Acidity of boreal Picea abies-canopy lichens and their substratum, modified by local soils and airborne acidic depositions

Flora (1998) 193 249-257

© by Gustav Fischer Verlag

Acidity of boreal Picea abies-canopy lichens and their substratum, modified by local soils and airborne acidic depositions YNGVAR GAUSLAA 1 and HAKON HOLIEN 2 1 Department of Biology and Nature Conservation, The Agricultural University of Norway, P.O. Box 5014, N -1432 As, Norway. 2 Department of Resource Sciences, Nord-Tr!/lndelag College, P.O. Box 145, N-7701 Steinkjer, Norway.

Accepted: April 16, 1997

Summary Lichens of the rare and predominantly epiphytic old forest community Lobarion were attached to Picea abies twigs with significantly higher bark pH (KCI) than members of the common and ubiquitous Pseudevernion community. The Lobarion species of spruce twigs, mainly members of the order Peltigerales, had distinc1y higher thallus pH than substratum pH, while the greenalgal Pseudevernion species, mainly belonging to the Lecanorales, were consistently more acidic than their substratum. pH of lichens and bark of P. abies twigs responded to a forest vegetation gradient reflecting the soil nutrient condition at the forest floor. However, the two groups of epiphytes seem to modify the bark pH in a way that enlarges a difference originally determined by soils in the root zone of the phorophyte. The lack of the Lobarion on spruce twigs in eastern Norway is probably a result of acid rain, as the bark and thallus pH in spruce canopies of eastern Norway appeared too low to support the Lobarion, even in stands with a species-rich epiphytic assemblage of alectorioid species . Key words: epiphytic lichens, Picea abies, pH, Lobarion, air pollution, secondary components

1. Introduction Canopy lichens modify the deposition of water and nutrients in the throughfall collected beneath a canopy (LANG et al. 1976, KNOPS et al. 1996). Lichens with cyanobacterial photobionts also add significant amounts of nitrogen to a forest ecosystem (FORMAN 1975) . Within the boreal region, a rich assembly of green-algal lichens normally belong to the common and frequently intergrading ubiquitous Pseudevemion and Usneion communities (sensu JAMES et al. 1977), while lichens with cyanobacteria dominate the rare and spatially scattered Lobarion community. The Lobarion, considered to be a characteristic epiphytic community of broadleaved forests with a long ecological continuity (ROSE 1974, 1976, 1988, 1992), extends northwards into old conifer-dominated ecosystems influenced by an oceanic climate along the seaboards oflarge oceans (e.g. AHLNER 1948, RHOADES 1981, 1995, MCCUNE 1993). Nowadays, the Lobarion is normally restricted to scattered deciduous trees situated in a matrix of conifers within European boreal forests, probably because of its requirements for a high pH of the substratum (GAUSLAA

1995). The bark of the dominant conifers in NW Europe, Picea abies and Pinus sylvestris, is generally considered to be too acidic for the Lobarion (e.g. ROSE 1988), and the more acidophytic Pseudevemion is therefore a dominant epiphytic community. BARKMAN (1958) does not report the Lobarion from these phorophytes. Nevertheless, a species-rich Lobarion community represents a major epiphytic biomass component of P. abies twigs in sheltered old forest stands in the boreal rainforest zone of central Norway (AHLNER 1948, HAUGAN et al. 1995, HOLIEN & T(ZJNSBERG 1996, T(ZJNSBERG et al. 1996), with the only or main European populations of the very rare lichens Erioderma pedicellatum, Lobaria hallii and Pannaria ahlneri. The richness of cyanobacterial lichens in pure P. abies forests suggests a unique ionic environment within the canopy which is apparently undescribed. This boreal Lobarion community is highly threatened, in a short-term perspective mainly because of modem forestry (T(ZJNSBERG et al. 1996, GAUSLAA & OHLSON 1997). The Lobarion is also highly susceptible to acid rain (GILBERT 1986, LOONEY & JAMES 1988, FARMER et al. 1991a, b, 1992, GAUSLAA 1995, GAUSLAA etal. 1996), FLORA (1998) 193

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probably because of its high pH requirements. In the first part of this century, a species-poor Lobarion-community was found on P. abies twigs even in eastern parts of Scandinavia (SERNANDER 1936, HAKULINEN 1964), but has declined or become extinct even in protected forest stands without any logging. This decline over major areas is probably due to airborne acidic depositions, as the bark of conifers is likely to be poorly buffered against acidic depositions (SKYE 1968). The Lobarion-rich P. abies forests of central Norway are shielded behind large mountain ranges, resulting in low concentrations and depositions of acidifying components (T0RSETH & PEDERSEN 1994, T0RSETH 1996), unlike the more exposed boreal zone of southeastern Norway where the Lobarion nowadays is virtually absent from conifer twigs. A main objective of the present study is to measure ion exchange by means of pH measurements of twigs and lichens submerged in KCI, sampled in the localized and highly fragmented remnants of old, Lobarion-rich P. abies stands of central Norway. For comparison, the ubiquitous Pseudevernion community, normally replacing the Lobarion after clear cutting, will be subjected to a similar analysis. In this study, the term Pseudevernion is used in a fairly wide sense. It includes an epiphytic vegetation dominated by pure green-algal fruticose and more or less erect foliose lichens that commonly dominate the more oligotrophic phorophytes, which means that Usneion-like communities are included. A second objective is to evaluate the effect of acid rain by comparing pH (KCI) of the ubiquitous Pseudevernion community and its substratum in natural P. abies stands of relatively unpolluted parts of central Norway with acid rain-influenced areas of SE Norway. As especially green algal lichens contain large amounts of secondary components, up to 30% of the thallus dry weight (HUNECK 1973), a third objective is to study the effect of secondary components upon the pH in lichen thalli.

2. Materials and methods

2.1. Study areas Central Norway, represented by the northern cluster of study sites in Fig. 1, is one of the least polluted parts of Europe, with a mean pH in the rainfall of 5.2. Nitrate and ammonium-concentrations in the rainfall were both around 0.1 mg N I-lor below for 1995 (TfZlRSETH 1996). The total deposition for the period 1988-92 was less than 300 mg S m-~ year-I, the total nitrogen deposition less than 200 mg N m-2 year- I for oxidised und reduced nitrogen (TfZlRSETH & PEDERSEN 1994). These deposition values are below measured values of Loch Sunart in NW Britain, one of the richest Lobarion sites in England (FARMER et al. 1991 b). Sampled areas in southeastern Norway have a total sulphur deposition of 700 -1200 mg S m-2 year-I,

250

FLORA (1998) 193

Fig. 1. Location of study areas. The southern cluster of dots refers to eastern Norway, the northern cluster to central Norway. Mean pH in the precipitation for 1995 according to TfZlRSETH (1996) is included. The pH lines were transferred from an original map of a smaller scale, so their positions are less accurate than topographical details. a deposition of oxidised and reduced nitrogen of respectively 500-900 and 400-800 mg N m-2 year- I (TfZlRSETH & PEDERSEN 1994). The regional distribution of pH in the rainfall (Fig. 1) corresponds well to the regional distribution of respectively sulphate-, nitrate, and ammonium-concentrations of the rainfall (TfZlRSETH 1996), but also to the regional distribution of respectively the total nitrogen and sulphur content of Hypogymnia physodes thalli (BRUTEIG 1993). In central Norway the Lobarion is locally abundant on Picea abies twigs, especially in shielded P. abies-covered

brook ravines on nutrient-rich marine sediments rich in clay. In such ravines there is typically a gradient in ground vegetation from nutrient-demanding herbs and tall ferns along the brook and lower slopes to an oligotrophic vegetation dominated by ericaeous species on the upper slopes that often border ombrotrophic bogs at the plateau separating the numerous meandering ravines. The Lobarion community was found in nutrient-rich parts of the vegetation gradient, representing Eu-Piceetum dryopteridosum and Eu-Piceetum athyrietosum (KIELLAND-LuND 1981). Lobarion-twigs collected for measurements harboured characteristic species like Degelia plumbea, Lobaria amplissima, L. pulmonaria, L. scrobiculata, Nephroma bellum, N. parile, Normandina pulchella, Pannaria ahlneri, P. rubiginosa, Parmeliella parvula, Peltigera collina, Pseudocyphellaria crocata, Stictafuliginosa, sometimes with minor components of non-Lob arion species like Cavernularia hultenii, Platismatia glauca and Ramalina thrausta intermingled among the characteristic species. Species in bold represent the most widespread species in central Norway, the remaining are restricted to sites near the open ocean. The Pseudevernion community dominated the oligotrophic part of the gradient with forest types like Vaccinio-Pinetum and Eu-Piceetum myrtilletosum (KIELLAND-LuND 1981). However, in richer vegetation types in central Norway, the Pseudevernion was found intermingled with the Lobarion. Sampled twigs contained species like Alectoria sarmentosa, Cavernularia hultenii (c), Bryoria capillaris, B. fuscescens, B. nadvornikiana (e), Hypogymnia physodes, H. tubulosa, Parmelia sulcata (c), Platismatia glauca, P. norvegica (c), Ramalina thrausta (c), Pseudevernia furfuracea, Usnea jilipendula, and U. longissima (e), but with no traces of any cynanobacteriallichen. Species in bold are common on Picea abies and occur on sampled twigs in both eastern (e) and central Norway (c), remaining species are absent or very rare in one of the two regions.

2.2. Methods Twigs of the lower branches of mature and naturally occurring Picea abies supporting a rich flora of epiphytic lichens, belonging to either the Pseudevernion or the Lobarion, were selected. Forest vegetation types were recorded according to KIELLAND-LuND (1981). Sampling sites are shown in Fig. 1. Both Pseudevernion and Lobarion twigs were sampled from the localities of central Norway, only the former was present in SE Norway. Twigs were sampled while moist, put in plastic bags and kept cool, brought to the laboratory, and analysed within 1-2 days while still hydrated. From each twig, one 6 cm long and 5-7 mm thick, needle-free segment with a high cover of foliose and/or fruticose lichens was cut. Crustose lichens were absent or scarcely represented in selected sections. All lichens were removed, and the alive lichen biomass without contaminations of bark fragments or dead material was submerged in a vial contaning 6 ml 25 mM KCl, an ion exchange method, slightly modified after FARMER et al. (1990). Since fresh thalli were used, the lichen biomasses were not weighed, but approximated 400 mg dry weight. Only twigs with apparently similar amounts of lichen biomass were selected. The cut ends of the 6 cm lichen-free twig were sealed

by melted wax, and the sealed segment without remains of dead or alive lichen biomass was given the same treatment as its corresponding lichen biomass. Samples were kept one hour at room temperature in corked vials with KCI and shaken by regular intervals. The samples were then removed, and pH immediately measured in the KCl. pH measured in control vials with pure KCl was 5.65 ± 0.06 (mean ± standard error of means, n =10). Preliminary experiments showed that increasing the duration of the KCI treatment from 1 to 20 hours hardly had any influence on the pH measurements. According to FARMER et al. (1990), readings of pH in KCI can be taken already after 5 minutes. Since the Lobarion seemed to be an old forest community, 5 twigs from an old as well as from a neighbouring stand, originating from a clear felling 40 years ago, were sampled in one single locality. Exposition and ground vegetation was the same in the two stands, but the canopy of the 40 years old stand was completely devoid of Lobarion species. In order to check the significance of the weakly acidic secondary components upon pH of lichen thalli, air-dry thalli of Hypogymnia physodes, Platismatia glauca, Alectoria sarmentosa and Usneafilipendula were rinsed repeatedly 5 times, 5 minutes each time with acetone. Repeated acetone-rinsings of air dry lichen thalli neither affected photosynthesis nor long-term growth and survival in the field (SOLHAUG & GAUSLAA 1996). Eight randomly selected replicates consisting of 160 mg air-dry lichen material were taken from one large sample of each species separately. Four of these were rinsed with aceton before being submerged in KCl for I hour, the remaining 4 were not aceton-rinsed.

3. Results Bark pH (KCI) of Picea abies-twigs varied from around 3.7 to 4.9, which represents a considerably smaller pH range than of corresponding epiphytic biomass (3.4-5.4; Fig. 2). However, the variation within one single epiphytic community was much less, being 3.4-4.3 in Pseudevemion lichens compared to a total range of 4.4-5.4 in Lobarion lichens. Thalli of Lobarion species were therefore seemingly of a special constitution with respect to ion-exchange capacity, by rising the pH in 25 mM KCI to a significantly higher level (4.72± 0.03) than sympatric Pseudevemion species (4.03 ± 0.02; Tab. I). Species-specific differences were small within a given epiphytic community (Tab. 1). The Lobarion species were distinct also in having a higher pH than their substratum, indicated by a well-defined position above the 1: I-line in Fig. 2, while Pseudevernion lichens were more acidic than their substratum. The pH of the substratum differed highly significantly between the Lobarion (4.38 ± 0.03) and even sympatric Pseudevemion (4.17 ± 0.03; Tab. 1). However, unlike the pH of the lichens themselves, a considerable degree of overlap was found between individual pHvalues of the bark (Fig. 2). Highly significant correlaFLORA (1998) 193

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tions between pH of lichens and bark were found in all major sampled groups, as well as in the pooled sample (Tab. 2). The regression coefficients of the two sampled epiphytic communities within central Norway were similar, but deviated considerably from the regression coefficient of a pooled sample. Significant correlations for individual species were only found for Platismatia glauca from central Norway, Lobaria scrobiculata, and for Usnea longissima (Tab. 2), but the numbers of observations for most single-species dominances (Tab. 1) were generally too low for regression analyses. While the Pseudevernion could be sampled from the most oligotrophic forests to forests on rich and flushed soils, the Lobarion was only found in the richer part of this gradient (Tab. 3). Within the ubiquitous Pseudever-

nion, bark pH as well as lichen pH differed highly significant between sampled forest types (P < 0.001, ANOVA). The lowest pH values were measured in the most oligotrophic environment, the highest in the edaphically richest sites (Tab. 3). However, the pH-values of the rarer and more specialized Lobarion showed little variation between forest types (Tab. 3). In the richest part of the edaphic gradient, no difference between bark pH of the two contrasting epiphytic communities was found, in spite of a significant difference in lichen pH (Tab. 3). Some evidence was found suggesting that stand age also plays a role for the high pH of the P. abies twigs supporting the Lobarion in central Norway. pH of the P. abies twigs in the old growth forest were 4.77 ± 0.04

Table 1. pH of bark of Picea abies-twigs and of their lichen cover, measured in 25 mM KCl. Means ± standard errors of means are given for the two epiphytic communities Lobarion and Pseudevernion, and for individual species separately in cases when one species totally dominated the lichen community in sampled twig segments. n represents number of observations. Epiphytic vegetation types

n

Bark pH

Lichen pH

Lobarion, central Norway Pseudevernion, central Norway Pseudevernion, eastern Norway

62 40 101

4.38 ± 0.03 4.17 ± 0.03 3.95 ± 0.01

4.72± 0.03 4.03 ± 0.02 3.71 ± 0.01

Lobarion, single species dominance: Lobaria pulmonaria Lobaria scrobiculata Nephroma bellum Pseudocyphellaria crocata

3 25 2 3

4.12± 0.06 4.35 ± 0.04 4.16 4.26 ± 0.09

4.40 ± 0.16 4.82± 0.05 4.58 4.48 ± 0.06

Pseudevernion, single species dominance Alectoria sarmentosa Bryoria spp. Hypogymnia spp., mainly H. physodes Platismatia glauca, eastern Norway Platismatia glauca, central Norway Pseudevernia furfuracea Usnea jilipendula Usnea longissima

10 5 23 12 14 10 2 14

3.96± 0.02 3.91 ± 0.06 3.98 ± 0.02 3.98 ± 0.03 4.24± 0.06 3.88 ± 0.03 3.88 3.96± 0.02

3.75 ± 0.02 3.75 ± 0.02 3.69 ± 0.02 3.77 ± 0.01 4.10 ± 0.04 3.62± 0.05 3.58 3.76± 0.02

Table 2. Linear regression equations for pH of lichens, correlation coefficients (r), level of significance (P), and number of observations (n) for the major sampled groups in Fig. 2. Only single species in Tab. 1 with a significant correlation were included. Regression equation

r

P

n

All samples

- 2.129 + l.506 pH (bark)

0.819

0.001

203

Lobarion, central Norway Pseudevernion, central Norway Pseudevernion, eastern Norway

2.217 + 0.572 pH (bark) l.773 + 0.541 pH (bark) 2.026 + 0.427 pH (bark)

0.588 0.751 0.410

0.001 0.001 0.001

62 40 101

Single species dominance P. glauca, central Norway only Lobaria scrobiculata Usnea longissima

1.630 + 0.583 pH (bark) 2.576 + 0.516 pH (bark) l.451 + 0.583 pH (bark)

0.938 0.433 0.534

0.001 0.031 0.049

14 25 14

252

FLORA (1998) 193

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Table 3. pH of bark of Picea abies-twigs and of their lichen cover, measured in 25 mM KCl. Means ± standard errors of means are given for the epiphytic communities Lobarion and Pseudevernion in 4 forest communities ranked from the Vaccinio-Pinetum (KrELLAND-LuND 1982) on very oligotrophic soils to the Eu-Piceetum athyrietosum on rich and flushed soils. n represents number of observations. Forest vegetation types

n

Bark pH

Lichen pH

Vaccinio-Pinetum, with Pseudevernion only Eu-Piceetum myrtilletosum, Pseudevernion only Eu-Piceetum dryopteridetosum, Pseudo + Lob. Pseudevernion only Lobarion only Eu-Piceetum athyrietosum, Pseudo + Lobarion Pseudevernion only Lobarion only

15 93 47 28 19 48 5 43

3.92± 0.02 3.99 ± 0.02 4.25 ±0.05 4.06± 0.03 4.52± 0.06 4.34± 0.03 4.44±0.09 4.32± 0.03

3.63 ± 0.04 3.78 ± 0.02 4.22± 0.07 3.87 ± 0.03 4.74 ± 0.05 4.68 ± 0.04 4.22± 0.06 4.72±0.04

(mean ± st. errors of means, n = 5) compared to 3.87 ± 0.07 (n =5) in the 40 years old stand, while lichen pH was respectively 4.94 ± 0.03 (Lobarion species) and 3.83 ± 0.03 (Pseudevernion species). Eastern Norway, highly influenced by acid rain (Fig. 1), showed lower pH-values both in lichens and their substratum, compared to the nearly unpolluted sites of central Norway (Fig. 2 and Tab. 1). One species, Platismatia glauca frequently dominated sampled Pseudevernion twigs in both central and eastern Norway. The pH values for this species were therefore given

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pH, control thalli

pH, acetonerinsed thalli

Hypogymnia physodes Platismatia glauca Alectoria sarmentosa Usnea jilipendula

3.58 ± 0.018 3.84±0.030 4.05 ±0.048 3.93 ±0.038

3.62 ± 0.018 3.89±0.018 3.97 ± 0.047 3.80± 0.043

, •.

for the two regions separately (Tab. 1). The pH level and the difference in pH between the two regions for this particular species corresponded well to the pH-measurements of the whole epiphytic community (Tab. 1), indicating that the difference between the pH of the two regions was not influenced by contrasting species composition. Extraction of secondary components by repeated acetone-rinsing did not influence the thallus pH of any of the four tested Pseudevernion species (Tab. 4) that were selected because of their diverse secondary chemistry. The four species sampled from the same tree differed highly significantly (P < 0.001) from each other, but no effect of the acetone treatment was detected (two-way analysis of variance).

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Table 4. pH in control thalli and in actone-rinsed air-dry thalli from one single Picea abies tree of eastern Norway. A sample of 160 mg air-dry thalli of each species was submerged in 6 ml KCl for 1 hour before measurements. Mean values ± standard errors of means (n = 4) are given. A two-way analysis of variance gave a significant effect of species only (P < 0.001), not of secondary components.

4.6

4.8

5.0

pH of Picea abies-bark

Fig. 2. The relationship between pH (KCl) of epiphytic lichen thalli on twigs of Picea abies and of the phorophyte bark on which they were situated. The 1: I-line is given. Circles represent the Lobarion species and their local substratum, quadrats represent Pseudevernion species. Filled symbols represent the pH values in central Norway, open symbols refer to eastern Norway.

4. Discussion A high leaching of protons from the vegetation is likely to cause acidification of the environment, as has been documented for some bryophytes (CLYMO 1964, 1973, KOOIJMAN & BAKKER 1994). The present results (Fig. 2) indicate that also some lichens acidify their substratum, FLORA (1998) 193

253

even when the substratum is Picea abies which acidifies its own soils (e.g. NIHLG,.\RD 1971). Lobarion lichens are, however, less acidic than their substratum (Fig. 2). Their influence of pH in distilled and deionized water (GAUSLAA et al. 1996) suggests that they at least temporarily might release more cations than protons from available ion-exchanging sites. Measurements of pH in distilled and deionized water after rinsing Lobaria pulmona ria thalli, gave a pH of 5.60±0.05 (mean± standard error of mean, n =90, total range 4.8 - 6.7 ; GAUSLAA et al. 1996), i.e. 0.88 pH-units above the present KCl measurements (Tab. 1); (see also TURK et al. 1974). Similar measurements on Usnea longissima resulted in a pH (H20) of 5.01 ± 0.05, n =33; GAUSLAA, unpublished data), i.e. slightly more than one pH unit above the pH (KCl) values given in Tab. 1. Platismatia glauca lowered the pH of simulated rain water from 6.0 to 4.6 within one hour of thallus submergence (LANG et al. 1976). While several L. pulmonaria thalli often increased the pH of rinsing water (GAUSLAA et al. 1996), the two mentioned Pseudevemion species consistently acidified the rinsing water or the simulated rain water. Unlike distilled water, KCl always caused a net release of protons from lichens. However, Lobarion samples released small amounts of protons in KCl, the second most acidic Lobarion sample released less protons than the least acidic Pseudevemion sample (Fig. 2). The Lobarion is normally restricted to the lower half of the canopy, which is consistent to the assumption of PIKE (1978) that canopy leaching experiences higher concentrations of minerals in solution than lichens of the upper canopy. GAUSLAA (1985) found a two-peaked distribution of bark pH of randomly selected Quercus stems in an apparently homogenous oak forest in southern Norway, with less acidic stems dominated by the Lobarion intermingled between more acidic stems supporting the Pseudevemion. A closer study revealed pockets of richer soils that could explain the areal distribution of Lobarion stems, but not the two-peaked pH-distribution. This pH-distribution, additionally supported by the present results (Fig. 2, Tab. 1), indicates that the two studied groups of lichen epiphytes are able to modify the bark pH in a way that enlarges a difference originally determined by soils in the root zone of the phorophytes. Similar pH-modifying responses of the environment have already been documented for contrasting wetland bryophytes (KOOIJMAN & BAKKER 1994), and ground-dwelling forest bryophytes (ZIEGENSPECK 1937). The dominant species within each of the two sampled communities are not only ecologically similar. All dominant Lobarion species on sampled twigs belong to the Peltigerales, while Pseudevemion species are members of the Lecanorales sensu CANNON et al. (1985). A contrasting secondary chemistry (CULBERSON 1969, 254

FLORA (1998) 193

CULBERSON et al. 1977), possibly also contrasting polysaccharides in cell walls (SHIBATA 1973), of members of the two groups reflect this taxonomic division. Secondary components have been demonstrated to play a role in chemical weathering of rocks by forming soluble metal complexes (ISKANDAR & SYERS 1971, 1972, AscAso et al. 1976, PURVIS et al. 1987). Unlike the Lobarion species, Pseudevemion species have substantial amounts of lichen acids, that could potentially reduce the pH (BARKMAN 1958). However, Tab. 4 confirms the conclusions of BROWN (1976) and RICHARDSON et al. (1985) that secondary components hardly influence the lichen pool of cation exchange sites. While uptake of cations by the reversible passive mechanism in lichens has been interpreted as an ion exchange phenomenom (TuOMINEN 1967, PUCKETT et al. 1973), the nature of the binding molecules in lichens seems to be unsufficiently known. The distinct difference between the two taxonomic groups (Tab. 1) suggests that such binding molecules could be of different types and/or of different frequencies. Although cell wall characteristics might prove useful, they have not so far been used or regarded as important criteria for classification oflichenized fungi (HAFELLNER 1988). Chitin seems to be a ubiquitous and quantitatively important hyphal wall component of members of Peltigerales, while Pseudevemion species have less chitin, apparently restricted to hyphae of the algal layer (SCHLARMANN et al. 1990). Chitin, being considered a useful material for the removal of metals from contaminated water (YANG & ZALL 1984), could possibly be a decisive component, see also BROWN (1976). Cell-wall proteins might, however, also be important (RICHARDSON et al. 1985). Some lichens within Peltigerales apparently have greater sensitivity to heavy metals than other lichens (BROWN & BECKETT 1984). The two studies groups also differ in type of photobiont. Since photobionts comprise a small fraction of a lichen thallus, their contribution to ion uptake can be expected to be small. The cyanobacterial Lobarion species fix nitrogen that ultimately enriches the ecosystem (FORMAN 1975). PIKE (1978) reported that organic nitrogen compounds leach from nitrogen fixing lichens during misting experiments. However, it is far from obvious how nitrogen as such could have produced the contrasting pH of the two communities. Nitrogen might indirectly playa role since there seems to be a correlation between amount of chitin and total nitrogen in lichens (SCHLARMANN et al. 1990). Otherwise nitrogen fixation in various symbiotic and free-living bacteria seems to be asscociated with natural ecosystems or microsites with an intermediate or high pH, rather than being able to reduce acidity. The pollution sensitivity of Lobarion lichens and several Pseudevemion species is well documented, but

r !

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r I

J

has normally been related to S02' e.g. HAWKSWORTH (1990). In Norway, even maximal concentrations of S02 in rural areas of southern Norway (T0RSETH 1996) are far below the 30 f-tg m-3 level which HAWKSWORTH & ROSE (1970) considered to be a threshold level for the existence of the Lobarion. The decline of Scandinavian distribution of the Lobarion (e.g. HALLINGBACK 1986, HALLINGBACK & MARTINSSON 1987, HALLINGBACK & THOR 1988, T0NSBERG et al. 1996) is probably mainly a result of long-transported acidifying components from foreign sources, not of S02' These acidifying components have not only caused a reduction in soil pH (FALKENGREN-GRERuP 1986, 1989, NILSSON & TYLER 1995), but also in lichen thalli. The acidification of Pseudevernion thalli in eastern compared to central Norway (Tab. 1) is comparable to a reported decline in pH (H20) of Hypogymnia physodes along an ambient acidification gradient in eastern Canada (ROBITAILLE et al. 1977). Within southern Norway the lowest pH-records were associated with a more stunted appearance of lichen thalli, there was a tendency that pH-values were slightly higher in sites with the most vigorous Pseudevernion-vegetation of alectorioid lichens, i.e. in the northernmost locality of eastern Norway (Fig. 2). In the more polluted Germany, the Pseudevernion species Hypogymnia physodes and Platismatia glauca had thallus pH (H20) of only 3.5, reduced to respectively 3.2 and 3.4 during an S02-fumigation experiment (TURK et al. 1974), which probably corresponds to an even lower KCl-pH. Evergreen south Scandinavian Picea abies canopies receive a total deposition of H+ two to eight times the deposition to deciduous-dominated canopies, due to a more efficient air filtration (BERGKVIST & FOLKEsoN 1995), which could explain why the decline of Lobarion has been especially high in spruce forests. A higher epiphytic biomass and more alectorioid lichens was often observed on lower branches of Picea abies situated within the canopy-dripping zone of a neighbouring Betula tree in the most acidified stands, suggesting either a reduced filtration of acidic components, or a neutralizing effect of deciduous trees. Lobarion species have also been shown to be especially susceptible to high light. Logging operations are therefore detrimental to these species by causing a sudden increase in light intensity on remaining lichens (GAUSLAA & SOLHAUG 1996). However, since total proton load may be 7 times higher at a spruce forest edge, than in the interior of the stand (BALSBERG PAHLSSON & BERGKVIST 1995), clear fellings are likely to aggravate the effects or air pollution. The influence of forestry and acid depositions are therefore normally confounded in forests of eastern Norway. Low levels of acidic depositions could be one contributing factor why the Lobarion in central Norway appear more resistant to forestry

manipulations than the Lobarion in eastern Norway. Recorded data indicating a positive relationship between stand age and pH should be regarded preliminary, as only one pair of stands was compared. Further, a negative correlation has been documented in P. abies stands where the Pseudevernion represents the climax epiphytic vegetation (HYVARINEN et al. 1992). In conclusion, the results indicate that the mineral status of different components, like epiphytes, trees and soils are strongly coupled within a mycorrhiza-dependent forest ecosystem, which means that a change in one of these components is likely to influence the structure and function of a shallow-rooted and leached Scandinavian spruce ecosystem in a long-term perspective. The coupling between the three components is highly modified by long-transported acidic components over major areas, as was also concluded by GAUSLAA (1995).

Acknowledgements This study was funded by the Norwegian Research Council, and is a part of a project focussing on forest history and biological processes. Thanks to KIETIL T0RSETH at the Norwegian Institute for Air Research for providing the pollution data used in Fig. 1, and to MIKAEL OHLSON for interesting discussions.

References AHLNER, S. (1948): Utbredningstyper bland Nordiska barrtradslavar. Acta Phytogeogr. Suecica 22: 1-257. ASCASO, A., GALVAN, 1., & ORTEGA, C. (1976): The pedogenic action of Parmelia conspersa, Rhizocarpon geographicum and Umbilicaria pustulata. Lichenologist 8:

151-171. BALSBERG PAHLSSON, A.-M., & BERGKVIST, B. (1995): Acid deposition and soil acidification at a southwest facing edge of Norway spruce and European beech in south Sweden. Eco!. Bull. 44: 43-53. BARKMAN, J. J. (1958): Phytosociology and ecology of cryptogamic epiphytes. Van Gorcum, Assen. BERGKVIST, B., & FOLKESON, L. (1995): The influence of tree species on acid deposition, proton budgets and element fluxes in south Swedish forest ecosystems. Eco!. Bull. 44:

90-99. BROWN, D. H. (1976): Mineral uptake by lichens. In: BROWN, D. H., HAWKSWORTH, D. L., & BAILEY, R. H. (eds.): Lichenology: progress and problems. Academic Press, London, 419-439. -, & BECKETT, R. P. (1984): Uptake and effect of cations on lichen metabolism. Lichenologist 16: 173 -188. BRUTEIG, I. E. (1993): The epiphytic lichen Hypogymnia physodes as a biomonitor of atmospheric nitrogen and sulphur deposition in Norway. Environmental Monitoring and Assessment 26: 27-47.

FLORA (1998) 193

255

CANNON, P. F., HAWKSWORTH, D. L. & SHERWOOD-PIKE, M. A. (1985): The British Ascomycotina. An annotated checklist. Commonwealth Mycological Institute, Slough. CLYMO, R. S. (1964): The origin of acidity in Sphagnum bogs. Bryologist 67: 427-431. - (1973): The growth of Sphagnum: some effects of environment. J. Ecol. 61: 849-869. CULBERSON, C. F. (1969): Chemical and botanical guide to lichen products. The University of North Carolina Press, Chapel Hill. - CULBERSON, W. L., & JOHNSON, A. (1977): Second Supplement to "Chemical and botanical guide to lichen products". The American Bryological and Lichenological Society, Missouri Botanical Garden, St. Louis. FALKENGREN-GRERUP, U. (1986): Soil acidification and vegetational changes in deciduous forest in southern Sweden. Oecologia 70: 339-347. - (1989): Effect of stemflow on beech forest soils and vegetation in southern Sweden. 1. Appl. Ecol. 26: 341-352. FARMER, A. M., BATES, 1. w., & BELL, 1. N. B. (1990): Acomparison of methods for the measurement of bark pH. Lichenologist 22: 191-197. -, -, - (1991a): Comparison of three woodland sites in NW Britain differing in richness of the epiphytic Lobarion pulmonariae community and levels of wet acidic deposition. Holarctic Ecol. 14: 85-91. -, -, - (1991b): Seasonal variations in acidic pollutant inputs and their effects on the chemistry of stemflow, bark and epiphyte tissues in three oak woodlands in N. W. Britain. New Phytol. 118: 441-451. - (1992): The transplantation of four species of Lobaria lichens to demonstrate a field acid rain. In: SCHNEIDER, T. (ed.): Acid rain research, evaluation and policy application. Elsevier, Amsterdam, 295-300. FORMAN, R. T. T. (1975): Canopy lichens with blue-green algae: a nitrogen source in a Colombian rain forest. Ecology 56: 1176-1184. GAUSLAA, Y. (1985): The ecology of Lobarion pulmonariae and Parmelion caperatae in Quercus dominated forest in South-west Norway. Lichenologist 17: 117-140. - (1995): The Lobarion, an epiphytic community of ancient forests, threatened by acid rain. Lichenologist 27: 59-76. - KOPPERUD, c., & SOLHAUG, K. A. (1996): Optimal quantum yield of photosystem II and chlorophyll degradation of Lobaria pulmonaria in relation to pH. Lichenologist 28: 267-278. -, & OHLSON, M. (1997): Et historisk perspektiv pa kontinuitet og forekomst av epifyttiske laver. Blyttia 55: 15-27. -, & SOLHAUG, K. A. (1996): Differences in the susceptibility to light stress between epiphytic lichens of ancient and young boreal forest stands. Funct. Ecol. 10: 344-354. GILBERT, O. L. (1986): Field evidence for an acid rain effect on lichens. Environ. Poll. 40: 227-231. HAFELLNER, J. (1988): Principles of classification and main taxonomic groups. In: GALUN, M. (ed.): CRC handbook of lichenology. Vol. 3. CRC Press, Boca Raton, 41-52. HAKULINEN, R. (1964) : Die Flechtengattung Lobaria SCHREB. in Ostfennoskandien. Ann. Bot. Fennici 1: 202-213. 256

FLORA (1998) 193

HALLINGBACK, T. (1986): Lunglavarna, Lobaria, pa retratt i Sverige. Svensk Bot. Tidskr. 80: 373-381. -, & MARTINSSON, P.-O. (1987): The retreat of two lichens, Lobaria pulmonaria and L. scrobiculata in the district of Gasene (SW Sweden). Windahlia 17: 27-32. -, & THOR, G. (1988): Jattelav, Lobaria amplissima, i Sverige. Svensk Bot. Tidskr. 82: 125-139. HAUGAN, R., HOLIEN, H., & RYDGREN, K. (1995): Liaheia, Bflllnnpy kommune, Nordland, en oseanisk granskog med verdens nordligste forekomst av rund porelav, Sticta fuliginosa (DICKS.) Ach. Blyttia 53: 15-24. HAWKSWORTH, D. L. (1990): The long-term effects of air pollutants on lichen communities in Europe and North America. In: WOODWELL, G. M. (ed.): The earth in transition. Cambridge University Press, Cambridge, 45-64. -, & ROSE, F. (1970): Qualitative scale for estimating sulphur dioxide air pollution in England and Wales using eiphytic lichens. Nature 227: 145-148. HOLIEN, H., & TQlNSBERG, T. (1996): Boreal regnskog i Norge - habitater for trpndelagselementets lavarter. Blyttia 54: 157-177. HUNECK, S. (1973): Nature of lichen substances. In: AHMADHAN, V., & HALE, M. E. (eds.): The lichens. Academic Press, London, 495-522. HYVARINEN, M., HALONEN, P., & KAUPPI, M. (1992): Influence of stand age and structure on the epiphytic lichen vegetation in the middle-boreal forests of Finland. Lichenolo gist 24: 165-180. ISKANDAR, I. K., & SYERS, 1. K. (1971): Solubility of lichen compounds in water: pedogenetic implications. Lichenologist 5: 45-50. - (1972): Metal-complex formation by lichen compounds. J. Soil Sci. 23: 255-265. JAMES, P. w., HAWKSWORTH, D. L., & ROSE, F. (1977): Lichen communities in the British Isles. In: SEAWARD, M. R. D. (ed.): Lichen ecology. Academic Press, London, 295-4l3. KIELLAND-LuND,1. (1981): Die Waldgesellschaften SO-Norwegens. Phytocoenologia 9: 53-250. KNOPS, 1. M. H., NASH III, T. H., & SCHLESINGER, w. H. (1996): The influence of epiphytic lichens on the nutrient cycling of an oak woodland. Ecol. Monogr. 66: 159-179. KOOIJMAN, A. M., & BAKKER, c. (1994): The acidification capacity of wetland bryophytes as influenced by simulated clean and polluted rain. Aquatic Bot. 48: 133-144. LANG, G. E., REINERS, W. A., & HEIER, R. K. (1976): Potential alteration of precipitation chemistry by epiphytic lichens. Oecologia 25: 229- 241. LOONEY, 1. H. H., & JAMES, P. W. (1988): Effects on lichens. In: ASHMORE, M. R., BELL, 1. N. B., & GARRETTY, C. (eds.): Acid rain and Britain's natural ecosystems. Imperial College, Centre for Environmental Technology, London, 13 - 25. MCCUNE, B. (1993): Gradients in epiphyte biomass in three Pseudotsuga- Tsuga forests of different ages in western Oregon and Washington. Bryologist 96: 405-411. NIHLGARD, B. (1971) : Pedological influence of spruce planted on former beech forest soils in Scanina, South Sweden. Oikos 22: 302-314.

rI

NILSSON, S. I., & TYLER, G. (1995): Acidification-induced chemical changes of forest soils during recent decades - a review. Ecol. Bull. 44: 54-64. PIKE, L. H. (1978): The importance of epiphytic lichens in mineral cycling. Bryologist 81: 247 -257. PUCKETT, K. J., NIEBOER, E., GORZYNSKI, M. 1., & RICHARDSON, D. H. S. (1973): The uptake of metal ions by lichens: a modified ion-exchange process. New Phytol. 72: 329-342.

PURVIS, O. W., ELIX, J. A., BROOMHEAD, J. A., & JONES, G. C. (1987): The occurrence of copper-norstictic acid in lichens from cupriferous substrata. Lichenologist 19: 193-203.

RHOADES, F. M. (1981): Biomass of epiphytic lichens and bryophytes on Abies iasiocarpa on a Mt. Baker lava flow, Washington. Bryologist 84: 39-47. - (1995): Nonvascular epiphytes in forest canopies: worldwide distribution, abundance, and ecological roles. In: LOWMAN, M. D., & NADKARNI, N. (eds.): Forest canopies. Academic Press, New York, 353-408. RICHARDSON, D. H. S., KIANG, S., AHMADJIAN, v., & NIEBOER, E. (1985): Lead and uranium uptake by lichens. In: BROWN, D. H. (ed.): Lichen physiology and cell biology. Plenum Press, New York, 227-246. ROBITAILLE, G., LEBLANC, F., & RAo, D. N. (1977): Acid rain: a factor contributing to the paucity of epiphytic cryptogams in the vicinity of a copper smelter. Rev. Bryol. Lichenol. 43: 53-66. ROSE, F. (1974): The epiphytes of oak. In: MORRIS, M. G., & PERRlNG, F. H. (ed.): The British oak. E. W. Glassey Ltd, Berkshire, 250-273. - (1976): Lichenological indicators of age and environmental continuity in woodlands. In: BROWN, D. H., HAWKSWORTH, D. L., & BAILEY, R. H. (eds.): Lichenology: progress and problems. Academic Press, London, 279-307. - (1988): Phytogeographical and ecological aspects of Lobarion communities in Europe. Bot. J. Linnean Soc. 96: 69-79. - (1992): Temperate forest management: its effects on bryo-

phyte and lichen floras and habitats. In: BATES, J. W., & FARMER, A. D. (eds.): Bryophytes and lichens in a changing environment. Clarendon Press, Oxford, 211-233. SCHLARMANN, G., PEVELING, E., & TENBERGE, K. (1990). The occurence of chitin in the cell walls of ascomycetes mycobionts. Bibl. Lichenol. 38: 395-409. SERNANDER, R. (1936): Granskiir och Fiby urskog. Acta Phytogeogr. Suecica 8: 1-232. SHIBATA, s. (1973): Some aspects oflichen chemotaxonomy. In: BENDZ, G., & SANTESSON, J. (eds.): Chemistry in botanical classification, Nobel Symposium ed., Vol. 25. Nobel Foundation, Stockholm, 241-249. SKYE, E. (1968): Lichens and air pollution. Acta Phytogeogr. Suecica52: 1-123. SOLHAUG, K. A., & GAUSLAA, Y. (1996): Parietin, a photoproductive secondary product of the lichen Xanthoria parietina. Oecologia 108: 412-418. T0NSBERG, T., GAUSLAA, Y., HAUGAN, R., HOLIEN, H., & TrMDAL, E. (1996): The threatened macrolichens of Norway - 1995. Sommerfeltia 23: 1-283. T0RSETH, K. (1996): Overvlling av langtransportert fomrenset luft og nedb!1Jr. Atmosfrerisk tilf!1Jrsel, 1995. Norwegian Institute for Air Research (NILU OR 38/96), Kjeller. -, & PEDERSEN, U. (1994). Depositions of sulphur and nitrogen components in Norway 1988-1992. Norwegian Institute for Air Research (NILU, OR 16/94), Kjeller. TURK, R., WIRTH, v., & LANGE, O. L. (1974): CO2-Gaswechsel-Untersuchungen zur S02-Resistenz von Flechten. Oecologia 15: 33-64. TuOMINEN, Y. (1967): Studies on the strontium uptake of the Cladonia alpestris thallus. Ann. Bot. Fennici 4: 1-28. YANG, T. C., & ZALL, R. R. (1984): Absorption of metals by natural polymers generated from seafood processing wastes. Ind. Eng. Chern. Prod. Res. Dev. 23: 168-172. ZIEGENSPECK, H. (1937): In wieweit sind die Sphagnen und andere Moose befahigt, im Leben ihre Umgebung auf ein bestimmtes pH-Optimum einzustellen? Bot. Archiv 38: 1-15.

FLORA (1998) 193

257