Skip to main content
Log in

A review of the nature, role and control of lithobionts on stone cultural heritage: weighing-up and managing biodeterioration and bioprotection

  • Review
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

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.

Graphic abstract

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adamo P, Violante P (2000) Weathering of rocks and neogenesis of minerals associated with lichen activity. Appl Clay Sci 16:229–256

    CAS  Google Scholar 

  • Albertano P (2012) Cyanobacterial biofilms in monuments and caves. In: Whitton BA (ed) Ecology of cyanobacteria II. Springer, Dordrecht, pp 317–343

    Google Scholar 

  • 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

    Google Scholar 

  • Ascaso C, Galván J, Rodríguez-Pascual C (1976) Studies on the pedogenetic action of lichen acids. Pedobiologia 16:321–331

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Bell FG (1993) Durability of carbonate rock as building stone with comments on its preservation. Environ Geol 21:187–200

    CAS  Google Scholar 

  • Bellezza S, Albertano P, de Philippis R, Paradossi G (2006) Exopolysaccharides of two cyanobacterial strains from Roman hypogea. Geomicrobiol J 23:301–310

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Brimblecombe P, Grossi CM (2005) Aesthetic thresholds and blackening of stone buildings. Sci Total Environ 349:175–189

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Bungartz F, Garvie LA (2004) Anatomy of the endolithic Sonoran Desert lichen Verrucaria rubrocincta Breuss: implications for biodeterioration and biomineralization. Lichenol 36:55–73

    Google Scholar 

  • 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

    Google Scholar 

  • Caneva G (1993) Ecological approach to the genesis of calcium oxalate patinas on stone monuments. Aerobiol 9:149–156

    Google Scholar 

  • Caneva G, Nugari MP, Salvadori O (2008) Plant biology for cultural heritage: biodeterioration and conservation. Getty Conservation Institute, Los Angeles

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Carter NEA, Viles HA (2004) Lichen hotspots: raised rock temperatures beneath Verrucaria nigrescens on limestone. Geomorphol 62:1–16

    Google Scholar 

  • Carter NEA, Viles HA (2005) Bioprotection explored: the story of a little known earth surface process. Geomorphol 67:273–281

    Google Scholar 

  • Casanova Municchia A, Percario Z, Caneva G (2014) Detection of endolithic spatial distribution in marble stone. J Microsc 256:37–45

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Charter M, Tischner U (2017) Sustainable solutions: developing products and services for the future. Routledge, London

    Google Scholar 

  • Chen J, Blume HP, Beyer L (2000) Weathering of rocks induced by lichen colonization—a review. Catena 39:121–146

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Crispim CA, Gaylarde CC (2005) Cyanobacteria and biodeterioration of cultural heritage: a review. Microb Ecol 49:1–9

    CAS  PubMed  Google Scholar 

  • Cuadros J (2017) Clay minerals interaction with microorganisms: a review. Clay Min 52:235–262

    CAS  Google Scholar 

  • Davidson TM, Altieri AH, Ruiz GM, Torchin ME (2018) Bioerosion in a changing world: a conceptual framework. Ecol Lett 21:422–438

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • de los Rios A, Ascaso C (2005) Contributions of in situ microscopy to the current understanding of stone biodeterioration. Int Microbiol 8:181–188

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Dorn R (2013) Rock coatings. In: Shroder JF (ed) Treatise on geomorphology. Academic Press, San Diego, pp 70–97

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Fatorić S, Seekamp E (2017) Are cultural heritage and resources threatened by climate change? A systematic literature review. Clim Chang 142:227–254

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Fernandes P (2006) Applied microbiology and biotechnology in the conservation of stone cultural heritage materials. Appl Microbiol Biotechnol 73:291–296

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Fidanza MR, Caneva G (2019) Natural biocides for the conservation of stone cultural heritage: a review. J Cult Herit 38:271–286

    Google Scholar 

  • 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

    Google Scholar 

  • Flemming HC, Neu TR, Wozniak DJ (2007) The EPS matrix: the “house of biofilm cells”. J of Bacteriol 189:7945–7947

    CAS  Google Scholar 

  • Flemming HC, Neu TR, Wingender J (2017) The perfect slime: microbial extracellular polymeric substances (EPS). IWA publishing, London

    Google Scholar 

  • Fomina M, Burford EP, Hillier S, Kierans M, Gadd GM (2010) Rock-building fungi. Geomicrobiol J 27:624–629

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Fry EJ (1924) A suggested explanation of the mechanical action of lithophytic lichens on rocks (shale). Ann Bot 38:175–196

    CAS  Google Scholar 

  • Fry EJ (1927) The mechanical action of crustaceous lichens on substrata of shale, schist, gneiss, limestone, and obsidian. Ann Bot 41:437–460

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Gadd GM, Dyer TD (2017) Bioprotection of the built environment and cultural heritage. Microb Biotechnol 10:1152–1156

    PubMed  PubMed Central  Google Scholar 

  • Gadd GM (2017) Fungi, rocks, and minerals. Elements 13:171–176

    Google Scholar 

  • Garty J (1990) Influence of epilithic microorganisms on the surface temperature of building walls. Can J Bot 68:1349–1353

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Golubic S, Friedmann EI, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J Sedim Res 51:475–478

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Gorbushina A (2003) Microcolonial fungi: survival potential of terrestrial vegetative structures. Astrobiology 3:543–554

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Guillitte O (1995) Bioreceptivity: a new concept for building ecology studies. Sci Total Environ 167:215–220

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Hueck HJ (1965) The biodeterioration of materials as a part of hylobiology. Materi und Org 1:5–34

    Google Scholar 

  • Huyssen A (2006) Nostalgia for ruins Grey Room 23:6–21

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Kampf G (2018) Adaptive microbial response to low-level benzalkonium chloride exposure. J of Hosp Infect 100:e1–e22

    CAS  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Mandrioli P, Caneva G, Sabbioni C (2003) Cultural heritage and aerobiology. Methods and measurement techniques for biodeterioration monitoring.  Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • McCarroll D, Viles H (1995) Rock-weathering by the lichen Lecidea auriculata in an arctic alpine environment. Earth Surf Process Landf 20:199–206

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Mottershead D, Lucas G (2000) The role of lichens in inhibiting erosion of a soluble rock. Lichenol 32:601–609

    Google Scholar 

  • Nascimbene J, Salvadori O, Nimis PL (2009) Monitoring lichen recolonization on a restored calcareous statue. Sci Total Environ 407:2420–2426

    CAS  PubMed  Google Scholar 

  • Negi A, Sarethy IP (2019) Microbial biodeterioration of cultural heritage: events, colonization, and analyses. Microb Ecol 78:1014–1029

    PubMed  Google Scholar 

  • Nimis PL, Monte M, Tretiach M (1987) Flora e vegetazione lichenica di aree archeologiche del Lazio. Studia Geobotanica 7:3–161

    Google Scholar 

  • Nimis PL, Pinna D, Salvadori O (1992) Licheni e Conservazione dei Monumenti. Cooperativa Libraria Universitaria Editrice, Bologna

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Piervittori R, Favero-Longo SE, Gazzano C (2009) Lichens and biodeterioration of stonework: a review. Chimica oggi-Chem Today 27:8–11

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Pinna D (2014) Biofilms and lichens on stone monuments: Do they damage or protect? Front Microbiol 5:1–3

    Google Scholar 

  • Pinna D (2017) Coping with biological growth on stone heritage objects: methods, products, applications, and perspectives. Apple Academic Press, Oakville

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Prieto B, Aira N, Silva B (2007) Comparative study of dark patinas on granitic outcrops and buildings. Sci Total Environ 381:280–289

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Rampazzi L (2019) Calcium oxalate films on works of art: a review. J Cult Herit 40:195–214

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Saiz-Jimenez C, Garcia Rowe J, Rodriguez Hidalgo JM (1991) Biodeterioration of polychrome Roman mosaics. Int Biodeterior Biodegrad 28:65–79

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Scheerer S, Ortega-Morales O, Gaylarde C (2009) Microbial deterioration of stone monuments—an updated overview. Adv Appl Microbiol 66:97–139

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Shraddha G, Darshan M (2019) Microbially induced calcite precipitation through urolytic organisms—a review. Int J Life Sci 7:133–139

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Silverman MP (1979) Biological and organic chemical decomposition of silicates. Stud Environl Sci 3:445–465

    CAS  Google Scholar 

  • Slater JW (1856) On some reactions of oxalic acid. Chem Gaz 14:130–131

    Google Scholar 

  • Smith AL (1921) Lichens. Cambridge University Press, Cambridge

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Stanford C (2000) On preserving our ruins. J Archit Conserv 6:28–43

    Google Scholar 

  • 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

    Google Scholar 

  • Sterflinger K (2010) Fungi: their role in deterioration of cultural heritage. Fungal Biol Rev 24:47–55

    Google Scholar 

  • Sterflinger K, Krumbein WE (1997) Dematiaceous fungi as a major agent for biopitting on Mediterranean marbles and limestones. Geomicrobiol J 14:219–230

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Uloth W (1861) Beiträge zur Flora der Laubmoose und Flechten von Kurhessen. Flora 44:565–576

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Vázquez-Nion D, Silva B, Prieto B (2018) Bioreceptivity index for granitic rocks used as construction material. Sci Total Environ 633:112–121

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Viles HA, Goudie AS (2004) Biofilms and case hardening on sandstones from Al-Quwayra, Jordan. Earth Surf Process Landf 29:1473–1485

    CAS  Google Scholar 

  • 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

    PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Weber B, Scherr C, Bicker F, Friedl T, Büdel B (2011) Respiration-induced weathering patterns of two endolithically growing lichens. Geobiol 9:34–43

    CAS  Google Scholar 

  • Wei Z, Kierans M, Gadd GM (2012) A model sheet mineral system to study fungal bioweathering of mica. Geomicrobiol J 29:323–331

    Google Scholar 

  • Wessels S, Ingmer H (2013) Modes of action of three disinfectant active substances: a review. Regul Toxicol Pharmacol 67:456–467

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sergio Enrico Favero-Longo.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-020-02878-3

Keywords

Navigation