International Biodeterioration & Biodegradation 73 (2012) 8e15
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An interactive database for an ecological analysis of stone biopitting V. Lombardozzi a, T. Castrignanò b, M. D’Antonio b, A. Casanova Municchia a, *, G. Caneva a a b
Roma Tre University, Dep. of Environmental Biology, viale Marconi 446, 00146 Rome, Italy Caspur, Consorzio interuniversitario per le Applicazioni di Supercalcolo per Università e Ricerca, Via dei Tizi 6, 00185 Rome, Italy
a r t i c l e i n f o
a b s t r a c t
Article history: Received 29 December 2011 Received in revised form 29 February 2012 Accepted 9 April 2012 Available online xxx
Despite the wide spectrum of literature on stone biodeterioration associated with pitting, there has not been sufficient description of some general topics related to stone biopitting in terrestrial conditions, nor of the taxonomy of the organisms supporting it. In order to synthesize the information available in the literature, and to give a critical analysis of the bibliographic data, an interactive on-line database has been created. Among the about 800 papers selected in the first step of creating this database. Only 24 studies reported on biopitting, giving information on the object, material composition and associated organisms. These first data concern 83 different sites, for a total of 249 samples, coming mainly from the Mediterranean bioclimatic area, even though the biopitting phenomenon is not exclusive to this climate. The most commonly occurring organisms are cyanobacteria, and the associated environmental conditions are dryness, arising from various factors, such as the low porosity of the stone; the exposure conditions; and the bioclimate. These factors explain very high appearance of organisms and especially cyanobacteria in marble, their preference for vertical or subvertical surfaces, and their high occurrence in Mediterranean and desert climate. The lack of information describing the entire phenomenon i.e., type of stone, exposure conditions, and all biodeteriogens present, doesn’t permit the full use of the database’s interactive potential. Ó 2012 Elsevier Ltd. All rights reserved.
Keywords: Stone biodeterioration Pitting Endolithic organisms Cyanobacteria Database
1. Introduction Rocks, as well as stone buildings, can be colonized by different microorganisms and plants, showing a differential biodeterioration related to their own characteristics, the surrounding environmental conditions, and the extent of outdoor exposure (Ortega-Calvo et al., 1995; Viles, 1995; Tomaselli et al., 2000; Warscheid and Braams, 2000; Pohl and Schneider, 2002; Crispim and Gaylarde, 2005; McNamara and Mitchell, 2005; Walker and Pace, 2007; Caneva and Ceschin, 2009). Deterioration due to biological agents is, however, often underestimated when the growth of microorganisms does not form typical colored patinas or crusts, and it is frequently mistaken for chemical and physical phenomena (Hueck, 1965; Ortega-Calvo et al., 1995; Viles et al., 1997; Pinna and Salvadori, 2000; Garcia-Pilcher, 2006; Urzì and De Leo, 2008; Caneva et al., 2009). Moreover, organisms can be epilithic, when they colonize and grow on the upper surface of the stone, or endolithic, when
* Corresponding author. Tel.: þ39 (06) 5757336374; fax: þ39 (06) 5757336321. E-mail addresses:
[email protected] (V. Lombardozzi),
[email protected] (T. Castrignanò),
[email protected] (M. D’Antonio),
[email protected] (A. Casanova Municchia),
[email protected] (G. Caneva). 0964-8305/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ibiod.2012.04.016
they grow inside the stone. Endoliths can be subdivided into chasmo-endolithic organisms, which grow inside already existing fissures; cryptoendolithic organisms, which colonize structural cavities inside the stone without external evidence of their penetration;or euendolithic organisms, which penetrate actively inside the stone, giving rise to the formation of blind holes that are close together and generally cylindrical, i.e., pitting (Golubic et al., 1975, 1980) (Fig. 1). Golubic et al. (1975) described the boring behavior of endolithic organisms, emphasizing that different species penetrating into the same substrate under uniform ecological conditions produce distinctive boring patterns. Later, many authors have mentioned an assumed correlation between pitting and biological colonization (Del Monte, 1991; Krumbein and Urzì, 1992; Viles, 1995; Sterflinger, 2000; Bungartz et al., 2004; Gaylarde et al., 2006). However, few authors have tried to describe and classify pitting phenomena, or to associate different types of pitting with specific causes. For example, according to Danin (1986), in the Judean desert different pitting patterns can be distinguished: micropitting, formed by funnel-shaped pits (containing non-lichenized ascomycetous fungi); pitting formed by pits 0.5e3 cm deep (caused by euendolithic coccoid cyanobacteria and microscopic cyanophilous lichens); spongy-pattern pitting, formed by globular microscopic
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Fig. 1. Morphology of pitting from the Trajan Column (Rome): (a) Detail of SE exposure (drum XI), (from replicas of 1862); (b) Details from different morphology of pits.
holes (caused by euendolithic coccoid cyanobacteria and microscopic cyanophilous lichens); and a jigsaw-puzzle deterioration pattern, characterized by a very typical shape of irregular patches, delimited by borders and containing small pits (caused by endolithic lichens). In reference to endolithic lichens, Gehrmann et al. (1992) distinguish micro-, meso-, and macro-pits: Micropits are holes with an average diameter of 0.5e20 mm; mesopits are circular or oval pocket-like impressions, with sizes that ranges between 20 and 100 mm on average and a diameter four to five times longer than the depth of the crater; macropits are depressions with diameters from 1 mm to 2 cm and four to five times bigger than the depth of the crater. In reality, an objective distinction among the different kinds of pitting can arise only after a wide analysis of the literature, such as that resulting from a database. The origin of stone pitting is controversial due to the difficulty of determining whether the organisms present inside the pits have actively contributed to their formation or simply found more favorable ecological conditions there (Caneva et al., 1992; Salvadori, 2000). Whether of biotic or abiotic origins, pitting causes damage to
rocks that can cause significant damage to stone of cultural heritage. Due to this fact, there has been increasing attention given to pitting and the physiology and ecology of the organisms linked to it. Prior to the advent of the Internet, biological databases and scientific publications were absolutely separate entities. Today, although scientists use cyberinfrastructure in their daily research, databases and publications continue to be very distinct from each other. There are a lot of ways in which the content of an article can be used in a computational manner, and the technology to make this happen already exists. This is demonstrated by the existence of biological databases and related data-mining tools. Indeed, a successful biological database is integration via data-mining with other related databases or resources. Yet integration with literature, which is unquestionably the primary medium through which scientists communicate their research, is still lacking. A high number of taxa found on a substratum does not necessarily imply high bioreceptivity of that substratum, since many other environmental parameters (solar radiation, temperature, water regime, climate) play an important role in a successful
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colonization; nevertheless, specific microclimatic parameters (orientation, exposure to shadow, permanent capillary humidity) are generally missing in the available literature, and the extent to which microclimate determines colonization is unknown (Macedo et al., 2009). Databases help in collecting and analyzing the available data in literature, even if problems arising from the absence of standards on methods of analysis, and the different aims of the various papers, often create difficulties in data processing and correlating (Caneva et al., 1985; Caneva and Roccardi, 1989). An interactive online database has been developed for two main purposes: (1) To synthesize the available information in the literature on the stone-pitting phenomena; and (2) to provide a critical analysis of the bibliographic data. In particular, we intend to identify trends of these phenomena, such as the most favorable environmental conditions, the most affected kind of stone, the most common biodeteriogens, and the most significant association among the interacting factors. 2. Materials and methods The design and development of the biopitting database have been based upon a critical survey of the existing literature. In particular, we selected papers meeting the following three requirements: They included a precise description of the object under examination (both stone monuments or rocks in natural sites), a description of the stone affected by this damage, and an analytical report on the pitting biodeterioration found. Considering
our interest in the biodeterioration of monuments, we limited the literature selection to that dealing with euendolithic organisms of terrestrial habitat. We selected the database descriptors with a goal of giving an optimum ecological, biological, and technical description of pitting and the related organisms: including, the bibliographical references, information about the object, considered as “sampling site”, including constitutive material, geographical location, physical, and environmental parameters. Afterward we considered the descriptors of each reported sampling, such as the sampling technique and the season in which it was collected, the morphology of biodeterioration (diameter, depth, shape, and chromatic variations of the pits), the rate of deterioration, and chemical and biochemical analyses applied to it. Finally we searched for taxonomic and physio-ecological information (the type and species of organisms found in the pits, whether they are endolithic and are still present, whether the pits are a sign of past colonization, and any information about cultural techniques applied) (Fig. 2). For each paper selected to be uploaded into the database we provided a window where we reported samples and sample collecting descriptors. After filling the database with the selected papers, we were able to compare specific parameters between them and make some observations concerning their relationships. The results were entered into Excel tables. Due to the heterogeneity of the information in the database, in order to make some generalizations, we grouped some of the information into larger ensembles, in particular information about the substrate and the type of organisms. The
Fig. 2. Structure of the database (http://mi.caspur.it/biopitting/biop_home.php).
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18 lithological types were sorted into four groups. These are: carbonate rock (which includes calcitic rock, calcareous litharenite, Lioz and Turonian limestone, Verona red stone and Istrian stone, calcarenite, massive biocalcarenite, and dolomia), marble (which includes pentelic and Carrara marbles), granite, and concrete. Moreover, we normalized the highly different ways of referring to the organisms found in the pits into only four major taxonomic groups: cyanobacteria, algae, lichens, and fungi. We included information concerning the descriptor “Bioclimatic Region,” important from the ecological point of view. “BioPitting” (interactively accessible at http://www.caspur.it/ biopitting/) is a relational database available through a dedicated web interface. The database is implemented on a SUSE Linux Enterprise Server (SLES 10) running MySQL 5.1 enterprise. The web interface (written in PHP) runs on the Scientific Linux Server (version 6.1) through an Apache server. 3. Results Among almost 800 papers that deal with stone biodeterioration, only 24 have matched the three characteristics useful for building this biopitting database and the papers used are listed in Table 1. However, the total number of sites was considerable; 83 different sites, for a total of 111 sampling zones (i.e., the part of the sampling site where samples were collected) and a total number of 249 samples. Among the sampling sites, 57 are monuments and 26 are natural sites, as described in Table 2. However, much information was only sketchily reported, such as stationary parameters (exposures, inclination); as well as precise geographical information, such as latitude, longitude, and altitude; and climatic data (pluviometric rate and minimal and maximal temperature). When different samples were described, the information on each sampling often seemed to be incomplete and lacking in detail. Information about the methodology, techniques, sampling season, and sampling zone was also lacking. Moreover, information concerning the use of biocides, i.e., type, employment method, treatment period, and collateral effects, was often missing.
Table 1 Papers entered into the “BioPitting” database. Database ID
Reference
15 19 21 29 7 6 9 28 20 17 8 12 30 26 27 16 22 11 10 13 5 23 14 18
Ascaso et al., 1998a Ascaso et al., 1998b Ascaso et al., 2002 Bungartz and Wirth, 2007 Caneva et al., 1992 Caneva et al., 1994 Danin, 1983 Danin and Garty, 1983 Danin et al., 1983 Danin, 1986 Danin and Caneva, 1990 Danin, 1992a Danin, 1992b Danin, 2008a Danin, 2008b De los Rios et al., 2004a De los Rios et al., 2004b Garcia-Vallès et al., 2000 Giaccone and Di Martino, 1999 Pinna et al., 1998 Pinna and Salvadori, 2000 Pocs, 2009 Salvadori, 2000 Wollenzien et al., 1995
Database available at: http://www.caspur.it/biopitting/.
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Table 2 Geographical location of the 83 different sites considered in the “BioPitting” database. Monuments Greece, Athens, Dyonysos Theatre Greece, Corfù, obelisque Israel, Jerusalem, Bet Hakerem Israel, Jerusalem, el-Kebkebi Mausoleum Israel, Jerusalem, Emir Adughdi el Kubaki Israel, Jerusalem, house’s walls (2 sites) Israel, Jerusalem, Moslem cemetery (3 sites) Israel, Jerusalem, walls of the old city (2 sites) Israel, Maale Efrayim Israel, Qidron Valley, Grave of Pharaoah’s Daughter Israel, Qidron Valley, Zacharia’s grave Israel, Sede Boqer, northern Negev Highlands Israel, Tomb of Pharaoh’s Daughter Italy, Agrigento, Concordia Temple Italy, Catania, balaustrade, S. Francesco d’Assisi Italy, Catania, rail’s arches, Pacini Villa Italy, Catania, Bianchi’s Confraternity Italy, Catania, Archbishopric Italy, Catania, colonnade, Mazzini Square Italy, Catania, Fac Liberal-arts Faculty/Unversity Italy, Catania, fountain “the kidnapping of Proserpina” Italy, Catania, fountain, Botanical garden Italy, Catania, main facade, S. Placido Italy, Catania, Benedectines Monastery Italy, Catania, stock market Palace Italy, Catania, porch, De Felice Inst Italy, Catania, Garibaldi town’s gate Italy, Catania, Uzeda town’s gate Italy, Catania, General Post office Italy,Catania,rectorate/arcades, University Italy, Catania, S. Camillo Italy, Catania, staircase, Greek theater Italy, Catania, SS. Trinità Italy, Messina, statue Italy, Ragusa Cathedral’s mountain Italy, Rome, Caestiu’s pyramid Italy, Rome, capital Santo Eustachio street
Italy, Rome, Italy, Rome, statue Italy, Rome, Italy, Rome, Italy, Rome,
Forum Traianum Forum Traianum, Pasquino’s statue St. Stephen Basilica Trajan’s column
Italy, Trento, Neptune fountain Italy, Venice, Ducal Palace Italy, Sanctuary of Macereto, Visso (Macerata) Portugal, Lisbon, Jeronimos Monastery Portugal, Lisbon, tower of Belem Spain, Jaca, Roman Cathedral Spain, Segovia, Convent of Santa Cruz la Real Turkey, Didim, Temple of Apollo Natural sites Antarctica, McMurdo valley, Commonwealth Glacier Antarctica, McMurdo valley, Goldman Glacier Antarctica, McMurdo valley, Mont Falconer Australia, Naumburg Nat. Park, Pinnacles desert Egypt, desert of Sinai Greece, Crete cliffs Greece, Crete, wetter areas Hungary, Bukk Mnt Israel, Jerusalem, desert Israel, Jerusalem, hilltop Israel, Jerusalem, near Hebrew University Israel, Jordan Valley N of Jericho Israel, Lake Kinneret Israel, Mediterranean Israel cliffs Israel, Negev Highlands Israel, SE Judean Desert Israel, Southern Negev Italy, Carrara, quarry (2 sites) Italy, Trieste karst (2 sites) Namibia, Namib Desert, NE of Wlotzasbaken Namibia, near Swakapmund, mist desert Turkey, Belevi, Ephesus, quarry
Most of the sampling sites described in the literature were in the Mediterranean Basin and are distributed in 10 countries for a total of 47 geographical localities (i.e., municipalities) (Fig. 3). Specifically, 67 sites are included in the bioclimatic Mediterranean region (87% of the samples), while only seven are in the Saharan one (4%), six are in the temperate zone of Eurasia (5.4%), and three are in the polar one (2%). Looking at the selected cases of study, the most precise environmental conditions, when data about inclination and exposure of the surfaces were collected (especially in the case of monuments in Rome), biopitting was mainly described in vertical and subvertical surfaces, showing a certain preference for southern exposures
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Fig. 3. Location of the 83 case studies on stone biopitting used data, corresponding to 47 municipalities (14 in Italy, 18 in Israel, four in Greece, two in Namibia, Turkey, Spain, and Portugal, one in Australia, Antarctica, and Egypt) (Worldwide Bioclimatic Classification System, 1996e2009).
Fig. 4. Frequency of exposure of the sampling sites (mainly from Roman monuments).
(Fig. 4). Concerning the substrate, the database information showed that the stone most frequently associated with this kind of deterioration was marble, accounting for 53% of the total number of samples; this was followed by carbonate rock, with 44%. The remaining 3% of the samples are granite and concrete (Fig. 5a). According to the papers uploaded into the database, cyanobacteria (50%) are the most commonly described biodeteriogens found in association with pitting, followed by fungi and lichens (11 and 10%, respectively) and algae (5%). The remaining 24% of the samples are from studies in which there is no precise indication of the type of organisms found in the sampled pits (Fig. 5b). Looking at the organisms in relation to different kinds of stone, on carbonate rocks we found the most evidence of appearance of cyanobacteria (24%) as well as for the marble but in smaller amount (22%), probably due the highest number of not reported
Fig. 5. Some associations observed from the BioPitting data base: (a) Type of substrates affected; (b) frequency of the organisms detected; (c) frequency of the organisms on the different substrates.
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identification. Lichens in particular are most frequently mentioned on carbonate rocks than on any other material (Fig. 5c). Table 3 shows the species collected from pittings, with the related number of citations and the papers from which data was extracted. It shows that the cyanobacteria have the highest biodiversity of collected taxa; with many species mentioned as being endolithic (e.g., Hyella and Lichenotelia). When only the genus is identified, it is difficult to interpret if they were epi- or endolithic. Looking at the correlation among the factors, we can observe once again the highest repetition of the pair (Mediterranean/cyanobacteria) with carbonate or marble stones (Fig. 6). In particular, we can also note that the data on marble originate only from the Mediterranean climate, and we do not posses data on this material in other climatic contexts. In the case of carbonate rocks we see the greatest range for growth in the different climatic contexts, but in all the conditions cyanobacteria are the most frequent group. Lichens are also not negligible. 4. Discussion In order to have better data we need to improve the information, taking into account case studies coming from wider contexts. As previously stressed (Caneva and Roccardi, 1989), correlation analysis for biodeterioration data is difficult, due to the lack of information on environmental and edaphic parameters and difficulties in integrating data from various authors. Due to the heterogeneity of the collected data, a final classification of biopitting in exact types of shapes cannot yet be made. However, we can try to make some preliminary generalizations and some critical comment based upon the current database. 4.1. Environmental conditions and stone biopitting The predominance of the Mediterranean bioclimatic region in the selected samples probably does not reflect the real distribution of the biopitting phenomenon. Indeed, we excluded from the general literature papers where pitting was mentioned in other localities, due to the absence of one of the necessary requirements for the database. For example, we can mention the diffusion of the phenomenon on the Dalmatian coasts (one of the first places it was described, thanks to Golubic et al. (1975)), and in different Italian calcareous cliffs as well. Moreover the phenomenon was often observed on exposed rocks both in cold and hot deserts, as mentioned by many authors. We also observed biopitting in temperate climates on limestone of the walls of a Georgian church near the Black Sea (Caneva et al., 2008) and in northern Europe, e.g., in Dresden (Germany). Even on stones found in tropical countries, such as Mayan calcareous monuments in Mesoamerica, colonies of endolithic cyanobacteria are sometimes detected (McNamara et al., 2006). There are also references to colonization of endolithic cyanobacteria reported in northern Europe, such as in the Basilica in Tongeren, in Belgium (Saiz-Jimenez et al., 1990), that were not included in the database because the pitting phenomena are not present on the stone. In addition, we need to consider that most stone monuments, especially marble ones, are located in the Mediterranean area, and that a lot of studies on biodeterioration of stone monuments come from this area. That gives rise to a potential overestimation of a linkage to the pitting with this climatic area. However, when ecological conditions favoring this phenomenon are considered, as a common factor characterizing the biopitting, a connection between climatic or edaphic dryness seems to be recurrent. The data on exposure and inclination of the surfaces suffering biopitting suggest an association of this phenomenon with dry conditions, since, as much the surface is vertical, water is less easily drained.
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Table 3 List of the species collected from the “BioPitting” database. n tot presence Cyanobacteria Aphanocapsa muscicola (Meneghini) Wille Aphanocapsa roeseana de Bary Calothrix marchica Lemmermann Calothrix marchica Lemmermann var. crassa Rao Chroococcus minor (Kutz) Nageli Chroococcidiopsis sp. Clastidium setigerum Kirchner Cyanothece sp. Dalmatella sp. Entophysalis deusta (Meneghini) Drouet et Daily Entophysalis rivularis (Kutzing) Drouet Entophysalis sp. Gloeocapsa alpina Gloeocapsa biformis Ercegovic Gloeocapsa calcarea Tilden Gloeocapsa sp. Gloeothece rupestris (Lyngbye) Bornet in Wittrock et Nordstedt Hyella sp. Lyngbya aff. limnetica Microcoleus chthonoplastes Thuret ex Gomont Microcystis sp. Myxosarcina sp. Myxosarcina spectabilis Geitler Myxosarcina concinna Printz Phormidium foveolarum Gomont Plectonema radiosum (Schiederm.) Gomont Plectonema sp. Pseudocapsa dubia Ercegovic Pseudocapsa sp. Schizothrix sp. Stigonema muscicola Borzì ex Bornet et Flahault Synechococcus sp. Synechocystis sp. Symploca dubia Gomont ex Gomont Tolypothrix byssoidea (Berk.) No. spp Fungi Cladosporium sp. Diplodia sp. Lichenothelia intertexta Henssen Lichenothelia globosa Lichenotelia sp. Ochroconis sp. Phoma sp. Trichoderma sp. Ulocladium sp. Coniothyrium sp. Alternaria sp. Hormonema sp. No. spp Lichens Buellia peregrina Bungartz & V.Wirth Caloplaca alociza (A. Massal.) Mig. Caloplaca sp. Encephalographa elisae A. Massal Petractis clausa (Hoffm.) Kremp. Verrucaria baldensis A. Massal No. spp Algae Chlorococcum sp.1 Chlorococcum sp.2 Haematococcus pluvialis Flotow Heterococcus caespitusus Vischer Stichococcus bacillaris Nageli Ulothrix sp. No. spp
n paper
n sampling site
1 3 1 3
1 1 1 1
1 2 1 1
1 1 1 1 1 4
1 1 1 1 1 1
1 1 1 1 1 3
21 1 1 3 2 2 1
1 1 1 1 1 2 1
20 1 1 2 2 2 1
1 1 1 3 1 3 9 6 2 1 1 1 1 1
1 1 1 1 1 1 1 1 1 1 1 1 1 1
1 1 1 2 1 1 2 2 2 1 1 1 1 1
4 2 1 2 33
1 2 1 1 13
2 2 1 1
1 1 1 1 3 1 3 1 3 1 1 1 13
1 1 1 1 2 1 1 1 2 1 1 1 5
1 1 1 1 3 1 3 1 3 1 1 1
1 5 1 1 1 1 13
1 2 1 1 1 1 3
1 2 1 1 1 1
3 4 1 1 1 1 3
1 1 1 1 1 1 2
2 2 1 1 1 1
The columns show the total appearance in the database, the paper number, and the sampling sites where each species was reported.
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Also, we need to stress the great heterogeneity in the approach to the study of the biological agents that may be found on stone. Here it seems that literature has the greatest diversity. Qualitatively the organisms found are reported at all systematic levels, from kingdom to single species, with the result that it is difficult to have a general view of the distribution of the different kinds. On the other hand, quantitative data (e.g., microorganisms/stone) are not generally reported. Moreover, sometimes it appears that depending on the specific field of research of the authors themselves, there have been detected and therefore reported with detail (naming species) only certain kind of organisms. That leads to a possible risk of artificial account of the biodiversity of the microbial communities growing on the site. 5. Conclusions
Fig. 6. Distribution of the organisms detected, on different substrata in each bioclimate. The gray scale indicates the frequency of the organisms. C ¼ cyanobacteria; A ¼ algae; L ¼ lichens; F ¼ fungi. White boxes indicate the absence of organisms.
The preference of organisms for the southern exposure and vertical surfaces can be explained in the case of Rome, because this exposure is the only one exposed to incident rainfall, receiving though a minimum input of water, which is able to counteract drying due to high solar radiation (Caneva et al., 1992). Thus, here, under such extremely dry conditions, endolithic microorganisms are the only ones able to grow. 4.2. Stone and pitting Marble is often described as the most affected material, and it, as well as calcareous rocks, can be greatly deteriorated by this phenomenon. However, the reason of the high incidence of biopitting on marble might arise from the previously cited high incidence of studies coming from Roman monuments, where marble was often used in the construction of important Imperial buildings, columns, and statues. It should be stressed that much work still has to be done on precise classification of stone type vis-a-vis biodeterioration under various environmental conditions. 4.3. Pitting and organisms Cyanobacteria are the dominant group associated with pitting, but for a more precise description of the phenomenon we have to consider that, in general, the taxonomic information shows a different level of definition. On the whole, of the 249 samples that have been uploaded into the database up to now, 99 go into species details, while 45 indicate only genus level, and 62 finish at a general description as to type of organism. Regarding the remaining samples, there is not a clear correspondence between each sampling and the organisms that are mentioned in the papers, which can prove to be an arbitrary attempt to assign a specific species to a single sampling.
The existing bibliography on this subject is extremely heterogeneous, with a wide variation of the scientific approach used to study biopitting. The database reported here just hints at what might be possible if the literature provided a more homogenous method of reporting results. There is a need for normalization of the terminology, analyses, and methods, as suggested by many authors through national (NORMAL) and international (CEN, Comité Européen de Normalisation) working groups on stone conservation. From whatever scientific point of view the research is carried out, it is important that some elements should always be taken into consideration while collecting and analyzing samples. These include precise information on the environment surrounding the sampling site, the stationary parameters of the area from which the samples are collected (exposures, inclination of the surface, height from soil), measurements of the pits (diameter and depth), coverage percentage of the phenomena on the surfaces, specific description of the substrata by means of petrographic and physical analyses, and description of organisms found inside the pits at a finer systematic level. This level of detail should never be missing in studies dealing with this problem area since once recognized, the repetition of similar elements could permit the building of generalized models of development of these phenomena. It is, indeed, important to stress the need for the literature to include more detailed information on stone parameters, such as porosity, pore size distribution, and mineral compounds, in order to understand and differentiate the chemical and microbial sensitivity of the material in question. Moreover, generic papers on stone deterioration focused on taxonomy or biochemical processes related to pitting could prove useful from a systematic or physiological point of view, but they do not usually report information useful in creating an ecological description of the phenomenon. Many papers synthesize information from different cases without exact sampling references; these are useful in defining the ecological niche of the associated microorganisms. We couldn’t give a contribution on the classification of the different morphologies of pitting, that we expected from the literature, due to the lack of a detailed description of the appearance of the phenomenon. Nevertheless, we can show that, as the most recurrent cause seems to be cyanobacteria and the most recurrent environmental conditions are dryness, arising from the low porosity of the stone (the reason of very high presence on marble) and also from the exposure conditions (the reason for the preference for vertical or subvertical surfaces), and from the bioclimate (the reason of the high recurrence of Mediterranean and desert climate). For the future, a database containing all this information will be made available on the network in order to serve as a useful tool in the field of conservation of cultural heritage.
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References Ascaso, C., Wierzchos, J., Castello, R., 1998a. Study of the biogenic weathering of calcareous litheranite stones caused by lichens and endolithic organisms. International Biodeterioration and Biodegradation 42, 29e38. Ascaso, C., Wierzchos, J., Delgado Rodrigues, J., Aires-Barros, L., Henriques, F.M.A., Charola, A.E., 1998b. Endolithic microorganisms in the biodeterioration of the Tower of Belem. International Zeirschrift fur Bauinstandsetzen 4, 627e640. Ascaso, C., Wierzchos, J., Souza-Egipsy, V., De Los Rios, A., Delgado Rodrigues, J., 2002. In situ evaluation of the biodeteriorating action of microorganisms and the effects on carbonate rock of the Jeronimos Monastery (Lisbon). International Biodeterioration and Biodegradation 49, 1e12. Bungartz, F., Garvie, L.A.J., Nash, T.H., 2004. Anatomy of the endolithic Sonoran Desert lichen Verrucaria rubrocincta Breuss: implications for biodeterioration and biomineralization. Lichenologist 36, 55e73. Bungartz, F., Wirth, V., 2007. Buellia peregrina sp. nov. a new euendolithic calcicolous lichen species from the Namib Desert. The Lichenologist 39, 41e45. Caneva, G., Roccardi, A., Marenzi, A., Napoleone, I., 1985. Proposal for a data base on biodeterioration of stone artworks. In: Felix, G. (Ed.), Vth International Congress on Deterioration and Conservation of Stone. Presses Polytechnique Romandes, Lausanne, pp. 587e596. Caneva, G., Roccardi, A., 1989. Correlation analysis in the biodeterioration of stone artworks. International Biodeterioration 25, 161e167. Caneva, G., Nugari, M.P., Salvadori, O., 1992. Pitting of marble roman monuments and the related microflora. In: Rodriguez, J.D., Henriques, F., Jeremias, F.T. (Eds.), Proceedings of the Seventh International Congress on Deterioration and Conservation of Stone. Portugal, Lisbon, pp. 521e530. Caneva, G., Danin, A., Ricci, S., Conti, C., 1994. The pitting of Trajan’s column, Rome: an ecological model of its origin. Contributo del Centro Linceo Interdisciplinare “Beniamino Segre” 88, 77e102. Caneva, G., Lombardozzi, V., Savo, V., 2008. Biodeterioration of mural paintings in the Church of the Virgin in Martvili (Georgia). In: Skinner, P., Tumanishvili, D., Shanshiashvili, A. (Eds.), Proceedings of the International Symposium of Georgian Art, Tbilisi, Georgia, June 21ste29th, pp. 351e356. Caneva, G., Ceschin, S., 2009. Ecology of biodeterioration. In: Caneva, G., Nugari, M.P., Salvadori, O. (Eds.), Plant Biology for Cultural Heritage. Biodeterioration and Conservation. The Getty Conservation Institute, Los Angeles, pp. 35e58. Caneva, G., Nugari, M.P., Salvadori, O. (Eds.), 2009. Plant Biology for Cultural Heritage. Biodeterioration and Conservation. The Getty Conservation Institute, Los Angeles. Crispim, C.A., Gaylarde, C.C., 2005. Cyanobacteria and biodeterioration of cultural heritage: a review. Microbial Ecology 49, 1e9. Danin, A., 1983. Weathering of limestone in Jerusalem by cyanobacteria. Zeitschrift für Geomorphologie N. F 27, 413e421. Danin, A., Garty, J., 1983. Distribution of cyanobacteria and lichens on hillsides of the Negev Highlands and their impact on biogenic weathering. Zeitschrift für Geomorphologie N. F 27, 423e444. Danin, A., Gerson, R., Garty, J., 1983. Weathering patterns on hard limestone and dolomite by endolithic lichens and cyanobacteria: supporting evidence for eolian contribution to terra rossa soil. Soil Science vol. 136, 213e217. Danin, A., 1986. Patterns of biogenic weathering as indicators of paleoclimates in Israel. In: Proceedings of the Royal Society of Edinburgh, vol. 89B, pp. 243e253. Danin, A., Caneva, G., 1990. Deterioration on limestone walls in Jerusalem and marble monuments in Rome caused by cyanobacteria and cyanophilous lichens. International Biodeterioration 26, 397e417. Danin, A., 1992a. Biogenic Weathering of Marble Monuments in Didim, Turkey and in Trajan’s Column, Rome, vol. V/B. Environmental Quality and Ecosystem Stability. 675e680. Danin, A., 1992b. Pitting of calcareous rocks by organisms under terrestrial conditions. Israel Journal of Earth Sciences 41, 201e207. Danin, A., 2008a. Color of walls in Jerusalem: continued. In: Plants-This Time Just the Story. chapter 6, Flora of Israel Online. Online at: http://flora.huji.ac.il/ browse.asp%3flang%3den. Danin, A., 2008b. Color of walls in Jerusalem: continued. In: The Walls of the Old City. Plants, This Time Just the Story. chapter F (Part 5), Flora of Israel Online. Online at: http://flora.huji.ac.il/browse.asp%3flang%3den. De los Rios, A., Galvan, V., Ascaso, C., 2004a. In situ microscopical diagnosis of biodeterioration processes at the convent of Santa Cruz la Real, Segovia, Spain. International Biodeterioration and Biodegradation 54, 113e120. De los Rios, A., Wierzchos, J.G., Sancho, L., Ascaso, C., 2004b. Exploring the physiological state of continental Antarctic endolithic microorganisms by microscopy. FEMS Microbiology Ecology 50, 143e152. Del Monte, M., 1991. Trajan’s column: lichens don’t live here anymore. Endeavour 15, 86e93. Garcia-Pilcher, F., 2006. Plausible mechanisms for the boring on carbonates by microbial phototrophs. Sedimentary Geology 185, 205e213.
15
Garcia-Vallès, M., Urzì, C., De Leo, F., Salamone, P., Vendrell-Saz, M., 2000. Biological weathering and mineral deposits of the Belevi marble quarry (Ephesus, Turkey). International Biodeterioration 46, 221e227. Gaylarde, P., Englert, G., Ortega-Morales, O., Gaylarde, C., 2006. Lichen-like colonies of pure Trentepohlia on limestone monuments. International Biodeterioration and Biodegradation 58, 119e123. Gehrmann, C.K., Krumbein, W.E., Peterson, K., 1992. Endolithic lichens and corrosion of carbonate rocks. A study of biopitting. International Journal of Mycololgy and Lichenology 5, 37e48. Giaccone, G., Di Martino, V., 1999. Biologia delle alghe e conservazione dei monumenti. Bollettino delle sedute della Accademia Gioenia di Scienze Naturali in Catania 32, 53e81. Golubic, S., Perkins, R.D., Lukas, K.J., 1975. Boring microorganisms and microborings in carbonate substrates. In: Frey, R. (Ed.), Study of Trace Fossils. Springler-Verlag, New York, pp. 229e259. Golubic, S., Friedmann, I., Schneider, J., 1980. The lithobionthic ecological niche, with special reference to micro-organisms. Journal of Sedimentary Petrology 51, 475e478. Hueck, H.J., 1965. The biodeterioration of materials as part of hylobiology. Material und Organism 1, 5e34. Krumbein, W.E., Urzì, C., 1992. Biologically induced decay phenomena of antique marbles -some general considerations. In: Decrouez, D., Chamy, J., Zezza, F. (Eds.), The Conservation of Monuments in the Mediterranean Basin, Proc 2nd Int Symp. Musee d’Art et d’Histoire Naturelle, Geneve, pp. 305e325. Macedo, M.F., Miller, A.Z., Dionisio, A., Saiz-Jimenez, C., 2009. Biodiversity of cyanobacteria and green algae on monuments in the Mediterranean Basin: an overview. Microbiology 155, 3476e3490. McNamara, C.J., Mitchell, R., 2005. Microbial deterioration of historic stone. Frontiers in Ecology and Environment 3, 445e451. McNamara, C.J., Perry, T.D., Bearce, K.A., Hernandez-Duque, G., Mitchell, R., 2006. Epilithic and endolithic bacterial communities in limestone from a Maya archaeological site. Microbial Ecology 51, 51e64. Ortega-Calvo, J.J., Ariño, X., Hernandez-Marine, M., Saiz-Jimenez, C., 1995. Factors affecting the weathering and colonization of monuments by phototrophic microorganisms. The Science of the Total Environment 167, 329e341. Pinna, D., Salvadori, O., Tretiach, M., 1998. An anatomical investigation of calcicolous endolithc lichens from the Trieste karst (NE Italy). Plant Biosystems 132, 183e195. Pinna, D., Salvadori, O., 2000. Endolithic lichens and conservation: an underestimate question. In: Fassina, V. (Ed.), Proceedings of the Ninth International Congress on Deterioration and Conservation of Stone, Venice, pp. 513e519. Pocs, T., 2009. Cyanobacterial crust types, as strategies for survival in extreme habitats. Acta Botanica Hungarica 51, 147e178. Pohl, W., Schneider, J., 2002. Impact of endolithic biofilms on carbonate rock surfaces. In: Siegesmund, S., Weiss, T., Vollbrecht, A. (Eds.), Natural Stone, Weathering Phenomena, Conservation Strategies and Case Studies. Geological Society, London, pp. 177e194. Special Publication 205. Saiz-Jimenez, C., Garcia-Rowe, J., Garcia Del Cura, M.A., Ortega-C0alvo, J.J., Roekens, E., Van Grieken, R., 1990. Endolithic cyanobacteria in Maastricht limestone. Science of the Total Environment 94, 209e220. Salvadori, O., 2000. Characterisation of endolithic communities of stone monuments and natural outcrops. In: Ciferri, O., Tiano, P., Mastromei, G. (Eds.), Of Microbes and Art. The Role of Microbial Communities in the Degradation and Protection of Cultural Heritage, pp. 89e101. Sterflinger, K., 2000. Fungi as geologic agents. Geomicrobiology Journal 17, 97e124. Tomaselli, L., Lamenti, G., Bosco, M., Tiano, P., 2000. Biodiversity of photosynthetic micro-organisms dwelling on stone monuments. International Biodeterioration and Biodegradation 46, 251e258. Urzì, C., De Leo, F., 2008. Biodeterioration of Cultural Heritage in Italy: State of Art. Online at: http://www.arcchip.cz/w08/w08_de_leo.pdf. Viles, H.A., 1995. Ecological perspectives on rock surface weathering: towards a conceptual model. Geomorphology 13, 21e35. Viles, H.A., Camuffo, D., Fitz, S., Fitzner, B., Lindquist, O., Livingstone, R.A., Maravelaki, P.N.V., Sabbioni, C., Warscheid, T., 1997. Group report: what is the state of our knowledge of the mechanisms of deterioration and how good are our estimates of rates of deterioration. In: Baer, N.S., Snethlage, R. (Eds.), Saving Our Architectural Heritage: The Conservation of Historic Stone Structures. Wiley, pp. 95e112. Dahlem Workshop Report. Walker, J.J., Pace, N.R., 2007. Endolithic microbial ecosystems. Annual Review of Microbiology 61, 331e347. Warscheid, Th., Braams, J., 2000. Biodeterioration of stone: a review. International Biodeterioration and Biodegradation 46, 343e368. Wollenzien, U., De Hoog, G.S., Krumbein, W.E., Urzì, C., 1995. On the isolation of microcolonial fungi occurring on and in marble ant other calcareous rocks. The Science of the Total Environment 167, 287e294. Rivas-Martinez, S., Rivas-Saenz, S. 1996e2009. Worldwide Bioclimatic Classification System. Phytosociological Research Center, Spain. http://www.globalbioclimatics. org.