Abstract
Lithobionts (rock-dwelling organisms) have been recognized as agents of aesthetic and physico-chemical deterioration of stonework. In consequence, their removal from cultural heritage stone surfaces (CHSS) is widely considered a necessary step in conservation interventions. On the other hand, lithobiontic communities, including microbial biofilms (‘biological patinas’), can help integrate CHSS with their environmental setting and enhance biodiversity. Moreover, in some cases bioprotective effects have been reported and even interpreted as potential biotechnological solutions for conservation. This paper reviews the plethora of traditional and innovative methodologies to characterize lithobionts on CHSS in terms of biodiversity, interaction with the stone substrate and impacts on durability. In order to develop the best management and conservation strategies for CHSS, such diagnosis should be acquired on a case-by-case basis, as generalized approaches are unlikely to be suitable for all lithobionts, lithologies, environmental and cultural contexts or types of stonework. Strategies to control biodeteriogenic lithobionts on CHSS should similarly be based on experimental evaluation of their efficacy, including long-term monitoring of the effects on bioreceptivity, and of their environmental safety. This review examines what is known about the efficacy of control methods based on traditional-commercial biocides, as well as those based on innovative application of substances of plant and microbial origin, and physical techniques. A framework for providing a balanced scientific assessment of the role of lithobionts on CHSS and integrating this knowledge into management and conservation decision-making is presented.
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Adamo P, Violante P (2000) Weathering of rocks and neogenesis of minerals associated with lichen activity. Appl Clay Sci 16:229–256
Albertano P (2012) Cyanobacterial biofilms in monuments and caves. In: Whitton BA (ed) Ecology of cyanobacteria II. Springer, Dordrecht, pp 317–343
Albertano P, Bruno L (2003) The importance of light in the conservation of hypogean monuments. In: Saiz-Jimenez C (ed) Molecular Biology and Cultural Heritage. Balkema, Lisse, pp 171–177
Ascaso C, Galván J, Rodríguez-Pascual C (1976) Studies on the pedogenetic action of lichen acids. Pedobiologia 16:321–331
Banfield JF, Barker WW, Welch SA, Taunton A (1999) Biological impact on mineral dissolution: application of the lichen model to understanding mineral weathering in the rhizosphere. Proc Natl Acad Sci USA 96:3404–3411
Barriuso BC, Botticelli G, Cuzman OA, Osticioli I, Tiano P, Matteini M (2017) Conservation of calcareous stone monuments: Screening different diammonium phosphate based formulations for countering phototrophic colonization. J Cult Herit 27:97–106
Bartoli F, Casanova-Municchia A, Futagami Y, Kashiwadani H, Moon KH, Caneva G (2014) Biological colonization patterns on the ruins of Angkor temples (Cambodia) in the biodeterioration vs bioprotection debate. Int Biodeterior Biodegrad 96:157–165
Bartoli F, Romiti F, Caneva G (2017) Aggressiveness of Hedera helix L. growing on monuments: evaluation in Roman archaeological sites and guidelines for a general methodological approach. Plant Biosyst 151:866–877
Bell FG (1993) Durability of carbonate rock as building stone with comments on its preservation. Environ Geol 21:187–200
Bellezza S, Albertano P, de Philippis R, Paradossi G (2006) Exopolysaccharides of two cyanobacterial strains from Roman hypogea. Geomicrobiol J 23:301–310
Bertuzzi S, Candotto Carniel F, Pipan G, Tretiach M (2013) Devitalization of poikilohydric lithobionts of open-air monuments by heat shock treatments: a new case study centred on bryophytes. Int Biodeterior Biodegrad 84:44–53
Bertuzzi S, Gustavs L, Pandolfini G, Tretiach M (2017) Heat shock treatments for the control of lithobionts: a case study with epilithic green microalgae. Int Biodeterior Biodegrad 123:236–243
Bjelland T, Grube M, Hoem S, Jorgensen SL, Daae FL, Thorseth IH, Øvreås L (2011) Microbial metacommunities in the lichen–rock habitat. Environ Microbiol Rep 3:434–442
BLS (British Lichen Society) (2020). Churchyard lichen conservation. https://www.britishlichensociety.org.uk/activities/churchyard-survey/churchyard-lichen-conservation. Accessed 02 April 2020
Bolívar FC, Sánchez-Castillo PM (1997) Biomineralization processes in the fountains of the Alhambra, Granada, Spain. Int Biodeterior Biodegrad 40:205–215
Breitenbach R, Silbernagl D, Toepel J, Sturm H, Broughton WJ, Sassaki GL, Gorbushina AA (2018) Corrosive extracellular polysaccharides of the rock-inhabiting model fungus Knufia petricola. Extremophiles 22:165–175
Brimblecombe P, Grossi CM (2005) Aesthetic thresholds and blackening of stone buildings. Sci Total Environ 349:175–189
Bruno L, Rugnini L, Spizzichino V, Caneve L, Canini A, Ellwood NTW (2019) Biodeterioration of Roman hypogea: the case study of the Catacombs of SS. Marcellino and Pietro (Rome, Italy). Ann Microbiol 69:1023–1032
Bungartz F, Garvie LA (2004) Anatomy of the endolithic Sonoran Desert lichen Verrucaria rubrocincta Breuss: implications for biodeterioration and biomineralization. Lichenol 36:55–73
Cámara B, de los Ríos A, Urizal M, De Buergo MA, Varas MJ, Fort R, Ascaso C (2011) Characterizing the microbial colonization of a dolostone quarry: implications for stone biodeterioration and response to biocide treatments. Microb Ecol 62:299–313
Caneva G (1993) Ecological approach to the genesis of calcium oxalate patinas on stone monuments. Aerobiol 9:149–156
Caneva G, Nugari MP, Salvadori O (2008) Plant biology for cultural heritage: biodeterioration and conservation. Getty Conservation Institute, Los Angeles
Caneva G, Galotta G, Cancellieri L, Savo V (2009) Tree roots and damages in the Jewish catacombs of Villa Torlonia (Roma). J Cult Herit 10:53–62
Caneva G, Bartoli F, Savo V, Futagami Y, Strona G (2016) Combining statistical tools and ecological assessments in the study of biodeterioration patterns of stone temples in Angkor (Cambodia). Sci Rep 6:32601
Cappitelli F, Principi P, Pedrazzani R, Toniolo L, Sorlini C (2007) Bacterial and fungal deterioration of the Milan Cathedral marble treated with protective synthetic resins. Sci Total Environ 385:172–181
Cappitelli F, Abbruscato P, Foladori P, Zanardini E, Ranalli G, Principi P, Villa F, Polo A, Sorlini C (2009) Detection and elimination of cyanobacteria from frescoes: the case of the St. Brizio Chapel (Orvieto Cathedral, Italy). Microb Ecol 57:633–639
Carter NEA, Viles HA (2004) Lichen hotspots: raised rock temperatures beneath Verrucaria nigrescens on limestone. Geomorphol 62:1–16
Carter NEA, Viles HA (2005) Bioprotection explored: the story of a little known earth surface process. Geomorphol 67:273–281
Casanova Municchia A, Percario Z, Caneva G (2014) Detection of endolithic spatial distribution in marble stone. J Microsc 256:37–45
Casanova-Municchia A, Bartoli F, Taniguchi Y, Giordani P, Caneva G (2018) Evaluation of the biodeterioration activity of lichens in the Cave Church of Üzümlü (Cappadocia, Turkey). Int Biodeterior Biodegrad 127:160–169
Charter M, Tischner U (2017) Sustainable solutions: developing products and services for the future. Routledge, London
Chen J, Blume HP, Beyer L (2000) Weathering of rocks induced by lichen colonization—a review. Catena 39:121–146
Cicinelli E, Salerno G, Caneva G (2018) An assessment methodology to combine the preservation of biodiversity and cultural heritage: the San Vincenzo al Volturno historical site (Molise, Italy). Biodivers Conserv 27:1073–1093
Cicinelli E, Benelli F, Bartoli F, Traversetti L, Caneva G (2020) Trends of plant communities growing on the Etruscan tombs (Cerveteri, Italy) related to different management practices. Plant Biosyst 154:158–164
Convention Concerning the Protection of the World Cultural and Natural Heritage, 1972. https://whc.unesco.org/en/conventiontext/. Accessed 02 April 2020
Coombes MA, Viles HA, Zhang H (2018) Thermal blanketing by ivy (Hedera helix L.) can protect building stone from damaging frosts. Sci Rep 8:9834
Costantini I, Castro K, Madariaga JM (2018) Portable and laboratory analytical instruments for the study of materials, techniques and environmental impacts in mediaeval mural paintings. Anal Methods 10:4854–4870
Crispim CA, Gaylarde CC (2005) Cyanobacteria and biodeterioration of cultural heritage: a review. Microb Ecol 49:1–9
Cuadros J (2017) Clay minerals interaction with microorganisms: a review. Clay Min 52:235–262
Davidson TM, Altieri AH, Ruiz GM, Torchin ME (2018) Bioerosion in a changing world: a conceptual framework. Ecol Lett 21:422–438
De Leo F, Antonelli F, Pietrini AM, Ricci S, Urzì C (2019) Study of the euendolithic activity of black meristematic fungi isolated from a marble statue in the Quirinale Palace’s Gardens in Rome. Italy Facies 65:18
de los Rios A, Ascaso C (2005) Contributions of in situ microscopy to the current understanding of stone biodeterioration. Int Microbiol 8:181–188
de los Rios A, Pérez-Ortega S, Wierzchos J, Ascaso C (2012) Differential effects of biocide treatments on saxicolous communities: case study of the Segovia cathedral cloister (Spain). Int Biodeterior Biodegrad 67:64–72
Dorn R (2013) Rock coatings. In: Shroder JF (ed) Treatise on geomorphology. Academic Press, San Diego, pp 70–97
Edwards HG, Seaward MR, Attwood SJ, Little SJ, de Oliveira LF, Tretiach M (2003) FT-Raman spectroscopy of lichens on dolomitic rocks: an assessment of metal oxalate formation. Analyst 128:1218–1221
Eriksson O (2018) What is biological cultural heritage and why should we care about it? An example from Swedish rural landscapes and forests. Nat Conserv 28:1–32
Fatorić S, Seekamp E (2017) Are cultural heritage and resources threatened by climate change? A systematic literature review. Clim Chang 142:227–254
Favero-Longo SE, Castelli D, Salvadori O, Belluso E, Piervittori R (2005) Pedogenetic action of the lichens Lecidea atrobrunnea, Rhizocarpon geographicum gr. and Sporastatia testudinea on serpentinized ultramafic rocks in an alpine environment. Int Biodeterior Biodegrad 56:17–27
Favero-Longo SE, Borghi A, Tretiach M, Piervittori R (2009) In vitro receptivity of carbonate rocks to endolithic lichen-forming aposymbionts. Mycol Res 113:1216–1227
Favero-Longo SE, Gazzano C, Girlanda M, Castelli D, Tretiach M, Baiocchi C, Piervittori R (2011) Physical and chemical deterioration of silicate and carbonate rocks by meristematic microcolonial fungi and endolithic lichens (Chaetothyriomycetidae). Geomicrobiol J 28:732–744
Favero-Longo SE, Accattino E, Matteucci E, Borghi A, Piervittori R (2015) Weakening of gneiss surfaces colonized by endolithic lichens in the temperate climate area of northwest Italy. Earth Surf Process and Landf 40:2000–2012
Favero-Longo SE, Benesperi R, Bertuzzi S, Bianchi E, Buffa G, Giordani P, Loppi S, Malaspina P, Matteucci E, Paoli L, Ravera S, Roccardi A, Segimiro A, Vannini A (2017) Species-and site-specific efficacy of commercial biocides and application solvents against lichens. Int Biodeterior Biodegrad 123:127–137
Favero-Longo SE, Brigadeci F, Segimiro A, Voyron S, Cardinali M, Girlanda M, Piervittori R (2018) Biocide efficacy and consolidant effect on the mycoflora of historical stuccos in indoor environment. J Cult Herit 34:33–42
Favero-Longo SE, Turci F, Fubini B, Castelli D, Piervittori R (2013) Lichen deterioration of asbestos and asbestiform minerals of serpentinite rocks in Western Alps. Int Biodeterior Biodegrad 84:342–350
Favero-Longo SE, Matteucci E, Ruggiero MG (2019) Caratterizzazione di licheni e patine microbiologiche sulle rocce istoriate del Parco Nazionale delle Incisioni Rupestri di Naquane (Valle Camonica) e metodiche per il loro controllo. Not Soc Lichenol Ital 32:31
Fernandes P (2006) Applied microbiology and biotechnology in the conservation of stone cultural heritage materials. Appl Microbiol Biotechnol 73:291–296
Ferretti V, Comino E (2015) An integrated framework to assess complex cultural and natural heritage systems with multi-attribute value theory. J Cult Herit 16:688–697
Fidanza MR, Caneva G (2019) Natural biocides for the conservation of stone cultural heritage: a review. J Cult Herit 38:271–286
Fitzsimons A, Morrissey S, Woods J (2012) Between East and West. In: De Angelis I (ed) The Japanese effect in contemporary Irish poetry. Springer, Berlin, pp 138–158
Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the “house of biofilm cells”. J of Bacteriol 189:7945–7947
Flemming HC, Neu TR, Wingender J (2017) The perfect slime: microbial extracellular polymeric substances (EPS). IWA publishing, London
Fomina M, Burford EP, Hillier S, Kierans M, Gadd GM (2010) Rock-building fungi. Geomicrobiol J 27:624–629
Fonseca AJ, Pina F, Macedo MF, Leal N, Romanowska-Deskins A, Laiz L, Gómez-Bolea A, Saiz-Jimenez C (2010) Anatase as an alternative application for preventing biodeterioration of mortars: evaluation and comparison with other biocides. Int Biodeterior Biodegrad 64:388–396
Fry EJ (1924) A suggested explanation of the mechanical action of lithophytic lichens on rocks (shale). Ann Bot 38:175–196
Fry EJ (1927) The mechanical action of crustaceous lichens on substrata of shale, schist, gneiss, limestone, and obsidian. Ann Bot 41:437–460
Garcia-Vallès M, Topal T, Vendrell-Saz M (2003) Lichenic growth as a factor in the physical deterioration or protection of Cappadocian monuments. Environ Geol 43:776–781
Gadd GM, Bahri-Esfahani J, Li Q, Rhee YJ, Wei Z, Fomina M, Liang X (2014) Oxalate production by fungi: significance in geomycology, biodeterioration and bioremediation. Fungal Biol Rev 28:36–55
Gadd GM, Dyer TD (2017) Bioprotection of the built environment and cultural heritage. Microb Biotechnol 10:1152–1156
Gadd GM (2017) Fungi, rocks, and minerals. Elements 13:171–176
Garty J (1990) Influence of epilithic microorganisms on the surface temperature of building walls. Can J Bot 68:1349–1353
Garvie LA, Knauth LP, Bungartz F, Klonowski S, Nash TH (2008) Life in extreme environments: survival strategy of the endolithic desert lichen Verrucaria rubrocincta. Naturwissenschaften 95:705–712
Gazzano C, Favero-Longo SE, Matteucci E, Piervittori R. (2011). Index of Lichen Potential Biodeteriogenic Activity: towards a statistical validation and the extension to other biodeteriogens. In: Book of abstract of the XV International Biodeterioration & Biodegradation Symposium (IBBS-15), 20–23 Vienna (Austria), p. 104
Gazzano C, Favero-Longo SE, Matteucci E, Roccardi A, Piervittori R (2009) Index of Lichen Potential Biodeteriogenic Activity (LPBA): a tentative tool to evaluate the lichen impact on stonework. Int Biodeterior Biodegrad 63:836–843
Golubic S, Friedmann EI, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sedim Res 51:475–478
Golubic S, Schneider J (2001) Microbial endoliths as internal biofilms. In: Krumbein WE, Paterson DM, Zavarzin GA (eds) Fossil and recent biofilms. Springer, Dordrecht, pp 249–263
Gómez-Bolea A, Llop E, Ariño X, Saiz-Jimenez C, Bonazza A, Messina P, Sabbioni C (2012) Mapping the impact of climate change on biomass accumulation on stone. J Cult Herit 13:254–258
Gorbushina A (2003) Microcolonial fungi: survival potential of terrestrial vegetative structures. Astrobiology 3:543–554
Gorbushina AA, Broughton WJ (2009) Microbiology of the atmosphere-rock interface: how biological interactions and physical stresses modulate a sophisticated microbial ecosystem. Ann Rev Microbiol 63:431–450
Grottoli A, Beccaccioli M, Zoppis E, Fratini RS, Schifano E, Santarelli ML, Uccelletti D, Reverberi M (2020) Nanopore sequencing and bioinformatics for rapidly identifying cultural heritage spoilage microorganisms. Front Mater 7:14
Grove R, Evans Pim J, Serrano M, Cidrás D, Viles H, Sanmartín P (2020) Pastoral stone enclosures as biological cultural heritage: Galician and Cornish examples of community conservation. Land 9:9
Guglielmin M, Favero-Longo SE, Cannone N, Piervittori R, Strini A (2011) Role of lichens in granite weathering in cold and arid environments of continental Antarctica. Geol Soc Spec Publ 354:195–204
Guillitte O (1995) Bioreceptivity: a new concept for building ecology studies. Sci Total Environ 167:215–220
Gümbel CW (1856) Mittheilungen über die neue Färberflechte Lecanora ventosa Ach., nebst Beitrag zur Entwicklungsgeschichte der Flechten. Denkschriften der Mathematisch-Naturwissenschaftlichen Classe der Kaiserlichen Akademie der Wissenschaften Besonders Abgedruckt 11. Kaiserlich-Königijchen Hof- und Staatsdruckhrei, Wien
Haas JR, Purvis OW (2006) Lichen biogeochemistry. In: Gadd GM (ed) Fungi in biogeochemical cycles. Cambridge University Press, Cambridge, pp 344–376
Hueck HJ (1965) The biodeterioration of materials as a part of hylobiology. Materi und Org 1:5–34
Huyssen A (2006) Nostalgia for ruins Grey Room 23:6–21
Italian Ministry for Cultural Heritage and Activities. (2004). Legislative Decree no. 42 of 22 January 2004 - Code of the Cultural and Landscape Heritage, pursuant to article 10 of law no. 137 of 6 July 2002. https://whc.unesco.org/document/155711. Accessed 3 April 2020
Kakakhel MA, Wu F, Gu JD, Feng H, Shah K, Wang W (2019) Controlling biodeterioration of cultural heritage objects with biocides: A review. Int Biodeterior Biodegrad 143:104721
Kampf G (2018) Adaptive microbial response to low-level benzalkonium chloride exposure. J of Hosp Infect 100:e1–e22
Kim M, Weigand MR, Oh S, Hatt JK, Krishnan R, Tezel U, Pavlostathis SG, Konstantinidis KT (2018) Widely used benzalkonium chloride disinfectants can promote antibiotic resistance. Appl Environ Microbiol 84:e01201–e1218
Krumbein WE (1968) Zur Frage der biologischen Verwitterung: Einfluß der Mikroflora auf die Bausteinverwitterung und ihre Abhängigkeit von edaphischen Faktoren. Z allg Mikrobiol 8:107–117
Lee MR, Parsons I (1999) Biomechanical and biochemical weathering of lichen-encrusted granite: textural controls on organic–mineral interactions and deposition of silica-rich layers. Chem Geol 161:385–397
Löki V, Deák B, Lukács AB, Molnár VA. (2019). Biodiversity potential of burial places–a review on the flora and fauna of cemeteries and churchyards. Glob Ecol Conserv, e00614
Maguregui M, Knuutinen U, Trebolazabala J, Morillas H, Castro K, Martinez-Arkarazo I, Madariaga JM (2012) Use of in situ and confocal Raman spectroscopy to study the nature and distribution of carotenoids in brown patinas from a deteriorated wall painting in Marcus Lucretius House (Pompeii). Anal Bioanal Chem 402:1529–1539
Mandrioli P, Caneva G, Sabbioni C (2003) Cultural heritage and aerobiology. Methods and measurement techniques for biodeterioration monitoring. Kluwer Academic Publishers, Dordrecht
Mapelli F, Marasco R, Balloi A, Rolli E, Cappitelli F, Daffonchio D, Borin S (2012) Mineral–microbe interactions: biotechnological potential of bioweathering. J Biotechnol 157:473–481
Marques J, Gonçalves J, Oliveira C, Favero-Longo SE, Paz-Bermúdez G, Almeida R, Prieto B (2016) On the dual nature of lichen-induced rock surface weathering in contrasting micro-environments. Ecol 97:2844–2857
Marvasi M, Cavalieri D, Mastromei G, Casaccia A, Perito B (2019) Omics technologies for an in-depth investigation of biodeterioration of cultural heritage. Int Biodeterior Biodegrad 144:104736
Matteucci E, Scarcella AV, Croveri P, Marengo A, Borghi A, Benelli C, Hamdan O, Favero-Longo SE (2019) Lichens and other lithobionts on the carbonate rock surfaces of the heritage site of the tomb of Lazarus (Palestinian territories): diversity, biodeterioration, and control issues in a semi-arid environment. Ann Microbiol 69:1033–1046
McCarroll D, Viles H (1995) Rock-weathering by the lichen Lecidea auriculata in an arctic alpine environment. Earth Surf Process Landf 20:199–206
McIlroy de la Rosa JP, Warke PA, Smith BJ (2012) Lichen-induced biomodification of calcareous surfaces: bioprotection versus biodeterioration. Prog Phys Geogr 37:325–351
McIlroy de la Rosa JP, Warke PA, Smith BJ (2014) The effects of lichen cover upon the rate of solutional weathering of limestone. Geomorphol 220:81–92
Miller AZ, Sanmartín P, Pereira-Pardo L, Dionísio A, Sáiz-Jiménez C, Macedo MF, Prieto B (2012) Bioreceptivity of building stones: a review. Sci Total Environ 426:1–12
Molina E, Cultrone G, Sebastian E, Alonso FJ (2013) Evaluation of stone durability using a combination of ultrasound, mechanical and accelerated aging tests. J Geophys Eng 10:035003
Morando M, Wilhelm K, Matteucci E, Martire L, Piervittori R, Viles HA, Favero-Longo SE (2017) The influence of structural organization of epilithic and endolithic lichens on limestone weathering. Earth Surf Process Landf 42:1666–1679
Mottershead D, Lucas G (2000) The role of lichens in inhibiting erosion of a soluble rock. Lichenol 32:601–609
Nascimbene J, Salvadori O, Nimis PL (2009) Monitoring lichen recolonization on a restored calcareous statue. Sci Total Environ 407:2420–2426
Negi A, Sarethy IP (2019) Microbial biodeterioration of cultural heritage: events, colonization, and analyses. Microb Ecol 78:1014–1029
Nimis PL, Monte M, Tretiach M (1987) Flora e vegetazione lichenica di aree archeologiche del Lazio. Studia Geobotanica 7:3–161
Nimis PL, Pinna D, Salvadori O (1992) Licheni e Conservazione dei Monumenti. Cooperativa Libraria Universitaria Editrice, Bologna
Ortega-Morales O, Guezennec J, Hernandez-Duque G, Gaylarde CC, Gaylarde PM (2000) Phototrophic biofilms on ancient Mayan buildings in Yucatan, Mexico. Curr Microbiol 40:81–85
Özvan A, Dinçer İ, Akın M, Oyan V, Tapan M (2015) Experimental studies on ignimbrite and the effect of lichens and capillarity on the deterioration of Seljuk Gravestones. Eng Geol 185:81–95
Parchert KJ, Spilde MN, Porras-Alfaro A, Nyberg AM, Northup DE (2012) Fungal communities associated with rock varnish in Black Canyon, New Mexico: casual inhabitants or essential partners? Geomicrobiol J 29:752–766
Pawlik Ł, Phillips JD, Šamonil P (2016) Roots, rock, and regolith: Biomechanical and biochemical weathering by trees and its impact on hillslopes—a critical literature review. Earth Sci Rev 159:142–159
Pena-Poza J, Ascaso C, Sanz M, Pérez-Ortega S, Oujja M, Wierzchos J, Souza-Egipsy V, Cañamares MV, Urizal M, Castillejo M, García-Heras M (2018) Effect of biological colonization on ceramic roofing tiles by lichens and a combined laser and biocide procedure for its removal. Int Biodeterior Biodegrad 126:86–94
Piervittori R, Favero-Longo SE, Gazzano C (2009) Lichens and biodeterioration of stonework: a review. Chimica oggi-Chem Today 27:8–11
Piñar G, Sterflinger K. (2018). Two decades using molecular techniques to study biodeterioration of cultural heritage: An amazing biotechnological development. In: Mosquera MJ, Almoraima Gil ML (eds) Conserving Cultural Heritage: Proceedings of the 3rd International Congress on Science and Technology for the Conservation of Cultural Heritage (TechnoHeritage 2017), May 21–24, 2017, Cadiz, Spain. CRC Press, Boca Raton, pp. 299–302
Pinheiro AC, Mesquita N, Trovão J, Soares F, Tiago I, Coelho C, Paiva de Carvalho H, Gil F, Catarino L, Piñar G, Portugal A (2019) Limestone biodeterioration: a review on the Portuguese cultural heritage scenario. J Cult Herit 36:275–285
Pinna D (2014) Biofilms and lichens on stone monuments: Do they damage or protect? Front Microbiol 5:1–3
Pinna D (2017) Coping with biological growth on stone heritage objects: methods, products, applications, and perspectives. Apple Academic Press, Oakville
Pinna D, Galeotti M, Perito B, Daly G, Salvadori B (2018) In situ long-term monitoring of recolonization by fungi and lichens after innovative and traditional conservative treatments of archaeological stones in Fiesole (Italy). Int Biodeterior Biodegrad 132:49–58
Pinna D, Salvadori O, Tretiach M (1998) An anatomical investigation of calcicolous endolithic lichens from the Trieste karst (NE Italy). Plant Biosyst 132:183–195
Pokharel R, Gerrits R, Schuessler JA, Floor GH, Gorbushina AA, von Blanckenburg F (2017) Mg isotope fractionation during uptake by a rock-inhabiting, model microcolonial fungus Knufia petricola at acidic and neutral pH. Environ Sci Technol 51:9691–9699
Poursat BA, van Spanning RJ, de Voogt P, Parsons JR (2019) Implications of microbial adaptation for the assessment of environmental persistence of chemicals. Crit Rev Environ Sci Technol 49:2220–2255
Pozo-Antonio JS, Barreiro P, González P, Paz-Bermúdez G (2019) Nd: YAG and Er: YAG laser cleaning to remove Circinaria hoffmanniana (Lichenes, Ascomycota) from schist located in the Côa Valley Archaeological Park. Int Biodeterior Biodegrad 144:104748
Prieto B, Aira N, Silva B (2007) Comparative study of dark patinas on granitic outcrops and buildings. Sci Total Environ 381:280–289
Prieto B, Vázquez-Nion D, Fuentes E, Durán-Román AG (2020) Response of subaerial biofilms growing on stone-built cultural heritage to changing water regime and CO2 conditions. Int Biodeterior Biodegrad 148:104882
Rampazzi L (2019) Calcium oxalate films on works of art: a review. J Cult Herit 40:195–214
Ricci S, Altieri A. (2008). Il ruolo delle briofite nel deterioramento dei Beni Culturali. In: Aleffi M (ed) Biologia ed ecologia delle Briofite. Antonio Delfino, Roma, pp. 417–434
Riminesi C, Olmi R (2016) Localized microwave heating for controlling biodeteriogens on cultural heritage assets. Int J Conserv Sci 7(1):281–294
Rivas T, Pozo-Antonio JS, de Silanes ML, Ramil A, López AJ (2018) Laser versus scalpel cleaning of crustose lichens on granite. Appl Surf Sci 440:467–476
Saiz-Jimenez C, Garcia Rowe J, Rodriguez Hidalgo JM (1991) Biodeterioration of polychrome Roman mosaics. Int Biodeterior Biodegrad 28:65–79
Salvadori O, Charola AE. (2011). Methods to prevent biocolonization and recolonization: an overview of current research for architectural and archaeological heritage. In: Charola AE, McNamara C, Koestler RJ (eds) Biocolonization of stone: Control and preventive methods. Proceedings from the MCI Workshop Series. Smithsonian Contributions to Museum Conservation (Vol 2). Smithsonian Inst. Press, Washington, pp. 37–50
Salvadori O, Casanova-Municchia A. (2016). The role of fungi and lichens in the biodeterioration of stone monuments. Open Conf Proc J, 7 (suppl. 1: M4), 39–54
Sanmartín P, DeAraujo A, Vasanthakumar A (2018) Melding the old with the new: trends in methods used to identify, monitor, and control microorganisms on cultural heritage materials. Microb Ecol 76:64–80
Sanmartín P, Rodríguez A, Aguiar U (2020a) Medium-term field evaluation of several widely used cleaning-restoration techniques applied to algal biofilm formed on a granite-built historical monument. Int Biodeterior Biodegrad 147:104870
Sanmartín P, Vázquez-Nion D, Arines J, Cabo-Domínguez L, Prieto B (2017) Controlling growth and colour of phototrophs by using simple and inexpensive coloured lighting: a preliminary study in the Light4Heritage project towards future strategies for outdoor illumination. Int Biodeterior Biodegrad 122:107–115
Sanmartín P, Villa F, Cappitelli F, Balboa S, Carballeira R (2020b) Characterization of a biofilm and the pattern outlined by its growth on a granite-built cloister in the Monastery of San Martiño Pinario (Santiago de Compostela, NW Spain). Int Biodeter Biodegrad 147:104871
Sanz M, Oujja M, Ascaso C, Pérez-Ortega S, Souza-Egipsy V, Fort R, de los Rίos A, Wierzchos J, Cañamares MV, Castillejo M (2017) Influence of wavelength on the laser removal of lichens colonizing heritage stone. Appl Surf Sci 399:758–768
Sazanova KV, Vlasov DY, Osmolovskay NG, Schiparev SM, Rusakov AV (2016) Significance and regulation of acids production by rock-inhabited fungi. In: Frank-Kamenetskaya OV, Panova EG, Vlasov DY (eds) Biogenic - abiogenic interactions in natural and anthropogenic systems. Springer, Cham, pp 379–392
Scarciglia F, Saporito N, La Russa MF, Le Pera E, Macchione M, Puntillo D, Crisci GM, Pezzino A (2012) Role of lichens in weathering of granodiorite in the Sila uplands (Calabria, southern Italy). Sediment Geol 280:119–134
Scheerer S, Ortega-Morales O, Gaylarde C (2009) Microbial deterioration of stone monuments—an updated overview. Adv Appl Microbiol 66:97–139
Schröder V, Turcanu-Carutiu D, Honcea A, Ion RM (2019) Microscopical methods for the in situ investigation of biodegradation on Cultural Heritage. In: Turcanu-Carutiu D, Ion RM, Hmood K (eds) Advanced methods and new materials for Cultural Heritage preservation. IntechOpen. https://doi.org/10.5772/intechopen.77505
Schumacher J, Gorbushina A (2020) Light sensing in plant-and rock-associated black fungi. Fungal Biol 124:407–417
Seaward MRD (2015) Lichens as agents of biodeterioration. In: Upreti DK, Divakar PK, Shukla V, Bajpai R (eds) Recent advances in Lichenology. Modern methods and approaches in biomonitoring and bioprospection, vol 1. Springer, New Delhi, pp 189–211
Seiffert F, Bandow N, Kalbe U, Milke R, Gorbushina AA (2016) Laboratory tools to quantify biogenic dissolution of rocks and minerals: a model rock biofilm growing in percolation columns. Front Earth Sci 4:31
Shraddha G, Darshan M (2019) Microbially induced calcite precipitation through urolytic organisms—a review. Int J Life Sci 7:133–139
Sierra-Fernandez A, Gomez-Villalba LS, Rabanal ME, Fort R (2017) New nanomaterials for applications in conservation and restoration of stony materials: a review. Materiales de Construcción 67:107
Signorini MA (1996) L’Indice di Pericolosità: un contributo del botanico al controllo della vegetazione infestante nelle aree monumentali. Inf Bot Ital 28:7–14
Silverman MP (1979) Biological and organic chemical decomposition of silicates. Stud Environl Sci 3:445–465
Slater JW (1856) On some reactions of oxalic acid. Chem Gaz 14:130–131
Smith AL (1921) Lichens. Cambridge University Press, Cambridge
Sohrabi M, Favero-Longo SE, Pérez-Ortega S, Ascaso C, Haghighat Z, Talebian MH, Fadaei H, de los Ríos A (2017) Lichen colonization and associated deterioration processes in Pasargadae, UNESCO world heritage site, Iran. Int Biodeterior Biodegrad 117:171–182
Sollas WJ. (1880). On the activity of a lichen on limestone. Rep Br Assoc Adv Sci, 586
Souza-Egipsy V, Wierzchos J, Sancho C, Belmonte A, Ascaso C (2004) Role of biological soil crust cover in bioweathering and protection of sandstones in a semi-arid landscape (Torrollones de Gabarda, Huesca, Spain). Earth Surf Process Landf 29:1651–1661
Stanford C (2000) On preserving our ruins. J Archit Conserv 6:28–43
Steinbauer MJ, Gohlke A, Mahler C, Schmiedinger A, Beierkuhnlein C (2013) Quantification of wall surface heterogeneity and its influence on species diversity at medieval castles–implications for the environmentally friendly preservation of cultural heritage. J Cult Herit 14:219–228
Sterflinger K (2010) Fungi: their role in deterioration of cultural heritage. Fungal Biol Rev 24:47–55
Sterflinger K, Krumbein WE (1997) Dematiaceous fungi as a major agent for biopitting on Mediterranean marbles and limestones. Geomicrobiol J 14:219–230
Sterflinger K, Little B, Pinar G, Pinzari F, de los Rίos A, Gu JD (2018) Future directions and challenges in biodeterioration research on historic materials and cultural properties. Int Biodeterior Biodegrad 129:10–12
Sternberg T, Viles HA, Cathersides A, Edwards M (2010) Dust particulate absorption by ivy (Hedera helix L) on historic walls in urban environments. Sci Total Environ 409:162–168
Stupar M, Grbić ML, Džamić A, Unković N, Ristić M, Jelikić A, Vukojević J (2014) Antifungal activity of selected essential oils and biocide benzalkonium chloride against the fungi isolated from cultural heritage objects. S Afr J Bot 93:118–124
Taylor-George S, Palmer F, Staley JT, Borns DJ, Curtiss B, Adams JB (1983) Fungi and bacteria involved in desert varnish formation. Microb Ecol 9:227–245
Tonon C, Favero-Longo SE, Matteucci E, Piervittori R, Croveri P, Appolonia L, Meirano V, Serina M, Elia D (2019) Microenvironmental features drive the distribution of lichens in the House of the Ancient Hunt, Pompeii, Italy. Int Biodeterior Biodegrad 136:71–81
Totsche KU, Rennert T, Gerzabek MH, Kögel-Knabner I, Smalla K, Spiteller M, Vogel HJ (2010) Biogeochemical interfaces in soil: The interdisciplinary challenge for soil science. J Plant Nutr Soil Sci 173:88–99
Tratebas AM (2004) Biodeterioration of Prehistoric rock art and issues in site preservation. In: St. Clair LL, Seaward MRD (eds) Biodeterioration of stone surfaces. Springer, Dordrecht, pp 195–228
Tretiach M, Bertuzzi S, Candotto Carniel F (2012) Heat shock treatments: a new safe approach against lichen growth on outdoor stone surfaces. Environ Sci Technol 46:6851–6859
Tretiach M, Bertuzzi S, Salvadori O (2010) Chlorophyll a fluorescence as a practical tool for checking the effects of biocide treatments on endolithic lichens. Int Biodeterior Biodegrad 64:452–460
Trovão J, Portugal A, Soares F, Paiva DS, Mesquita N, Coelho C, Pinheiro C, Catarino L, Gil F, Tiago I (2019) Fungal diversity and distribution across distinct biodeterioration phenomena in limestone walls of the old cathedral of Coimbra, UNESCO World Heritage Site. Int Biodeterior Biodegrad 142:91–102
Uloth W (1861) Beiträge zur Flora der Laubmoose und Flechten von Kurhessen. Flora 44:565–576
UNESCO. (2014). Culture, creativity and sustainable development. Research, innovation, opportunities. Florence declaration - 4 October 2014. https://unesdoc.unesco.org/ark:/48223/pf0000230394. Accessed 03 April 2020
Valkó O, Tóth K, Kelemen A, Miglécz T, Radócz S, Sonkoly J, Tóthmérész B, Török P, Deák B (2018) Cultural heritage and biodiversity conservation–plant introduction and practical restoration on ancient burial mounds. Nat Conserv 24:65–80
Vannini A, Contardo T, Paoli L, Scattoni M, Favero-Longo SE, Loppi S (2018) Application of commercial biocides to lichens: Does a physiological recovery occur over time? Int Biodeterior Biodegrad 129:189–194
Vázquez-Nion D, Silva B, Prieto B (2018) Bioreceptivity index for granitic rocks used as construction material. Sci Total Environ 633:112–121
Viles H. (2019). Biogeomorphology: Past, present and future. Geomorphol. In press (https://doi.org/10.1016/j.geomorph.2019.06.022)
Viles HA, Cutler NA (2012) Global environmental change and the biology of heritage structures. Glob Chang Biol 18:2406–2418
Viles HA, Goudie AS (2004) Biofilms and case hardening on sandstones from Al-Quwayra, Jordan. Earth Surf Process Landf 29:1473–1485
Villa F, Pitts B, Lauchnor E, Cappitelli F, Stewart PS (2015) Development of a laboratory model of a phototroph-heterotroph mixed-species biofilm at the stone/air interface. Front Microbiol 6:1251
Villa F, Stewart PS, Klapper I, Jacob JM, Cappitelli F (2016) Subaerial biofilms on outdoor stone monuments: changing the perspective toward an ecological framework. Bioscience 66:285–294
Wang J, Ersan YC, Boon N, De Belie N (2016) Application of microorganisms in concrete: a promising sustainable strategy to improve concrete durability. Appl Microbiol Biotechnol 100:2993–3007
Warscheid T, Braams J (2000) Biodeterioration of stone: a review. Int Biodeterior Biodegrad 46:343–368
Weber B, Scherr C, Bicker F, Friedl T, Büdel B (2011) Respiration-induced weathering patterns of two endolithically growing lichens. Geobiol 9:34–43
Wei Z, Kierans M, Gadd GM (2012) A model sheet mineral system to study fungal bioweathering of mica. Geomicrobiol J 29:323–331
Wessels S, Ingmer H (2013) Modes of action of three disinfectant active substances: a review. Regul Toxicol Pharmacol 67:456–467
Wilhelm K, Viles H, Burke O, Mayaud J (2016) Surface hardness as a proxy for weathering behaviour of limestone heritage: a case study on dated headstones on the Isle of Portland. UK Environ Earth Sci 75:931
Zhang G, Gong C, Gu J, Katayama Y, Someya T, Gu JD (2019) Biochemical reactions and mechanisms involved in the biodeterioration of stone world cultural heritage under the tropical climate conditions. Int Biodeterior Biodegrad 143:104723
Acknowledgements
The authors thank Prof. em. Ian Maddox for the kind invitation to contribute this review article and four anonymous reviewers for helpful suggestions. SEFL and HV are also grateful to institutions and authorities which allowed their research work in the following heritage sites represented in Figs. 1 and 3: Residences of the Royal House of Savoy (Polo Museale del Piemonte, Italy); Archaeological Park of Seradina and Bedolina (Comune di Capo di Ponte, Valle Camonica, Italy), Soprintendenza Archeologia della Lombardia (Milano, Italy); Gardens of Boboli (Gallerie degli Uffizi, Italy); the graveyard of Gressoney-La-Trinité (Comune di Gressoney-La-Trinité, Italy); North Grotto Temple (Dunhuang Academy, China). SEFL also thanks prof. Rosanna Piervittori, dr. Enrica Matteucci (Università di Torino), dr. Ada Roccardi (Istituto Superiore per la Conservazione e il Restauro, Roma), and all the colleagues of the Working Group for Cultural Heritage of the Italian Lichen Society for many stimulating discussions on lichens and other lithobionts in the last two decades.
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Favero-Longo, S.E., Viles, H.A. A review of the nature, role and control of lithobionts on stone cultural heritage: weighing-up and managing biodeterioration and bioprotection. World J Microbiol Biotechnol 36, 100 (2020). https://doi.org/10.1007/s11274-020-02878-3
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DOI: https://doi.org/10.1007/s11274-020-02878-3