Bioreceptivity of building stones: A review

Abstract

In 1995, Guillitte defined bioreceptivity, a new term in ecology, as the ability of a material to be colonized by living organisms. Information about the bioreceptivity of stone is of great importance since it will help us to understand the material properties which influence the development of biological colonization in the built environment, and will also provide useful information as regards selecting stones for the conservation of heritage monuments and construction of new buildings. Studies of the bioreceptivity of stone materials are reviewed here with the aim of providing a clear set of conclusions on the topic. Definitions of bioreceptivity are given, stone bioreceptivity experiments are described, and finally the stone properties related to bioreceptivity are discussed. We suggest that a standardized laboratory protocol for evaluating stone bioreceptivity and definition of a stone bioreceptivity index are required to enable creation of a database on the primary bioreceptivity of stone materials.

Introduction

Stone is one of the most important materials traditionally used for both construction and ornamental purposes. Most of the worldwide cultural heritage monuments are built using this porous material. Nowadays, concrete is the most widely used material in civil engineering for different kind of applications: buildings, bridges and in some case during restoration of cultural heritage monuments.

Natural and man-made stone materials (concrete, brickwork, mortar) of specific colors and textures are used to fulfill the physical and technical requirements demanded by engineers and architects as well as to guarantee aesthetic and artistic values.

Natural stone exhibits a wide range of mineral composition, texture and structure. Therefore, the physical and chemical properties of different types of stone are extremely variable, resulting in stone with widely different abilities to resist weathering (durability). Decay of stone materials as a result of their interaction with the environment can lead to loss of the essential messages of the architectural object, in terms of cultural or artistic values. The most immediate consequence of this interaction is chemical and physical alteration followed, in most cases, by biological colonization. Several papers focused on synergist effects of climatic change (temperature and rainfall) with air pollution on the decay and biodeterioration of stone materials in the building envelope have been published (Caneva et al., 1995, Saiz-Jimenez, 1997, Thornbush and Viles, 2006, Brimblecombe and Grossi, 2009). The response to environmental changes is largely dependent on the nature of stone and thus, stone materials particularly susceptible to colonizing organisms will respond more and more quickly to climate change and atmospheric pollution (Caneva et al., 1995, Gorbushina, 2007, Smith et al., 2011).

It is well known that rocks, either in natural geological outcrops (Ascaso and Wierzchos, 2002, Garcia-Vallès et al., 2002, Prieto et al., 2007) or in buildings and monuments (Ascaso et al., 1998, Ortega-Morales, 2006), are common habitats for a wide variety of microorganisms. Several authors reported that microorganisms may play an important and substantial role in all rock alteration processes, inducing aesthetical, physical and chemical changes (Krumbein, 1988, Saiz-Jimenez, 1994, Gorbushina, 2007). In some natural environments, chemical and physical transformations in the materials, such as the biotransfer process of rocks for soil formation (pedogenesis), can be seen as a necessary and positive process. However, when a rock is used as building material, the transformations induced by the microflora in association with other environmental agents are clearly seen as a negative or destructive process, both from cultural and economical viewpoints. Therefore, the concepts “biodegradation” and “biodeterioration” leads to a systematization of these fields of science (Hueck, 2001). The term biodeterioration was defined by Hueck (1965) as “any undesirable change in the properties of a material caused by the vital activities of living organisms”. This term involves a negative connotation, whereas the term biodegradation involves a positive or useful connotation in relation to ecology, waste management and environmental remediation. For a detailed historic review of these and related terms it is recommended the following literature: Krumbein (1988), Krumbein et al. (2003) and Gorbushina and Krumbein (2005).

Microbial communities are truly ubiquitous on stone objects, including cultural heritage assets that are exposed outdoors (Ariño et al., 1995, De los Ríos and Ascaso, 2005, De los Ríos et al., 2009, Macedo et al., 2009). These works clearly demonstrated the aptitude of different type of substrata to be colonized by diverse microbial communities composed of bacteria, cyanobacteria, algae, fungi, and lichens (Fig. 1), either epilithically or endolithically (Golubic et al., 1981). It is important to stress that biofilms occur on contact surfaces at the interface between the mineral substratum and the atmosphere (Gorbushina and Broughton, 2009). Thus, they are constantly subjected to adverse environmental conditions, such as, intense solar radiation, desiccation, temperature and moisture fluctuations, lack of nutrients, etc. Endolithic colonization is a successful strategy of survival when surface environmental conditions are adverse for life on stone since the endolithic microhabitat gives protection from intense solar radiation and desiccation, and it provides mineral nutrients, moisture and growth surfaces (Saiz-Jimenez et al., 1990, Walker et al., 2005). Cockel and Herrera (2008) present several hypotheses, in the context of microbial evolutionary biology, to explain why certain microorganisms started to bore into rocks, contributing to rock weathering. A variety of selection pressures are proposed as the origin of this behavior: acquisition of nutrients, finding a niche with limited competition, avoiding adverse conditions on the surface of rocks or prevention of mineralization. Also, Walker and Pace (2007) reviewed ribosomal RNA-based studies that evaluate hypotheses about endolithic ecosystems, providing insight for a better understanding of microbial ecology, biodiversity and geobiological processes. Wierzchos and Ascaso (2001) and De los Ríos et al., 2004, De los Ríos et al., 2005, De los Ríos et al., 2007 reported endolithic colonization in rocks from Antarctic extreme environments as protection against the extremely dry and cold climatic conditions. Pohl and Schneider (2002) applied computerized image analysis to detect and quantify the depth of penetration of endolithic microorganisms into carbonate rock surfaces. They observed that phototrophic microorganisms from intensely insulated dry sites retreated to depths of 150–250 μm below the rock surface and revealed “cushions” of extracellular polymeric substances (EPS) oriented toward the surface, which protect them against intense light and provide water retention. Miller et al. (2010a) corroborated a successful survival strategy inside of stone probes artificially colonized with phototrophic microorganisms under laboratory conditions. Biogeophysical and biogeochemical deterioration were noticed due to the penetration of the phototrophic microorganisms into the calcarenite probes.

Photoautotrophic microorganisms (green microalgae, cyanobacteria and lichens) can develop on stone surfaces even when there is no organic matter present, and are of particular importance as pioneer organisms in the colonization of stone materials (Bock and Sand, 1993, Gómez-Alarcón et al., 1995, Lamenti et al., 2000, Tomaselli et al., 2000, Bellinzoni et al., 2003, Gaylarde and Gaylarde, 2005, Crispim et al., 2006). Due to the fact that organisms such as lichens and cyanobacteria are poikylohydric, i.e. organisms able to induce or reduce their metabolism as a function of the water input, their growth is not limited by unfavorable xeric periods, although a better bioclimate favors their colonization (Caneva et al., 1991, Caneva et al., 1995). These phototrophic microorganisms can become the dominant primary producers in environments considered as extreme, such as hot springs, deserts, alkali lakes and polar areas (Friedmann, 1982, Bell, 1993a, Büdel et al., 2004, De los Ríos et al., 2005, De los Ríos et al., 2007), and may also predominate on the vertical surfaces of monuments or other cultural heritage assets (Ariño et al., 1997, Prieto et al., 1997, Tomaselli et al., 2000, Ascaso et al., 2002, McNamara et al., 2006, Sarró et al., 2006).

A number of reviews provide a comprehensive picture of the role of microorganisms in the deterioration of stone monuments (Piervittori et al., 1994, Piervittori et al., 1996, Piervittori et al., 1998, Piervittori et al., 2004, Saiz-Jimenez, 1994, Saiz-Jimenez, 1995, Saiz-Jimenez, 1999, Saiz-Jimenez, 2001, Ortega-Calvo et al., 1995, Tiano, 1998, Warscheid and Braams, 2000, Gaylarde et al., 2003, Favero-Longo et al., 2004, Fernandes, 2006, Gorbushina, 2007, Gorbushina and Broughton, 2009, Macedo et al., 2009, Cutler and Viles, 2010). Most of these papers review the colonization of stone and its effects on the substrata but only few of them include the characteristics of the material that allow colonization to take place. The degree of biological colonization of a stone surface depends not only on environmental factors but also on the intrinsic properties of the material (Guillitte, 1995), thus two different types of stone may undergo different degrees of colonization under the same environmental conditions. All stone material is bioreceptive and therefore able, to some extent, to be colonized. Since the term bioreceptivity was defined by Guillitte (1995), a number of studies have addressed this subject. The present paper reviews the literature, published between 1995 and the present, that assess the bioreceptivity of stone building materials, i.e., the material properties which influence the development of biological colonization in the built environment, such as surface roughness, porosity and chemical composition of the lithic substrata (Guillitte, 1995). This may provide useful information about selection of stone for use in the conservation of cultural heritage assets as well as for the control of materials used in building construction.

The review is organized in different sections, each one deals with particular aspects, such as the differentiation between the different types of bioreceptivity, stone bioreceptivity experiments and stone properties related to bioreceptivity. In the conclusion section the intrinsic factors pointed out as the ones that control the bioreceptivity of different types of stones is summarized. This topic is still a matter of controversy and advances in experimental work and field measurements are still needed in order to create a database concerning the primary bioreceptivity of lithotypes applied to building construction.