Susceptibility to acidic precipitation contributes to the decline of the terricolous lichens Cetraria aculeata and Cetraria islandica in central Europe

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Environmental Pollution 152 (2008) 731e735 www.elsevier.com/locate/envpol

Susceptibility to acidic precipitation contributes to the decline of the terricolous lichens Cetraria aculeata and Cetraria islandica in central Europe Markus Hauck* Albrecht von Haller Institute of Plant Sciences, Department of Plant Ecology, University of Go¨ttingen, Untere Karspu¨le 2, D-37073 Go¨ttingen, Germany Received 30 April 2007; received in revised form 18 June 2007; accepted 20 June 2007

Artificial acidic precipitation with aqueous sulphur dioxide at pH 2.8e3.5 affects terricolous Cetraria species. Abstract The effective quantum yield of photochemical energy conversion in photosystem II (F2) was shown to be reduced in the terricolous lichens Cetraria aculeata and Cetraria islandica by short-term exposure to aqueous SO2 at pH values occurring in the precipitation of areas with high SO2 pollution. Significant reduction of F2 was found at pH  3.3. At pH 2.8, F2 was close to zero and did not recover within 24 h. This suggests that sensitivity to SO2 (primarily associated with epiphytic lichens in the past) has contributed to the decline of both species in central Europe. In C. islandica, but not in C. aculeata, thalli with the natural content of lichen substances were more tolerant to SO2 than thalli where the extracellular lichen substances were extracted before the experiment. This supports published results that the depsidone fumarprotocetraric acid, a major lichen substance of C. islandica, increases the pollution tolerance in lichens. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Air pollution; Chlorophyll fluorescence; Fumarprotocetraric acid; Lichen substances; Sulphur dioxide

1. Introduction Lichens are long since known to be damaged by SO2 and its derivatives formed in aqueous solution (Conti and Cecchetti, 2001; Nash and Gries, 2002). Studies to the SO2 sensitivity of lichens, however, have mostly been limited to epiphytic species (Giordani, 2006). This is because epiphyte vegetation is thought to be most susceptible to SO2, as the buffer capacity of tree bark is generally low (Skye, 1968). Studies on the impact of SO2 on terricolous and saxicolous species are relatively rare. Though terricolous and saxicolous species of, e.g., the genera Cladonia, Peltigera, Stereocaulon or Umbilicaria, were repeatedly studied in the laboratory (Ha¨llgren and

* Tel.: þ49 551 39 5721; fax: þ49 551 39 5701. E-mail address: [email protected] 0269-7491/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.envpol.2007.06.046

Huss, 1975; Sharma et al., 1982; Fields and St. Clair, 1984; Eversman and Sigal, 1987), results were rarely related to the trends for decrease or increase of the species in the field (Hallingba¨ck and Kellner, 1992). Rather, the decline of soil or rock-dwelling species in industrialized countries was primarily related to the loss of suitable habitats (Ka¨rnefelt and Mattsson, 1989; Wirth et al., 1996) or to the mechanical damage resulting from overgrazing or leisure-time activities (Runge, 1961; Thiel and Spribille, 2007). Low significance of acidic air pollution is plausible for lichens of calcareous substrates. Calcareous soils and rocks protect lichens growing on them by their high buffer capacity, as acidification is a major component of SO2 toxicity (Tu¨rk and Wirth, 1975; Wirth, 1985). Similarly, epiphytic lichens on relatively well-buffered nutrient-rich bark can withstand higher levels of atmospheric SO2 than lichens on nutrient-poor bark (Gilbert, 1970). Xanthoria parietina is a typical example of

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a lichen species that shows the substrate influence on SO2 toxicity. Epiphytic populations strongly declined in Europe during the periods of high SO2 pollution, but are currently spreading after SO2 emissions decreased. Populations of X. parietina on limestone and artificial calcareous substrates, such as concrete, have been much less affected by the atmospheric SO2 level (Gilbert, 1969; Wirth, 1995; Silberstein et al., 1996). Acidic soils and rocks, however, are unlikely to exert a significant buffering to acidic air pollution. This is especially true for nutrient-poor, acidic sands or rocks such as quartzite. Cetraria aculeata and Cetraria islandica are examples of terricolous lichen species of nutrient-poor, acidic soils, which have undergone a decline in central Europe during the 20th century (Wirth et al., 1996). The loss of nutrient-poor grasslands, heathlands and peatlands is a widely accepted cause of the retreat (Hauck, 1992; Wirth, 1995). In northern Germany, however, the species also vanished from sites, where the structural habitat characteristics remained unchanged (Hauck, 1992, 1996). Therefore, eutrophication has frequently been discussed as a cause of the decline of cryptogam species within existing grasslands (Bu¨ltmann, 2005). However, eutrophication is unlikely to occur without promoting vascular plant growth and thereby destroying the gaps in vascular plant vegetation, which are essential for terricolous lichens (Rodenkirchen, 1991). Thus, it is plausible to assume that acidic pollution with inorganic S has contributed to the decline of terricolous lichens in nutrient-poor habitats, where open soil patches without vascular plant competition are still available. Therefore, the present study aimed at testing the hypothesis that the two foliose lichens C. aculeata and C. islandica are susceptible to acidic precipitation containing dissolved SO2. To test this hypothesis, the two lichen species were incubated with sulphuric solutions in the growth chamber. Hauck and Huneck (2007a,b) and Hauck et al. (in press) suggested that heavy metal tolerance of lichens is related to their content of lichen substances. This is because lichen substances modify the binding of metal ions to cation exchange sites. To figure out whether lichen substances are also related to SO2 toxicity, two treatments of C. aculeata and C. islandica were compared, viz. one with the natural content of lichen substances and another one where lichen substances were removed from the apoplast with acetone. Soaking lichens with acetone has no sustainable effect on their viability, as proven by chlorophyll fluorescence measurements (Solhaug and Gauslaa, 2001). C. aculeata produces the fatty acids, lichesterinic and protolichesterinic acids, whereas C. islandica contains the depsidone fumarprotocetraric acid, the fatty acid protolichesterinic acid and varying amounts of the depsidone protocetraric acid (Purvis et al., 1992; Gudjo´nsdo´ttir and Ingo´lfsdo´ttir, 1997). The hypothesis tested was that these lichen substances affect the susceptibility of C. aculeata and C. islandica to sulphuric, acidic solution. The effect of the treatments on lichen viability was assessed by measuring the chlorophyll fluorescence yield of lightadapted samples.

2. Materials and methods 2.1. Experimental details Lichen thalli of the fruticose species C. aculeata (Schreb.) Fr. and C. islandica (L.) Ach. were sampled ca. two weeks before the experiment in Germany (C. aculeata: Sachsen-Anhalt, heathland near Halle/Saale, C. islandica: Baden-Wu¨rttemberg, Black Forest). Air-dry thalli were kept at 18  C in the dark before the experiment. After unfreezing, thalli were divided into single thallus lobes (C. islandica) or cushions of about 1 cm2 (C. aculeata). In one half of the material extracellular lichen substances were removed from air-dry thalli with acetone (Solhaug and Gauslaa, 2001). Four extraction steps of 10 min interrupted by breaks of 10 min were applied. Five pieces of lichen were put together on one Petri dish with a moist cellulose filter. The dry weight of lichen thalli per plate approximated 200 mg (C. aculeata: 211  9 mg; C. islandica: 165  7 mg). The Petri dishes with the lichen samples were stored for two days at 80% relative humidity, a day temperature (for 13 h daily) of 13  C during a photon flux of 30 mmol m2 s1, and a night temperature of 10  C in the growth chamber. After these two days given for acclimatization, the effective quantum yield (F2) of photochemical energy conversion in photosystem II (PSII) was measured in light-adapted thalli with a PAM-2100 chlorophyll fluorometer (Walz Mess- und Regeltechnik, Effeltrich, Germany) (Paul and Hauck, 2006). F2 specifies the proportion of excited chlorophyll a molecules in PSII returning in their ground state by yielding an electron into the photosynthetic electron transport chain (Roha´cek, 2002). After acclimatization, lichen samples were exposed for 30 min to aqueous SO2 at (1) pH 3.5, (2) pH 3.3, (3) pH 2.8 or (4) to deionized water at pH 5.5. The pH of the SO2 solutions corresponded to pH values found in areas with high industrial SO2 emissions including Europe, eastern North America and (more recently) China (Rohde et al., 2002; Hao et al., 2007). Annual mean values measured in these areas in incident precipitation during periods of high SO2 pollution typically ranged from pH 3.9 to 4.5 (Falconer and Falconer, 1980; Hauck, 2000; Rohde et al., 2002; Tost et al., 2007). Minimum values of pH in incident precipitation were found to amount, e.g., 3.3 (Hauck, 2000), 3.4 (Matzner and Ulrich, 1984), or 3.5 (Reynolds et al., 2004). Precipitation that passes tree canopies as throughfall or stemflow can be much more acidic with mean pH values below 3.5 (e.g. 3.3; Cassens-Sasse, 1987) and temporary pH minima below 3.0 (e.g. 2.8e2.9; Cassens-Sasse, 1987; Hauck, 2000). The pH of fog frequently goes down to pH 2.0 (Kues, 1984). SO2 concentrations in the incubation media amounted to 7.7 mM at pH 3.5, 19 mM at pH 3.3 and 193 mM at pH 2.8. Subsequent to the incubation procedure, the samples were put back in the growth chamber and F2 was measured after 30 min. In the case of the samples exposed to aqueous SO2 at pH 2.8 an additional measurement of F2 was recorded subsequent to one day in the growth chamber to detect possible recovery from the SO2 treatment. The experiment was conducted with five replicate plates per treatment, and on each plate five replicate measurements of F2 were taken.

2.2. Statistics All data are given as arithmetic means  standard error and were tested for normal distribution with the ShapiroeWilk test. Samples were tested for significant differences with Duncan’s multiple range test. Statistical analysis was computed with SAS 6.04 software (SAS Institute Inc., Cary, North Carolina, USA).

3. Results Before the lichen samples were exposed to SO2 solution, F2 amounted to 0.771  0.006 in C. aculeata and 0.730  0.006 in C. islandica. The acetone treatment for the extraction of lichen substances itself had no significant effect on F2 (Table 1). Dissolved SO2 at pH  3.3 significantly reduced F2 in C. aculeata (Fig. 1). Extracting lichesterinic and protolichesterinic acids from C. aculeata did not affect its SO2 tolerance. In C. islandica,

M. Hauck / Environmental Pollution 152 (2008) 731e735 Table 1 Effective quantum yield of photochemical energy conversion in PSII (F2) in Cetraria aculeata and Cetraria islandica prior to the exposure to SO2 With lichen substances

Without lichen substances

Controla

Control

SO2

C. aculeata 0.784  0.014 C. islandica 0.730  0.001

SO2

0.780  0.010 0.762  0.011 0.759  0.010 0.719  0.018 0.728  0.003 0.722  0.010

a Control and SO2 term the collectives incubated with water or aqueous SO2 after the determination of initial F2 values presented here. Within-species differences are statistically not significant (P  0.05; Duncan’s multiple range test; d.f. ¼ 16).

F2 was significantly reduced by aqueous SO2 at pH  3.3 in samples with the natural content of lichen substances, but at pH  3.5 in thalli where the extracellular lichen substances had been removed with acetone (Fig. 1). At pH 2.8, F2 was almost reduced to zero amounting to 0.044  0.010 (with lichen substances) or 0.047  0.008 (lichen substances extracted) in C. aculeata and 0.032  0.005 or 0.015  0.007, respectively, in C. islandica. Recovery from these low F2 values was not possible within 24 h (Fig. 1). 4. Discussion

Change of chlorophyll fluorescence yield

The experiment shows that both C. aculeata and C. islandica are susceptible even to short exposures of dissolved SO2 at pH values that regularly occur in the precipitation of areas with high SO2 pollution. A pH  3.3, at which F2 of both species is significantly reduced, is regularly achieved in precipitation below canopies, such as in light pine or oak forests, which are habitats of either Cetraria species (Wirth, 1995; Hauck, 1996). Furthermore, such pH is occasionally found in incident precipitation and frequently under-run by 0.1 0.0 -0.1

*

-0.2 -0.3 -0.4 -0.5

*

*

*

*

-0.6 -0.7

*

-0.8

*

*

CaWA CaWL CaSA

**

* CaSL

CiWA

CiWL

CiSA

*

*

CiSL

Treatment pH 3.5

pH 3.3

pH 2.8

pH 2.8 (2 days recovery)

Fig. 1. Change of the chlorophyll fluorescence yield of light-adapted samples at photosystem II in Cetraria aculeata (Ca) and Cetraria islandica (Ci) incubated for 30 min with dissolved SO2 (S) at pH 3.5, 3.3, 2.8 or water (W). Lichens either contain their natural content of lichen substances (L) or lichen substances have been extracted with acetone before the experiment (A). Changes of yield values refer to measurements made on the day before the incubation with SO2 or water. Asterisks indicate significant difference from control (P  0.05, Duncan’s multiple range test, d.f. ¼ 128).

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fog. At pH 2.8, damage is more or less complete and irreversible in the PSII of both species. Such acidic conditions, too, occur in potential environments of C. aculeata and C. islandica in SO2 polluted areas. Therefore, the present data suggest that acidic precipitation containing SO2 contributed to the decline of C. aculeata and C. islandica in central Europe. A stronger decline especially of C. islandica in the more heavily polluted northern Germany than in southern Germany supports this conclusion, as the latter was generally less SO2 polluted during the 20th century than the former (Wirth, 1995; Hauck, 1996; Wirth et al., 1996). While the present data agree with the results of a transplant experiment, where C. islandica was transferred to a heavily SO2 polluted site in Germany and showed a decrease of net photosynthesis and respiration as well as thallus bleaching (Ha¨ffner et al., 2001), the SO2 sensitivity of C. aculeata has apparently not been studied, so far. Experimental results obtained with other terricolous lichens, which have undergone a decline in central Europe during the 20th century, suggest that also in these cases SO2 pollution has contributed to their retreat. Such lichens include species of Cladonia subgenus Cladina (Grace et al., 1985; Plakunova and Plakunova, 1987; Coxson, 1988), Peltigera (Henriksson and Pearson, 1981; Hallingba¨ck and Kellner, 1992), and Stereocaulon (Ha¨llgren and Huss, 1975). Since terricolous lichens take up inorganic S from the atmosphere as readily as epiphytic species (Case and Krouse, 1980), a detrimental influence of SO2 on terricolous species in the field seems plausible. The significance of SO2 pollution for the disproportionate decline of some terricolous lichens of acidic soils during the 20th century, especially in northern Germany, was probably strongly underestimated, so far. Lichen species, which have declined much more than other species of the same habitats in northern Germany include C. islandica, Cladonia rangiferina, Icmadophila ericetorum, Peltigera leucophlebia, Peltigera venosa, Pycnothelia papillaria and several species of Stereocaulon (Hauck, 1996). In central Europe, SO2 effects on terricolous lichens can be assumed to be primarily historic, as atmospheric SO2 concentration and, with it, their potential to damage lichen vegetation decreased recently (Heibel et al., 1999; Marı´n et al., 2001). Acidic precipitation with SO2 is certainly not the only limiting factor for terricolous lichens. Rather, it might exert an effect in addition to other factors that have been considered before to be responsible for the decline of terricolous lichen species. These factors include habitat loss, fertilization and overgrazing (Wirth, 1995; Hauck, 1996; Bu¨ltmann, 2005), though moderate fertilization was shown even to promote the growth of lichens from acidic soils (Scott et al., 1989; Vagts and Kinder, 1999). The late 20th century warming has also been discussed to contribute to the decline of some cold-tolerant terricolous lichens in western and central Europe (Aptroot and van Dobben, 2002). While lichesterinic and protolichesterinic acids did not affect the sensitivity to SO2 in C. aculeata, C. islandica was less susceptible to acidity combined with SO2 with than without the natural content of secondary metabolites. As protolichesterinic

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acid occurred in both study species, a function of this fatty acid to affect SO2 tolerance can be ruled out. There are, however, two hints that the depsidone fumarprotocetraric acid could be involved in the pollution tolerance of C. islandica. Firstly, fumarprotocetraric acid is produced by some lichens, which are outstanding for their high SO2 tolerance. Such species include Cladonia coniocraea, Cladonia pyxidata, Lecanora conizaeoides, and Mycoblastus fucatus (Hauck and Huneck, 2007b). Secondly, fumarprotocetraric acid is known to interfere with the heavy metal adsorption in lichens (Hauck and Huneck, 2007a,b; Hauck et al., in press). 5. Conclusions The present results suggest that sulphuric, acidic precipitation contributed to the decline of C. aculeata and C. islandica in Europe. Furthermore, the experiments support former results by Hauck and Huneck (2007a,b) and Hauck et al. (in press) that the depsidone fumarprotocetraric acid, a major secondary metabolite of C. islandica, might stimulate the pollution tolerance in lichens. Acknowledgments The study has been supported by a grant of the Deutsche Forschungsgemeinschaft to M. Hauck (Ha 3152/8-1). Dr. habil. Siegfried Huneck (Halle) and Prof. Dr. Volkmar Wirth (Karlsruhe) are warmly thanked for supplying the samples of C. aculeata and C. islandica for the experiment. References Aptroot, A., van Dobben, H.F., 2002. Long-term monitoring in the Netherlands suggests that lichens respond to global warming. Lichenologist 34, 141e154. Bu¨ltmann, H., 2005. Strategien und Artenreichtum von Erdflechten in Sandtrockenrasen. Tuexenia 25, 425e443. Case, J.W., Krouse, H.R., 1980. Variations in sulphur content and stable sulphur isotope composition of vegetation near a SO2 source at Fox Creek, Alberta, Canada. Oecologia 44, 248e257. Cassens-Sasse, E., 1987. Witterungsbedingte saisonale Versauerungsschu¨be im Boden zweier Waldo¨kosysteme. Berichte des Forschungszentrums Waldo¨kosysteme/Waldsterben A 30, 1e287. Conti, M.E., Cecchetti, G., 2001. Biological monitoring: lichens as bioindicators of air pollution assessment e a review. Environmental Pollution 114, 471e492. Coxson, D.S., 1988. Recovery of net photosynthesis and dark respiration on rehydration of the lichen, Cladina mitis, and the influence of prior exposure to sulphur dioxide while desiccated. New Phytologist 108, 483e487. Eversman, S., Sigal, L.L., 1987. Effects of SO2, O3, and SO2 and O3 in combination on photosynthesis and ultrastructure of two lichen species. Canadian Journal of Botany 65, 1806e1818. Falconer, R.E., Falconer, P.D., 1980. Determination of cloud water acidity at a mountain observatory in the Adirondack Mountains of New York State. Journal of Geophysical Research C 85, 7465e7470. Fields, R.D., St. Clair, L.L., 1984. A comparison of methods for evaluating SO2 impact on selected lichen species: Parmelia chlorochroa, Collema polycarpon and Lecanora muralis. Bryologist 87, 297e301. Gilbert, O.L., 1969. The effect of SO2 on lichens and bryophytes around Newcastle upon Tyne. In: Proceedings of the First European Congress on the Influence of Air Pollution on Plants and Animals, pp. 223e235.

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