Abstract
The functional roles of secondary lichen compounds are reviewed with focus on sun-screening and herbivore-deterring functions. Hypotheses on ecological functions can be tested because lichen compounds can nondestructively be extracted from air-dry lichens with 100% acetone. Substantial evidence supports a sun-screening function of cortical compounds. They screen solar radiation by absorptance (parietin, melanins) or by reflectance (atranorin). Their concentration correlates with light exposure and they protect the photobiont against excessive visible light. UV-B induces the formation of parietin, usnic acid, and melanins; the synthesis of the two first compounds has been shown to be boosted by photosynthates. The numerous extractable medullary lichen compounds hardly function as sun-screens. Some of these carbon-based compounds deter generalist herbivores, particularly in lichens in oligotrophic sites. Lichens in nitrogen-rich sites often deter grazing animals as efficient as those from oligotrophic sites despite low contents of lichen compounds. Acetone rinsing of nitrophytic lichens does not lead to increased grazing, meaning that their defense remains to be described. Thanks to grazing experiments using acetone rinsing, there is now solid support for the optimal defense theory in lichen–herbivore interactions. Recent studies have shown that lichen-feeding gastropods can shape epiphytic lichen communities.
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References
Asplund J, Gauslaa Y (2007) Content of secondary compounds depends on thallus size in the foliose lichen Lobaria pulmonaria. Lichenologist 39:273–278
Asplund J, Gauslaa Y (2008) Mollusc grazing limits growth and early development of the old forest lichen Lobaria pulmonaria in broadleaved deciduous forests. Oecologia 155:93–99
Asplund J, Solhaug KA, Gauslaa Y (2009) Fungal depsidones – an inducible or constitutive defence against herbivores in the lichen Lobaria pulmonaria? Basic Appl Ecol 10:273–278
Asplund J, Johansson O, Nybakken L, Palmqvist K, Gauslaa Y (2010a) Simulated nitrogen deposition influences gastropod grazing in lichens. Ecoscience 17:83–89
Asplund J, Larsson P, Vatne S, Gauslaa Y (2010b) Gastropod grazing shapes the vertical distribution of epiphytic lichens in forest canopies. J Ecol 98:218–225
Asplund J, Solhaug KA, Gauslaa Y (2010c) Optimal defense: snails avoid reproductive parts of the lichen Lobaria scrobiculata due to internal defense allocation. Ecology 91:3100–3105
Bjerke JW, Elvebakk A, Domínguez E, Dahlback A (2005) Seasonal trends in usnic acid concentrations of Arctic, alpine and Patagonian populations of the lichen Flavocetraria nivalis. Phytochemistry 66:337–344
Björn LO, McKenzie RL (2002) Ozone depletion and effects of ultraviolet radiation. In: Björn LO (ed) Photobiology: the science of light and life. Kluwer Academic, Dordrecht, pp 239–263
Brown RT, Mikola P (1974) The influence of fruticose soil lichens upon the mychorrhiza and seedling growth of forest trees. Acta For Fenn 141:1–23
Buffoni Hall RS, Paulsson M, Duncan K, Tobin AK, Widell S, Bornman JF (2003) Water- and temperature-dependence of DNA damage and repair in the fruticose lichen Cladonia arbuscula ssp. mitis exposed to UV-B radiation. Physiol Plant 118:371–379
Cameron R (2009) Are non-native gastropods a threat to endangered lichens? Can Field Nat 123:169–171
Cockell CS, Knowland J (1999) Ultraviolet radiation screening compounds. Biol Rev Camb Philos Soc 74:311–345
Dailey RN, Montgomery DL, Ingham JT, Siemion R, Vasquez M, Raisbeck MF (2008) Toxicity of the lichen secondary metabolite (+)-usnic acid in domestic sheep. Vet Pathol 45:19–25
de la Torre R, Sancho LG, Horneck G, de los Rios A, Wierzchos J, Olsson-Francis K, Cockell CS, Rettberg P, Berger T, de Vera JPP, Ott S, Frias JM, Melendi PG, Lucas MM, Reina M, Pintado A, Demets R (2010) Survival of lichens and bacteria exposed to outer space conditions – results of the Lithopanspermia experiments. Icarus 208:735–748
de Vera JP, Rettberg P, Ott S (2008) Life at the limits: capacities of isolated and cultured lichen symbionts to resist extreme environmental stresses. Origins Life Evol Biosph 38:457–468
Demmig-Adams B, Adams WW III, Green TGA, Czygan FC, Lange OL (1990) Differences in the susceptibility to light stress in two lichens forming a phycosymbiodeme, one partner possessing and one lacking the xanthophyll cycle. Oecologia 84:451–456
Dietz S, Büdel B, Lange OL, Bilger W (2000) Transmittance of light through the cortex of lichens from contrasting habitats. Bibl Lichenol 75:171–182
Dubay SA, Hayward GD, Martínez del Rio C (2008) Nutritional value and diet preference of arboreal lichens and hypogeous fungi for small mammals in the Rocky Mountains. Can J Zool 86:851–862
Emmerich R, Giez I, Lange OL, Proksch P (1993) Toxicity and antifeedant activity of lichen compounds against the polyphagous herbivorous insect Spodoptera littoralis. Phytochemistry 33:1389–1394
Ertl L (1951) Über die Lichtverhältnisse in Laubflechten. Planta 39:245–270
Fahselt D (1994) Secondary biochemistry of lichens. Symbiosis 16:117–165
Fahselt D, Alstrup V (1997) Visualization of extracellular deposits in recent and subfossil Umbilicaria hyperborea. Lichenologist 29:547–557
Favero-Longo SE, Piervittori R (2010) Lichen-plant interactions. J Plant Interact 5:163–177
Fisher RF (1979) Possible allelopathic effects of reindeer-moss (Cladonia) on Jack pine and white spruce. For Sci 25:256–260
Gauslaa Y (1985) The ecology of Lobarion pulmonariae and Parmelion caperatae in Quercus dominated forests in south-west Norway. Lichenologist 17:117–140
Gauslaa Y (2005) Lichen palatability depends on investments in herbivore defence. Oecologia 143:94–105
Gauslaa Y (2008) Mollusc grazing may constrain the ecological niche of the old forest lichen Pseudocyphellaria crocata. Plant Biol 10:711–717
Gauslaa Y, McEvoy M (2005) Seasonal changes in solar radiation drive acclimation of the sun-screening compound parietin in the lichen Xanthoria parietina. Basic Appl Ecol 6:75–82
Gauslaa Y, Solhaug KA (1996) Differences in the susceptibility to light stress between epiphytic lichens of ancient and young boreal forest stands. Funct Ecol 10:344–354
Gauslaa Y, Solhaug KA (1999) High-light damage in air-dry thalli of the old forest lichen Lobaria pulmonaria-interactions of irradiance, exposure duration and high temperature. J Exp Bot 50:697–705
Gauslaa Y, Solhaug KA (2000) High-light-intensity damage to the foliose lichen Lobaria pulmonaria within a natural forest: the applicability of chlorophyll fluorescence methods. Lichenologist 32:271–289
Gauslaa Y, Solhaug KA (2001) Fungal melanins as a sun screen for symbiotic green algae in the lichen Lobaria pulmonaria. Oecologia 126:462–471
Gauslaa Y, Ustvedt EM (2003) Is parietin a UV-B or a blue-light screening pigment in the lichen Xanthoria parietina? Photochem Photobiol Sci 2:424–432
Gauslaa Y, Lie M, Solhaug KA, Ohlson M (2006) Growth and ecophysiological acclimation of the foliose lichen Lobaria pulmonaria in forests with contrasting light climates. Oecologia 147:406–416
Gerson U, Seaward MRD (1977) Lichen-invertebrate associations. In: Seaward MRD (ed) Lichen ecology. Academic, London, pp 69–119
Hauck M (2008) Metal homeostasis in Hypogymnia physodes is controlled by lichen substances. Environ Pollut 153:304–308
Hesbacher S, Giez I, Embacher G, Fiedler K, Max W, Trawoger A, Turk R, Lange OL, Proksch P (1995) Sequestration of lichen compounds by lichen-feeding members of the Arctiidae (Lepidoptera). J Chem Ecol 21:2079–2089
Hill DJ, Woolhouse HW (1966) Aspects of the autecology of Xanthoria parietina agg. Lichenologist 3:207–214
Honegger R (1991) Functional aspects of lichen symbiosis. Annu Rev Plant Physiol Plant Mol Biol 42:553–578
Huneck S (1973) Nature of lichen substances. In: Ahmadjian V (ed) The lichens. Academic, London, pp 495–522
Huneck S (1999) The significance of lichens and their metabolites. Naturwissenschaften 86:559–570
Huneck S, Yoshimura I (1996) Identification of lichen substances. Springer, Berlin
Imshaug HA, Brodo IM (1966) Biosystematic studies in Lecanora pallida and some related lichens in the Americas. Nova Hedwigia 12:1–59
Ingólfsdóttir K (2002) Usnic acid. Phytochemistry 61:729–736
Jansen MAK, Gaba V, Greenberg BM (1998) Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci 3:131–135
Jenkins GI (2009) Signal transduction in responses to UV-B radiation. Annu Rev Plant Biol 60:407–431
Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, Chicago
Lange OL, Green TGA, Reichenberger H, Hesbacher S, Proksch P (1997) Do secondary substances in the thallus of a lichen promote CO2 diffusion and prevent depression of net photosynthesis at high water content? Oecologia 112:1–3
Lawrey JD (1980) Correlations between lichen secondary chemistry and grazing activity by Pallifera-varia. Bryologist 83:328–334
Lawrey JD (1983) Lichen herbivore preference: a test of two hypotheses. Am J Bot 70:1188–1194
Lawrey JD (1986) Biological role of lichen substances. Bryologist 89:111–122
Lawrey JD (2000) Chemical interactions between two lichen-degrading fungi. J Chem Ecol 26:1821–1831
Legaz ME, Fontaniella B, Millanes AM, Vicente C (2004) Secreted arginases from phylogenetically far-related lichen species act as cross-recognition factors for two different algal cells. Eur J Cell Biol 83:435–446
Mattson W (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161
McEvoy M, Nybakken L, Solhaug KA, Gauslaa Y (2006) UV triggers the synthesis of the widely distributed secondary lichen compound usnic acid. Mycol Prog 5:221–229
McEvoy M, Solhaug KA, Gauslaa Y (2007a) Solar radiation screening in usnic acid-containing cortices of the lichen Nephroma arcticum. Symbiosis 43:143–150
McEvoy M, Gauslaa Y, Solhaug KA (2007b) Changes in pools of depsidones and melanins, and their function, during growth and acclimation under contrasting natural light in the lichen Lobaria pulmonaria. New Phytol 175:271–282
McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320
Merzlyak MN, Chivkunova OB, Zhigalova TV, Naqvi KR (2009) Light absorption by isolated chloroplasts and leaves: effects of scattering and ‘packing’. Photosynth Res 102:31–41
Milborrow BV (1963) Penetration of seeds by acetone solutes. Nature 199:716–717
Molnár K, Farkas E (2010) Current results on biological activities of lichen secondary metabolites: a review. Z Naturforsch 65c:157–173
Nybakken L, Julkunen-Tiitto R (2006) UV-B induces usnic acid in reindeer lichens. Lichenologist 38:477–485
Nybakken L, Solhaug KA, Bilger W, Gauslaa Y (2004) The lichens Xanthoria elegans and Cetraria islandica maintain a high protection against UV-B radiation in Arctic habitats. Oecologia 140:211–216
Nybakken L, Asplund J, Solhaug KA, Gauslaa Y (2007) Forest successional stage affects the cortical secondary chemistry of three old forest lichens. J Chem Ecol 33:1607–1618
Nybakken L, Johansson O, Palmqvist K (2009) Defensive compound concentration in boreal lichens in response to simulated nitrogen deposition. Glob Change Biol 15:2247–2260
Nybakken L, Helmersen AM, Gauslaa Y, Selås V (2010) Lichen compounds restrain lichen feeding by bank voles (Myodes glareolus). J Chem Ecol 36:298–304
Peumans WJ, Van Damme EJM (1995) Lectins as plant defense proteins. Plant Physiol 109:347–352
Pöykkö H, Hyvärinen M, Backor M (2005) Removal of lichen secondary metabolites affects food choice and survival of lichenivorous moth larvae. Ecology 86:2623–2632
Pyatt FB (1967) The inhibitory influence of Peltigera canina on the germination of graminaceous seeds and the subsequent growth of the seedlings. Bryologist 70:326–329
Ranković B, Mišić M, Sukdolak S (2008) The antimicrobial activity of substances derived from the lichens Physcia aipolia, Umbilicaria polyphylla, Parmelia caperata and Hypogymnia physodes. World J Microbiol Biotechnol 24:1239–1242
Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic, New York
Richardson DHS, Young CM (1977) Lichens and vertebrates. In: Seaward MRD (ed) Lichen ecology. Academic, London, pp 121–144
Rundel PW (1969) Clinal variation in the production of usnic acid in Cladonia subtenuis along light gradients. Bryologist 72:40–44
Sancho LG, de la Torre R, Horneck G, Ascaso C, de los Rios A, Pintado A, Wierzchos J, Schuster M (2007) Lichens survive in space: results from the 2005 LICHENS experiment. Astrobiology 7:443–454
Scheidegger C (1995) Early development of transplanted isidioid soredia of Lobaria pulmonaria in an endangered population. Lichenologist 27:361–374
Scheidegger C, Frey B, Zoller S (1995) Transplantation of symbiotic propagules and thallus fragments: Methods for the conservation of threatened epiphytic lichen population. Mitteilungen der Eidgenössischen Forschungsanstalt für Wald, Schnee und Landschaft 70:41–62
Slansky F (1979) Effect of the lichen chemicals atranorin and vulpinic acid upon feeding and growth of larvae of the yellow-striped armyworm, Spodoptera-ornithogalli (Lepidoptera, Noctuidae). Environ Entomol 8:865–868
Smith CW, Aptroot A, Coppins BJ, Fletcher A, Gilbert OL, James PW, Wolseley PA (2009) The lichens of Great Britain and Ireland. The British Lichen Society, London
Solberg YJ (1971) Studies on the chemistry of lichens. X. Chemical investigation of the lichen species Xanthoria parietina (L.) Th. Fr. Bryologist 74:144–150
Solhaug KA, Gauslaa Y (1996) Parietin, a photoprotective secondary product of the lichen Xanthoria parietina. Oecologia 108:412–418
Solhaug KA, Gauslaa Y (2001) Acetone rinsing – a method for testing ecological and physiological roles of secondary compounds in living lichens. Symbiosis 30:301–315
Solhaug KA, Gauslaa Y (2004) Photosynthates stimulate the UV-B induced fungal anthraquinone synthesis in the foliose lichen Xanthoria parietina. Plant Cell Environ 27:167–176
Solhaug KA, Gauslaa Y, Haugen J (1995) Adverse effects of epiphytic crustose lichens upon stem photosynthesis and chlorophyll of Populus tremula L. Bot Acta 108:233–239
Solhaug KA, Gauslaa Y, Nybakken L, Bilger W (2003) UV-induction of sun-screening pigments in lichens. New Phytol 158:91–100
Solhaug KA, Lind M, Nybakken L, Gauslaa Y (2009) Possible functional roles of cortical depsides and medullary depsidones in the foliose lichen Hypogymnia physodes. Flora Morphol Distrib Funct Ecol Plants 204:40–48
Solhaug K, Larsson P, Gauslaa Y (2010) Light screening in lichen cortices can be quantified by chlorophyll fluorescence techniques for both reflecting and absorbing pigments. Planta 231:1003–1011
Souza-Egipsy V, Valladares F, Ascaso C (2000) Water distribution in foliose lichen species: interactions between method of hydration, lichen substances and thallus anatomy. Ann Bot 86:595–601
Stamp N (2003) Out of the quagmire of plant defense hypotheses. Quart Rev Biol 78:23–55
Stark S, Kytöviita M-M, Neumann AB (2007) The phenolic compounds in Cladonia are not antimicrobial in soil. Oecologia 152:299–306
Sundset MA, Kohn A, Mathiesen SD, Præsteng KE (2008) Eubacterium rangiferina, a novel usnic acid-resistant bacterium from the reindeer rumen. Naturwissenschaften 95:741–749
Tao KL, Khan AA (1974) Penetration of dry seeds with chemicals applied in acetone. Plant Physiol 54:956–958
Temina M, Levitsky DO, Dembitsky VM (2010) Chemical constituents of the epiphytic and lithophilic lichens of the genus Collema. Rec Nat Prod 4:79–86
Tønsberg T (1992) The sorediate and isidiate, corticolous, crustose lichens in Norway. Sommerfeltia 14:1–331
Vatne S, Solhoy T, Asplund J, Gauslaa Y (2010) Grazing damage in the old forest lichen Lobaria pulmonaria increases with gastropod abundance in deciduous forests. Lichenologist 42:615–619
Vavasseur A, Gautier H, Thibaud MC, Lasceve G (1991) Effects of usnic acid on the oxygen-exchange properties of mesophyll cell protoplasts from Commelina communis L. J Plant Physiol 139:90–94
Vráblíková H, McEvoy M, Solhaug KA, Barták M, Gauslaa Y (2006) Annual variation in photo acclimation and photoprotection of the photobiont in the foliose lichen Xanthoria parietina. J Photochem Photobiol B Biol 83:151–162
White T (1993) The inadequate environment: nitrogen and the abundance of animals. Springer, Heidelberg
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Solhaug, K.A., Gauslaa, Y. (2012). Secondary Lichen Compounds as Protection Against Excess Solar Radiation and Herbivores. In: Lüttge, U., Beyschlag, W., Büdel, B., Francis, D. (eds) Progress in Botany 73. Progress in Botany, vol 73. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-22746-2_11
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