Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

Purpose

Investigations on the lithobiontic colonization of the stone cultural heritage in (semi-)arid regions are needed to address conservation strategies. In this work, lithobiontic communities were examined on the carbonate rock surfaces of the heritage site of the Tomb of Lazarus. We aimed to evaluate their distribution and interaction with the lithic substrate, together with the efficacy of biocidal treatments for their control.

Methods

Diversity and abundance of lithobionts were surveyed on the Jerusalem stone blocks of three architectural elements. Observations at the lichen-rock interface were carried out by reflected light and scanning electron microscopy. The efficacy against lichens of the widely used biocide benzalkonium chloride (BZC) was compared for different concentrations and application methods, and evaluated by epifluorescence microscopy.

Results

Chlorolichens were the dominant component of lithobiontic communities, more thoroughly adapted to the semi-arid conditions of the site than mosses and black biofilms of cyanobacteria and dematiaceous fungi. A different structural organization, in terms of thallus thickness and depth of the hyphal penetration component, characterized epilithic and endolithic lichen species, responsible for different deteriogenic activities. Biocidal assays showed that even the methodologies that are usually effective in temperate conditions (as the application of BZC 1.5% by poultice) may not completely devitalize lichens adapted to the stress conditions of semi-arid climates, unless a pervasive biocide diffusion through metabolically active thalli is carefully guaranteed.

Conclusion

Lithobionts act as biodeteriogens on the semi-arid surfaces of the investigated heritage site. Their removal is thus recommendable, but it needs to be adequately supported with a careful calibration of devitalization strategies.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

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

    Article  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

    Chapter  Google Scholar 

  • Aptroot A, James PW (2002) Monitoring lichens on monuments. In: Nimis PL, Scheidegger C, Wolseley P (eds) Monitoring with lichens-monitoring lichens. Springer, Dordrecht, pp 239–253

    Chapter  Google Scholar 

  • Argan GC (1938) Restauro delle opere d’arte. Progettata istituzione di un Gabinetto Centrale del Restauro. In: Il Convegno dei Soprintendenti, Bollettino d’arte, pp 133–137

  • ARIJ – The Applied Research Institute - Jerusalem (2012) El 'Eizariya (including Al Ka’abina) Town Profile. Accessed on line at: http://vprofile.arij.org/jerusalem/pdfs/vprofile/El%20Eizariya_EN.pdf. Accessed 22 Nov 2018

  • Ariño X, Ortega-Calvo JJ, Gomez-Bolea A, Sáiz-Jiménez C (1995) Lichen colonization of the Roman pavement at Baelo Claudia (Cadiz, Spain): biodeterioration vs. bioprotection. Sci Total Environ 167:353–363

    Article  Google Scholar 

  • Arup U, Søchting U, Frödén P (2013) A new taxonomy of the family Teloschistaceae. Nordic J Bot 31:016–083

    Article  Google Scholar 

  • Avnimelech M (1966) Influence of geological conditions on the development of Jerusalem. Bull Am Schools Orient Res 181:24–31

    Article  Google Scholar 

  • Barresi G, Cammarata M, Palla F (2017) Biocide. In: Palla F, Barresi G (eds) Biotechnology and conservation of cultural heritage. Springer, Cham, pp 49–65

    Chapter  Google Scholar 

  • Brandi C (1963) Teoria del Restauro. Editori di Storia e Letteratura, Roma

    Google Scholar 

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

    Article  Google Scholar 

  • Caleri A (2014) La prima chiesa di Betania: nuove proposte interpretative. In: Temporis Signa. Archeologia della tarda antichità e del medioevo 9. CISAM, Spoleto, pp 181–194

  • Calvo JP, Regueiro M (2010) Carbonate rocks in the Mediterranean region—from classical to innovative uses of building stone. In: Smith BJ, Gomez-Heras M, Viles HA, Cassar J (eds) Limestone in the built environment: present-day challenges for the preservation of the past. Geol Soc Lond, Spec Publ 331:27–35

  • Caneva G, Pacini A (2008) Biodeterioration problems in relation to geographycal and climatic contexts. In: Caneva G, Nugari MP, Nugari MP, Salvadori O (eds) Plant biology for cultural heritage: biodeterioration and conservation. Getty Publications, Los Angeles, pp 219–237

    Google Scholar 

  • Caneva G, Nugari MP, Salvadori S (2008) Control of biodeterioration and bioremediation techniques. In: Caneva G, Nugari MP, Salvadori S (eds) Plant biology for cultural heritage: biodeterioration and conservation. Getty Publications, Los Angeles, pp 309–346

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

    Article  CAS  Google Scholar 

  • Clauzade G, Roux C (1985) Likenoj de Okcidenta Europo, ilustrita determinlibro. Bull Soc Bot Centre-Ouest 7:3–893

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

    Article  CAS  Google Scholar 

  • Danin A (1985) Palaeoclimates in Israel: evidence from weathering patterns of stones in and near archaeological sites. Bull Am Sch Orient Res 259:33–43

    Article  Google Scholar 

  • Danin A (1992) Pitting of calcareous rocks by organisms under terrestrial conditions. Isr J Earth Sci 41:201–207

    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

    Article  Google Scholar 

  • Danin A, Gerson R, Marton K, Garty J (1982) Patterns of limestone and dolomite weathering by lichens and blue-green algae and their palaeoclimatic significance. Palaeogeogr Palaeoclimatol Palaeoecol 37:221–233

    Article  Google Scholar 

  • de los Ríos A, Cámara B, del Cura MÁG, Rico VJ, Galván V, Ascaso C (2009) Deteriorating effects of lichen and microbial colonization of carbonate building rocks in the Romanesque churches of Segovia (Spain). Sci Total Environ 407:1123–1134

    Article  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

    Article  CAS  Google Scholar 

  • Favero-Longo SE, Borghi A, Tretiach M, Piervittori R (2009) In vitro receptivity of carbonate rocks to endolithic lichen-forming aposymbionts. Myc Res 113:1216–1227

    Article  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

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Gadd GM (2017) Geomicrobiology of the built environment. Nat Microbiol 2:16275

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Garty J (1999) Lithobionts in the eastern Mediterranean. In: Seckbach J (ed) Enigmatic microorganisms and life in extreme environments. Springer, Dordrecht, pp 255–276

    Chapter  Google Scholar 

  • Gazzano C, Favero-Longo SE, Matteucci E, Castelli D, Piervittori R (2007) Allestimento di una collezione licheno-petrografica presso l'Erbario Crittogamico di Torino per lo studio del biodeterioramento di rocce e materiali lapidei. In: Proceedings of “Lo Stato Dell'arte 5: V Congresso Nazionale IGIIC; Cremona, 11–13 Ottobre 2007”. Nardini, Firenze, pp 669–677

  • Ghadban SS, Ashhab M (2011) Stone restoration practice in Palestinian territories: a case study from Jerusalem. J Archit Conserv 17:75–96

    Article  Google Scholar 

  • Giordani P, Matteucci E, Redana M, Ferrarese A, Isocrono D (2014) Unsustainable cattle load in alpine pastures alters the diversity and the composition of lichen functional groups for nitrogen requirement. Fungal Ecol 9:69–72

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Honegger R (2012) The symbiotic phenotype of lichen-forming ascomycetes and their endo-and epibionts. In: Hock B (ed) Fungal associations. The Mycota IX, 2nd edn. Springer, Berlin, pp 287–339

    Chapter  Google Scholar 

  • Jurado V, Miller AZ, Cuezva S, Fernandez-Cortes A, Benavente D, Rogerio-Candelera MA, Reyes J, Cañaveras JC, Sanchez-Moral S, Saiz-Jimenez C (2014) Recolonization of mortars by endolithic organisms on the walls of San Roque church in Campeche (Mexico): a case of tertiary bioreceptivity. Constr Build Mater 53:348–359

    Article  Google Scholar 

  • Kidron GJ, Temina M (2008) The mycobiont role in crustose lichen expansion on cobbles in the Negev Desert. Geomicrobiol J 25:95–100

    Article  CAS  Google Scholar 

  • Kidron GJ, Temina M (2013) The effect of dew and fog on lithic lichens along an altitudinal gradient in the Negev Desert. Geomicrobiol J 30:281–290

    Article  Google Scholar 

  • Kidron GJ, Kronenfeld R, Starinsky A (2016) Wind as a cooling agent: substrate temperatures are responsible for variable lithobiont-induced weathering patterns on west-and east-facing limestone bedrock of the Negev. Earth Surf Process Landf 41:2078–2084

    Article  Google Scholar 

  • Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Köppen-Geiger climate classification updated. Meteorol Z 15:259–263

    Article  Google Scholar 

  • Lakatos M (2011) Lichens and bryophytes: habitats and species. In: Lüttge U, Beck E, Bartels D (eds) Plant desiccation tolerance. Springer, Berlin, pp 65–87

    Chapter  Google Scholar 

  • MiBACT - Italian Ministry of Cultural heritage and Activities and Tourism (2014) Linee Guida Applicative dell’articolo 182 del Codice dei Beni Culturali e del Paesaggio di cui al decreto legislativo 22 gennaio 2004, n. 42 e ss.mm.ii, pp. 1–19

  • Mihajlovski A, Seyer D, Benamara H, Bousta F, Di Martino P (2015) An overview of techniques for the characterization and quantification of microbial colonization on stone monuments. Ann Microbiol 65:1243–1255

    Article  Google Scholar 

  • Miller AZ, Dionísio A, Laiz L, Macedo MF, Saiz-Jimenez C (2009) The influence of inherent properties of building limestones on their bioreceptivity to phototrophic microorganisms. Ann Microbiol 59:705–713

    Article  CAS  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 Proc Land 42:1666–1679

    Article  Google Scholar 

  • Nascimbene J, Salvadori O (2008) Lichen recolonization on restored calcareous statues of three venetian villas. Int Biodeterior Biodegrad 62:313–318

    Article  CAS  Google Scholar 

  • Nimis PL (2016) The lichens of Italy. A second annotated catalogue. EUT Edizioni Università di Trieste

  • Nimis PL, Seaward MRD, Arino X, Barreno E (1998) Lichen-induced chromatic changes on monuments: a case-study on the Roman amphitheater of Italica (S. Spain). Plant Biosyst 132:53–61

    Article  Google Scholar 

  • Pinheiro AC, Mesquita N, Trovão J, Soares F, Tiago I, Coelho C, Paiva de Carvalho H, Gilb F, Catarino L, Piñar G, Portugal A (2018) Limestone biodeterioration: a review on the Portuguese cultural heritage scenario. J Cult Herit in press. https://doi.org/10.1016/j.culher.2018.07.008

    Article  Google Scholar 

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

    Book  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

    Article  Google Scholar 

  • Podani J, Schmera D (2011) A new conceptual and methodological framework for exploring and explaining pattern in presence–absence data. Oikos 120:1625–1638

    Article  Google Scholar 

  • Rabinovich R, Ginat H, Schudack M, Schudack U, Ashckenazi-Polivoda S, Rogolsky G (2014) A late cretaceous elasmosaurid of the Tethys Sea margins (southern Negev, Israel) and its palaeogeographic reconstruction. Neth J Geosci 94:73–86

    Google Scholar 

  • 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):39e54

    Google Scholar 

  • Sardini P, Siitari-Kauppi M, Beaufirt D, Hellmuth KH (2006) On the connected porosity of mineral aggregates in crystalline rocks. Am Min 91:1068–1080

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Smith CW, Aptroot A, Coppins BJ, Fletcher A, Gilbert OL, James PW, Wolseley PA (2009) Lichens of Great Britain and Ireland. British Lichen Society, London

    Google Scholar 

  • Sohrabi M, Favero-Longo SE, Pérez-Ortega S, Ascaso C, Haghighat Z, Talebian MH, Hamid 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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Tiano P (2016) Biodeterioration of stone monuments a worldwide issue. Open Conf Proc J 7(Suppl. 1 M3:29–38

    Article  CAS  Google Scholar 

  • Tonon C, Favero-Longo SE, Matteucci E, Piervittori R, Croveri P, Appolonia L, Meirano V, Serino 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

    Article  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

    Article  CAS  Google Scholar 

  • Vella HCR (2017) Bethany in early Christian times. In: Cassar E (ed) Who was saint Lazarus? Lulu Press, Malta, pp 9–22

    Google Scholar 

  • Warscheid T (2003) The evaluation of biodeterioration processes on cultural objects and approaches for their effective control. In: Koestler RJ, Charola AE, Nieto-Fernandez FE (eds) Art, biology and conservation. Biodeterioration of works of art. The Metropolitan Museum of Art, New York, pp 14–27

    Google Scholar 

  • Wierzchos J, de los Ríos A, Ascaso C (2012) Microorganisms in desert rocks: the edge of life on earth. Int Microbiol 15:171–181

    Google Scholar 

Download references

Acknowledgements

The authors are grateful to the students attending the training school, all the people working for the conservation of the site of the Tomb of Lazarus, Najati Fitiani for the precious interpreter work, Sara Aveni for the English revision, and all colleagues of ATS Terra Sancta, Centro Conservazione e Restauro “La Venaria Reale,” Jericho Mosaic Center, Municipality of Torino and University of Torino, participating in the project.

Funding

Investigations were carried out in the framework of the international cooperation Palestinian Municipality Support Program EJE CH-096 17, financially supported by Italian Ministry of Foreign Affairs.

Author information

Authors and Affiliations

  1. Dipartimento di Scienze della Vita e Biologia dei Sistemi, University of Turin, Viale Mattioli 25, 10125, Turin, Italy

    Enrica Matteucci & Sergio Enrico Favero-Longo

  2. Centro Conservazione e Restauro “La Venaria Reale”, Venaria Reale (TO), Italy

    Enrica Matteucci, Arianna Valentina Scarcella & Paola Croveri

  3. Dipartimento di Chimica, University of Turin, Turin, Italy

    Paola Croveri

  4. Dipartimento di Scienze della Terra, University of Turin, Turin, Italy

    Alessandra Marengo & Alessandro Borghi

  5. Associazione pro Terra Sancta (ATS), St. Saviour Convent, Jerusalem, Israel

    Carla Benelli

  6. Jericho Mosaic Centre, Jericho, Palestinian Territories

    Osama Hamdan

Authors
  1. Enrica Matteucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Arianna Valentina Scarcella
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paola Croveri
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alessandra Marengo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alessandro Borghi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Carla Benelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Osama Hamdan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sergio Enrico Favero-Longo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sergio Enrico Favero-Longo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants

N/A

Informed consent

N/A

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

Matteucci, E., Scarcella, A.V., Croveri, P. et al. 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 (2019). https://doi.org/10.1007/s13213-019-01465-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-019-01465-8

Keywords

Search

Navigation