoot morphology and density of the moss carpet in relation to environmental factors.

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Table 1 Description of the study sites in the Helsinki Metropolitan Area including main NOx emission source in the vicinity of each site, modelled annual mean NOx and NO2 concentrations, forest site type, tree canopy cover, and average cover of plant functional groups in the 1 m2 quadrats studied at each site. Site number

Site name

Emission sources

NO2 (␮g m−3 a−1 )

NOx (␮g m−3 a−1 )

Forest type

Canopy (%)

Moss (%)

Grass (%)

Forb (%)

Shrub (%)

Lichen (%)

1 2H 3H 4 5H 6 7 10H 11 12 13H 14 15H 16H 17 18 19 20 21H 22 23 24 25H 26 27 28H 29H 31H 32 33 34H 35 36H 37 38 39 40 41 42 43 44

Viikki Kulosaari Mustikkamaa W Mustkkamaa SE Mustikkamaa N Eläintarhan kenttä Laakso Herttoniemi S Herttoniemi N Roihupelto Nuuksio Bemböle Luukki Sipoonkorpi Talosaari Vuosaari Ramsinniemi Keskuspuisto Hakamäentie Krämertskogsvägen Pirkkola Kehä I Paloheinä Pihlajamäki Viikinmäki Veräjämäki Kalastajatorppa Seurasaari Mäntyniemi Lauttasaari Lehtisaari Lehtisaari Munkkiniemi Viikki Myllypuro W Myllypuro N1 Myllypuro N2 Laajasalo Kallahdenniemi Vuosaari Kivikko

A T E, T E, T E, T T, E T T T T B T B B B E B T T T, E T T T T T T T E, T T, E T T T T A A, T T T, E B B E, I T, E

14.4 20.9 17.8 15.2 15.5 22.2 17.1 14.7 16.2 16.0 8.1 12.2 8.5 10.2 10.1 11.4 11.8 17.1 19.3 18.7 23.9 20.4 14.8 27.1 24.3 17.0 20.2 13.7 14.3 13.0 13.7 14.0 17.2 15.3 14.8 17.0 26.0 13.4 10.7 10.5 17.3

17.8 27.5 47.7 22.4 23.5 30.6 21.4 18.4 20.4 20.1 9.0 14.3 9.5 11.7 12.2 13.8 14.2 21.4 24.2 23.6 31.2 26.1 17.5 29.0 32.2 20.0 26.3 17.0 18.0 16.5 16.7 17.2 22.2 19.2 18.3 23.0 36.6 17.0 12.7 12.7 22.0

ClT ClT ClT CT ClT/CT urban ClT ClT ClT ClT ClT/CT ClT ClT CT/VT ClT CT ClT/CT ClT ClT ClT/CT ClT CT ClT/CT ClT ClT/CT ClT/CT ClT ClT/CT ClT/CT ClT urban CT CT ClT/CT CT ClT/CT ClT/CT ClT/CT ClT/CT CT ClT/CT

0 0 0 1–10 0 0 1–10 0 0 0 11–30 0 1–10 11–30 1–10 1–10 1–10 1–10 1–10 1–10 1–10 1–10 1–10 1–10 0 1–10 0 1–10 0 1–10 1–10 1–10 1–10 0 1–10 1–10 0 1–10 1–10 1–10 1–10

50.3 60.0 80.0 53.3 71.7 85.7 72.0 91.7 83.0 73.3 85.0 64.7 91.7 72.0 82.3 94.7 72.0 89.3 92.7 79.3 69.7 93.0 52.0 37.7 77.7 85.0 90.0 54.7 75.3 69.0 88.0 81.0 80.3 76.3 75.3 82.3 85.0 62.0 62.7 63.3 54.0

42.7 30.3 15.0 18.3 16.7 5.3 22.0 1.0 7.7 23.3 2.3 10.7 0.2 0.0 9.3 2.0 12.3 0.8 2.7 5.0 10.7 0.2 38.0 45.3 4.3 8.3 4.3 44.3 3.3 18.7 8.0 4.7 3.7 13.0 6.0 12.0 7.0 9.7 7.7 29.3 2.0

0.3 6.3 5.0 3.3 3.3 1.2 1.3 6.3 1.0 2.7 0.0 1.5 0.0 0.2 0.0 0.7 1.7 7.2 0.8 0.3 13.7 1.0 5.7 1.0 0.7 1.5 3.7 0.7 1.0 4.7 3.0 6.0 3.0 8.0 0.3 0.0 1.3 0.0 0.0 1.0 1.3

5.7 0.0 1.3 11.7 0.0 1.0 1.0 0.0 0.0 0.0 8.7 0.7 4.3 5.3 2.3 1.8 1.7 0.0 0.3 10.0 0.0 3.7 0.0 4.0 7.7 0.0 0.7 0.0 0.0 1.7 0.0 0.0 2.3 2.0 8.7 0.0 1.3 4.0 0.7 1.7 2.3

1.5 0.0 0.0 0.0 0.0 1.7 1.7 0.0 4.0 0.3 7.0 15.3 4.0 21.7 6.0 1.0 1.7 0.8 1.0 1.0 0.2 1.2 0.5 0.5 5.7 3.0 0.7 0.3 1.3 0.0 0.0 10.0 0.3 0.0 2.3 8.0 3.0 3.3 21.7 2.7 35.3

16.0 4.5

20.9 7.6

74.6 13.8

12.4 12.6

2.5 2.9

2.4 3.1

4.1 7.2

Mean SD

HM, Hylocomium splendens also sampled. A, agriculture; B, background; E, energy; I, industry; T, traffic. Cl, Cladina-; C, Calluna-; V, Vaccinium-type forest.

2.3. Statistical analyses Relationships between the variables were tested with factor analysis carried out using Varimax rotation with Kaiser Normalization (IBM SPSS Statistics 19) and the Spearman rank correlation test (2-tailed). The non-parametric Spearman rank correlation test was used because transforming the data did not improve the normality much. A regression is also presented for the relationship between the annual mean NO2 concentration and moss total N concentration. Differences in moss total C concentration, total N concentration, and C:N ratio between P. schreberi and H. splendens were analysed with paired samples t-test. The relationships and differences were considered significant at p < 0.05.

3. Results 3.1. Main findings Factor analysis on NOx concentrations, tree canopy cover, plant functional group covers, green moss characteristics, and soil total

N concentration was carried out to discern the major effects of elevated NOx concentrations on them, and other strong relationships between the variables studied. The six principal component (PC) factors presented in Table 2 explained altogether 81% of the total variation in the data (Fig. 2). Contrary to our hypothesis, moss total N concentration in the Helsinki Metropolitan Area seemed mainly to be governed by other abiotic and/or biotic factors and processes than atmospheric NOx concentrations. Moss total N was solely loaded on the PC3 axis. Moss C:N ratio was also most strongly loaded on it, although oppositely to total N. Therefore the PC3 axis is attributed to N “cycling” in moss carpet in relation to C assimilation by P. screberi. By “cycling” we refer to total N deposition and retention of N within the moss carpet, i.e. uptake, assimilation, accumulation, and leaching of excess N. The PC1 axis represents an urban-rural NOx pollution gradient and supports the hypothesis of negative impact of elevated NOx concentrations on P. schreberi vitality in terms of moss shoot length. Moss green shoot length was actually most strongly loaded on PC6 axis, which is considered to indicate a light and temperature (i.e. radiation) gradient with reference to the opposite loadings of lichen cover and moss total C concentration with moss green shoot length. The PC2 axis,

S. Manninen et al. / Ecological Indicators 24 (2013) 485–493 Table 2 Results of the factor analysis (rotated component matrix) indicating the loadings of environmental variables and the characteristics of the green moss shoot sections on the six major principal components (PC1–PC6). Loadings ≥0.5 are given in bold. Variable

Component PC1

NOx NO2 NO Green dw to length Green dw Canopycover Moss N Moss C to N Mosscover Grasscover Forbcover Shrubcover Soil N Lichencover Moss C Green length

PC2

0.966 0.800 0.797

PC3

PC4

PC5

−0.236 0.948

−0.255 −0.408

0.252

0.869 −0.703

−0.277 −0.955 0.949

−0.208 0.247 0.343

0.922 −0.918 0.246

0.751 −0.703 0.694

−0.373 −0.203 −0.342 −0.516

PC6

−0.440 0.325 0.294

0.275 0.385

−0.750 −0.590 0.578

489

Table 3 Descriptive data for green and brown moss shoot sections and surface soil (0–5 cm) variables (nmoss = 41, nsoil = 39). Variable Moss Total dw (g 100 cm−2 ) Green dw (g 100 cm−2 ) Brown dw (g 100 cm−2 ) Green:brown dw ratio Total length (cm) Green length (cm) Brown length (cm) Green:brown length ratio Total dw:length ratio Green dw:length ratio Green N (%) Green C (%) Green C:N Soil N (%) C (%) C:N

Mean ± SD

Min

Max

1.35 0.58 1.06 0.19 0.7 0.4 0.6 0.56 31 25 0.13 0.4 3.8

3.49 1.47 1.84 0.39 3.2 1.7 1.2 0.60 0.81 0.55 0.98 44.1 29.4

9.91 3.71 6.66 1.16 6.2 3.7 3.5 3.08 2.30 1.95 1.56 46.1 45.5

1.69 ± 0.36 33.7 ± 5.8 20.6 ± 4.3

0.77 14.6 15.8

2.43 43.2 37.4

6.02 2.35 3.70 0.71 4.6 2.7 1.9 1.71 1.33 0.90 1.23 45.2 37.6

± ± ± ± ± ± ± ± ± ± ± ± ±

3.2. Vegetation

in turn, most probably represents a microclimatic and soil moisture gradient which relates to tree canopy cover and especially affects shoot morphology of P. schreberi, modifying its dry biomass per land surface area and the dry weight:length ratio. It was also hypothesised that there would be changes in ground vegetation composition. Firstly, there was a strong negative correlation between moss cover and grass cover, but neither of them was loaded on PC1, i.e. NOx axis. Instead, they were loaded on the PC4 axis, which may represent competition for various resources between the two plant functional groups. In addition, forb cover and surface soil total N concentration were correlated positively, and the cover of dwarf shrubs was negatively loaded on the PC5 axis. The PC5 axis therefore represents a soil fertility gradient from sites with higher soil total N concentration and forb cover to more forest-like sites, with a nutrient-poor soil and a higher cover of dwarf shrubs.

The mean ± SD of moss cover was 75 ± 14%, followed by grasses (12 ± 13%), lichens (4.1 ± 7.2%), forbs (2.5 ± 2.9%), and dwarf shrubs (2.4 ± 3.1%) (Table 1). The values for rock, litter and bare soil were 2.8 ± 3.7%, 1.4 ± 2.5% and 0.2 ± 0.8%, respectively. Other bryophytes, especially Polytrichum and Dicranum species were found in most of the 1 m2 quadrats in addition to P. schreberi, as were lichens of the genus Cladonia. The most frequent grass was Deschampsia flexuosa ((L.) Trin) and the most frequent forb Rumex acetosella (L.). Other common species, especially at the most urban sites close to the city centre were Sedum telephium (L.), Rubus idaeus (L.), Epilobium angustifolium (L.) and Sorbus aucuparia (L.), while the dwarf shrubs Vaccinium myrtillus (L.), Vaccinium vitis-idaea (L.) and Calluna vulgaris ((L.) Hull) were found at the more rural forest sites near the sea shore, and in forests farther away from the city centre with higher (but always <30%) tree canopy cover. The cover values presented in Table 1 overestimate the actual abundance of bryophytes. This is because we had to locate the 1 m2 quadrats so that we got a monospecific 100 cm2 P. schreberi sample from each quadrat. However, moss cover also showed a strong negative correlation with grass cover based on the Spearman rank correlation test (rS = −0.699, p < 0.001). Grasses were most abundant in Viikki (site 1, 42.7%), Pihlajamäki (site 26, 45.3%) and Seurasaari (site 31, 44.1%). The first site is characterised by its vicinity to agricultural activities, the second by vehicle exhausts and recreational use, for example by dog walkers, and the third is considered mainly to be affected by N emissions from vehicles and the Salmisaari coal power plant about 1 km south of the site. Two of the three background sites, Luukki (site 15) and Sipoonkorpi (site 16), where among the sites with the lowest grass cover (0.2% and 0.0%, respectively). Lichens appeared as the most sensitive functional group to NOx with reference to negative correlations between lichen cover and NOx concentrations, while forbs were the most tolerant group (rS all p < 0.05). 3.3. Moss shoot biomass and length

Fig. 2. Plot of the first two principal components (PC) from the principal component analysis of modelled annual mean NOx concentrations (NO, NO2 and NOx ), tree canopy cover (canopycover), covers of functional groups (forbs, grasses, lichens, mosses, dwarfshrubs), moss green shoot variables (moss dw, moss length, moss dw to length, moss C, moss N, moss C to N), and soil total N concentration (soil N) in the Helsinki Metropolitan Area.

The largest green shoot dry weight was about 2.5 times the smallest value (3.71 cf. 1.47 g 100 cm−2 ), while the difference in length was about double (3.7 cf. 1.7 cm) (Table 3). The green shoot section made up an average 39% of the total dry biomass, and 59% of the total shoot length. Green shoot length did not show any clear spatial pattern, while green shoot dry weight, and dry weight:length ratios below the mean values mainly occurred at

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Fig. 3. Relationships between annual mean NO2 concentration and moss total N concentration in the Helsinki Metropolitan Area, southern Finland, and when the data from Kevo, northern Finland, was included in the regression analysis.

sites within larger forest stands. Given that the green shoot section represented the last 2 years’ growth, the potential annual dry biomass production of P. schreberi may be estimated to be approximately 118 g m−2 , the range being from 74 to 185 g m−2 . The clear decrease in the green shoot dry biomass of P. schreberi with increasing tree canopy cover was verified by the Spearman rank correlation analysis (rS = −0.528, p < 0.001), as was that in the green shoot total dry biomass:length ratio (rS = −0.651, p < 0.001). The decrease in green shoot length with increasing NOx concentrations was significant at p < 0.05. NOx concentrations did not apparently affect moss decomposition rate, as they did not correlate with brown shoot dry weight or length, or with green:brown shoot dry weight ratio or green:brown shoot length ratio (data not shown). 3.4. Moss total N and C The highest total N concentrations of >1.40% in the green shoot sections were measured in Eläintarhan kenttä (site 6), Seurasaari (site 31) and Lehtisaari (site 34). Eläintarhan kenttä is the site closest to the city centre, and the sites in Lehtisaari and Seurasaari are the ones nearest to the sea shore. The highest total N concentration in the green shoot sections of P. schreberi (1.56%, Eläintarhan kenttä) was only 1.5 times the lowest one (0.98%, site 2 in Kulosaari). In other words, the moss total N concentration in the Helsinki Metropolitan Area only showed a weak positive correlation with NO and NO2 concentration (p < 0.1 for both rS ) (Fig. 3). Nevertheless, the mean total N concentrations of 1.07–1.11% in the local/regional background areas in Nuuksio (site 13, outside the map in Fig. 1), Luukki (site 15) and Sipoonkorpi (site 16) were 2.5 times that of 0.43(±0.03)% in Kevo. As the data from the Helsinki Metropolitan Area clearly indicated increased atmospheric NO2 and total moss N concentrations in the local/regional background area, as compared to the data from Kevo, we combined the two data sets for regression analysis. As a result, a significant non-linear relationship was suggested with annual mean NO2 concentration explaining 73% of the variation in the total N concentration of P. schreberi. The total C concentration in the green shoot sections of P. schreberi increased with increasing tree canopy cover (rS = 0.477, p = 0.002) and decreased with increasing NOx concentrations (all p < 0.01), grass cover (rS = −0.387, p = 0.012), and moss total N concentration (rS = −0.323, p = 0.040). As the mean total C concentration of the green shoot sections of P. schreberi in Kevo (44.1 ± 0.2%) was almost equal to that in the Helsinki Metropolitan Area (45.2 ± 0.4%), the mean C:N ratio in the northern mosses (104.6 ± 9.6) was almost 3 times that found in the southern ones

Fig. 4. Relationship between annual mean NO2 concentration and C:N ratio in the surface soil in the Helsinki Metropolitan Area.

(37.6 ± 3.8). Moreover, the differences in moss total C and N concentrations and C:N ratio between P. schreberi and H. splendens at the 14 sites were significant (all p < 0.001). The average values in Pleurozium cf. Hylocomium were: 1.22 cf. 1.37% for N (t = −4.825), 45.2 cf. 44.3% for C (t = 5.015), and 37.5 cf. 32.7 for C:N (t = 5.485). 3.5. Soil total N and C The range for total N concentration in surface soil (0.77–2.43%) was larger than that for P. schreberi, and the mean was higher than that in moss (Table 3). The lowest total N concentration was measured at the site 12, where soil was very thin and the sample analysed apparently contained some sand – suggested by the lowest total C concentration. The sites with a total N concentration higher than the mean 1.70% were all rocky ones. The highest C:N ratios of >25 were found at sites 15–18, of which 15–17 are background sites, while site 18 is located less than 1 km west of the main cargo harbour, in operation since 2003 and the Vuosaari power plants. Soil total N concentration did not correlate with NOx concentrations, but it increased with increasing moss total N concentration (rS = 0.460, p = 0.003). Soil total C concentration, in turn, decreased with increasing NOx concentrations (data not shown) as did that of P. schreberi. The overall effect was seen as a decrease in soil C:N ratio with increasing NO2 concentration (Fig. 4). 4. Discussion 4.1. Moss total N concentration as bioindicator of ambient NOx concentrations Contrary to the hypothesis, there was no strong correlation between total N concentrations in moss and ambient NOx concentrations in the Helsinki Metropolitan Area. This may be due to fact that the total N concentration of P. schreberi is also clearly elevated in southern Finnish background areas, due to long term elevated deposition of both reduced and oxidised N compounds – also found by Poikolainen et al. (2009) on H. splendens. Thus the moss carpet may have become N saturated, i.e. the higher the N deposition, the higher the proportion of water-soluble N that just runs through the moss carpet, resulting in increased soil total N concentration and decreased C:N ratio. Some N may also have been leached from the mosses due to membrane breakdown. However, the overall proportion of N leakage from moss tissue is apparently small, due to the ability of mosses to quickly re-absorb released N from surrounding solutions (Startsev and Lieffers, 2006). P. schreberi can also derive N from the substratum (Bates, 1992, 2000), but this is considered to be negligible in areas with elevated atmospheric N supply.

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According to Gundale et al. (2011), total N deposition of as little as 0.2 g m−2 a−1 is likely to increase bryophyte tissue N content and decrease N2 -fixation rate by associated cyanobacteria to some extent. The nonlinear regression curve shown in Fig. 3 is similar to that found in some other studies for the relationship between bryophyte total N concentration and total N deposition. The total N concentration in mosses seems to increase in a linear way, and faster per unit of atmospheric N deposition in low (0.1–0.6 g N m−2 a−1 ) than in moderate to high N deposition areas (Harmens et al., 2011). In the moderate to high deposition areas, there is usually a non-linear relationship between the moss total N concentration and N deposition measures. Our results support the earlier findings which suggest that the moss carpet becomes saturated at a tissue N level of 1–1.5% (Nordin et al., 1998; Solga and Frahm, 2006), or a total N deposition level of 0.5–1.5 g m−2 a−1 (Nordin et al., 1998; Harmens et al., 2011). Total N deposition at highly polluted sites in our study area probably corresponds to about 1.5 g m−2 a−1 , given that the total background deposition is 0.8–1.0 g N m−2 a−1 (Dentener et al., 2006; Jussi Vuorenmaa, personal communication), and an air concentration of 10 ␮g NO2 m−3 a−1 corresponds to an additional input of ca. 0.29 g N m−2 a−1 to short vegetation (Cape et al., 2004). 4.2. Contribution of microclimatic factors on moss results The estimated annual dry biomass production of green shoot sections found in this study is equal to that of P. schreberi at more southern sites in Germany with annual mean bulk deposition of 1.3–1.4 g N m−2 (Solga et al., 2005). One reason behind low correlation between moss total N concentration and modelled NOx concentrations may be the relatively high biomass of P. schreberi per soil surface area pointing to growth dilution of N deposition especially in the open urban open sites with the highest NOx concentrations. Overall, the dry biomass production of P. schreberi does not seem to be sensitive to N deposition (Nordin et al., 1998; Carroll et al., 2000; Gundale et al., 2011), as it grows both apically and laterally, adding relatively large new branches continuously along the stem from lateral buds and extending the length of the previous year’s branches (Longton and Greene, 1969; Benscoter and Vitt, 2007). The high dry biomass:length ratio found in this study especially at the more open sites thus indicates a preference for maximising shoot dry weight per ground surface area (Bonnett et al., 2010; Tobias and Niinemets, 2010; Manninen et al., 2011), given the important role of the canopy interior branches in water storage as well as in nutrient sequestration by mosses (Rice et al., 2008). It was probably mainly due to such acclimatisation that no NOx effect was found on moss dry biomass. Moreover, P. schreberi has been shown to maintain photosynthesis even with low availability of moisture and recover photosynthetic ability soon after a dry period (Williams and Flanagan, 1998). Enhanced N deposition can disturb cellular C metabolism and reduce the moss C storage pool by markedly enhancing turnover rate of lipids, sugars and proteins in particular. The acceleration of cellular C metabolism also implies enhanced respiratory C losses (Koranda et al., 2007). The weak but significant negative correlation between total C and N concentrations in P. schreberi supports this and may partly explain the observed decreases in moss length and total C concentration in relation to NOx concentrations. However, given that mosses allocate to shoot height growth when grown in the shade (Rice et al., 2008), the strong opposite loadings of moss total C concentration and shoot length indicate that moss total C concentration was also affected by the amount of light. Consequently, as most of our sites were open, P. schreberi was apparently able to both photosynthesise and reduce NO3 − efficiently and hence the overall negative effects of NOx and N deposition on it seem minor.

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The low C:N ratio in the green shoots sections of P. schreberi as compared to that at Kevo and the ratios reported for example for forest ecosystems in Alaska (Weber and van Cleve, 1981) clearly indicate NOx -related changes in moss litter quality. However, brown shoot sections may have had a lower total N concentration and a higher C:N ratio (Weber and van Cleve, 1981) due to differences in physiological activity and organic nutrient content between these two regions of the shoot (Hicklenton and Oechel, 1976, 1977; Busby et al., 1978). The results on brown shoot sections and green:brown shoot ratios do not suggest NOx -related changes in moss senescence, and the decomposition rate of moss litter at the most urban and NOx -polluted sites may actually be even faster than in the more rural sites, as shown to be the case with aspen (Populus tremula L.) leaf litter (Nikula et al., 2010). 4.3. Soil C:N ratios also suggest N saturation Supporting the results of Manninen et al. (2010) on urban meadows, soil total N concentration seemed to be elevated especially at rocky sites with a thin humus layer. In the urban meadows, surface soil NO3 − concentration was positively related to the proportion of roads in the 1-km buffer zone around meadows, while soil NH4 + concentration increased with increasing distance from roads. This probably also applies to forest soil in the area. The average total N concentration corresponded to or slightly exceeded the average values measured for the humus layer in urban and rural forests in the area in the summers of 2006–2008 (Nikula et al., 2010). The C:N ratio, in turn, corresponded to the C:N ratio measured for the humus layer in the same area by Nikula et al. (2010) and to that in the organic soil layer of a 40- to 60-year-old Scots pine forest in a heavily polluted area in Germany (Bergmann et al., 1999). Soil total N concentration in the urban forests was about 1.5-fold and the average C:N was far below the value of 37.4 (Pennanen et al., 1999) reported for the humus layer in Calluna type forests in a southern Finnish background area with an atmospheric N deposition of about 0.6 g m−2 a−1 (Kulmala et al., 1998). As N mineralisation and nitrification increase below the threshold C:N ratio of 25–30 (Curtis et al., 2004), the soil C:N ratios measured may indicate NO3 − leaching from the system (Dise et al., 1998; Curtis et al., 2004; Emmett, 2007). Both the input–output budget and the regressions from the survey of Dise and Wright (1995) indicated a critical deposition threshold of <1 g N m−2 a−1 for NO3 − leaching in European forests. We only measured C:N ratios above 15 as did, for example, White et al. (1996), Dise et al. (1998), and Curtis et al. (2004). C:N ratio apparently depends, in addition to N deposition, on soil pH and the effect of soil acidification upon organic matter accumulation rate (White et al., 1996). We did not measure surface soil pH, but the soils in the study area are mainly acidic – the pH of the forest humus layer was 4.71 at urban sites and 4.52 at the local background sites in the study carried out by Nikula et al. (2010), and 5.58 in the surface soil of meadows (Manninen et al., 2010). 4.4. Vegetation changes We also expected to find vegetation changes such as grass cover being increased by elevated NOx -derived N supply (Angold, 1997) and, consequently, decreased moss cover. We found a negative, probably competition-related, correlation between grass and moss cover as often found especially in grasslands, although vascular plants may also have a facilitative effect on mosses (Ingerpuu et al., 2005; and references therein). Overall, it is apparent that higher N deposition rates than found in the study area are needed to impose major effects on moss cover, although there are differences in N tolerance between bryophyte species (Carroll et al., 2003; Payne et al., 2011). The increase in forb cover with increasing NOx

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concentration and soil total N concentration indicate a NOx -related increase in soil N supply and the abundance of species with higher Ellenberg fertility indices (Truscott et al., 2005). Rubus species, for instance, have been found to be typical of vegetation adjacent to motorways (Bernhardt-Römermann et al., 2006). Interactive effects of base cations and N deposition (Payne et al., 2011), which modify soil pH, and effects of pH in general cannot be excluded either (Löbel et al., 2006). Occurrence of S. telephium together with R. acetosella, E. angustifolium, R. idaeus, and S. aucuparia further indicates that the sites most influenced by human activity were rather extreme in terms of light and water, as all these species thrive in dry and relatively well lit sites or are light-loving species (Ellenberg et al., 2001). The Spearman rank correlation test suggested direct negative effects of NOx on the cover of lichens, but it can be supposed that lichen cover was also affected indirectly due to competition for light, especially with forbs and grasses (Angold, 1997). Potential negative effects of NH3 can neither be excluded, especially on lichens. For example Cladonia may be affected negatively by long term exposure to concentrations as low as ≈1 ␮g NH3 m−3 a−1 (Sheppard et al., 2009). 5. Conclusions The small variation in moss total N concentration and the low average C:N ratio in surface soil suggest that N deposition in the study area exceeds N retention capacity of P. schreberi, i.e. its tissue may become N saturated at a total deposition level of 0.8–1.5 g N m−2 a−1 . N deposition had a negative, but apparently minor, impact on moss vitality in terms of decreased shoot length. This is because P. schreberi seems to acclimatise well to open and dry urban sites by forming a more dense carpet and being able to photosynthesise and reduce NOx -derived NO3 − efficiently. These results challenge the use of total N concentration of P. schreberi as a bioindicator of N deposition, especially when there is no real background “control”. Moreover, the effects of elevated NOx concentrations on forb cover compared to lichen cover suggest ecosystem level changes. Microclimatic factors are considered to be as important environmental drivers as atmospheric pollution for the composition of ground vegetation in urban forests. Acknowledgement The revision of English was done by Sally Ulich. References Angold, P.G., 1997. The impact of a road upon adjacent heathland vegetation: effects on plant species composition. J. Appl. Ecol. 34, 409–417. Asman, W.A.H., Sutton, M.A., Schjørring, J.K., 1998. Ammonia: emissions, atmospheric transport and deposition. New Phytol. 139, 27–48. Bates, J.W., 1987. Nutrient retention by Pseudoscleropodium purum and its relation to growth. J. Bryol. 14, 565–580. Bates, J.W., 1992. Mineral nutrient acquisition and retention by bryophytes. J. Bryol. 17, 223–240. Bates, J.W., 2000. Mineral nutrition, substratum ecology, and pollution. In: Shaw, A.J., Goffinet, B. (Eds.), Bryophyte Biology. Cambridge University Press, Cambridge, pp. 248–311. Bell, J.N.B., Honour, S.L., Power, S.A., 2011. Effects of vehicle exhaust emissions on urban wild plant species. Environ. Pollut. 159, 1984–1990. Benscoter, B.W., Vitt, D.H., 2007. Evaluating feather moss growth: a challenge to traditional methods and implications for boreal carbon budget. J. Ecol. 95, 151–158. Bergmann, C., Fischer, T., Hüttl, R.F., 1999. Significance of litter- and humus-layer quality for rates and forms of N cycling in moder- to rawhumus-moder profiles under Scots pine (Pinus sylvestris L.). Plant Soil 213, 11–21. Bernhardt-Römermann, M., Kirchner, M., Kudernatsch, T., Jakobi, G., Fischer, A., 2006. Changed vegetation composition in coniferous forests near to motorways in Southern Germany: the effects of traffic-born pollution. Environ. Pollut. 143, 572–581. Bonnett, S.A.F., Ostle, N., Freeman, C., 2010. Short-term effect of deep shade and enhanced nitrogen supply on Sphagnum capillifolium morphophysiology. Plant Ecol. 207, 347–358.

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