Skip to main content

Advertisement

Log in

Diversity of cyanobacteria on rock surfaces

  • Review Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Terrestrial cyanobacteria dwelling on rocks and stone walls represent an important but still understudied part of global biodiversity, despite their substantial importance to the environment. Microbial biofilms, including those formed by cyanobacteria, play an essential role in the succession on rock habitats as they possess a unique ability to gradually change the biotope. In this review, we have gathered 180 research publications reporting on occurrence of 762 species of terrestrial cyanobacteria on rock surfaces worldwide. Despite the long history of phycological research in general, Europe remains the most thoroughly explored region in the field of terrestrial phycology. A total of 401 taxa records from aerial epilithic habitats have been reported from this subcontinent. With regard to the lack of comparably comprehensive studies from different areas of the world, reliable comparisons of species richness among different geographical regions and climatic zones are not available at the moment. Heterocytous and coccoid cyanobacteria prevailed on the rocks and stones in terms of biomass, however, the species richness seemed to be distributed equally among coccoid (269 taxa), simple filamentous (275 taxa), and heterocytous (218 taxa) forms. As the heterogeneity of the available data shows, further thorough research on this often neglected group of organisms is desirable. To set a starting point for such an effort, this review summarizes the current state of knowledge on aerial epilithic cyanobacterial communities on both natural and anthropogenic stone surfaces around the world.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdelahad N (1989) On four Myxosarcina-like species (Cyanophyta) living in the Inferniglio cave (Italy). Algol Stud 54:3–13

    Google Scholar 

  • Aboal M, Asencio AD, Prefasi M (1994) Studies on cave cyanophytes from southeastern Spain: Scytonema julianum. Algol Stud 74:31–36

    Google Scholar 

  • Adhikari SP, Kováčik L (2010) Comparative analysis of cyanobacteria and micro-algae in the biofilms on the exterior of stone monuments in Bratislava, Slovakia and Bhubaneswar, India. J Indian Bot Soc 89(1–2):19–23

    Google Scholar 

  • Albertano P (1993) Epilithic algal communities in hypogean environments. G Bot Ital 127:386–392

    Google Scholar 

  • Albertano P, Bruno L, D’Ottavi D, Moscone D, Palleschi G (2000) Effect of photosyntesis on pH variation in cyanobacterial biofilms from Roman catacombs. J Appl Phycol 12:379–384

    Google Scholar 

  • Anagnostidis K, Economou-Amilli A, Pantazidou A (1981) Studies in the microflora of the cave Perma, Ioannina, Greece. Bull Soc Speleol Greece 18:458–530

    Google Scholar 

  • Anagnostidis K, Economou-Amilli A, Roussomoustakaki M (1983) Epilithic and chasmolithic microflora (Cyanophyta, Bacillariophyta) from marbles of the Parthenon (Acropolis-Athens, Greece). Nova Hedwigia 38:227–287

    Google Scholar 

  • Asencio AD, Aboal M (1996) Cyanophytes from Andragulla abrigo (Murcia, SE Spain) and their environmental conditions. Algol Stud 83:55–72

    Google Scholar 

  • Asencio AD, Aboal M (2000) Algae from Serreta cave (Murcia, SE Spain) and their environmental conditions. Algol Stud 96:59–78

    Google Scholar 

  • Asencio AD, Aboal M (2011) In situ nitrogen fixation by cyanobacteria at the Andragulla cave, Spain. J Cave Karst Stud 73(2):50–54

    CAS  Google Scholar 

  • Aubrecht R, Brewer-Carías Ch, Šmída B, Audy M, Kováčik L (2008) Anatomy of biologically mediated opal speleothems in the World’s largest sandstone cave: Cueva Charles Brewer, Chimantá Plateau, Venezuela. Sediment Geol 203:181–195

    Google Scholar 

  • Barberousse H, Tell G, Yéprémian C, Couté A (2006) Diversity of algae and cyanobacteria growing on building facades in France. Arch Hydrobiol/Algol Stud 120:81–105

    Google Scholar 

  • Beck-Mannagetta G (1926) Algenfunde im Riesengebirge. Ein Beitrag zur Kenntnis der Algenflora des Riesengebirges. Věstník Král Čes Spol Nauk Tř II:1–18

    Google Scholar 

  • Beck-Mannagetta G (1929) Algenfunde im Riesengebirge. Ein zweiter Beitrag zur Kenntnis der Algenflora des Riesengebirges. Lotos 77:92–100

    Google Scholar 

  • Bellinzoni AM, Caneva G, Ricci S (2003) Ecological trends in travertine colonisation by pioneer algae and plant communities. Int Biodeterior Biodegr 51:203–210

    Google Scholar 

  • Bohunická M, Johansen JR, Fučíková K (2011) Tapinothrix clintonii sp. nov. (Pseudanabaenaceae, Cyanobacteria), a new species at the nexus of five genera. Fottea 11(1):127–140

    Google Scholar 

  • Broady P (1996) Diversity, distribution, and dispersal of Antarctic terrestrial algae. Biodivers Conserv 5:1307–1335

    Google Scholar 

  • Büdel B (1999) Ecology and diversity of rock-inhabiting cyanobacteria in tropical regions. Eur J Phycol 34:361–370

    Google Scholar 

  • Büdel B, Lüttge U, Stelzer R, Huber O, Medina E (1994) Cyanobacteria of rocks and soils of the Orinoco Lowlands and the Guayana Uplands, Venezuela. Bot Acta 107:422–431

    Google Scholar 

  • Büdel B, Becker U, Porembski S, Barthlott W (1997) Cyanobacteria and cyanobacterial lichens from Inselbergs of the Ivory Coast, Africa. Bot Acta 110:458–465

    Google Scholar 

  • Büdel B, Weber HM, Porembski S, Barthlott W (2002) Cyanobacteria of inselbergs in the Atlantic rainforest zone of eastern Brazil. Phycologia 41:498–506

    Google Scholar 

  • Camburn KE (1983) Subaerial algae from eastern Kentucky. Castanea 48(2):83–88

    Google Scholar 

  • Casamatta DA, Verb RG, Beaver JR, Vis ML (2002) An investigation of the cryptobiotic community from sandstone cliffs in Southeast Ohio. Int J Plant Sci 163(5):837–845

    Google Scholar 

  • Casamatta DA, Gomez SR, Johansen JR (2006) Rexia erecta gen. et sp. nov. and Capsosira lowei sp. nov., two newly described cyanobacterial taxa from the Great Smoky Mountains National Park (USA). Hydrobiologia 561:13–26

    Google Scholar 

  • Cassar L (2004) Photocatalysis of cementitious materials: clean buildings and clean air. MRS Bull 29:328–331

    CAS  Google Scholar 

  • Chang TP, Chang-Schneider H (1994) Algen in vier suddeutschen Hohlen. Ber Bayer Bot Ges 62:221–229

    Google Scholar 

  • Claus G (1962) Data on the ecology of the algae of the Peace Cave in Hungary. Nova Hedwigia 4:55–80

    Google Scholar 

  • Couté A (1985) Preliminary comparative study of two calcareous cyanophytes from caves: Geitleria calcarea Friedmann and Scytonema julianum Meneghin. Arch Hydrobiol 71:91–98

    Google Scholar 

  • Couté A, Tell G, Thérézien Y (1999) Cyanophyceae (Cyanobacteria) aérophiles de Nouvelle-Calédonie. Cryptogam Algol 20:30–144

    Google Scholar 

  • Crispim CA, Gaylarde CC (2004) Cyanobacteria and biodeterioration of cultural heritage: a review. Microb Ecol 49:1–10

    PubMed  Google Scholar 

  • Czerwik–Marcinkowska J, Mrozinska T (2011) Algae and cyanobacteria in Caves of the Polish Jura. Pol Bot J 56(2):203–243

    Google Scholar 

  • Danin A, Caneva G (1990) Deterioration of limestone walls in Jerusalem and marble monuments in Rome caused by cyanobacteria and cyanophilous lichens. Int Biodeterior 26:397–417

    Google Scholar 

  • Darby BJ, Neher DA (2012) Stable isotope composition of microfauna supports the occurrence of biologically fixed nitrogen from cyanobacteria in desert soil food webs. J Arid Environ 85:76–78

    Google Scholar 

  • Darienko T, Hoffmann L (2003) Algal growth on cultural monuments in Ukraine. Biologia, Bratislava 58(4):575–587

    Google Scholar 

  • Dayner DM, Johansen JR (1991) Observations on the algal flora of Seneca Cavern, Seneca County, Ohio. Ohio J Sci 91:118–121

    Google Scholar 

  • de los Ríos A, Wierzchos J, Sancho LG, Ascaso C (2004) Exploring the physiological state of continental Antarctic endolithic microorganisms by microscopy. FEMS Microbiol Ecol 50:143–152

    Google Scholar 

  • de los Ríos A, Grube M, Sancho LG, Ascaso C (2007) Ultrastructural and genetic characterization of endolithic cyanobacterial biofilms colonizing Antarctic granite rocks. FEMS Microbiol Ecol 59:386–395

    Google Scholar 

  • De Miguel JMG, Sanchez-Castilo L, Ortega-Calvo JJ, Gil JA, Saiz-Jimenez C (1995) Deterioration of building material from great Jaguar Pyramid at Tikal, Guatemala. Build Environ 30(4):591–598

    Google Scholar 

  • De Wildeman E (1900) Les algues de la flore de Buitenzorg (Essai d’une flore algologique de Java). E. G. Brill, Leiden

    Google Scholar 

  • Dickie G (1881) Notes on the algae from the Amazonas and its tributaries. Bot J Linn Soc 18:123–132

    Google Scholar 

  • Diels L (1914) Die Algen-Vegetation der Südtiroler Dolomitriffe. Ein Beitrag zur Ökologie der Lithophyten. Ber Dtsch Bot Ges 32:502–526

    Google Scholar 

  • Dillon JG, Tatsumi CM, Tandingan PG, Castenholz RW (2002) Effect of environmental factors on the synyhesis of scytonemin, a UV-screening pigment, in cyanobacterium (Chroococcidiopsis sp.). Arch Microbiol 177:322–331

    CAS  PubMed  Google Scholar 

  • Dobat K (1970) Considérations sur la végétation cryptogamique des grottes du Jura Souabe (sud-ouest de l’Allemagne). Ann Spéléol 25(4):872–907

    Google Scholar 

  • Dobat K (1972) Ein Ökosystem in Aufbau: Die “Lampenflora Schauhöhlen”. Umsch Wiss Tech 72(15):493–494

    Google Scholar 

  • Dobat K (1977) Zur Ökogenese und Ökologie der Lampenflora deutscher Schauhohlen. Gustav Fischer Verlag, Stuttgart

    Google Scholar 

  • Dobat K (1998) Flore de la lumiére artificiélle (lampen-flora-maladie verte). In: Juberthie C, Decu V (eds) Encyclopaedia biospeleologica, Tome 2. Société de Biospéologie, Moulis-Bucares

    Google Scholar 

  • Dojani S, Lakatos M, Rascher U, Wanek W, Lüttge U, Büdel B (2007) Nitrogen input by cyanobacterial biofilms of an inselberg into a tropical rainforest in French Guiana. Flora 202:521–529

    Google Scholar 

  • Dor I, Dor Y (1999) Cyanobacterial flora of the Soreq stalactite Cave (Israel) and way of its control. Algol Stud 94:115–120

    Google Scholar 

  • Drouet FA (1942) The filamentous Myxophyceae of Jamaica. Bot Ser Field Museum Nat Hist 20:107–122

    Google Scholar 

  • Drouet FA (1957) Contributions to the flora of Venezuela. Algae. Fieldiana 28:681–688

    Google Scholar 

  • Drouet FA (1967) Flora del Auyan-tepui. Algae. Acta Bot Venez 2:70–72

    Google Scholar 

  • Ehling-Schulz M, Scherer S (1999) UV protection in cyanobacteria. Eur J Phycol 34:329–338

    Google Scholar 

  • Faimon J, Štelcl J, Kubešová S, Zima J (2003) Environmentally acceptable effect of hydrogen peroxide on cave ‘‘lamp-flora’’, calcite speleothems and limestones. Environ Poll 122:417–422

    CAS  Google Scholar 

  • Ferreira V, Branco LHZ, Kaštovský J (2013) True branched nostocalean cyanobacteria from tropical aerophytic habitats and molecular assessment of two species from field samples. Rev Biol Trop 61:455–466

    PubMed  Google Scholar 

  • Frémy P (1924) Contribuition à la flore algologique de l’Afrique équatoriale française. Rev Algol 1:1–23

    Google Scholar 

  • Frémy P (1925) Essai sur l’écologie des algues saxicoles, aériennes et subaériennes, en Normandie. Nuova Notarisia 36:297–304

    Google Scholar 

  • Frémy P (1929) Les Myxophycées de l’Afrique équatoriale française. Arch Bot 3:1–508

    Google Scholar 

  • Frémy P (1930) Les Myxophycées de Madagascar. Ann Cryptogam Exot 3:200–230

    Google Scholar 

  • Frémy P (1932) Cyanophycées de la Nouvelle-Guinée. Ann Cryptogam Exot 5:190–197

    Google Scholar 

  • Friedmann I (1961) Chroococcidiopsis kashaii sp. nov. and the genus Chroococcidiopsis (Study of cave algae of Izrael IV). Osterr Bot Zetschrift 108:354–367

    Google Scholar 

  • Friedmann I (1962) Ecology of atmophytic-nitrate alga Chroococcidiopsis kashaii. Arch Microbiol 42:42–45

    Google Scholar 

  • Friedmann EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215(4536):1045–1053

    CAS  PubMed  Google Scholar 

  • Friedmann EI, Ocampo R (1972) Endolithic blue–green algae in the dry valleys: primary producers in the Antarctic desert ecosystem. Science 193(4259):1247–1249

    Google Scholar 

  • Fritsch FE (1907) A general consideration of the subaerial and fresh-water algal flora of Ceylon. A contribution to the study of tropical algal ecology. Part I. -subaerial algae and algae of the Inland fresh-waters. P Roy Soc Lond B Bio 79:197–254

    Google Scholar 

  • Furey PC, Lowe RL, Johansen JR (2007) Wet wall algal community response to in-field nutrient manipulation in the Great Smoky Mountains National Park, USA. Algol Stud 125:17–43

    CAS  Google Scholar 

  • Garbacki N, Ector L, Kostikov I, Hoffmann L (1999) Contribution a l’etude de la fl ore des grottes de Belgique. Belg J Bot 132:43–76

    Google Scholar 

  • Garcia-Pichel F, Castenholz RW (1993) Occurrence of UV-absorbing mycosporine-like compounds among cyanobacterial isolates and an estimate of their sreening capacity. Appl Environ Microbiol 59:163–169

    PubMed Central  CAS  PubMed  Google Scholar 

  • Garcia-Vallés M, Vendrell-Saz M, Molera J, Blazquez F (1998) Interaction of rock and atmosphere: patinas on Mediterranean monuments. Environ Geol 36(1–2):137–149

    Google Scholar 

  • Gardner NL (1927) New Myxophyceae from Porto Rico. Mem the N Y Bot Gard 7:1–144

    Google Scholar 

  • Garthy J (1992) The postfire recovery of rock-inhabiting algae, microfungi and lichens. Can J Botany 70(2):301–312

    Google Scholar 

  • Gaylarde CC, Gaylarde PM (2005) A comparative study of the major microbial biomass of biofilms on exteriors of buildings in Latin America. Int Biodeterior Biodegr 55(2):131–139

    Google Scholar 

  • Geitler L (1933) Diagnosen neuer Blaualgen von den Sunda-Inseln. Arch Hydrobiol 12:622–634

    Google Scholar 

  • Golubić S (1967a) Algenvegetation der Felsen. In: Elster HJ, Ohle W (eds) Die Binnengewässer. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart

    Google Scholar 

  • Golubić S (1967b) Die Algenvegetation an Sandsteinfelsen Ost-Venezuelas (Cumaná). Int Revue gesamten Hydrobiol Hydrogr 52:693–699

    Google Scholar 

  • Golubić S, Friedmann EI, Schneider J (1981) The lithobiontic niche, with special reference to microorganisms. J Sediment Petrol 51:475–478

    Google Scholar 

  • Gomez SR, Johansen JR, Lowe RL (2003) Epilithic aerial algae of Great Smoky Mountains National Park. Biologia 58(4):603–615

    Google Scholar 

  • Goméz-Alarcón G, Muñoz M, Ariño X, Ortega-Calvo JJ (1995) Microbial communities in weathered sandstone: the case of Carrascosa del Campo church, Spain. Sci Total Environ 167:249–254

    Google Scholar 

  • Gomont M (1901) Myxophyceae hormogoneae in Johs. Schmidt. Flora of Koh Chang IV 24:202–211

    Google Scholar 

  • Gorbushina AA (2007) Life on the Rocks (Mini-Review). Environ Microbiol 9:1613–1631

    CAS  PubMed  Google Scholar 

  • Hambler DJ (1964) The vegetation of granitic outcrops in western Nigeria. J Ecol 52:573–594

    Google Scholar 

  • Hariot MP (1913) Quelques cryptogames du Sahara et des régions voisines. Bull Muséum d’histoire Nat 1:113–115

    Google Scholar 

  • Hauer T (2007) Rock-inhabiting cyanoprokaryota from South Bohemia (Czech Republic). Nova Hedwigia 85(3–4):379–392

    Google Scholar 

  • Hauer T (2008) Epilithic cyanobacterial flora of Mohelenská hadcová steppe Nature Reserve (western Moravia, Czech Republic) 70 years ago and now. Fottea 8(2):129–132

    Google Scholar 

  • Hauer T (2010) Phototrophic biofilms on the interior walls of concrete Iterson-type cooling towers. J Appl Phycol 22:733–736

    Google Scholar 

  • Hauer T, Bohunická M, Johansen JR, Mareš J, Berrendero-Gomez E (2014) Reassessment of the cyanobacterial family Microchaetaceae and establishment of new families Tolypothrichaceae and Godleyaceae. J Phycol 50:1089–1100

    CAS  Google Scholar 

  • Häyrén E (1940) Die Algenvegetation der Sickerwasserstreifen auf den Felsen in Sudfinnland. Soc Sci Fenn Comment Biol 7:1–19

    Google Scholar 

  • Hernández-Mariné M, Asencio A, Canals A, Ariño X, Aboal M, Hoffmann L (1999) Discovery of populations of the lime-incrusting genus Loriella (Stigonematales) in Spanish caves. Algol Stud 94:122–137

    Google Scholar 

  • Hindák F, Wolowski K, Hindáková A (2011) The epilithon of a cooling tower of the power plant at Belchatow. Poland. Oceanol Hydrobiol Stud 40(4):38–43

    Google Scholar 

  • Hirsch P, Eckhardt FEW, Palmer RJ Jr (1995) Methods for the study of rock-inhabiting microorganisms—A mini-review. J Microbiol Methods 23:143–167

    Google Scholar 

  • Hoffmann L (1986) Cyanophycées aériennes et subaériennes du Grand-Duché de Luxembourg. Bull Jardin Bot Nat Belg 56(1–2):77–125

    Google Scholar 

  • Hoffmann L (1991) Terrestrial Cyanophyceae of Papua New Guinea. 1. The genus Stigonema. Arch Hydrobiol Suppl 92:333–348

    Google Scholar 

  • Hoffmann L (2002) Caves and other low-light environments: aerophytic photoautotrophic microorganisms. In: Bitton G (ed) Encyclopedia of environmental microbiology. Wiley, New York

    Google Scholar 

  • Hoffmann L, Darienko T (2005) Algal biodiversity on sandstone in Luxembourg. Ferrantia 44:99–101

    Google Scholar 

  • Hoffmann L, Gugger M, Asencio A (2003) Morphological and molecular characterisation of a stigonematalean cyanobacterium isolated from Spanish cave. Algol Stud 109:259–265

    Google Scholar 

  • Iliopoulou-Georgoudaki J, Pantazidou A, Theoulakis P (1993) An Assessment of cleaning photoautotrophic microflora: the case of Perama cave, Ioannina Greece. Mem Biospeleol 20:117–120

    Google Scholar 

  • Jaag O (1945) Untersuchungen über die Vegetation und Biologie der Algen des nackten Gesteins in den Alpen, im Jura und im schweizerischen Mittelland. In: Jaag O (ed) Beiträge zur Kryptogamenflora der Schweiz IX, Heft 3. Kommisionsverlag Buchdruckerei Büchler & Co., Bern

  • Johansen JR (1999) Diatoms of aerial habitats. In: Stoermer EF, Smol JP (eds) The diatoms: applications for the environmental and earth sciences. Cambridge University Press, Cambridge, pp 264–273

    Google Scholar 

  • Johansen JR, Rushforth SR, Brotherson JD (1983a) The algal flora of Navajo National Monument, Arizona, U.S.A. Nova Hedwigia 38:501–553

    Google Scholar 

  • Johansen JR, Rushforth SR, Orbendorfer R, Fungladda N, Grimes JA (1983b) The algal flora of selected wet walls in Zion National Park, Utah, USA. Nova Hedwigia 38:765–808

    Google Scholar 

  • Johansen JR, Lowe RL, Carty S, Fučíková K, Olsen CE, Fitzpatrick MH, Ress JA, Furey PC (2007) New algal species records for Great Smoky Mountains National Park with an annotated checklist of all reported algal taxa for the park. Southeast Nat 6(1):99–134

    Google Scholar 

  • Johansen JR, Olsen CE, Lowe RL, Fučíková K, Casamatta DA (2008) Leptolyngbya species from selected seep walls in the Great Smoky Mountains National Park. Algol Stud 126:21–36

    Google Scholar 

  • Kaštovský J (1997) Řasy v Mladečských a Javoříčských jeskyních. Živa 3(97):101–102

    Google Scholar 

  • Kaštovský J, Fučíková K, Hauer T, Bohunická M (2011) Microvegetation on the top of Mt. Roraima, Venezuela. Fottea 11:171–186

    Google Scholar 

  • Keshari N, Adhikary SP (2014) Diversity of cyanobacteria on stone monuments and building facades of India and their phylogenetic analysis. Int Biodeterior Biodegr 90:45–91

    CAS  Google Scholar 

  • Kol E (1966) Algal Vagrowth experiments in the Baradla Cave at Aggletek. Int J Speleol 2:457–474

    Google Scholar 

  • Komárek J (1999) Diversity of cyanoprokaryotes (cyanobacteria) of King George Island, maritime Antarctica—a survey. Algol Stud 94:181–193

    Google Scholar 

  • Komárek J, Elster J (2008) Ecological background of cyanobacterial assemblages of the northern part of James Ross Island, Antarctica. Pol Polar Res 29(1):17–32

    Google Scholar 

  • Komárek O, Komárek J (1999) Diversity of freshwater and terrestrial habitats and their oxyphototroph microflora in the Arctowski Station region, South Shetland Islands. Pol Polar Res 20(3):259–282

    Google Scholar 

  • Komárek J, Montejano G (1994) Taxonomic evaluation of several Chlorogloea-species (Cyanoprokaryota) from inland biotopes. Algol Stud 74:1–26

    Google Scholar 

  • Komárek J, Kováčik L, Elster J, Komárek O (2012) Cyanobacterial diversity of Petuniabukta, Billefjorden, central Spitsbergen. Pol Polar Res 33(4):347–368

    Google Scholar 

  • Komárek J, Kaštovský J, Mareš J, Johansen JR (2014) Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) to the end of 2013 according to polyphasic approach. Preslia (in rev.)

  • Komáromy ZP, Padisák J, Rajczy M (1985) Flora in the lamp-lit areas of the cave „Annabarlang“near Lillafured (Hungary). Ann Hist-Nat Musei Nat Hung 77:103–122

    Google Scholar 

  • Krautová M (2008) Cyanobacteria of wet walls and seeps in Grand Staircase–Escalante National Monument, Utah. M.S. thesis, John Carroll University, Cleveland

  • Krumbein WE (2004) Life on and in stone - an endless story? In: Kwiatkowski D, Löfvendahl R (eds) Proceedings of the 10th International congress on deterioration and conservation of stone, Stockholm. ICOMOS, Stockholm

    Google Scholar 

  • Lakatos M, Bilger W, Büdel B (2001) Carotenoid composition of terrestrial Cyanobacteria: response to natural light conditions in open rock habitats in Venezuela. Eur J Phycol 36:367–375

    Google Scholar 

  • Lamenti G, Tiano P, Tomaselli L (2000) Biodeterioration of ornamental marble statues in the Boboli Gardens (Florence, Italy). J Appl Phycol 12:427–433

    Google Scholar 

  • Lamprinou V, Pantazidou A, Papadogiannaki G, Radea C, Economou-Amili A (2009) Cyanobacteria and associated invertebrates in Leontari cave. Fottea 9:155–164

    Google Scholar 

  • Lamprinou V, Hernández-Mariné M, Canals T, Kormas K, Economou-Amilli A, Pantazidou A (2011) Two new stigonematalean cyanobacteria: Iphinoe spelaeobios gen. nov., sp. nov. and Loriellopsis cavernicola gen. nov., sp. nov. from Greek and Spanish caves. Morphology and Molecular Evaluation. Int J Syst Evol Microbiol 61(12):2907–2915

    CAS  PubMed  Google Scholar 

  • Lamprinou V, Skaraki K, Kotoulas G, Economou-Amilli A, Pantazidou A (2012) Toxopsis calypsus gen. nov., sp. nov (Cyanobacteria, Nostocales) from cave ‘Francthi’, Peloponnese, Greece: a morphological and molecular evaluation. Int J Syst Evol Microbiol 62(12):2870–2877

  • Lamprinou V, Mammali M, Katsifas EA, Pantazidou AI, Karagouni AD (2013a) Phenotypic and molecular biological characterization of cyanobacteria from marble surfaces of treated and untreated sites of Propylaea (Acropolis, Athens). Geomicrobiol J 30:371–378

    CAS  Google Scholar 

  • Lamprinou V, Hernández-Mariné M, Pachiadaki MG, Kormas KA, Economou-Amilli A, Pantazidou A (2013b) New findings on the true–branched monotypic genus Iphinoe (Cyanobacteria) from geographically isolated caves (Greece). Fottea 13(1):15–23

    Google Scholar 

  • Lundberg J, McFarlane DA, Brewer-Carias C (2010) An extraordinary example of photokarren in a sandstone cave, Cueva Charles Brewer, Chimantá Plateau, Venezuela: biogeomorphology on a small scale. Geomorphology 121:342–357

    Google Scholar 

  • Lüttge U (1997) Cyanobacterial tintenstrich communities and their ecology. Naturwissenschlaften 84:526–534

    Google Scholar 

  • Lüttge U, Büdel B, Ball E, Strube F, Weber P (1995) Photosyntesis of terrestrial cyanobacteria under light and dessication stress as expressed by chlorophyll fluorescence and gas-exchange. J Exp Bot 46(284):309–319

    Google Scholar 

  • Macedo MF, Miller AZ, Dionísio A, Saiz-Jimenez C (2009) Biodiversity of cyanobacteria and green algae on monuments in the Mediterranean Basin: an overview. Microbiology 155:3476–3490

    CAS  PubMed  Google Scholar 

  • MacGaughey V (1918) Algae of the Hawaiian archipelago. II. Bot Gaz 65:121–149

    Google Scholar 

  • Mareš J, Lara Y, Dadáková I, Hauer T, Uher B, Wilmotte A, Kaštovský J (in press) Phylogenetic analysis of cultivation-resistant terrestrial cyanobacteria with massive sheaths (Stigonema spp. and Petalonema alatum, Nostocales, Cyanobacteria) using single-cell and filament sequencing of environmental samples. Journal of Phycology, DOI: 10.1111/jpy.12273

  • Martinez A, Asencio AD (2010) Distribution of cyanobacteria at the Gelada Cave (Spain) by physical parameters. J Cave Karst Stud 72(1):11–20

    Google Scholar 

  • Mason-Williams MA (1966) Further investigations into bacterial and algal populations of caves in South Wales. Int J Speleol 2:389–395

    Google Scholar 

  • Mataloni G, Komárek J (2004) Gloeocapsopsis aurea, a new subaerophytic cyanobacterium from maritime Antarctica. Polar Biol 27(10):623–628

    Google Scholar 

  • McNamara CJ, Mitchell R (2005) Microbial deterioration of historic stone. Front Ecol Environ 3(8):445–451

    Google Scholar 

  • Miszalski Z, Büdel B, Lüttge U (1995) Sensitivity of terrestrial Cyanobacteria to light and sulphite stress. Pol J Environ Stud 4(4):55–59

    CAS  Google Scholar 

  • Mühlsteinová R, Hauer T (2013) Pilot survey of cyanobacterial diversity from the neighborhood of San Gerardo de Rivas, Costa Rica with a brief summary of current knowledge of terrestrial cyanobacteria in Central America. Braz J Bot 36:299–307

    Google Scholar 

  • Mulec J, Kosi G (2008) Algae in the aerophytic habitat of Račiše ponikve cave (Slovenia). Nat Sloven 10(1):39–49

    Google Scholar 

  • Mulec J, Kosi G (2009) Lampenflora algae and methods of growth control. J Cave Karst Stud 71(2):109–115

    CAS  Google Scholar 

  • Mulec J, Kosi G, Vrhovšek D (2008) Characterization of cave aerophytic algal communities and effects of irradiance levels on production of pigments. J Cave Karst Stud 70(1):3–12

    CAS  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    CAS  PubMed  Google Scholar 

  • Nabout JC, da Silva Rocha B, Carneiro FM, Sant´Anna CL (2013) How many species of Cyanobacteria are there? Using a discovery curve to predict the species number. Biodivers Conserv 22:2907–2918

    Google Scholar 

  • Neuhof T, Schmieder P, Preussel K, Dieckmann R, Pham H, Bartl F, von Döhren H (2005) Hassallidin A, a glycosylated lipopeptide with antifungal activity from the cyanobacterium Hassallia sp. J Nat Prod 68:695–700

    CAS  PubMed  Google Scholar 

  • Noguerol-Seoane A, Rifón-Lastra AB (1996) Aportación al conocimiento de la ficoflora epilítica en monumentos del noroeste de España: estudio del monasterio de Samos (Lugo). Anales Jard Bot Madrid 54:37–42

    Google Scholar 

  • Noguerol-Seoane A, Rifón-Lastra AB (2000) Estudio de la ficoflora epilíthica de las paredes graníticas exteriors de la iglesia románica de Sta. María de Fisterra (A Coruña, N.O. España). Portigaliae Acta Biol 19:91–96

    Google Scholar 

  • Nováček F (1934) Epilithické sinice serpentinů mohelenských. Pars I.: Chroococcales. In: Podpěra, J. (ed) Mohelno. Svaz pro ochranu přírody a domoviny v zemi Moravskoslezské, Brno

  • Nowicka-Krawczyk P, Żelazna-Wieczorek J, Otlewska A, Koziróg A, Rajkowska K, Piotrowska M, Gutarowska B, Żydzik-Białek A (2014) Diversity of an aerial phototrophic coating of historic buildings in the former Auschwitz II-Birkenau concentration camp. Sci Tot Environ 493:116–123

    CAS  Google Scholar 

  • Olsen CE, Johansen JR, Gomez SR, Lowe RL, Casamatta DA (2003) New records of cyanobacteria from epilithic habitats in the Great Smoky Mountains National Park. J Phycol 39(s1):46

    Google Scholar 

  • Olson R (2006) Control of lamp flora in developed caves. In: Hildreth-Werker V, Werker JC (eds) Cave conservation and restoration. National Speleological Society, Huntsville

    Google Scholar 

  • Ortega-Calvo JJ, Hernández-Mariné M, Sáiz-Jimenez C (1991) Biodeterioration of building materials by cyanobacteria and algae. Int Biodeterior 28(1–4):165–185

    Google Scholar 

  • Ortega-Calvo JJ, Sánchez-Castillo PM, Hernández-Mariné M, Sáiz-Jimenez C (1993) Isolation and characterization of epilithic chlorophytes and cyanobacteria from two Spanish cathedrals (Salamanca and Toledo). Nova Hedwigia 54(1–2):239–253

    Google Scholar 

  • Ortega-Calvo JJ, Ariño X, Hernández-Mariné M, Saiz-Jimenez C (1995) Factors affecting the weathering and colonization of monuments by phototrophic microorganisms. Sci Tot Environ 167:329–341

    CAS  Google Scholar 

  • Ortega-Morales O, Guezennec J, Hernandéz-Duque G, Gaylarde CC, Gaylarde PM (2000) Phototrophic Biofilms on Ancient Mayan Buildings in Yucatan, Mexico. Curr Microbiol 40:81–85

    CAS  PubMed  Google Scholar 

  • Osorio-Santos K, Pietrasiak N, Bohunická M, Miscoe LH, Kováčik Ľ, Martin MP, Johansen JR (2014) Seven new species of Oculatella (Pseudanabaenales, Cyanobacteria): taxonomically recognizing cryptic diversification. Eur J Phycol 49(4):450–470

    Google Scholar 

  • Palik P (1960) Study into the algal flora of caves. Hidrologiai Kozlony 40:417–422

    Google Scholar 

  • Pentecost A (1992) A note on the colonization of limestone rocks by cyanobacteria. Arch Hydrobiol 124(2):167–172

    Google Scholar 

  • Pocs T (2005) Aerophytic Cyanobacteria from the Monti Apuseni (Romanian Western Carpathians, Transylvania), I. The epilithic crusts at the entrance of Huda lui Papara Cave. Kanitzia 13:99–108

    Google Scholar 

  • Potts M (1999) Mechanisms of desiccation tolerance in cyanobacteria (Minireview). Eur J Phycol 34:319–328

    Google Scholar 

  • Ramírez M, Hernández-Mariné M, Novelo E, Roldán M (2010) Cyanobacteria-containing biofilms from a Mayan monument in Palenque, Mexico. Biofouling 24(4):399–409

    Google Scholar 

  • Rascher U, Lakatos M, Büdel B, Lüttge U (2003) Photosynthetic field capacity of cyanobacteria of a tropical inselberg of the Guiana Highlands. Eur J Phycol 38:247–256

    Google Scholar 

  • Ress RJ, Lowe RL (2013) Contrast and comparison of aerial algal communities from two distinct regions in the U.S.A., the Great Smoky Mountains National Park (TN) and the Lake Superior region. Fottea 13(2):165–172

    Google Scholar 

  • Roldán M, Hernández-Mariné M (2009) Exploring the secrets of the three-dimensional architecture of phototrophic biofilms in caves. Int J Speleol 38:41–53

    Google Scholar 

  • Roldán M, Clavero E, Canals T, Gomez-Bolea A, Ariño X, Hernández-Mariné M (2004) Distribution of phototrophic biofilms in cavities (Garraf, Spain). Nova Hedwigia 78(3–4):329–351

    Google Scholar 

  • Saiz-Jimenez C (1997) Biodeterioration vs. biodegradation: the role of microorganisms in the removal of pollutants deposited on historic buildings. Int Biodeterior Biodegr 40(1–2):225–232

    CAS  Google Scholar 

  • Samad LK, Adhikary SP (2008) Diversity of micro-algae and cyanobacteria on building facades and monuments in India. Algae 23(2):91–114

    Google Scholar 

  • Sánchez-Antón F, Asencio Martínez AD (2007) Participation of Cyanophyceae in the biodeterioration of the stones of the Santo Domingo College in Orihuela, Alicante (SE Spain). Algol Stud 124:95–108

    Google Scholar 

  • Sant’Anna C, Branco L, Silva S (1991a) A new species of Gloeothece (Cyanophyceae, Microcystaceae) from São Paulo State, Brazil. Algol Stud 92:1–5

    Google Scholar 

  • Sant’Anna C, Silva S, Branco LHZ (1991b) Cyanophyceae da grutta que chora, municipio Ubatura, Esatdo de Sao Paulo, Brazil. Hoehnea 18:75–97

    Google Scholar 

  • Sant’Anna CL, Kaštovský J, Hentschke GS, Komárek J (2013) Phenotypic studies on terrestrial stigonematacean cyanobacteria from the Atlantic Rainforest, Sao Paulo State, Brazil. Phytotaxa 89:1–23

    Google Scholar 

  • Sarbu SM, Kane TC, Kinkle BK (1996) A chemo-autotrophically based cave ecosystem. Science 272:1953–1955

    CAS  PubMed  Google Scholar 

  • Sarthou C, Therezien Y, Coute A (1995) Cyanophycées de l’inselberg des Nouragues (Guyane française). Nova Hedwigia 61:85–109

    Google Scholar 

  • Satapathy DP, Adhikary SP (1993) Epilithic algae from temple walls and caves at Brubaneswar, Puri and Konark. Phykos 32:17–20

    Google Scholar 

  • Saw JHW, Schatz M, Brown MV, Kunkel DD, Foster JS, Shick H, Christensen S, Hou S, Wan X, Donachie SP (2013) Cultivation and Complete genome sequencing of Gloeobacter kilaueensis sp. nov., from a Lava Cave in Kılauea Caldera, Hawaii. PLoS One 8(10):e76376

    PubMed Central  CAS  PubMed  Google Scholar 

  • Schade A (1923) Die kryptogamischen Pflanzengesellschaften an den Felswänden der Sächsischen Schweiz. Ber German Bot Ges 41:49–59

    Google Scholar 

  • Schmidle W (1900) Algologische notizen. Allgemeine botanische Zeitschrift für Systematik, Floristik, Pflanzengeographie etc. 6:17–18, 33–35, 53–55, 77–79, 233–35

  • Selvi B, Altuner Z (2007) Algae of Ballica Cave (Tokat- Turkey). Int J Nat Eng Sci 1(3):99–103

    Google Scholar 

  • Siebert J, Hirsch P, Hoffmann B, Gliesche CG, Preissl K, Jendrach M (1996) Cryptoendolithic microorganisms from Antarctic sandstone of linnaeus terrace (Asgard range): diversity, properties and interactions. Biodivers Conserv 5(11):1337–1363

    Google Scholar 

  • Skuja H (1970) Alghe cavernicole nelle zone illuminate delle grotte di Castellana (Murge di Bari). La Grotte d’Italia 4:193–202

    Google Scholar 

  • Smith T, Olson R (2007) A taxonomic survey of Lamp flora (algae and cyanobacteria) in electrically lit passages within Mammoth Cave National Park, Kentucky. Int J Speleol 36:105–114

    Google Scholar 

  • Smith T, Piccin T (2004) Algal taxonomic survey of Zion National Park and Cedar Breaks National Monument, Utah, and Pipe Spring National Monument, Arizona. Soutwes Nat 49(3):395–417

    Google Scholar 

  • Souza-Egipsy V, Wierzchos J, Sancho C, Belmonte A, Ascaso C (2004) Role of biological soil crust cover in bioweathering and protection of sandstone in semi-arid landscape (Torrollones de Gabarda, Huesca, Spain). Earth Surf Pro Land 29(13):1651–1661

    CAS  Google Scholar 

  • Šramková K, Kováčik Ľ (2005) Výskyt cyanobactérií a rias v nárostoch “lampenflory” v šiestich sprístupnených jaskyniach na Slovensku. Bull Slovenskej Bot Spol (Bratislava) 27:17–21

    Google Scholar 

  • Strunecký O, Elster J, Komárek J (2011) Taxonomic revision of the freshwater cyanobacterium „Phormidium“murrayi = Wilmottia murrayi. Fottea 11(1):57–71

    Google Scholar 

  • Tian Y, Chen J, Zhang J, Li S, Bao H (2001) New taxa of Chroococcaceae from Yunnan, China. Acta Phytotaxon Sin 39:280–282

    Google Scholar 

  • Tian Y, Zhang J, Song L, Bao H (2002) A Study on aerial cyanophyta (cyanobacteria) on the surface of carbonate rock in Yunnan Stone Forest, Yunnan Province, China. Acta Oecol Sin 22:1793–1802

    Google Scholar 

  • Tian YP, Zhang J, Song LH, Bao HS (2004) The role of aerial algae in the formation of the landscape of the Yunnan Stone Forest, Yunnan Province, China. Sci China Ser D 47:846–864

    Google Scholar 

  • Uher B, Aboal M, Kováčik Ľ (2005) Epilithic and chasmoendolithic phycoflora of monuments and buildings in South-Eastern Spain. Cryptogam Algol 26(3):275–358

    Google Scholar 

  • Uzunov BA, Stoyneva MP, Gartner G (2008) Review of the studies on aero-terrestrial cyanoprokaryotes and algae in Bulgaria with a checklist oft he recorded species. II. Phytol Balc 14(1):11–18

    Google Scholar 

  • Vaccarino MA, Johansen JR (2011) Scytonematopsis contorta sp. nov. (Nostocales), a new species from the Hawaiian Islands. Fottea 11:149–161

    Google Scholar 

  • Videla HA, Guiamet PS, Gomez de Saravia S (2000) Biodeterioration of Mayan archaeological sites in the Yucatan Peninsula, Mexico. Int Biodeterior Biodegr 46:335–341

    CAS  Google Scholar 

  • Vinogradova ON, Mikhailyuk TI (2009) Algal flora of caves and grottoes in the national nature park, “Podilsky Tovtry” (Ukraine). Algologia 19(2):155–171

    Google Scholar 

  • Warscheid T, Braams J (2000) Biodeterioration of stone: a review. Int Biodeterior Biodegr 46:343–368

    CAS  Google Scholar 

  • Watanabe M, Komárek J (1988) Blue-green algae from Kathmandu. In: Watanabe M, Malla SB, Malla SB (eds) Cryptogames of the Himalaya, Vol. 1, The Kathmandu valley, vol 1. National Science Museum, Tsukuba

    Google Scholar 

  • Watanabe A, Komárek J (1994) Several cyanoprokaryotes from Sagarmatha National Park, Nepal Himalayas. Bull Nat Sci Museum, Tokyo, Ser B (Botany) 20:1–31

    Google Scholar 

  • Watanabe MM, Watanabe M, Yamagishi T (1979) Freshwater algae of Papua New Guinea (3) blue–green algae from Mt. Wilhelm. In: Kurokawa S (ed) Studies on cryptogams of Papua New Guinea. Academia Scientific Book, Tokyo

    Google Scholar 

  • Weber-van Bosse A (1913) Liste de algues du Siboga. I. Myxophyceae, Chlorophyceae, Phaeophyceae avec le concours de M. Th. Reinbold. Siboga-Expeditie 59:1–186

  • Welton RG, Cuthbert SJ, McLean R, Hursthouse A, Hughes J (2003) A preliminary study of the phycological degradation of natural stone masonry. Environ Geochem Health 25:139–145

    CAS  PubMed  Google Scholar 

  • Welwitsch F (1868) The Pedras Negras of Pundo Andongo in Angola. J Travel Nat Hist 1:22–36

    Google Scholar 

  • West W, West GS (1894) On some freshwater algae from the West Indies. Bot J Linn Soc 30:264–280

    Google Scholar 

  • West W, West GS (1897) Welwitsch’s African freshwater algae. J Bot 35:264–272

    Google Scholar 

  • West W, West GS (1899) A further contribution to the freshwater alfae of the West Indies. Bot J Linn Soc 34:279–295

    Google Scholar 

  • West W, West GS (1902) A contribution to the freshwater algae of Ceylon. Trans Linn Soc Lond. 2nd Ser 6:123–215

    Google Scholar 

  • Whitton BA (ed) (2012) Ecology of cyanobacteria II. Their diversity in space and time. Springer, Dordrecht

    Google Scholar 

  • Wille N (1915) Süsswasseralgen von den Samoainseln, Hawaii, den Salomonsinseln und Ceylon : gesammelt von Dr. Krechinger. Denkschriften der Kaiserlichen Akademie der Wissenschaften/Mathematisch-Naturwissenschaftliche Classe. 91:141–62

  • Zammit G, Kaštovský J, Albertano P (2010) A first cytomorphological and molecular characterisation of a new Stigonematalean cyanobacterial morphotype isolated from Maltese catacombs. Algol Stud 135:1–14

    CAS  Google Scholar 

  • Zammit G, Billi D, Shubert E, Kaštovský J, Albertano P (2011) The biodiversity of subaerophytic biofilms from Maltese hypogea. Fottea 11(1):187–201

    Google Scholar 

  • Zehnder A (1953) Beitrag zur Kenntnis von Mikroklima und Algenvegetation des nackten Gesteins in den Tropen. Ber Schweiz Bot Ges 63:5–26

    Google Scholar 

Download references

Acknowledgments

This research was supported by a long-term research development Project No. RVO 67985939 of the Institute of Botany CAS, and by the Grant GA CR 15-11912S. Keith Edwards corrected the language. Authors are grateful to all reviewers for their valuable comments leading to improvement of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tomáš Hauer.

Additional information

Communicated by Anurag chaurasia.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 269 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hauer, T., Mühlsteinová, R., Bohunická, M. et al. Diversity of cyanobacteria on rock surfaces. Biodivers Conserv 24, 759–779 (2015). https://doi.org/10.1007/s10531-015-0890-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-015-0890-z

Keywords

Navigation