The epiphytic lichen hypogymnia physodes as a biomonitor of atmospheric nitrogen and sulphur deposition in Norway

THE EPIPHYTIC LICHEN HYPOGYMNIA PHYSODES AS A

BIOMONITOR OF ATMOSPHERIC NITROGEN AND SULPHUR

DEPOSITION IN NORWAY

INGA E. BRUTEIG Department of Botany, University of Trondheim, N-7055 Dragvoll, Norway

(Received: May 1992)

Abstract. Hypogymnia physodes was sampled from 179 sites of Scots pine forests regularly distributed throughout Norway. The purpose was to map the nitrogen and sulphur contents of lichen thalli on a large-scale geographical basis, and to relate these values to differences in atmospheric deposition and climate.

The lichen nitrogen and sulphur concentrations showed large differences; the highest concentration values being 4-5 times greater than the lowest. The highest nitrogen and sulphur values occurred along the coast of southern Norway and on some sites in the inland of southern Norway. There was a close correlation between the two elements. The lichen N/S ratio decreased with increasing latitude.

The nitrogen and sulphur contents of Hypogymnia physodes were both significantly correlated to estimated atmospheric deposition of these two elements in Norway. The degree of explanation improved when climatic variables such as temperature sum, altitude, annual precipitation and temperature were included. Factors promoting growth, such as high bark pH, mild winters, hot summers, high precipitation, high ammonium deposition and high evapotranspiration, were all associated with lower lichen nitrogen and/or sulphur concentrations. Unfavourable growth conditions, such as at high altitude, was related to higher concentrations than expected from deposition models. This indicates that differences in element concentration between nearby localities might be related to local differences in climate and lichen growth conditions. This should be taken into consideration whenever using lichens for biomonitoring.

1. Introduction

Lichens have been shown to be outstanding bioindicators in a wide range of air pollution studies (e.g. Ferry et al., 1973; Arndt et al., 1987; Nash and Wirth, 1988; Henderson, 1992). This is due to physiological properties of the lichen thallus: its slow growth and its effectiveness in absorbing soluble and insoluble mineral nutrients from ambient air and precipitation with little subsequent loss.

Lichens are known to be vulnerable to sulphur compounds, especially SO2 (e.g. Hawksworth and Rose, 1970; Nash, 1973; Holopainen and K~irenlampi, 1984). Enhanced sulphur concentrations have been recorded in lichens in numerous areas with strong SO2 pollution (e.g. O'Hare, 1974; Horntvedt, 1975; Kauppi and Mikkonen, 1980; Case and Krouse, 1980) and also in a few large-scale surveys (Takala et al., 1985; Kubin, 1990). There are also some studies on the influence of nitrogen pollution on lichens (Nash, 1976; Kauppi, 1980; Holopainen and K~irenlampi, 1985; von Arb, 1987; de Bakker, 1989) and on nitrogen contents of lichen thalli (Pike, 1978; Pakarinen, 1985; Kubin, 1990). The main sources of lichen nitrogen and sulphur are atmospheric inputs as rain, horizontal intercep-

Environmental Monitoring and Assessment 26: 27-47, 1993. @ 1993 KluwerAcademic Publishers. Printed in the Netherlands.

28 INGA E. BRUTEIG

tion and dust, but contributions from stemflow and canopy leachates also favour accumulation of elements in corticolous species (Pike, 1978).

Both nitrogen and sulphur play a role in development of acid rain, since their oxides form chemical compounds which serve to increase the acidity of water. Until lately, most attention has been paid to sulphur compounds, as most anthropogenic soil and water acidification so far can be ascribed to sulphur rather than nitrogen (Tamm, 1991). This is partly because sulphur compounds have been emitted in larger quantities than acidifying nitrogen compounds, and partly because forest ecosystems in sensitive areas have been nitrogen-limited and thus able to absorb and accumulate deposited nitrogen up to present (Tamm, 1991).

Over the last 15 years, the mean concentration of sulphate in precipitation has decreased by 25-35% in Norway. Concentrations of nitrate and ammonium have remained largely unchanged during the same period. As the amount of precipitation in general has increased in Norway, the result is a small decrease of sulphate deposition and increased deposition of ammonium and nitrate during the last 15 years (The Norwegian State Pollution Control Agency, 1991b). There is now a larger long range supply of nitrogen (200 000 tons/year) than sulphur (190 000 tons/year) to Norway (L6vblad et al., 1992). A distinct deposition gradient is predominant; the level of nitrogen and sulphur deposition is five to ten times higher in the high deposition areas in the south than in the low deposition areas in the north (Pedersen et aL, 1990).

The aim of this study is to map the nitrogen and sulphur contents of the epiphytic lichen Hypogymnia physodes on a large-scale geographical basis, and to relate the concentration variation to differences in atmospheric deposition and climate. There have been two extensive large-scale surveys of trace metal concentrations in mosses in Norway, in 1977 (Steinnes et al., 1992) and 1985 (Steinnes et al., 1988). The present study is the first Norwegian national survey on nitrogen and sulphur concentrations in biomonitors.

Hypogymnia physodes was selected because it is widespread on nutrient poor bark throughout the country and is known to be relatively resistant to air pollution (Marti, 1985). Also, Hypogymnia physodes is widely used in biomonitoring investigations, as in experimental studies.

This study is part of an ongoing 'Programme for monitoring of terrestrial ecosystems' run by the Directorate for Nature Management in Norway. The aim of this programme is to monitor deposition and effects of long range transported air pollutants on various ecosystems and organisms.

2. Methods

2.1. SURVEY AREA

A monitoring network of 714 permanent sites in coniferous forests throughout Nor- way has been established by the Norwegian Institute of Land Inventory (Figure 1). The sites are distributed regularly in a 9 x 9 km formation, and sites not containing

HYPOGYMNIA PHYSODES AS A MONITOR OF N AND S DEPOSITION 29

at least six trees of Pinus sylvestris and/or Picea abies per 1000 m 2 are excluded. The lichen investigation was performed at all sites of mature forest with at least four trees of P. sylvestris, totally 193 sites (Figure 1). Since the sites are located on a regular grid, the net is sparse where pine forests are sparse, as in the mountain areas and in the north. The net is densest in eastern and southern Norway. Fourteen sites did not have enough Hypogymnia physodes for chemical analysis, leaving a total of 179 lichen sample sites.

2.2 . FIELD SAMPLING AND CHEMICAL ANALYSIS

Steinnes (1993) points out that the sampling strategy is extremely important when using epiphytic mosses or lichens for biomonitoring atmospheric deposition of trace elements. A major discrepancy between Swedish and Norwegian results is ascribed to porophyte species: Pinus trunks in the Swedish survey (Folkeson, 1979) and Betula twigs in the Norwegian (Steinnes, 1993). In the present survey, the following requirements were made for the lichen sampling: (1) samples should be taken from stems of four pines, preferably from trees surrounding the monitoring site; (2) the trees should be freely exposed to air movement; (3) the stem should be freely exposed, with no bushes or branches next to the sampling area; and (4) care should be taken to avoid stem areas affected by dripping water or winter snow c o v e r .

All samples were taken from the northern side of the stem, 1.5- 2.0 m above the ground. From each tree at least four lichen individuals were taken, at least eight individuals if they were small (< 3 cm). Disposable polyethylene gloves, scalpel and paper bags were used for the sampling. To minimize problems of contamination, gloves and scalpel blades were replaced before each new sampling. Contamination from the paper bags is negligible (Selmer Olsen, Norwegian Centre for Soil and Environmental Research, pets. com.).

The lichen samples were sent to the laboratory of the Norwegian Centre for Soil and Environmental Research, where they were air dried and stored at room temperature. The samples were cleaned of bark, needles, etc., and then dried at 105°C and ground to a fine powder. The sulphur content was determined by ICP emission spectrometry (Jarrel-Ash 1100) after a previous treatment of 1 g samples with Mg(NP3)2 and HNO3, evaporating to dryness, ashing at 550°C, and dissolving the residue in 100 ml HNO3 (5%). The nitrogen determinations were made on 0.5- 1.0 g of dry material using a macro-Kjeldahl apparatus (Kjeltec). The laboratory's quality assurance program is based on a standard grass sample from a circle test including twenty-eight laboratories in the Nordic countries. This reference sample is analysed prior to all new analyses of plant material. The mean results from the circle test were 2.419+0.0736 g N/100 g and 0.267+0.0315 g S/100 g, and the laboratory's results are 2.464+0.0574 g N/100 g and 0.2614-0.008 g S/100 g (r~ = 20).

Bark samples were also collected at the same sites, and pH was determined as described by Westman (1975). Sampling was mainly done from June to September

30 INGA E. BRUTEIG

• L ichen inves t iga t ion s i tes

o W i t h o u t l i chen inves t iga t ions

Fig. 1. The monitoring network of the Norwegian Institute of Land Inventory (NIJOS), including the sites for sampling Hypogymnia physodes on Pinus sylvestris.


1990, with six samples in October and November. Lichen sampling dates were divided into seven groups for the statistical analysis: June 1-15/June 16-30/July 1-15/July 16-31/August 1 - 15/August 16-31/September 1-December 1.

2.3. STATISTICS

Statistical analyses (correlation analyses, regression analyses) were carried out using the program StatView (Abacus Concepts, 1988). The lichen N and S concentration values were compared to the following datasets:

Nitrogen deposition NO3: annual mean concentration of nitrate in precipitation (mg N L -1)

NO3-wet: annual wet deposition of nitrate (g N m -2)

Nox-dry: annual dry deposition of nitrate, nitric acid and nitrogen dioxide (g N m -2)

NH4: annual mean concentration of ammonium in precipitation

( m g N L -1)

NH4-wet: annual wet deposition of ammonium (g N m -2)

Nred-dry: annual dry deposition of gaseous ammonia and ammonium (g N m -2)

Sulphur deposition 8 0 4 : annual mean concentration of sulphate in precipitation (mg S L -1)

SO4-wet: annual wet deposition of sulphate (g S m -2)

S-dry: annual dry deposition of sulphate and sulphur dioxide (g S m -2)

Environmental variables

pet: annual potential evapotranspiration (mm)

gdd: growing degree-days (°C)

mtwa: mean temperature of warmest month (°C)

mtco: mean temperature of coldest month (°C)

alt: altitude (m above sea level)

apr: annual mean precipitation (mm)

pH: pH in bark samples

season: collection time

2.4 . DEPOSITION DATA

Deposition data were provided from a database of estimated atmospheric deposition in Norway (Pedersen et al., 1990). This model is based on estimates of transboundary transport of sulphur and nitrogen over Europe by the European Monitoring

32 INGA E. BRUTEIG

and Evaluation Programme (EMEP) (Eliassen et al., 1988) and measured values at nineteen background stations (see below) in Norway. The modelled deposition values are calculated on a 50 km × 50 km grid basis. The sea salt contribution to the sulphate deposition is not included in the model. For each square grid estimated values of N and S dry deposition and concentration in precipitation for the time period 1986-1990 have been used. Wet deposition values were calculated from the respective annual mean concentration values (above) and estimated annual precipitation (see below).

Measurements of atmospheric deposition are done regularly at a number of Norwegian background stations, run by the Norwegian Institute for Air Research. For the time period 1986-1990, sulphate, nitrate and ammonium concentrations in precipitation were measured at thirteen stations located relatively close to sampling sites of the present survey. These data, including calculated wet deposition, were used in addition to the estimated deposition data (The Norwegian State Pollution Control Authority, 1987; 1988; 1989; 1991a; 1991b).

2.5. CLIMATIC DATA

Climatic data were obtained from a database on terrestrial climate, which includes weather records from most of the stations operated by the Norwegian Meteorolog- ical Institute (Leemans and Cramer, 1991). The climatic data (long-term monthly values of precipitation, temperature and sunshine hours) were spatially interpo- lated to the actual latitude and longitude values of Hypogymnia physodes sampling sites. The interpolation technique was a triangulation of all datapoints followed by smooth surface fitting (Leemans and Cramer, 1991). Before and after interpolation of temperature, the values were corrected to differences in altitude, using a lapse rate of-0.6°C per 100 m.

Bioclimatic indices were computed from the climatic data at each sampling site, as described by Prentice et al. (1993). 'Growing degree-days' is an index of accumulated temperatures above 5°C during the growth season:

gdd = Si max(0, (Ti - 5))

where Ti is the temperature of day i. 'Annual potential evapotranspiration' (pet) is an estimated value based on temperature, precipitation, latitude and sunshine hours. The estimation is based on a simple, deterministic 'bucket' model, with the assumption that the maximum water capacity of the soil is 150 mm (Cramer and Prentice, 1988).

3. Results

The nitrogen content of Hypogymnia physodes thalli varied in the range of 0.42- 1.96% N of lichen dry weight, the mean of the ten percent highest values being 3.1 times the mean of the ten percent lowest values (Table I). The lowest nitrogen concentrations were among the lowest reported values in lichens (Green et al.,


TABLE I Nitrogen and sulphur contents (% dry weight) of Hypogymnia physodes on stems of Pinus sylvestris in Norway. Sample number, mean, standard deviation, minimum value, maximum value and range of the total sample and of the highest and lowest 10% and 25% of the sample.

NITROGEN SULPHUR

count mean SD min. max. range mean SD min. max. range

total 179 0.83 0.30 0.42 1.96 1.54 0.087 0.024 0.046 0.183 0.137

lowest 10% 18 0.46 0.02 0.42 0.49 0.07 0.055 0.004 0.046 0.059 0.013

lowest 25% 45 0.50 0.04 0.42 0.55 0.13 0.060 0.005 0.046 0.067 0.021

highest 25% 45 1.24 0.20 1.02 1.96 0.94 0.118 0.016 0.103 0.183 0.080

highest 10% 18 1.43 0.19 1.25 1.96 0.71 0.133 0.017 0.118 0.183 0.065

.2,

L ~

t - O.

O3

.18,

.16,

.14,

.12

ol

.08

.06

.04

0 0 0

o o o O O O

o

o ° o

o o

i

o4 .B .8 1 1.2 1.4 1 .'6 1.8

0

Nit rogen

Fig. 2. The relat ionship be tween ni t rogen and sulphur contents (% of dry weight) o f Hypogymnia physodes on Pinus sylvestris at 179 moni to r ing sites th roughout Norway.

1980). The sulphur content values were about 10% of those for nitrogen, ranging from 0.046-0.183% S of lichen dry weight. The mean of the ten percent highest sulphur content values was 2.4 times the mean of the ten percent lowest. The concentrations of the two elements were closely related (Figure 2), with a correlation coefficient of 0.90.

The nitrogen/sulphur ratio ranged mainly from 6.4 to 14.3, with one extreme observation at 21.5, registered in Oslo. In the high deposition areas in southern Norway, the N/S ratio was higher than in the north (Figure 3a). The corresponding map of estimated deposition values also shows a declining tendency towards the

34 INGA E. BRUTEIG

north (Figure 3b), the slope being even steeper. The N/S ratio is higher in Hyp- ogymnia physodes than in deposition, ranging from 4.7 to 21.2 times higher in the lichen (Figure 3c).

The geographical variation of nitrogen and sulphur contents in Hypogymnia physodes is presented by maps showing N and S values divided into four classes (Figures 4 and 5). The highest nitrogen and sulphur concentrations were found mainly along the coast and at some sites in the inland of southem Norway.

A correlation matrix of nitrogen and sulphur contents of Hypogymnia physodes and the estimated and measured environmental parameters, is given in Table II. A large extent of significant correlations exists between the variables. To explore the nature of the relationship between the nitrogen and sulphur contents of Hypogymnia physodes and the available deposition and environmental parameters, stepwise multiple regression techniques were used (Sokal and Rohlf, 1981).

4. Nitrogen

Among the six parameters describing nitrogen deposition three contributed significantly to explain the variation in nitrogen concentration in Hypogymniaphysodes: NO 3 concentration, NH + concentration and NH + wet deposition (Table III). There was a linear relation between measured nitrogen content and NO 3 concentration and NH + wet deposition, while the relation to NH + concentration was best described by a polynomial third order curve (Figure 6). This model explained 48.7% of the variation in measured nitrogen concentration in Hypogymnia physodes. The other nitrogen deposition variables did not contribute significantly to the explanation of variation in lichen N content.

Including also the environmental dataset in the model, the R 2 increased to 0.588 (Table IV). The estimated nitrogen deposition variables were still the most important factors in the model. Growing degree-days and altitude were positively correlated to lichen nitrogen concentration, indicating that lichens growing at high altitudes and in areas with a high temperature sum have a tendency to have higher nitrogen concentration than might be expected from deposition alone. Annual precipitation, bark pH and mean temperature of coldest and warmest month were all negatively correlated to lichen nitrogen concentration. Thus, there is less nitrogen than expected from N-deposition in lichens growing on trees with high bark pH, in areas with mild winters, hot summers, and/or high precipitation.

5. Sulphur

Regression between sulphur concentration of Hypogymnia physodes and the three parameters in the sulphur deposition dataset gave a significant relation to SOl- wet deposition (Table V). This linear relation model accounted for 34.6% of the variation in measured lichen sulphur concentration, a somewhat lower degree of explanation than for nitrogen. The other sulphur deposition variables did not


a.

.9

~q

y = - 0.306x + 28.078; R2 = 0.248 15

14] 0 0

13 0 0 0

11, 10. @ 0

9. 0 0 8.

71 o

6 s? GO 6'2 64 66 6'8 70

1.8

1.6

1,4

1.2

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. 4 .

b. .2

y= -O.O64x+5 .117 ; R2=0.545

[ ]

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s; ob G? o~ G? G? 7b

y = 6 2 6 . 1 9 4 - 20.168x + 0.164x2 ; R2 = 0.629 22-

o

18

"i 16

14 v • v v

W ~ V V V V

C. ! V ~ v

s'8 o'o o'2 G~ G? G'8 latitude

7b

Fig. 3. The relationship between latitude and nitrogen/sulphur ratio of 178 pine forest sites in Norway (one extreme value omitted). (a) Measured N/S concentration ratio in thalli of Hypogymnia physodes; (b) Estimated mean annual N/S deposition ratio: (NO3 -wet + No×-dry + NH4-wet + Nreo-dry)/(SO4-wet + S- dry); (c) N/S lichen ratio/N/S deposition ratio.

36 INGA E. BRUTEIG

/

S

,

0 . 4 2 - 0 . 5 9 %

~:~j 0 . 6 0 - 0 . 8 9 %

0 . 9 0 - 1 .19 %

1 . 2 0 - 1 . 9 6 %

Fig. 4. Total ni trogen content (% of dry weight) o f Hypogymnia physodes thalli on stems o f Pinus sylvestris at 179 sites in Norway.


/ a

_ _ 0 . 0 4 6 - 0 . 0 6 4 %

i i::!iii::;.!l 0 . 0 6 5 - 0 . 0 8 9 %

0 . 0 9 0 - 0 . 1 0 9 %

i 0 . 1 1 0 - 0 . 1 8 3 %

Fig. 5. Total su lphur content (% of dry weight) o f Hypogymnia physodes thalli on s t ems o f Pinus sylvestris at 179 sites in Norway.

38 INGA E. BRUTEIG

g

=,

E

. ~ m l ~

~ ~1 I

o

o

~ ~ ~ ~ ~ ~ _ o o ~ o N o o o o , , , ,

~ ~ ~ ~ ~ ~ . ,

~ ~ ~ - - d d d d d d d d o d d ~

~ - - d d d d d d d d d d d d d d,

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o

o

o

~ v

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g ~ z g

'~. ~. CZ ~ '~. "r, g "

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'41 1.2

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O.8

0.6

0.4

0.2 ' i i I i I i I ' I J I i

0 0.1 0.2 0.3 0.4 0.5 0.6

Precipitation NH4 + (mg N/l)

Fig. 6. Polynomial third-order regression line describing the relationship between lichen nitrogen content and mean concentration of NH + in precipitation, based on samples from 179 monitoring sites in Norway.

TABLE III Multiple regression of nitrogen concentrations of Hypogymnia physodes from 179 sites throughout Norway, to estimated nitrogen deposition criteria.

A n o v a table: /~ = 0.698 •2 = 0.487

Source of variation DF Sum squares Mean square F-test Probability

Regression 3 7.884 2.628 55.447 0.0001

Residual 175 8.294 0.047

Total 178 16.178

Variable Coefficient partial R 2 Probability Intercept 0.363 NO3-conc 2.978 0.250 0.0001 NH4-conc 0.456z - 7.876x 2 + 6.879x 3 0.202 0.0001 NH4-wet 0.0003864 0.035 0.0072

NO3-conc: NH4-conc: NH4-wet:

annual mean concentration of NO~- in precipitation (mg N L -1) annual mean concentration of NH + in precipitation (mg N L - l ) annual wet deposition of NH + (g N m -z)

contribute significantly to explain the variation in lichen S content. As for nitrogen, the model improved when the environmental dataset was in-

cluded: R 2 increased to 0.464 (Table VI). The estimated sulphate wet deposition

40 INGA E. BRUTEIG

TABLE IV Multiple regression of nitrogen concentrations of Hypogymnia physodes from 179 sites throughout Norway.

Anova table: R = 0.747 R 2 = 0.558


Regression 9 9.031 1.003 23.728 0.0001 Residual 169 7.147 0.042 Total 178 16.178

Variable Coefficient partial/~2 Probability Intercept 1.385 NH4-conc -5.331z + 4.282x 2 - 1.924z 3 0.202 0.0001 NO3-conc 2.163 0.078 0.0001 NH4-wet 0.002 0.077 0.0001 gdd 0.002 0.073 0.0001 alt 0.001 0.048 0.0010 apr -0.0002545 0.029 0.0104 mtco -0.035 0.028 0.0111 mtwa -0.126 0.015 0.0594 pH -0.109 0.008 0.1662 Criteria: NO3-conc: NH4-conc: NH4-wet: gdd: alt: apr: mtco: mtwa: pH:

annual mean concentration of NO 3 in precipitation (mg N L -1) annual mean concentration of NH + in precipitation (mg N L -1) annual wet deposition of NH + (g N m -2) growing degree-days (°C) altitude (m above sea level) annual precipitation (mm) mean temperature of coldest month (°C) mean temperature of warmest month (°C) pH of bark samples

TABLE V Simple regression of sulphur concentrations of Hypogymnia physodes from 179 sites throughout Norway, to estimated annual sulphate wet deposition (g S m-2).

Anova table: R = 0.588 R 2 = 0.346


Regression 1 0.035 0.035 93.769 0.0001 Residual 177 0.066 0.000373 Total 178 0.101

Variable Coefficient partial _R 2 Probability Intercept 0.061 SO4-wet 0.0000452 0.346 0.0001


TABLE VI Multiple regression of sulphur concentrations of Hypogymnia physodes from 179 sites throughout Norway.

Anova table: R = 0.681 R 2 = 0.464 Source of variation DF Sum squares Mean square F-test Probability Regression 8 0.047 0.006 18.421 0.0001 Residual 170 0.054 0.00318 Total 178 0.101

Variable Coefficient partial ~2 Probability Intercept 0.159 SO4-wet 0.000098 0.172 0.0001 NH4-conc -0.088 0.073 0.0001 gdd 0.000152 0.073 0.0001 apr -0.0000308 0.072 0.0001 mtwa -0.012 0.022 0.0265 mtco -0.002 0.020 0.0309 alt 0.0000474 0.020 0.0317 pet -0.000157 0.011 0.1135 SO4-wet: NH4-conc: gdd: apr: mtwa: mtco: alt: pet:

annual wet deposition of SO4 z- (g S m -2) annual mean concentration of NH + in precipitation (mg N L -1) growing degree-days (°C) annual precipitation (ram) mean temperature of warmest month (° C) mean temperature of coldest month (° C) altitude (m above sea level) annual potential evapotranspiration (mm)

variable was still the single most important factor in the model. As for nitrogen, growing degree-days and altitude were posit ively correlated to lichen sulphur con-

centration. Annual precipitation and mean temperature of coldest and warmes t month were all negat ively correlated. In addition, there were negat ive correlations to es t imated a m m o n i u m concentrations in precipitation and to annual potential

evapotranspira t ion (pet). Thus, there is less sulphur than expected in lichens growing in areas where the a m m o n i u m concentration in precipitation is high and in mois t areas with high evapotranspiration.

6. Comparisons with Measurements at Background Stations

As the grid of the est imated deposition parameters is rather coarse (50 × 50 km),

and because there may be some uncertainty associated with these est imated factors, a compar ison was made between lichen N and S concentrations and the deposit ion measurements at thirteen Norwegian background stations. The lichen sampling site closest to each station was chosen for new regression analysis.

There was a significant correlation (p = 0.0003) between lichen N concentrat ion

42 INGA E. BRUTEIG

and measured NO 3 wet deposition, R 2 = 0.717 (Figure 7a). The corresponding results for lichen S concentrations and measured SO 2- wet deposition, were p = 0.0005 and R 2 = 0.681 (Figure 7b). The sample number was too small to reveal any significant statistical relations to the environmental variables.

7. Discussion

This survey gives a good large scale picture of the level of nitrogen and sulphur content in Hypogymnia physodes in Norway. There is a distinct tendency of declining concentration values at increasing latitudes. However, there are also recorded some rather large concentration differences between nearby localities.

The sulphur contents in Hypogymnia physodes from 908 cluster sites in a com- parable study in Finland (Kubin, 1990), ranged from 0.0599-0.261%, somewhat higher than in Norway. The nitrogen contents were also higher in Finland, ranging from 0.75-2.56% dry weight. The highest nitrogen concentrations in the present study correspond to levels in southern Finland ten years ago (Pakarinen, 1985). The geographical pattern resembles the Norwegian maps, with the highest concentrations predominantly recorded in the south and south-east (Kubin, 1990).

The high, positive correlation between the nitrogen and sulphur contents sug- gests that most of the variation (about 81%) of one parameter may be predicted given measurements of the other. This indicates that the sources of nitrogen and sulphur deposition in Norway have similar geographical location and that these components are transported along the same path. This agrees with the calculated budgets of airborne sulphur and nitrogen in Europe (Iversen et al., 1991), showing that the domestic contribution of oxidised sulphur and nitrogen wet deposition in Norway is only about 6% and 7%, respectively. The remaining depositions are mainly long range transported contributions from Central Europe and Great Britain. Therefore, even though their initial sources may be different, they follow the same air currents to Norway and their depositions are highly correlated. The figures for reduced nitrogen are more uncertain, but indicate a greater Norwegian domestic contribution (about 30%).

The lower regression coefficients for sulphur compared to nitrogen might be due to impact from sea salt sulphate, which is not included in the deposition model. The sea salt contribution may be substantial at some coastal sites, but decreases rapidly with distance from coast.

The decrease in nitrogen/sulphur ratio with latitude, indicates that nitrogen compounds are deposited faster than those of sulphur. This seems to contradict the general rule that oxidised nitrogen is transported longer than oxidised sulphur before it is deposited (Iversen et al., 1991). However, the lichen N/S ratio agrees well with the estimated N/S deposition ratio in Norway (Figure 3). The slope of the regression is steeper for the deposition parameters than for lichen content, but even at low latitudes the N/S ratio is five to twelve times higher in the lichen than in deposition (Figure 3c). This shows that the lichen uptake of nitrogen is more


a.

1 . 8 "

1.6. ¢-

• -~ 1.4.

~ 1.2.

1, Z ¢-

," .8, .M J

, 6

.4. 0

Y = 0 . 9 8 1 x + 0 . 3 4 7 ; R 2 = 0 . 7 1 8

0

o

0 0 0 0 . , - , - , . , - . . , - , - , . , - ,

.I .Z .3 .4 .S ,6 .7 .8 .9 1

NO3- wet deposition (g N/m z)

b.

.13

. lZ

.11

.09

.081

-8 "-i .07.

.06-

.05 0

y = 0.034x + 0.057; R2 = 0.680

[]

Q ~ El [] []

.z "4 .6 .~ ~ ~.'z 114 1.'0

S042- wet deposition (g S/m 2)

Fig. 7. The relationship between elemental concentrations of Hypogymnia physodes thalli and mean annual wet depositions (1986-1990) at thirteen Norwegian background stations. (a) Lichen N to NO~- wet deposition; (b) Lichen S to SO 2- wet deposition.

44 INGA E. BRUTEIG

efficient than uptake of sulphur, and indicates that the nitrogen uptake is relatively more efficient at low deposition concentrations as in the north.

Lichens grow slowly, but environmental alterations will still influence lichen growth rate (Kfirenlampi et aL, 1989). Factors affecting growth will also influence the accumulation of elements. The results of the present study support this. There is less nitrogen and/or sulphur than expected from deposition data in lichens growing on trees with high bark pH, in areas with mild winters, hot summers, high precipitation, high ammonium concentration, and/or high evapotranspiration. All these variables are growth promoting factors, and are therefore likely to cause a dilution of lichen elemental concentrations. The relatively high nitrogen and sulphur concentrations registered at some inland sites in southern Norway (Figures 4 and 5), may partly be explained by unfavourable growth conditions. These areas have long and cold winters and low summer precipitation.

Altitude can be viewed as a complete climatic factor. Shorter growing season accompanied with lower temperatures and higher wind speed generally results in lower annual growth rate. The positive regression coefficient to both nitrogen and sulphur lichen concentrations, indicates low lichen growth and enhanced elemental accumulation at high altitudes.

The positive correlation to growing degree-days is surprising. Under moist conditions, a moderately high temperature sum is assumed to promote photosynthesis (Kershaw, 1985), which will increase the lichen growth rate and cause a dilution of the elements. This would suggest a negative correlation between elemental content and growing degree-days. The highest temperature sums in Norway are found along the southem and westem coastline, coinciding with the high deposition areas. The positive correlation to growing degree-days may thus be expressing uncertainty in the deposition model, rather than anomalous lichen growth.

There have been some reports of seasonal differences in lichen and moss elemental concentrations throughout the year (Chapin et al., 1980; Pucket, 1985; Markert and Weckert, 1989). In the present work, there are no signs of systematic differences between samples collected at different parts of the growing season from May to November. However, this study is not designed to intercept such seasonal variance, and the existence of seasonal differences cannot be excluded.

The analysis of the main dataset in this study indicates that almost 50% of the variation in lichen N concentration and 35% of lichen S concentration could be explained by deposition of the two elements. The explanatory power of deposition is however probably underestimated. The analysis of the thirteen stations where actual deposition data are available indicate that about 70% of the variation in lichen N and S contents could be attributed to variations in deposition. Hence, actual deposition of nitrogen and sulphur may account for a larger part of the variation in Hypogymnia physodes N and S concentration than assumed from the regression analyses in Tables III and V.

From this study it seems likely that a major part of the variation in N and S concentration in thalli of Hypogymnia physodes can be explained by atmospheric


deposition of the two elements and by gross climatic variables. The relative importance of the deposition versus other environmental variables cannot be identified or estimated merely from regression analysis, but the environmental data complement the deposition estimates and improve the precision of the model. Influence from variables left out of the model cannot be excluded, as there is a large extent of correlation between the variables (Table II).

The regression and correlation analysis were carried out on mean annual deposition, average concentration levels and average macro-meteorological data. The lichen response, however, is a function of the number, frequency and duration of the deposition episodes and recovery periods, as well as of micro-environmental factors such as humidity, light and temperature fluxes. Local differences of the sample site forests, such as tree density, exposition, exposure to wind and fog, will influence growth and elemental uptake. Also, there may be local pollution sources causing enhanced elemental concentrations. The remaining unexplained variation may be caused by 'uncontrolled' factors such as influence from canopy leakage and different age of lichen individuals.

Acknowledgements

This study was financed by the Directorate for Nature Management as part of the Terrestrial Monitoring Programme. The field work was done by research teams of the Norwegian Institute of Land Inventory (NIJOS). The chemical analyses were done at the Centre for Soil and Environmental Research (Landbrukets Anal- ysesenter), ,~s. I am also grateful to Wolfgang Cramer, Department of Geography, University of Trondheim, for providing and processing the climatic data, and to Ulf Pedersen, Norwegian Institute of Air Research (NILU) for providing the estimated deposition data. Thanks are due to Kjell I. Flatberg, Staffan Karlsson, Eiliv Steinnes, and Wolfgang Cramer for critical comments on the manuscript.

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The epiphytic lichen hypogymnia physodes as a biomonitor of atmospheric nitrogen and sulphur deposition in Norway