Review
Biological colonization patterns on the ruins of Angkor temples (Cambodia) in the biodeterioration vs bioprotection debate

https://doi.org/10.1016/j.ibiod.2014.09.015Get rights and content

Highlights

  • We investigate the biodeterioration phenomena in two temples of Angkor park.

  • All samples show a complex biological community with a dominant organism.

  • The Pyxinetum is the most aggressive lichen species investigated.

  • Our results show biodeterioration process in relation to bioprotection action.

Abstract

The biological colonization present on the temples of the UNESCO World Heritage site of Angkor is wide and relevant, but a debate on its biodeteriorative and bioprotective effects is now developing. We investigated the biological patterns observed on two temples (Ta Nei and Ta Keo) exposed to different microclimatic conditions, in order to assess the damage caused by the communities present on the stone. We analyzed the penetration (depth and spread) into the stone, and the degree of decohesion of seven communities (green algae, cyanobacteria, lichens and mosses). The microscopic analyses highlighted a clear interaction between organism and stone, displaying a trend of increasing harmfulness from the community of the green algae (Trentepohlia) up to the moss communities. All the lichen communities show biodeterioration abilities: the Pyxine community seems more aggressive than the Lepraria and Cryptothecia communities, and more also than the cyanobacterial communities. The positive effects of the lichen cover in reducing dangerous evaporation processes cannot outweigh the negative effects of their hyphal penetration. Light forest cover seems beneficial for the conservation of the Angkor monuments since it reduces evaporation processes, but further studies should be carried out so as to find an optimal balance between contrasting factors.

Introduction

Stone biodeterioration involves numerous interactions between organisms, substrates and climates, giving rise to a variety of biodeterioration patterns (Caneva and Salvadori, 1989, Warscheid and Braams, 2000, Caneva et al., 2009). It is well known that biological colonization of stone monuments is always influenced by a favorable climate, so comparative analyses of colonization phenomena occurring in different climatic contexts have been undertaken in order to identify tendencies and correlations on a macroclimatic scale (Danin and Caneva, 1990, Warscheid et al., 1996, Gaylarde and Gaylarde, 2005, Caneva and Pacini, 2009).

Several studies deal with general processes of stone deterioration or the biological identification of communities observed on monuments in tropical areas such as India, Sri Lanka, Indonesia, Thailand, and Philippines (Lee and Wee, 1982, Sadirin, 1988, Aranyanak, 1992, Chihara et al., 1992, Tripathi et al., 1997, Kumar and Kumar, 1999, Uchida et al., 1999, Adhikary, 2000, Crispim et al., 2006, Gaylarde et al., 2012), and Central and South America, in particular Mexico, Guatemala, Honduras, Cuba, and Brazil, (De Miguel et al., 1995, Ortega-Morales et al., 1999, Ortega-Morales et al., 2005, Caneva et al., 2005, Ramírez et al., 2010), while there are very few, which deal with tropical Africa. However, despite the intense biological growth characteristic of tropical environments, there is a lack of studies that focus on the interaction between organisms and substrate with the aim of describing the relevant action of organisms on the monuments.

Many authors have shown that substrate weathering, where the biological cover meets the rock surface, can be substantially accelerated by the growth of several organisms (Rodrigues, 1991, Nimis et al., 1992, Seaward, 1997, Silva et al., 1997, Adamo and Violante, 2000, Chen et al., 2000). These authors have gone on to emphasize the aggressive action of these populations, in particular of lichen populations, which are able to penetrate deep into the substrate with the fungal hyphae and can also produce high levels of chelating substances, which have the power to extract ions from the substrate (Siever and Woodford, 1979, Prieto et al., 1994, Prieto Lamas et al., 1995, Wierzchos and Ascaso, 1996, Adamo et al., 1997).

However, the dual role of organisms, which colonize the surface as biodeteriogens or bioprotective, and how this dual role effects conservation strategies, is still being debated. Several authors take the view that organisms, especially lichens, should not be removed from stone surfaces in certain conditions because the biodeterioration they cause is less damaging than physic-chemical processes due to weathering (bioprotection effect) (Ariño et al., 1995, Fiol et al., 1996, Grondona et al., 1997, Mottershead and Lucas, 2000, Carter and Viles, 2003, Carter and Viles, 2005, Concha-Lozano et al., 2012, De la Rosa et al., 2012).

The debate on biodeterioration vs bioprotection seems particularly relevant to the archaeological site of Angkor, where Khmer temples that had been abandoned for many centuries suffer from a wide range of biological colonization due to dense forest cover (Delvert, 1963, Uchida et al., 1999, Warrack, 2000, Warscheid, 2000, Warscheid and Leisen, 2011, Caneva et al., 2012, Gaylarde et al., 2012).

The Angkor archaeological park (Cambodia), inscribed on the UNESCO World heritage List in 1992, includes about forty temples built over a period of six hundred years (9th–15th centuries) (Warrack, 2000). The park is distributed over 400 km2 in the plain around the Tonle Sap (Great lake), characterized by a tropical monsoon climate with distinctive rainy and dry seasons.

The archaeological park has been studied, but mainly from a floristic point of view. The lichen flora of this area has appeared in taxonomic studies by several authors (Nakanishi et al., 2010, Moon et al., 2011, Moon et al., 2013, Schumm and Aptroot, 2012, Aptroot et al., 2013). At present, a total of 63 species are known in Cambodia, mainly (45) from collection around Siem Reap: 19 species grow on rocks. Among the 63 species of lichen flora, 50 species in 42 genera discovered around the investigation area, are reported for the first time in Cambodia, including a few unidentified species (Moon et al., 2011, Moon et al., 2013, Moon et al., 2014). There are 19 species of moss flora in 14 genera and 11 families of Bryopsida (Higuchi, 2009), at Ta Nei 9 species in 8 genera of bryophytes and 3 species in 2 genera of liverworts were recorded.

National Research Institute for Cultural Properties, Tokyo (NRICPT), in cooperation with the Authority for the Protection and Management of Angkor, and the Siem Reap Region (APSARA National Authority) in 2001 selected for study the Ta Nei temple, which had previously been chosen for conservation studies and training courses by ICCROM (Warrack, 2000). The choice of this temple, built in the reign of Jayavarman VII (around the end of the 12th-beginning of the 13th centuries), was due to its relatively small size and its decentralized position in the shade of forest canopy cover, making it representative of base-case studies of stone conservation in shady environmental conditions (Futagami, 2009). Previous studies have shown the presence on stones of a rich micro- and macroflora constituted by communities (listed following the phytosociological style, see Westhoff and Van Der Maarel, 1978) of algae and cyanobacteria (respectively Trentepohlietum, Scytonemo-Gloeocapsetum), of lichens (Leprarietum, Cryptothecietum, Pyxinetum), mosses and higher plants, corresponding to different local ecological conditions (Caneva et al., 2012).

In opposite condition seems to be the Ta Keo temple, built in the reign of Jayavarman V (10th century) which is, in a cleared area of the archaeological park, and it suffers for the severe weathering underlined by André et al. (2011). This weathering has been caused by aggressive microclimatic conditions related to the complete cutting down of the forest canopy over recent decades (Chihara et al., 1992). Now it also displays lower levels of biological colonization, often limited to wide black patinas of cyanobacteria and lichen communities. On the basis of a comparison of the observed rate of weathering of this temple and that of the temples covered in vegetation, some authors (André et al., 2008, André et al., 2011) have concluded that most biological colonizations, and especially lichens, have a bioprotective action.

In this paper, the harmfulness of the biological colonization patterns which can be observed in these two temples exposed to different microclimatic conditions in the Angkor archaeological park was investigated, in order to assess the biodeterioration damage caused by the different communities found on the stone and therefore contribute to the on-going debate.

Section snippets

Study area: environmental and lithological characterization

The meteorological data were gathered by NRICPT, which estimated an annual mean maximum temperature for 2012 inside the gallery of the Ta Nei Temple of 33.2 °C, and a mean minimum temperature of 24.0 °C. Temperatures are very high at the end of the dry season (March and April), the highest temperature of the year was measured on April 25th as 39.1 °C. The coldest months of the year were December and January, the coldest day in 2012 was January 9th, with a temperature of 18.8 °C. Total

Results

All samples studied show a complex biological community with one dominant organism (Fig. 1). In all specimens filamentous and coccoid cyanobacteria, along with the probable presence of other bacteria and in some cases fungi, have been found on the surface and in the internal part of the substrate, as observed by Warscheid and Leisen (2011). The values of the three parameters: penetration, spread area and degree of cohesion for each community were calculated by SEM and staining techniques, and

Discussion

The microscopic analyses of the samples demonstrated a clear interaction between organisms and stone, with some differences when comparing the Ta Nei and Ta Keo samples.

A rising level of penetration (in depth and spread), such as an increase in observed damage to crystals, was also observed beginning with the first pioneer community of Trentepohlia through to the moss communities.

The algal community that we examined, dominated by Trentepohlia sp., seems to cause limited biogeophysical damage

Conclusions

The study shows that the biological communities colonizing the Ta Nei and Ta Keo temples have a differential interaction with the stone. In fact, each biological pattern showed a typical degree of penetration, colonization spread and decohesion through the substrate. These parameters, then, have been considered together to determine the potential dangerousness of microorganisms for these stones. Among the colonizations studied, we identified a rising trend of penetration, showing that the algal

Acknowledgments

The authors would like to thank Mr. Say Sophearin, His Excellency Bun Narith, His Excellency Ros Borath, His Excellency Tan Boun Suy and Ms. Mao Loa of the APSARA National Authority for their kind support during our field studies in Cambodia, Dr. O. Salvadori, Head of the Scientific Laboratory at the “Soprintendenza Speciale per il Polo Museale Veneziano, Laboratorio Scientifico”, for her technical and scientific support.

References (74)

  • C. Gazzano et al.

    Index of Lichen Potential Biodeteriogenic Activity (LPBA): a tentative tool to evaluate the lichen impact on stonework

    Int. Biodeterior. Biodegrad.

    (2009)
  • P.M. Gaylarde et al.

    Lichen-like colonies of pure Trentepohlia on limestone monuments

    Int. Biodeterior. Biodegrad.

    (2006)
  • C.C. Gaylarde et al.

    A comparative study of the major microbial biomass of biofilms on exteriors of buildings in Europe and Latin America

    Int. Biodeterior. Biodegrad.

    (2005)
  • I. Grondona et al.

    Lichenized association between Septonema tormes sp. nov., a coccoid cyanobacterium, and a green alga with an unforeseen biopreservation effect of Villamayor sandstone at “Casa Lis”

    Mycol. Res.

    (1997)
  • D. Mottershead et al.

    The role of lichens in inhibiting erosion of a soluble rock

    Lichenologist

    (2000)
  • B. Prieto et al.

    Colonization by lichens of granite dolmens in Galicia NW Spain

    Int. Biodeterior. Biodegrad.

    (1994)
  • B. Prieto Lamas et al.

    Colonization by lichens of granite churches in Galicia NW Spain

    Sci. Total Environ.

    (1995)
  • J.D. Rodrigues

    Causes, mechanisms and measurement of damage in stone monuments

  • M.R.D. Seaward

    Major impact made by lichens in biodeterioration processes

    Int. Biodeterior. Biodegrad.

    (1997)
  • R. Siever et al.

    Dissolution kinetics and weathering of mafic minerals

    Geochim. Cosmochim. Acta

    (1979)
  • B. Silva et al.

    Rapid biological colonization of a granitic building by lichens

    Int. Biodeterior. Biodegrad.

    (1997)
  • T. Warscheid et al.

    Biodeterioration of stone: a review

    Int. Biodeterior. Biodegrad.

    (2000)
  • P. Adamo et al.

    Iron oxides and hydroxides in the weathering interface between Stereocaulon ÍesuÍianum and volcanic rock

    Clay Miner.

    (1997)
  • S.P. Adhikary

    Epilithic cyanobacteria on the exposed rocks and walls of temples and monuments of India

    Ind. J. Microbiol.

    (2000)
  • A. Altieri et al.

    Il ruolo delle briofite nel biodeterioramento di materiali lapidei. La conservazione dei monumenti nel bacino del Mediterraneo

  • M.F. André et al.

    Assessment of sandstone deterioration at Ta Keo temple (Angkor): first results and future prospects

    Environ. Geol.

    (2008)
  • M.F. André et al.

    Contrasting weathering and climate regimes in forested and cleared sandstone temples of the Angkor region

    Earth Surf. Processes Landf.

    (2011)
  • A. Aptroot et al.

    Pyrenocarpous lichens in Cambodia, with the description of Celothelium longisporum sp. nov. (Pyrenulales)

    J. Jpn. Bot.

    (2013)
  • C. Aranyanak

    Biodeterioration of Cultural Materials in Thailand

  • H. Brandl

    Microbial leaching of metals

  • J. Braun-Blanquet

    Pflanzensoziologie: grundzüge der Vegetationskunde

    (1964)
  • G. Caneva et al.

    Biodeterioration of stone in relation to microclimate in the Ta Nei temple – Angkor (Cambodia)

  • G. Caneva et al.

    Biodeterioration problems in relation to geographical and climatic contexts

  • G. Caneva et al.

    Biodeterioration of stone

  • G. Caneva et al.

    Ecological analysis and biodeterioration processes over time at the Hieroglyphic Stairway in the Copán (Honduras) archaeological site

    Plant Biosyst.

    (2005)
  • D. Chihara et al.

    Considerations for the Conservation and Preservation of the Historic City of Angkor

    (1992)
  • Cited by (76)

    • Unearthing the global patterns of cultural heritage microbiome for conservation

      2024, International Biodeterioration and Biodegradation
    View all citing articles on Scopus
    View full text