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Lichens, Mosses, and Vascular Plants in Biodeterioration: History
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Contributor: Alessia Cozzolino , Paola Adamo , Giuliano Bonanomi , Riccardo Motti

Biodeterioration is defined as the alteration of a given substrate due to a combination of physical and chemical factors produced by living organisms when attached to such materials. This phenomenon attracts scientific research attention due to its risk in causing destruction to outdoor cultural rock heritage sites. Trees and shrubs are the most harmful plant life forms, for example, Ficus carica, Ailanthus altissima, and Capparis spinosa, while regarding building materials, those characterized by high porosity, such as andesite and argillaceous limestone, are more vulnerable to plant colonization.

  • biodeterioration
  • monument conservation
  • higher plants deterioration

1. Introduction

Biodeterioration is a type of damage generated by the growth and/or metabolic activities of organisms on various substrates. As defined by Hueck [1], biodeterioration is “any undesirable change in the properties of a material caused by the vital activities of organisms”, or, as defined by Rose [2], it is “the process by which living organisms are the cause of the [structural] loss of quality and, consequently, of value”. This definition separates the concept of biodeterioration from cases of wear and corrosion involving undesirable changes in the properties of a material caused by mechanical, physical, and chemical influences [3].
Historical buildings and stone monuments are the maximum expression of human heritage and, being subject to deterioration, their conservation has become a matter of concern for the scientific community to ensure the identity and cultural continuity of humanity [4][5].
Therefore, understanding the physiological and morphological characteristics of deteriogenic organisms, such as algae, fungi, lichens, mosses, and vascular plants, is necessary to establish the type of interaction that occurs with the material and to evaluate the cause–effect of the deteriorating action of a specific biological agent [6]. The colonization of stone monuments by an organism also depends on the chemical–physical properties of a material, giving rise to a particular susceptibility to colonization, defined as bioreceptivity, which is based on the surface roughness, porosity, exposure, and inclination of the wall [5][7][8][9]. Obviously, the building materials are more or less bioreceptive and therefore subject in different ways to biological degradation.

2. Biodeterioration Process

Deterioration occurs after a strong alteration due to weathering and aging of stone materials. Weathering is a combination of geochemical, geophysical, and biological processes responsible for the alteration of source rocks.
Physically, rock masses are eroded from an overlying rock resulting in fragmentation of the outcrop, aggravated by temperature differences which consequently emphasize the susceptibility to chemical attack [10]. Chemical weathering changes the chemical composition and structure of source rocks, leading to disintegration and in turn increasing the mineral surface area available for chemical weathering [11]. Bioweathering, instead, consists of the alteration of rock-forming minerals by biota (microorganisms, plants, and animals) which produce mechanical forces and metabolic compounds, including chelators and organic acids [10]. Generally, biodeterioration can be classified in three different types: physical or mechanical, aesthetic, and chemical. The physical type is related to the processes of growth and the movement of living organisms which destroy the material structure (e.g., root damage, gnawing by rodents). From an aesthetic point of view, the most significant effects depend on encrustation or soiling due to the presence of organisms, their metabolic products, and/or dead bodies, which form a microbial layer on the surface known as biofilm. Finally, chemical biodeterioration includes two different processes: assimilatory and dissimilatory. In the process of assimilation, organisms use the structural component as a food source by changing the properties of the material, while in the dissimilatory process, organisms excrete waste products or other substances that negatively affect the material [12][13].

2.1. Focus on Lichens

The succession of communities of living organisms growing on stone artifacts generally begins with the development of lichen flora depending on organic contamination caused by moisture and wind on the stone over time [14]. Lichens occupy environments normally hostile to many other forms of life, perhaps due to their resistance to desiccation and extreme temperatures, to longevity, and to their ability to store nutrients from the surrounding environment [15].
They have a simple structure known as thallus, consisting of a symbiotic union of a fungal element, the mycobiont (Ascomycetes or seldom Basidiomycetes), and a photosynthetic organism (cyanobacteria or green algae), the photobiont. The upper side of the thallus is covered by a cortical layer formed by organized hyphae, and besides the algal zone there is the medulla, which consists of interwoven hyphae [16][17].
The colonization of stone materials by lichens is favored by the wind, insects, and birds which disperse the spores in the atmosphere which, falling into pores or cavities with water, favors the development of new organisms [16]. According to Garcia-Rowe and Saiz-Jimenez [15], the large-bird excrement provides the organic nitrogen useful to the develop of an ornithocoprophilous flora, which, in the long term, can cause biodeterioration of materials. Indeed, on the cathedral of Salamanca (Spain) there are some species of lichens, such as Ramalina spp., which are characteristic of rainy climates and excrement-rich habitats [15].
The damage caused by lichens is both mechanical and chemical. The first is due especially to the penetration of the hyphae into the substrate, causing loss of cohesion due to the contraction and expansion of the thallus during fluctuations in the water supply. Chemical damage, instead, regards the production of organic carboxylic acids, such as citric, oxalic, lactic, and gluconic acids which favor the chemical processes by which the lichens are able to decompose lithic constituents [16][17].
On the other hand, a bioprotective condition also occurs. For example, in the case of sandstone, the oxalic acid can react with the calcite cement producing calcium oxalate crystals around the lichen hyphae. When the thallus dies, the union of oxalates and organic and mineral matter form a patina which provides good protection to the sandstone against weathering. In agreement with Arino et al. [18], this balance between biodeterioration and bioprotection was observed at the forum of Baelo Claudia, a Roman city located in southern Spain. The flagstones without lichen cover showed higher deterioration than those colonized by lichens thanks to several preventive actions: reduction of the abrasive effect produced by airborne sand particles, reduction of the dissolution effect of water lying on the surface, reduction of temperature changes, etc. [18].
Furthermore, some authors argue that when the growth of lichens does not damage a monument, their presence can even enrich its cultural value by strengthening its historical and artistic importance [16].

2.2. Focus on Mosses

With a sufficient accumulation of soil in the micro-cavities of rocks, the development of mosses and liverworts can begin [14]. Mosses generally prefer wetter climates in which humid environmental conditions and low temperature promote their regeneration and multiplications. Thus, they retain water and abundant nutrients providing favorable environments for microorganism growth, but consequently, the accumulation of moisture promotes the deterioration and weathering processes of building materials [19][20][21].
Focusing on dry climates, most dryland mosses have evolved to require desiccation by losing virtually all liquid water from their shoot tissues [19][22]. According to Jang and Viles [19], the mosses have a buffering effect that may be beneficial to buildings located in drier climates. This result was observed at the churchyard at Chipping Norton where the comparison between bare stone and moss-covered stone showed that the mosses can shield the substrates from lighter periods of rain and moisture. So, for built heritage sites in these climates, the removal of mosses may not be necessary for the health and preservation of the site. Even, additional tests (e.g., Karsten tube tests) illustrated that the impact of removing mosses may be more damaging than leaving them in situ.
Conversely, in wetter climates and in cases with dramatic and invasive growths, different methods are implemented to preserve and control relics: direct methods (mechanical, biological, chemical, and physical) to counter the microorganisms; and indirect methods to confine the microorganisms’ activity, thus eliminating or reducing their nutritional sources [19][20].
Removing mosses therefore implies a dramatic effect on the aesthetics and presentation of a cultural heritage asset because their presence may be beneficial to the appearance of the monuments as a result of a higher authenticity value. This is the case of Dryburgh Abbey where weathering and decay can accrue ‘age value’, marking the passage of time and creating aesthetically pleasing ‘character’, ‘patina’, and ‘ruination’ [19][23].

2.3. Focus on Higher Plants

Vascular plants’ colonization of stone artifacts is limited by the availability of suitable sites for the settlement, the type of substrate, the disturbance, and the variability of the microclimate in terms of moisture and temperatures [24][25][26].
Stone artifacts are a harsh environment for plant growth and, as underlined by Segal [24], they show ecological characteristics similar to those of rocks in natural environments and can be considered selective anthropic ecosystems [27][28]. The structural and environmental features of walls affect their ability to act as suitable habitats for plant growth. The factors that most influence the capacity of the walls to serve as habitats for higher plants are the size, construction materials, position, and age [28]. The settlement of vascular plants usually occurs in crevices and fractures in the wall, and if left undisturbed, a succession takes place of plants of increasing diversity and size [3][28]. Vascular plant colonization is essentially conditioned by the adaptability of the species and the efficiency of their mode of reproduction. The living organisms mentioned above are the most harmful biodeteriogens, causing cracking and disconnection of materials, leading to considerable problems for stability and safety. From a biophysical point of view, the decay is mainly caused by the roots, as the radial thickening during growth causes higher pressure on the structural parts of the building. The roots develop in fissures or cracks already present in the walls, in water seepage, and in more fragile parts (e.g., mortar between stones) by reducing the adhesion between the stones [16][29]. In addition, soil forms in the cracks creating niches favorable to the accumulation of nutrients and organic substance, which encourage the development of characteristic vegetation of the biogeographic area affected [24][27]. With regard to the biochemical processes, a dualism can be noted between a mechanism of assimilation where the organism obtains nourishment by exploiting the surface of stones and a mechanism of dissimilation in which the production of metabolites by organisms causes chemical reactions on building materials [27][30][31].
The type of damage that occurs on monuments varies in relation to the biological form of the plants or the characteristics of the root system [32]. Plant biological form has been considered by most authors as the main element for assessing the hazard risk [3][25][33][34]. There are different categories of plants, based on their life cycle and the position of the buds: therophytes-T: annual herbs (short life of few months); hemicryptophytes-H: perennial herbs with buds at the soil level; geophytes-G: perennial herbs with underground storage organs; chamaephytes-Ch: woody plants with buds at no more than 25 cm above the soil surface; and phanerophytes-P: trees and shrubs with buds over 25 cm above the soil surface [35]. After classifying the biological form, it is possible to evaluate the hazard of deteriogenic species according to Signorini [33], assigning a numerical index, defined as a hazard index (HI), ranging from 0 (minimal hazard) to 10 (high hazard). It differs for each species and is based on plant life form, invasiveness, vigor, and the size and shape of the root systems. Moreover, if there is visible damage, the risk assessment method proposed by Fitzner and Heinrichs [36] can be followed, which considers the recurrent damaging phenomena due to plant colonization, such as detachments, cracking, and deformation [25][27][32].
Generally, the phanerophytes have the highest impact with an average HI of 7, since their shape and characteristics make them more harmful. Then, there are the therophytes (1.1), geophytes (3.1), chamaephytes (4.3), and the hemicryptophytes (4.3) [3]. According to several authors, the most common trees and shrubs with the higher HI among the species are Ailanthus altissima (HI 10), Celtis australis (HI 10), Ficus carica (HI 10), Capparis orientalis (HI 10), Quercus ilex (HI 9), Cytisus infestus (HI 8), Spartium junceum (HI 8), Sambucus nigra (HI 8), Pistacia lentiscus (HI 8), etc. [3][8][26][27].
The floristic composition in the various historical sites is related to the type of construction material in association with exposure, inclination, and surrounding environmental characteristics, including human disturbance. According to Motti et al. [27], in the Phlegraean Fields Archaelogical Park (PFAP), located in the province of Naples (southern Italy), all the major deteriogenic higher plants grow on more or less porous construction materials such as yellow tuff, bricks, and conglomerate, with the average plant cover considerably higher on vertical surfaces and at western and southern exposure. In fact, the vertical surfaces show a higher abundance of species with the highest hazard index (HI > 5), such as Artemisia arborescens, Rubus ulmifolius, Reichardia picroides, Capparis orientalis, Pistacia lentiscus, Matthiola incana, and Ficus carica, while Ailanthus altissima grows almost exclusively over horizontal substrates. Regarding the substrate, some species (e.g., Rubus ulmifolius and Rhamnus alaternus) are not affected by the type of material, unlike other species, such as Artemisia arborescens, Matthiola incana, Spartium junceum, and Ailanthus altissima, which mostly grow on yellow tuff. So, based on the observations, herbaceous species colonize low porous lithotypes such as basalt, mosaic, and marble, while tree species grow preferably on volcanic rocks and materials characterized by a strong porosity that helps to retain more water. Moreover, woody plants (phanerophytes) are present mostly on western and eastern exposure; in contrast, herbaceous species (hemicryptophytes and therophytes) prefer the south-facing slopes.
Hosseini et al. [32] surveyed the monuments of the Pasargadae World Heritage Site in (Iran) to identify the substrate preference of plants in colonizing stone surfaces. There are two types of limestones called beige stone (BS), a pure aspartic limestone composed by calcite and dolomite, and green-gray stone (GGS), an argillaceous limestone small quartz and non-swelling clay minerals. Some species showed a clear preference for GGS: Glycyrrhiza glabra, Senecio glaucus, Crepis sancta, Euphorbia dracunculoides, Poa bulbosa, Medicago persica, Lepidium draba, Lactuca serriola, Tragopogon graminifolius, etc. Other species, instead, showed propensity for BS: Adonis aestivalis, Peganum harmala, Papaver argemone, Scandix stellata, Euphorbia sororia, Ficus johannis, and Nonea longiflora. On the basis of the various observations, a high number of species with a low abundance were observed on Beige stone; conversely, on Green-Gray stone, the number of species with a low abundance was particularly lower and species with a higher abundance were more numerous, which proved its suitability for plant colonization.
Another study to evaluate the relationship between plant biodiversity and exposure and building materials was carried out for three historical Calabrian (Southern Italy) churches by Mascaro et al. [8]. The facades of Santa Maria della Serra and Santissima Annunziata consist of white-yellowish or reddish fossiliferous calcarenites, while Santa Maria della Pietà is composed of carbonate rock. Among the 27 species recorded, 16 were present on vertical surfaces, all Geophytes and chamaephytes on horizontal surfaces, while therophytes were instead on vertical surfaces. Parietaria judaica was the only species present at all three sites. Regarding the hazard index values, only the site of Santa Maria della Pietà presented a high average value of HI (HI 6.3) due to the presence of Ailanthus altissima (HI 10), Ficus carica (HI 10), Rubus ulmifolius (HI 8), and Sambucus nigra (HI 8). At any rate, the colonizing species of the three sites suggested that the different substrates did not influence the growth of plants. Moreover, although previous studies have shown that most plants dwell on horizontal surfaces for the best growing conditions, in the case of the Calabrian churches, more species have been observed on vertical surfaces, which is in agreement with Motti et al. [27]. Nonetheless, in contrast with the abovementioned case study, therophytes were more common on horizontal surfaces, while geophytes and chamaephytes were on vertical surfaces.
It is actually in these microsites that birds and/or other organisms (e.g., ants) prefer to transport seeds during seasons characterized by high temperatures. The hemicryptophytes have been largely checked on the stone artifacts, and the seedy plants that were disseminated more involved: Ajuga chamaepitys, Verbascum sinuatum, Stipa holosericea, Noae mucronata, Sanguisorba minor, Descuriana sophia, Mercuralis annua, Scorzenora mollis, Scrophularia libanotica, Rubia tinctorum, Parietaria lusitanica, Alkanna orientalis, Alkanna tinctoria, Euphorbia macroclada, Isatis glauca, Lactuca scariola, Poa bulbosa, Scandix stellata, Galium verum, Lamium amlexicaule, Lepidium perfoliatum, Veronica triphyllos, Reseda lutea, Asperugo procumbens, and Bromus tectorum. After the growth of herbaceous plants, some habitats, in particular the roof section made of andesite, have improved and changed to host even small woody species including Capparis spinosa, Thuja orientalis, Berberis crataggina, Cerasus avium, Prunus armenica, and Prunus domestica.

3. Factors Affecting Biodeterioration

There are numerous ecological factors, such as physical, chemical, or biological factors, that condition the growth and the life of an organism, following generally two laws underlying ecology.
“Liebig’s law of the minimum” (1840) governs nutrient limitation, stating that in conditions of stationary equilibrium, the essential substances available in quantities close to the minimum necessary tend to become limiting (Van der Berg) [37]. At the same time, an environmental factor may represent a minimum or maximum limit for a species, determining the tolerance of the species to this factor. This is the Shelford’s law (or the law of tolerance, 1913) considered as an extension of the previous one, since not only the minimum value but also the maximum value may be a critical factor [29][38].
Generally, the most relevant environmental factors for the growth of an organism are water, temperature, light, and nutrients, because their values are often close to the minimum limit for the survival of the species. This explains why climatic factors play a primary role in biodeterioration processes [29].
Water accumulating in buildings is among the main causes of decay [39]. Its availability is a fundamental parameter which determines the initiation of microbial susceptibility and colonization, biofilm formation, and subsequent biological degradation. Moisture content in building stones is the result of a dynamic equilibrium between the material and the environment, and it is influenced by the movement of water that goes from inside to outside of the masonry and vice versa [40][41]. Water can reach building materials in several ways, from driving rain, capillary water rising from underground, run-off from the roof, and condensation of air humidity. Capillary rise is the main mechanism for water to infiltrate a building material, hence capillary water is very important for the establishment of microorganisms [39][40][42]. Moisture acts as a substrate for the growth of living organisms such as bacteria, fungi, or algae with consequent physical and chemical damage. For these reasons, it is important to find prevention strategies to avoid problems related to humidity, since eliminating the already existing problem is complicated, especially in structures of historical value [39].
Other important factors involved in the deterioration of stones are related to the substrates and construction materials, from a physical (roughness and porosity) and chemical (mineral composition and surface pH) point of view. In this regard, it is useful to mention the concept of biorecectivity proposed by Guillitte [9], considered as “the totality of material properties that contribute to the establishment, anchorage, and development of fauna and/or flora” or as “the aptitude of a material to be colonized by one or several groups of living organisms without necessarily undergoing any biodeterioration”. This concept originates from the term “susceptibility” and involves an ecological correlation between the colonizer and the substrate. Materials with high porosity have a high bioreceptivity index (BI), as more water is retained inducing worsening of the deterioration process [9][43]. Although a standard laboratory protocol for estimating stone biocerectivity and defining its index has not yet been established, Vázquez-Nion et al. [44] proposed a BI for granitic rocks including two components: BIgrowth that quantifies the extent of the biological growth and BIcolour that quantifies the color change undergone by the stone due to the colonization. BI values are adapted to a scale that allows the qualitative classification of lithotypes in a simple and easily comprehensible form.
Bioreceptivity cannot be described as a static property, rather it varies for each stone material according to different stages of deterioration. Thus, Guillitte [9] defined three types of bioreceptivity: “primary or intrinsic bioreceptivity”, which is related to the initial potential of biological colonization of sound stone, “secondary bioreceptivity”, which refers to the potential of biological colonization of weathered stone, and “tertiary bioreceptivity”, which is the colonization potential of a stone material subjected to conservation treatments [9][45].
Some researchers think that roughness has the most significant influence of all the properties. Firstly, microorganisms and organic materials that are transported to the building by wind and water adhere to the substrate. Then, especially when the substrate color is lighter, the surface roughness is directly proportional to the adsorption of solar radiation, thereby influencing the surface temperature [14]. In a study conducted by Korkanç and Savran [14], the mineralogical and engineering properties of the stones used in six historical buildings located in central Anatolia (Niğde region) were determined to describe the great impact that these characteristics have on plant growth. According to the data obtained, ignimbrites showed the highest water absorption and porosity rates and the highest surface abrasion values. Tuff showed higher compressive strength values than ignimbrites, but lower abrasion and compressive strength values were recorded for fine-grained tuffs.

This entry is adapted from the peer-reviewed paper 10.3390/plants11243429

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