Abstract
Verrucaria rubrocincta Breuss is an endolithic lichen that inhabits caliche plates exposed on the surface of the Sonoran Desert. Caliche surface temperatures are regularly in excess of 60°C during the summer and approach 0°C in the winter. Incident light intensities are high, with photosynthetically active radiation levels typically to 2,600 μmol/m2 s−1 during the summer. A cross-section of rock inhabited by V. rubrocincta shows an anatomical zonation comprising an upper micrite layer, a photobiont layer containing clusters of algal cells, and a pseudomedulla embedded in the caliche. Hyphae of the pseudomedulla become less numerous with depth below the rock surface. Stable carbon and oxygen isotopic data for the caliche and micrite fall into two sloping, well-separated arrays on a δ13C–δ18O plot. The δ13CPDB of the micrite ranges from 2.1 to 8.1 and δ18OSMOW from 25.4 to 28.9, whereas δ13CPDB of the caliche ranges from −4.7 to 0.7 and δ18OSMOW from 23.7 to 29.2. The isotopic data of the micrite can be explained by preferential fixing of 12C into the alga, leaving local 13C enrichment and evaporative enrichment of 18O in the water. The 14C dates of the micrite range from recent to 884 years b.p., indicating that “dead” carbon from the caliche is not a significant source for the lichen-precipitated micrite. The endolithic growth is an adaptation to the environmental extremes of exposed rock surfaces in the hot desert. The micrite layer is highly reflective and reduces light intensity to the algae below and acts as an efficient sunscreen that blocks harmful UV radiation. The micrite also acts as a cap to the lichen and helps trap moisture. The lichen survives by the combined effects of biodeterioration and biomineralization. Biodeterioration of the caliche concomitant with biomineralization of a protective surface coating of micrite results in the distinctive anatomy of V. rubrocincta.
Similar content being viewed by others
References
Batts JE, Calder LJ, Batts BD (2004) Utilizing stable isotope abundances of lichens to monitor environmental change. Chem Geol 204:345–368
Beazley MJ, Rickman RD, Ingram DK, Boutton TW, Russ J (2002) Natural abundances of carbon isotopes (14C, 13C) in lichens and calcium oxalate pruina: implications for archaeological and paleoenvironmental studies. Radiocarbon 44:675–683
Bell RA (1993) Cryptoendolithic algae of hot semiarid lands and deserts. J Phycol 29:133–139
Brown G, Schultz M, Robinson MD (2002) Saxicolous and terricolous lichens form the foothills of northern Oman. Nova Hedwig 75:177–188
Bungartz F, Garvie LAJ, Nash TH III (2004) Anatomy of the endolithic Sonoran desert lichen Verrucaria rubrocincta Breuss: implications for bioteterioration and biomineralization. Lichenologist 36:55–73
Bungartz F, Wirth V (2007) Buellia peregrina sp. nov., a new euendolithic calcicolous lichen species from the Namib Desert. Lichenologist 39:41–45
Burford EP, Fomina M, Gadd GM (2003) Fungal involvement in bioweathering and biotransformation of rocks and minerals. Mineral Mag 67:1127–1155
Burford EP, Hillier S, Gadd GM (2006) Biomineralization of fungal hyphae with calcite (CaCO3) and calcium oxalate mono- and dihydrate in carboniferous limestone microcosms. Geomicrobiol J 23:599–611
Cerling TE, Solomon DK, Quade J, Bowman JR (1991) On the isotopic composition of carbon in soil carbon dioxide. Geochim Cosmochim Acta 55:3403–3405
Chen J, Blume HP, Beyer L (2000) Weathering of rocks induced by lichen colonization—a review. Catena 39:121–146
Craig H (1957) Isotopic standards for carbon and oxygen and corrections factors for mass-spectrometric analysis of carbon dioxide. Geochim Cosmochim Acta 12:133–149
Cuna S, Balas G, Hauer E (2007) Effects of natural environmental factors on delta C-13 of lichens. Isot Environ Health Stud 43:95–104
Friedmann EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215:1045–1053
Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3–49
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
Hall K, Andre MF (2001) New insights into rock weathering from high-frequency rock temperature data: an Antarctic study of weathering by thermal stress. Geomorphology 41:23–35
Hoppert M, Flies C, Pohl W, Günzl B, Schneider J (2004) Colonization strategies of lithobiontic microorganisms on carbonate rocks. Environ Geol 46:421–428
Kappen L, Friedmann EI, Garty J (1981) Ecophysiology of lichens in the dry valleys of Southern Victoria-Land, Antarctica. I. Microclimate and the cryptoendolithic lichen habitat. Flora 171:216–235
Kidron GJ (2000) Dew moisture regime of endolithic and epilithic lichens inhabiting limestone cobbles and rock outcrops, Negev Highland, Israel. Flora 195:146–153
Knauth LP, Brill M, Klonowski S (2003) Isotope geochemistry of caliche developed on basalt. Geochim Cosmochim Acta 67:185–195
Knight KB, Clements DR, Gordillo LF, Jefferies JI, Tilley D, Workman TJ, Lloyd AF, St Clair LLS (2002) The lichen flora of two sites in the Mojave Desert, California, USA. Mycotaxon 84:27–32
Kranner I, Grill D (1997) Desiccation and the subsequent recovery of cryptogamics that are resistant to drought. Phyton-Annales Rei Botanicae 37:139–150
Kuhlman KR, Fusco WG, La Duc MT, Allenbach LB, Ball CL, Kuhlman GM, Anderson RC, Erickson IK, Stuecker T, Benardini J, Strap JL, Crawford RL (2006) Diversity of microorganisms within rock varnish in the Whipple Mountains, California. Appl Environ Microbiol 72:1708–1715
Máguas C, Brugnoli E (1996) Spatial variation in carbon isotope discrimination across the thalli of several lichen species. Plant Cell Environ 19:437–446
Matthes U, Turner SJ, Larson DW (2001) Light attenuation by limestone rock and its constraint on the depth distribution of endolithic algae and cyanobacteria. Int J Plant Sci 162:263–270
McCrea JM (1950) On the isotopic chemistry of carbonates and a paleotemperature scale. J Chem Phys 18:849–857
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
Nash TH III (1996a) Lichen biology. Cambridge University Press, Cambridge
Nash TH III (1996b) Photosynthesis, respiration, productivity and growth. In: Nash TH III (ed) Lichen Biology. Cambridge University Press, Cambridge, pp 88–120
Nash TH III, Reiner A, Demmig-Adams B, Kilian E, Kaiser WM, Lange OL (1990) The effect of atmospheric desiccation and osmotic water stress on photosynthesis and dark respiration of lichens. New Phytol 116:269–276
Nash TH III, White SL, Marsh JE (1977) Lichen and moss distribution and biomass in hot desert ecosystems. Bryologist 80:470–479
Nash TH III, Ryan BD, Gries C, Bungartz F (2002) Lichen flora of the Greater Sonoran Desert Region. Lichens, Tempe
Nash TH III, Ryan BD, Diederich P, Gries C, Bungartz F (2004) Lichen flora of the Greater Sonoran Desert Region. Lichen Unlimited, Tempe
O'Neil JR, Adami LH, Epstein S (1975) Revised value for the 18O fractionation between CO2 and H2O at 25°C. J Res US Geol Surv 3:623–624
O'Neil JR, Clayton RN, Mayeda TK (1969) Oxygen isotope fractionation in divalent metal carbonates. J Chem Phys 51:5547–5558
Omelon CR, Pollard WH, Ferris FG (2006) Environmental controls on microbial colonization of high Arctic cryptoendolithic habitats. Polar Biol 30:19–29
Quade J, Cerling TE, Bowman JR (1989) Systematic variations in the carbon and oxygen isotopic composition of pedogenic carbonate along elevation transects in the southern Great Basin, United States. Geol Soc Am Bull 101:464–475
Riera P (2005) δ13C and δ15N comparison among different co-occurring lichen species from littoral rocky substrata. Lichenologist 37:93–95
Sharma T, Clayton RN (1965) Measurements of 18O/16O ratios of total oxygen from carbonates. Geochim Cosmochim Acta 29:1347–1353
Scheidegger C, Schroeter B, Frey B (1995) Structural and functional processes during water-vapor uptake and desiccation in selected lichens with green algal photobionts. Planta 197:399–409
Staley JT, Palmer F, Adams JB (1982) Microcolonial fungi: common inhabitants on desert rock? Science 215:1093–1095
Tretiach M (1995) Ecophysiology of calcicolous endolithic lichens: progress and problems. G Bot Ital 129:159–184
Tretiach M, Muggia L (2006) Caloplaca badioreagens, a new calcicolous, endolithic lichen from Italy. Lichenologist 38:223–229
Tretiach M, Pecchiari M (1995) Gas exchange rates and chlorophyll content of epi- and endolithic lichens from the Trieste karst (NE Italy). New Phytol 130:585–592
Viles HA (2005) Microclimate and weathering in the central Namib Desert, Namibia. Geomorphology 67:189–209
Weissman L, Garty J, Hochman A (2005) Rehydration of the lichen Ramalina lacera results in production of reactive oxygen species and nitric oxide and a decrease in antioxidants. Appl Environ Microbiol 71:2121–2129
Acknowledgment
We thank Dr. Othmar Breuss, Naturhistorisches Museum Wien for the confirmation of the specimen identification as V. rubrocincta. Funding for this research was provided by the National Science Foundation (DEB-0103738) and NASA (NNG06GE37G). This is publication no. 1069 of the Charles Darwin Research Station.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Garvie, L.A.J., Knauth, L.P., Bungartz, F. et al. Life in extreme environments: survival strategy of the endolithic desert lichen Verrucaria rubrocincta . Naturwissenschaften 95, 705–712 (2008). https://doi.org/10.1007/s00114-008-0373-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-008-0373-0