AOBPreview originally published online on December 12, 2007
Annals of Botany 2008 101(4):531-539; doi:10.1093/aob/mcm306
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Surface Hydrophobicity Causes SO2 Tolerance in Lichens
1 Albrecht von Haller Institute of Plant Sciences, Dept. Plant Ecology, University of Göttingen, Untere Karspüle 2, D-37073 Göttingen, Germany
2 Max Planck Institute of Dynamics and Self-Organization, Dept. Dynamics of Complex Fluids, Bunsenstraße 10, D-37073 Göttingen, Germany
* For correspondence. E-mail mhauck{at}gwdg.de
Received: 12 July 2007 Returned for revision: 9 October 2007 Accepted: 13 November 2007 Published electronically: 12 December 2007
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ABSTRACT |
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Background and Aims: The superhydrophobicity of the thallus surface in one of the most SO2-tolerant lichen species, Lecanora conizaeoides, suggests that surface hydrophobicity could be a general feature of lichen symbioses controlling their tolerance to SO2. The study described here tests this hypothesis.
Methods: Water droplets of the size of a raindrop were placed on the surface of air-dry thalli in 50 lichen species of known SO2 tolerance and contact angles were measured to quantify hydrophobicity.
Key Results: The wettability of lichen thalli ranges from strongly hydrophobic to strongly hydrophilic. SO2 tolerance of the studied lichen species increased with increasing hydrophobicity of the thallus surface. Extraction of extracellular lichen secondary metabolites with acetone reduced, but did not abolish the hydrophobicity of lichen thalli.
Conclusions: Surface hydrophobicity is the main factor controlling SO2 tolerance in lichens. It presumably originally evolved as an adaptation to wet habitats preventing the depression of net photosynthesis due to supersaturation of the thallus with water. Hydrophilicity of lichen thalli is an adaptation to dry or humid, but not directly rain-exposed habitats. The crucial role of surface hydrophobicity in SO2 also explains why many markedly SO2-tolerant species are additionally tolerant to other (chemically unrelated) toxic substances including heavy metals.
Key words: Contact angle, hydrophilicity, hydrophobicity, lotus effect, cortex, sulphur dioxide, air pollution, water uptake, lichens
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INTRODUCTION |
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The affinity of a surface for water is usually characterized by the internal contact angle the water surface makes with the surface under study. This can be deduced, e.g. from the shape of a droplet deposited on that surface. If the contact angle is above 90°, the surface is described as being hydrophobic. Another commonly used quantity is the run-off angle, which describes how firmly the droplet sticks to the surface (Quéré, 2002). In recent years, there has been increasing interest in so-called superhydrophobic surfaces, which exhibit extremely high contact angles (150° or more) and low run-off angles (Marmur, 2004). A surface with such characteristics stays virtually dry when exposed to water. Possible physical origins of superhydrophobicity, which is common to many biological surfaces, include the chemical composition of the surface as well as its topography and mechanical properties (Otten and Herminghaus, 2004). The interplay of surface structures on different length scales may play an important role (Herminghaus, 2000). Irrespective of the specific mechanism, superhydrophobicity effectively inhibits the intrusion of water into the material.
Superhydrophobicity is used to produce water-repellent, but breathable technical surfaces including textiles (Jiang et al., 2004; Wang et al., 2005; Wong et al., 2006). Technical applications using superhydrophobicity attempt to mimic surfaces found in nature. Barthlott and Neihuis (1997) described superhydrophobicity in the lotus flower (Nelumbo nucifera). Since then the term ‘lotus effect’ is widely used for superhydrophobicity in plants. In lichen symbioses, superhydrophobicity has been studied in the crustose Lecanora conizaeoides (Shirtcliffe et al., 2006). This lichen is known for its extremely high tolerance to acidic precipitation containing dissolved SO2 and its derivatives formed in aqueous solution (Bates et al., 1996; Hauck et al., 2001). Because of its high SO2 and acid tolerance, L. conizaeoides spread enormously in the industrialized countries of Europe during the 20th century (Wirth, 1985) and also encroached on North America (LaGreca and Stutzman, 2006). Since SO2 is only toxic to lichens in the wet phase (Türk et al., 1974), Shirtcliffe et al. (2006) attributed the high SO2 tolerance of L. conizaeoides to its superhydrophobic surface. Superhydrophobicity in L. conizaeoides is attained by a highly structured, irregular thallus surface, here and there covered with crystals of the depsidone fumarprotocetraric acid. The rough surface of L. conizaeoides is due to its granular, homoiomerous thallus without a cortex. The lichen further lacks a hydrophilic polysaccharide matrix, which is found in many other (homoiomerous and heteromerous) lichen thalli (Paul et al., 2003). Furthermore, the cell walls of lichenized fungi are often coated with the water-repellent protein hydrophobin (Scherrer et al., 2002; Scherrer and Honegger, 2003), the distribution of which in L. conizaeoides, however, has not yet been studied.
Under natural conditions without SO2 pollution, superhydrophobicity is thought to increase the yield of photosynthesis in L. conizaeoides at high moisture levels. The carbon gain of lichens is frequently reduced during heavy precipitation events, as a high thallus water content hampers CO2 diffusion into the thallus (Lange et al., 1999). Measuring gas exchange in the non-superhydrophobic lichen Lecanora muralis in Germany for 15 months, Lange (2002, 2003a,b) showed that thallus supersaturation with water depressed net photosynthesis for about 40 % of the year even in a temperate area with modest rainfall (annual precipitation 600 mm). In high-precipitation areas, depression of photosynthesis due to thallus supersaturation is even more frequent (Lange et al., 1993). Lakatos et al. (2006) studied contact angles of the thallus surface in some tropical crustose epiphytes and found that such lichen species often have hydrophobic surfaces that prevent them from becoming supersaturated.
The superhydrophobicity of the thallus surface in one of the most SO2-tolerant lichen species, L. conizaeoides (Shirtcliffe et al., 2006), suggests that surface hydrophobicity could be a general feature of lichen symbioses controlling their tolerance to SO2. Although SO2 emissions strongly influences lichen vegetation in industrialized countries by repressing many SO2-sensitive species and by promoting a few SO2-tolerant taxa (Wirth, 1985; Nash and Gries, 2002; Hauck, 2003), a consistent explanation for the different sensitivities of different species is still lacking. The growth form of the thallus or the systematic position of the photobiont allow only tentative predictions of SO2 tolerance (Türk et al., 1974; Wirth and Türk, 1975; Nash and Gries, 2002). Lichens particularly tolerant to SO2 can strongly differ in morphology and systematic position, but always have green-algal photobionts (Wirth, 1985). Since SO2 can only be detrimental if it enters the lichen in aqueous solution, we tested the hypothesis that SO2 tolerance in lichens primarily depends on the wettability of the thallus surface, which we characterized with measurements of contact angles.
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MATERIALS AND METHODS |
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Selection of species
Selection of lichen species included in the study was primarily based on their known SO2 tolerance and aimed at covering a wide amplitude of low and high sensitivity. SO2 sensitivity of species can be deduced from numerous field studies on lichen vegetation in areas with known SO2 pollution. These field observations are compiled in lichen floras (Wirth, 1995; Hauck, 1996) or scales estimating the SO2 sensitivity of species relative to one another (Hawksworth and Rose, 1970; Wirth, 1992). Such observations are supplemented by experimental studies documenting physiological effects of SO2 on lichens. However, such direct evidence is only available for a limited number of lichen species (e.g. Hill, 1971; Türk et al., 1974; Häffner et al., 2001). Most studied species were epiphytes, as epiphytic lichens are particularly sensitive to SO2 pollution owing to the low buffering capacity of most bark surfaces and wood. However, some terricolous and saxicolous lichens were also included, because they were either known or assumed to be SO2-sensitive (Cetraria islandica, Peltigera aphthosa; Hallingbäck and Kellner, 1992; Häffner et al., 2001), SO2-tolerant (Lecanora muralis), or they were related to epiphytic species of known SO2 tolerance (Flavocetraria nivalis, Lobaria linita, Nephroma arcticum).
As surface hydrophobicity in lichens could not have evolved as a response to atmospheric SO2, but putatively to ensure gas exchange in differently water-supplied habitats (Lakatos et al., 2006), some species from particularly dry or wet habitats without known pollution tolerance were included in addition to the species studied with respect to SO2 tolerance. Such species include the aquatic lichen Bacidina inundata that inhabits periodically inundated siliceous rock in streams, the desert lichen Xanthomaculina convoluta from the Namib desert, and Chrysothrix chlorina, which grows on rain-sheltered vertical rock. Altogether a total of 50 lichen species was studied.
In the genus Cladonia, the influence of soralia on surface hydrophobicity was investigated by comparing the contact angles of C. coniocraea, C. fimbriata, C. glauca, C. macilenta, C. polydactyla and C. pyxidata with sorediate podetia and of C. furcata, C. gracilis, and C. rangiformis with corticated podetia. Contact angles of basal squamules and podetia were studied in comparison in C. coniocraea, C. glauca, C. macilenta and C. pyxidata. An alphabetical list of the studied lichen species with information on their habitat preferences is shown in Table 1. A rough assessment of the SO2 tolerance of these lichens is given in Table 2.
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Experimental details
Air-dry lichens were used to measure the contact angle of droplets of deionized water with a video-based Contact Angle Measuring System OCA 20 (Dataphysics Instruments, Filderstadt, Germany). Measurements were conducted with sessile droplets of approx. 500 µm in diameter placed on the surface. The size of 500 µm corresponds to the size of raindrops. Measurements were consistently made on the thallus side exposed to the environment, i.e. usually the upper side. The contact angle was calculated with the SCA 20 software delivered with the OCA 20. The accuracy of the measurements with the OCA 20 was ±1°. On strongly hydrophilic lichen thalli, contact angles could not be determined, as water droplets placed on the surface were immediately taken up by the lichen. Since the lowest measurable contact angle was 52°, the contact angle of the most hydrophilic species is specified as <50° (see Table 2). It was not feasible to detect differences in the surface hydrophilicity among these species. For calculations of mean contact angles (see Figs 2 and 3) values <50 % were set to 50 %. All measurements were replicated five times on different thalli (or lobes) from the same sample each collected at one site. Each replicate is a mean value calculated from the contact angles of the optically left and right margin of the water droplet.
In selected lichen species (Flavoparmelia caperata, Lepraria jackii, L. lobificans, Letharia vulpina, Parmeliopsis ambigua) the contribution of secondary lichen metabolites on surface hydrophobicity was assessed by measuring thalli with the natural content of lichen substances (i.e. mostly lichen-specific, extracellular secondary metabolites produced by the fungal partner of the lichen symbiosis; Huneck and Yoshimura, 1996) and thalli, where lichen substances were extracted from the apoplast by soaking the thalli with acetone for 10 min. The extraction achieved within 10 min was not quantitative.
Statistics
All data are given as arithmetic means ± s.e. and were tested for normal distribution with the Shapiro–Wilk test. Normally distributed samples were tested for significant differences with Student's t-test for pairwise comparisons and with Duncan's multiple range test for the comparison of more than two means. Multiple comparisons for non-normally distributed were made with the Kruskal-Wallis test. Statistical analyses were computed with SAS 6·04 software (SAS Institute Inc., Cary, NC, USA).
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RESULTS |
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Contact angles of water droplets placed on the surface of lichen thalli strongly differed between species (Table 2). While the thalli of some lichen species were strongly hydrophobic with contact angles up to 140°, the surface of other species was immediately soaked with water (Table 2 and Fig. 1). In hydrophobic species, water droplets persistently remained on the thallus surface, while the thallus stayed virtually dry (Fig. 1). Highly SO2-tolerant lichen species exhibited higher contact angles than SO2-sensitive species (Fig. 2A). This difference was statistically significant (Table 2). The growth form of lichen thalli was partly correlated with the contact angle (Fig. 2B). A Kruskal-Wallis test (P
0·05, d.f. = 2) showed that the crustose (126 ± 3°) and fruticose (112 ± 7°) lichen species studied were more hydrophobic than the foliose ones (84 ± 6°). Measurements in sorediate and corticated Cladonia species (Fig. 1D, E) showed significantly higher contact angles for water droplets placed on sorediate surfaces (Fig. 3). Contact angles were similar on basal squamules and podetia of Cladonia, though the t-test revealed a significant difference for C. macilenta (t = 8·295, d.f. = 8, P < 0·001) owing to the low variability between replicate measurements (Table 3). Extracting lichen substances with acetone generally reduced the hydrophobicity of the thallus (Table 4). However, the extent to which the contact angle was reduced differed between species. The effect of the extraction procedure was particularly high in Flavoparmelia caperata (Fig. 1G, H), moderate in Parmeliopsis ambigua, and relatively low in Lepraria and Letharia vulpina (Table 4).
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DISCUSSION |
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The data clearly support our hypothesis that SO2 tolerance in lichens is correlated with hydrophobicity of the thallus surface (Fig. 2A). All lichen species known for their high SO2 tolerance exhibited contact angles >120° for water droplets of the size of large raindrops placed on their surface. A contact angle >120° means that these species are highly hydrophobic. Contact angles in moderately SO2-tolerant species ranged from approx. 90 to 120°. Species susceptible to SO2 had hydrophilic surfaces with contact angles rarely exceeding 90° (Table 2 and Fig. 2A).
Despite long-lasting research on SO2 tolerance in lichens (Hawksworth, 1971; Türk et al., 1974; Nash and Gries, 2002), the correlation shown in the present study between surface hydrophobicity and SO2 tolerance is the first one that provides a plausible explanation for the species-specific differences found in the SO2 tolerance of lichen-forming fungi irrespective of their systematic position, thallus morphology, or photobiont choice.
Previous attempts to correlate the SO2 tolerance of lichen-forming fungi with intrinsic characters primarily focused on relationships with the growth form and the specifity of the fungus for green-algal or cyanobacterial photobionts. A rough tendency for increasing SO2 sensitivity from crustose via foliose to fruticose species does not stand scrutiny (Türk et al., 1974; Wirth and Türk, 1975). The lichen species with the lowest SO2 tolerance (and the lowest contact angles) included in the present study were foliose. Although many fruticose lichens prefer areas with low SO2 pollution, several of them, including many species of Cladonia (Wirth, 1985) or Letharia vulpina (Sigal and Nash, 1983), are markedly SO2-tolerant. Letharia vulpina, Pseudevernia furfuracea, and Evernia prunastri differ strongly in their tolerance to SO2 (Table 2), but are very similar with regard to their thallus morphology sharing few-cm long, fruticose, erect to pendent thalli attached at a single point to the substratum (Wirth, 1995; Brodo et al., 2001). SO2 sensitivity of foliose lichens ranges from extremely sensitive species (e.g. Lobaria, Nephroma) to very tolerant ones (Parmeliopsis ambigua, Physcia tenella). Among the crustose lichens, several markedly SO2-tolerant species are known, including Lecanora conizaeoides, Lepraria incana, L. jackii, Mycoblastus fucatus, Ropalospora viridis and Scoliciosporum chlorococcum (Wirth, 1985). Information on SO2-sensitive species is scarce, as foliose and fruticose lichens are easier to handle in laboratory experiments and have thus been preferentially used. It is therefore uncertain whether most crustose lichens, which are known to be sensitive to air pollutants from field observations, are susceptible to SO2 and its derivatives or to other substances like NH3 or NOX. Examples for such pollution-sensitive lichens from Europe include Arthonia cinnabarina, Bactrospora dryina, Gyalecta ulmi or Ochrolechia pallescens (Wirth, 1992). Pertusaria corallina is a species, for which SO2 sensitivity has been explicitly proven (Wirth and Türk, 1975).
A general trend for higher SO2 sensitivity of cyanolichens than chlorolichens is undisputed (Wirth and Türk, 1975). The high sensitivity of cyanolichens explains their strong decline in areas with high SO2 pollution (Wirth et al., 1996). However, the high susceptibility of cyanolichens does not explain why some chlorolichens are similarly SO2-sensitive. This applies, for example, to Lobaria pulmonaria and L. scrobiculata, two formerly abundant epiphytes in the deciduous forest belt of Europe (Hallingbäck, 1989; Gauslaa, 1995). While L. scrobiculata is a pure cyanolichen containing solely Nostoc, the primary photobiont of L. pulmonaria is the green alga Dictyochloropsis reticulata (Ettl and Gärtner, 1995). Although Nostoc also occurs in L. pulmonaria, it is limited to (rare) internal cephalodia and not essential for the carbon gain of the symbiosis. The high hydrophilicity of both Lobaria species explains their similar susceptibility to SO2 despite their different photobionts.
As pointed out by Lakatos et al. (2006) and Shirtcliffe et al. (2006), the primary ecological significance of surface hydrophobicity or hydrophilicity is undoubtedly the reduction of passive water uptake at wet sites to prevent thallus supersaturation and the promotion of water uptake at dry sites. Lichens with strongly hydrophilic surfaces include species depositing calcium oxalate crystals on their surface and species from humid terrestrial habitats (Table 2). Since calcium oxalate crystals are strongly hygroscopic, Wadsten and Moberg (1985) and Clark et al. (2001) suggested a function in water storage. In addition to their photoprotective effect, calcium oxalate layers on the surface of terricolous or saxicolous lichens are assumed to facilitate water uptake in xeric habitats (Souza-Egipsy et al., 2002; Hauck et al., 2007a). Such promotion of water uptake is apparent in the desert lichen Xanthomaculina convoluta, which turns its extremely hydrophilic lower side upward in the dry state. On the lower side, the medulla containing numerous calcium oxalate crystals separated from the environment only by a flimsy cortex (Modenesi et al., 2000).
The strong hydrophilicity of Parmelia ernstiae and Physconia grisea, which both have a thick layer of calcium oxalate crystals on their thallus surfaces, suggests that the role of calcium oxalate to enhance water uptake is not limited to extreme environments. The hydrophilicity of P. ernstiae (Fig. 1R) and the hydrophobicity of P. saxatilis (Fig. 1S) explain the ecological differences between these similar species (Feuerer and Thell, 2002). As P. saxatilis grows on horizontal, rain-exposed siliceous rock, surface hydrophobicity would be beneficial in reducing supersaturation of the thallus with water and, with it, depression of net photosynthesis (Lange, 2002, 2003a,b). In the epiphyte P. ernstiae, thallus supersaturation is of less significance, but fast absorption of water droplets is especially valuable on vertical and strongly inclined surfaces on trunks and branches.
The hydrophilicity of oceanic forest lichens, such as Lobaria pulmonaria, L. scrobiculata, Nephroma bellum, N. resupinatum, or Peltigera praetextata, and of terricolous lichens of moist and cool habitats, such as Cetraria islandica, Flavocetraria nivalis, Lobaria linita, Nephroma arcticum or Peltigera aphthosa, is probably not due to a mechanism that promotes water uptake, but to the lack of an efficient protection against evaporation. In their humid habitats, retention of water by hydrophobic surface layers would be either not necessary or even a disadvantage because of the risk of thallus supersaturation. Perhaps similar water relations are the reason why species of the same genera (Lobaria, Nephroma and Peltigera) are found in the superficially very different habitats of temperate, oceanic forests and arctic-alpine dwarf-shrub heathlands.
As in the lotus flower (Barthlott and Neihuis, 1997), surface hydrophobicity in lichens has probably not only been evolved to reduce water uptake, but also to keep lichens clean. This is inferred from the high contact angles measured in water droplets placed on the surfaces of leprarioid crusts (Chrysothrix chlorina, Lepraria incana, L. jackii and L. lobificans). All these species are found at rain-sheltered microhabitats, viz. under overhanging rock or in cracks of bark. A mechanism to avoid the uptake of fluid water makes little ecological sense at such microhabitats, as most lichens growing there will never have direct contact to rain. Rather, the absence of fluid water implies the risk that the surfaces of the (relatively slow-growing) lichens become increasingly contaminated by particles. This would reduce the incoming solar irradiation in already shady habitats. Since most lichens growing at rain-sheltered microsites have similar thalli like the investigated Chrysothrix and Lepraria species (Wirth, 1995), keeping lichens clean to prevent a depression of photosynthesis seems the most plausible function of hydrophobicity in these lichens.
The correlation of surface hydrophobicity with the tolerance to SO2 (Table 2 and Fig. 2) suggests that the adaptation of the thallus surface to environments differring in water supply, which had evolved in the absence of any atmospheric pollution, acquired a completely new ecological significance with rising SO2 emissions since the beginning of the industrial evolution (Hawksworth, 1971). Hydrophobicity of the thallus surface, once evolved to prevent thallus supersaturation with water in rain-exposed habitats, suddenly became essential to survive in areas with sulphuric, acidic precipitation. Possessing a strongly hydrophilic surface became fatal, as dissolved SO2 could penetrate unhindered into the thallus. This explains why oceanic lichen communities consisting of Lobaria, Nephroma, Peltigera and other many species were completely wiped out in industrialized areas, while other lichens were more tolerant (Wirth and Türk, 1975; Wirth et al., 1996).
The equivalence of surface hydrophobicity and SO2 tolerance makes former discussions on the origin of SO2-tolerant lichen species unnecessary (Wirth, 1985). In the case of Lecanora conizaeoides, a lichen which spread enormously in Europe after SO2 pollution, speculations that the species might have evolved at sites with high SO2 deposition (Ahti, 1965; Bailey, 1968) are obsolete if we accept the view that surface hydrophobicity is crucial for SO2 tolerance in lichens. The success of L. conizaeoides in SO2-polluted areas can now be attributed to (a) the hydrophobicity of its surface (though we could not reproduce the extremely high contact angles of Shirtcliffe et al., 2006) and (b) to its high dispersal ability (Hauck et al., 2007b). The oldest known localities of L. conizaeoides from the 19th century are from groves of Pinus mugo in the Austrian Alps and in prealpine bogs of southern Germany (Wirth, 1985). These areas are characterized by high annual precipitation (around 1000 – 1500 mm). Moreover, singles trees, as found in P. mugo stands, receive much more stemflow and throughfall than trees in the forest interior (Hauck, 2003). This supports the assumption that surface hydrophobicity originally evolved as a response to high moisture and not to high atmospheric SO2 levels.
The present study also confirms the importance of the buffering capacity of the substratum for the SO2 tolerance of lichens (Skye, 1968). Substrata with a high capacity to keep the pH constant when exposed to acidic solutions support SO2-sensitive lichens at higher atmospheric SO2 concentrations than substrata with low buffering capacity (Skye, 1968; Wirth, 1995). Calcareous soil, rock and anthropogenic substrata such as concrete and mortar are particularly effective buffers. Our study suggests that some prominent calciphilous lichens, which outlast high atmospheric SO2 pollution are not particularly SO2-resistant, but benefit from the substratum. Lecanora muralis, which originates from calcareous rock, is abundant on anthropogenic calcareous substrata even in cities with high SO2 pollution. A contact angle of water droplets placed on the surface hardly above 90° suggests that this high SO2 tolerance is not due to surface hydrophobicity, but primarily to the buffering capacity of the substratum (Table 2). The same applies to Xanthoria parietina and Physconia grisea (Table 2). Their hydrophilicity matches with the strong decline of both species in SO2-polluted areas on tree bark, but not on rock and concrete (Wirth, 1995; Hauck, 1996).
Surface hydrophobicity in lichens is due to a combined effect of surface structure and coating of the cell walls with hydrophobic substances. This is shown by the reduced hydrophobicity of lichen thalli subsequent to the extraction of extracellular lichen substances with acetone (Table 4). While this result substantiates the contribution of lichen substances to surface hydrophobicity, contact angles exceeding 130° in Bacidina inundata and Scoliciosporum chloroccum show that lichen substances are not essential for surface hydrophobicity in lichens, as both species are devoid of any lichen substance (Purvis et al., 1992). In contrast to lichen substances, extracellular polysaccharide matrices which are not extractable with acetone increase the hydrophilicity of lichen surfaces (Paul et al., 2003; Shirtcliffe et al., 2006). Such exopolysaccharides are common in the cortex of lichens of the family Parmeliaceae (e.g. Flavoparmelia, Hypogymnia, Parmelia) or gelatinous cyanolichens (e.g. Collema, Leptogium). The higher hydrophobicity of the surface of sorediate than corticated Cladonia species (Fig. 3) could explain why sorediate and granulose species are overrepresented among the SO2-tolerant lichens (Wirth, 1985).
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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Increasing SO2 tolerance with increasing hydrophobicity of the thallus surface in a set of 50 lichen species suggests that SO2 tolerance in lichens primarily depends on the ability to reduce the uptake of acidic precipitation containing SO2 and its derivatives formed in aqueous solution. This implies that SO2 tolerance in lichens is primarily based on avoidance of high SO2 concentrations and not due to a physiological response. Surface hydrophobicity is certainly not the only, but probably the most important factor controlling the SO2 tolerance of lichens. Since hydrophobicity not only inhibits the uptake of sulphuric acid solutions, but of aqueous solutions in general, the present results also explain why many SO2-tolerant lichen species show a general toxitolerance, especially a tolerance to heavy metals.
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ACKNOWLEDGEMENTS |
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The study has been supported by a grant of the Deutsche Forschungsgemeinschaft to M. Hauck (Ha 3152/8-1).
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LITERATURE CITED |
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