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225-A1678 8/6/01 10:38 AM Page 557 SECTION II / MAN AND THE ENVIRONMENT PIER LUIGI NIMIS Department of Biology University of Trieste Trieste, Italy Artistic and Historical Monuments: Threatened Ecosystems Italy has the largest heritage worldwide in historical monuments, ancient books, parchments, paintings, sculptures, ancient tapestries, and textiles. Some are kept outdoors, some indoors, and others even under water; their preservation is a responsibility of all Italians to mankind. These works of art are attacked by many organisms, and the biologist regards them as outright ecosystems. Open-air monuments mostly host photosynthetic organisms, such as cyanobacteria, algae, lichens, mosses, and higher plants, whereas those stored indoors are attacked by heterotrophic organisms, such as bacteria, fungi, and insects. Biology can help their conservation and restoration in that it can identify such organisms and the ecological conditions that allow their growth. This knowledge allows the biologist to judge the effectiveness of restoring treatments. Much has been done and much more still remains to be done. ◗ ................................................ Works of Art as Ecosystems The richness and variety of Italian artistic heritage is unequalled worldwide. All Italians are responsible for its conservation. However, it is not an easy task: Physical, chemical, and biological agents attack any item. Often, changes thus produced are irreversible. Living beings play an important part in this process; an ancient illumination in a library, a Roman statue in an archeological site, and a fresco or a painting in a church are all under aggression. Many organisms may destroy them or change them enough to mask the artist’s idea. Thus, the biologist’s knowledge can prevent these works of art from disappearing. Illuminations, statues, and paintings can be viewed in a biological light: They are ecosystems, with primary pro- PART TWO / DISCOVERY AND SPOLIATION OF THE BIOSPHERE ducers, decomposers, and predators, like any African plain seen in many television documentaries. An imaginary documentary titled “The Statue Ecosystem” would unveil a new and remote world in which no acacias grow and in which no elephants, hyenas, lions, or hunting dogs dwell. Instead, this ecosystem includes primordial cyanobacteria; weird colonies of algae (the sea is not the only place in which they live), attacked by squadrons of sneaky fungi; unearthly lichen landscapes; and tiny moss forests, inhabited by horrible creatures that human eyes have rarely seen— everything from sleepy herbivorous tardigrades to ferocious predator carabids. Therefore, a statue is in itself an environment in which all ecological phenomena can be observed: competition, host–parasite and prey–predator relationships, and succes- 557 225-A1678 8/6/01 10:38 AM Page 558 PIER LUIGI NIMIS sions. It is also the substratum for the complex reactions of biogeochemical cycles, such as nitrogen, carbon, and sulfur cycles. Restoration ecology is a recent field of study in which much still remains to be done. Italy holds a prominent position in this field, if not in others. The available knowledge is based on the work of many biologists, who work for prestigious institutions that study the decay and conservation of works of art. Examples of such institutions are the Istituto Centrale per il Restauro (Central Institute of Restoration), the Istituto per la Patologia del Libro (Institute for Book Pathologies), the Istituto per la Ricerca sul Legno (Institute for Wood Research), various centers of the Consiglio Nazionale delle Ricerche (National Council for Scientific Research), the Monuments and Fine Arts Office research laboratories in Bologna and Venice, university departments, and other research centers. This article aims to observe statues, churches, illuminations, and parchments from the biologist’s point of view; thus, the material traces of our cultural roots will become tiny, complex, and fragile ecosystems, threatened with destruction by the same laws of nature that generated them through human intelligence. ◗ ................................................ Biodeterioration of Works of Art 558 ................................................ ◗ Biodeterioration is the name biologists give to the damage that biological agents produce on various materials. Two types of organisms are involved: autotrophic and heterotrophic. The former— cyanobacteria, algae, lichens, mosses, and vascular plants— draw energy from sunlight through photosynthesis; thus, they do not use the substratum as an energy source but as a mere support or, at most, as a source of micronutrients or water or both. Therefore, these organisms can grow on inorganic substrata, such as monuments, stained-glass windows, or metal objects, when these are exposed to sunlight. On the other hand, heterotrophic organisms classified as decomposers (such as bacteria and fungi), herbivores, and predators (usually snails and insects) draw energy by decomposing organic molecules. These organisms live on organic matter (other organisms, paper, wood, parchment, and some types of paint) used as a direct source of energy irrespective of the lighting conditions; this makes them the primary biodeterioration agents for works of art kept indoors. Heterotrophic organisms often produce irreversible damage when they feed directly on artwork made of organic matter, whereas they are less involved in the biodeterioration of outdoor monuments. Autotrophic organisms, on the other hand, can cause both reversible and irreversible damage. For example, the color changes that algal patinas cause on church façades are easily restored— when not associated with physical or chemical damage— by removing the algae. Both hetero- and autotrophic organisms mainly bring about two types of biodeterioration: (i) physical actions (disintegration), such as the effect of tree roots on marble monuments, physical disruption of rock by lichens, and holes dug by insects in wood, and (ii) chemical actions (decomposition), such as the irreversible alterations that fungi cause to fabrics, paper, and wood, the chromatic changes due to fungal and bacterial pigments, and the solution of calcareous rocks by endolithic cyanobacteria and lichens. Biodeterioration can be both direct and indirect. The former is caused by organisms that permanently use a particular substratum for support or nourishment, such as the destruction of books by fungi and bacteria or the perforation of submerged columns by mollusks. Indirect biodeterioration is caused by organisms whose ecology is not tied to a particular substratum; examples are guano deposits on statues and monuments that, incidentally, can give rise to direct biodeterioration by other organisms or chemical and physical alterations. At the extreme, even human vandalism can be considered indirect biodeterioration. There is a marked ecological difference between works of art kept outdoors and those kept indoors. The former are attacked primarily by autotrophic organisms, which grow on inorganic materials (stone, glass, and metal). The latter, made entirely or in part of organic material (paper, parchment, wood, glue, and paint), host heterotrophic organisms. Outdoor monuments are the substratum for complete miniature ecosystems, inclusive of primary producers (photosynthetic organisms); on the contrary, indoor artwork is a “halved ecosystem” in which decomposers prevail. Ecological Study of Outdoor Monuments The use of inorganic constructing materials, such as stone, bricks, and mortar, throughout its history has left Italy with an amazing architectural heritage that endures through time. Other cultures, such as those of the Far East, having built their monuments in wood, are left with a much more deteriorated or recent memory of the past, mainly because of the action of biological agents. Nevertheless, Italian monuments are still prone to physical, chemical, and biological deterioration because they are mostly made of calcareous rock such as marble. Glass, of siliceous nature, is another lithic substratum, but it is not subject to colonization by microecosystems, except when air humidity levels are high. This condition is rare in Italy, but the stained-glass windows of French churches, for example, exposed to humid Atlantic winds, are attacked by fungi, lichens, and algae that discolor them or make them irreversibly opaque. Monuments built in stone are mainly colonized by photosynthetic organisms— cyanobacteria, algae, lichens, mosses, and vascular plants—that use the substratum uniquely as a support to reach light, their primary source of VOLUME IV / THE LIVING WORLD 225-A1678 8/6/01 10:38 AM Page 559 ARTISTIC AND HISTORICAL MONUMENTS energy. Sometimes, though, the colonization of stone surfaces starts with chemoautotrophic organisms, such as particular types of bacteria, which are able to draw energy from inorganic substances without light. These organisms prepare the substratum for the development of various series of biological successions. Heterotrophic organisms arrive later because they need to feed on the organic substances that autotrophic organisms have produced. These organisms are less important in the biodeterioration of lithic substrata and they will be discussed only with regard to organic substrata preserved indoors. As in any ecosystem, biological colonization of monuments depends on a variety of factors, such as exposure, substratum, and the availability of nitrogen compounds. Studying the ecology of the communities that invade monuments can help identify the factors that favored their growth, thus contributing to the planning of strategies for restoration and preservation. Bacteria Bacteria that colonize monuments are mainly autotrophic, such as sulfur and nitro- and cyanobacteria; the alterations that they cause are of a chemical nature. Nonphotosynthetic sulfur bacteria convert limestone into gypsum (especially in sulfur dioxide-polluted areas), irreversibly covering the surfaces of statues and capitals with horrible black crusts. Nitrobacteria cause less damage, although they can alter lithic substrata by producing sulfuric and nitric acids. Nitrifying bacteria are the first to colonize stone surfaces; they mainly produce nitrates, which often foster the growth of other microorganisms including lichens. Cyanobacteria were among the first prokaryotic organisms to colonize land; they have chlorophyll and play an important role in the deterioration of stone surfaces, especially calcareous ones. Some even penetrate beneath the surface, producing typical erosion phenomena; others become encrusted in thick calcium carbonate secretions, deforming their substratum. Free from competitors, many coccal cyanobacteria cover in dark patinas large vertical areas exposed to sunlight, such as walls facing south. In addition to the esthetic damage, these dark patinas, in the Mediterranean area, cause the temperature to increase by up to 8°C higher than that of the noncolonized, lighter-colored surfaces, facilitating further physical deterioration (Garty, 1990). Cyanobacteria need water in a liquid state to carry out photosynthesis. In their search for the long-lost and nearly lunar world they conquered alone, cyanobacteria colonize hot, arid, and sunny surfaces, with water flowing over them for brief periods; all these conditions can be found on any vertical surface facing south and washed down by rain. Cyanobacteria cells, enclosed in gelatinous secretions, can retain water for long periods, thus delaying desiccation of the stone surface and favoring chemical alterations, such as the solution of calcium carbonate. Nitrifying bacteria, like PART TWO / DISCOVERY AND SPOLIATION OF THE BIOSPHERE cyanobacteria, are able to fix atmospheric nitrogen, enriching the surface of statues and bas-relieves with nutrients for further harmful colonizing organisms. Algae The algae living on works of art are green algae, ancestors of higher plants. They are simple, unicellular, or threadlike organisms with few defenses against desiccation. Algal patinas, frequent on monuments, are among the first to colonize stone and glass surfaces after bacteria, but only damp, shady surfaces allow them to grow and cause damage. Typical places are usually the base of monuments or surfaces facing north. However, algae produce only chromatic alterations, coloring the substratum green or red-orange (if the algae are of the genus Trentpohlia). These patinas can be easily removed by using biocides or by mechanical means. Nevertheless, algae produce carbon dioxide, retain water, and often secrete chelating agents, such as aspartic acid, citric acid, and oxalic acid, that alter—if only slightly— the substratum. On stone surfaces, damage is limited to the most superficial layer and is usually repaired easily; on the contrary, on stained-glass windows, small chemical alterations can result in irreversible esthetic damage. Lichens Lichens are a symbiotic association between algae or cyanobacteria and fungi. These organisms are certainly the most conspicuous and important colonizers of outdoor monuments, including both glass and lead surfaces of ancient stained-glass windows; only heavy pollution can prevent their growth. The most noticeable effects of lichen colonization are of a chromatic nature: Italian archeological sites and parks are populated by mythological heroes, venuses, nymphs, and horses whose noses are Caloplaca red, whose heads are Candelariella yellow, and whose bodies are Aspicilia gray. The north façade of the Orvieto duomo is an example of the esthetic damage produced by lichens. The duomo was built with dark basalt and light-colored limestone in alternate bands. The dark bands are colonized by light-colored species, whereas the light-colored bands host orange or dark species (Nimis and Monte, 1988). The result is bizarre and may not be that unpleasant, but it is certainly far from what the artist had in mind (Fig. 1). However, threat due to lichens may be much more severe: They can produce much worse damage, such as major alterations of stone surfaces through biogeophysical and biogeochemical processes. Biogeophysical alterations are caused by the penetration of fungal hyphae (the thin filaments that make up the fungus) beneath the stone surface and by the contraction and expansion of the lichen subsequent to desiccation and rehydration (Seaward, 1988). These contraction– expansion cycles are due to the lichen content in gelatinous and mucilaginous substances, whose volume strongly depends on water content. These move- 559 225-A1678 8/6/01 10:38 AM Page 560 PIER LUIGI NIMIS a b FIGURE 1 (a) The south façade of the Orvieto duomo not colonized by lichens, with the typical alternate bands of dark basalt and light-colored limestone. (b) The north façade of the Orvieto duomo: three bands, two made of basalt and the central one of limestone, extensively colonized by lichens. ments result in the lifting of the marginal part of the lichen and in a “peeling” effect on the stone surface, with the detachment of superficial layers. The depth of penetration of the hyphae depends on the composition of the substratum, the type of lichen (foliose or crustose, epilithic or endolithic), and the species. The symbiotic algae rarely penetrate deeper than 2 mm and can usually be found less than 1 mm from the stone surface; the fungal hyphae may penetrate up to 15 mm in very porous carbonate rocks, although these too usually penetrate no more than 2 or 3 mm. The hyphae can at times penetrate through the mineral crystals, but more often, especially in siliceous rocks, it is much easier for them to dig their way between the crystals. Endolithic lichens are a particular case: Their growth 560 FIGURE 2 Scanning electron micrograph of the endolithic thallus of the lichen Verrucaria baldensis in calcareous rock, partially decalcified in acetic acid. The penetration of the fungal hyphae in the rock is evident (reproduced with permission from Pinna et al., 1998). takes place entirely inside rocks, usually calcareous ones, and they are often invisible to the naked eye because their color is identical to that of the rock (Fig. 2). Their fruiting bodies, however, protrude on the surface, leaving small VOLUME IV / THE LIVING WORLD 225-A1678 8/6/01 10:38 AM Page 561 ARTISTIC AND HISTORICAL MONUMENTS hollows as they fall; this effect is called pitting. The small holes, measuring 0.2 –2 mm across, are a typical weak spot for chemical aggressions, such as the solution of calcium carbonate in water or the penetration of pollutants. Little was known of these organisms before the studies carried out by Tretiach (1998). Some of the findings are truly unexpected: The amount of chlorophyll per unit area enclosed in rock may be the same as that found in tree leaves, but the primary productivity of an endolithic lichen is definitely smaller. The growth of these lichens is often very slow— not more than a fraction of a millimeter per year. Strange as it may seem, many statues, bas-relieves, or cathedral walls live, breath, and carry out photosynthesis; they contain as much chlorophyll as the trees in the parks in which they are situated. The chemical alterations lichens produce are due to three substances they secrete: carbon dioxide, lichen compounds with complex properties, and oxalic acid. Carbon dioxide, produced through respiration, when in an aqueous environment produces an acid solution that, although weak, can solubilize relatively insoluble salts such as calcium and magnesium carbonates in limestone, dolomite, a variety of marbles, and plasters that contain carbonates. All these are converted into much more soluble bicarbonates. This process is common to all organisms, and in the case of lichens it is not particularly relevant to biodeterioration. Many of the organic compounds secreted by lichens, commonly called lichen acids, have complex properties due to polar chemical groups that can chelate metallic cations by donating electron pairs. Lichens produce a variety of chelating substances in large amounts, and they often take on rusty colors due to iron accumulation, especially on siliceous rocks. Oxalic acid is one of the most active acids in metal deterioration and in cation exchange. Different lichen species have different oxalate production capacities; moreover, the type of oxalate produced depends on the cations available in the environment—that is, on the mineral composition of the substratum. Calcium oxalate is found in lichens in two different crystals: whewellite and weddellite. When secreted, calcium oxalate forms an extracellular insoluble deposit. Species obliged by their physiology to live on calcareous substrata have much higher calcium oxalate levels than species living on siliceous substrata. Lichen production of calcium oxalate has given rise to heated debate among restoration ecology experts. The difference between a “new” stone surface and the “age patinas” that cover ancient artwork is evident: Many restorations have been criticized for removing these patinas. When thus restored, churches, bas-relieves, and statues take on an almost modern appearance, as if they were made of plaster. Many perceive this type of restoration as artificial compared to the passing of time. The vast yellowish or brownish films (time patinas) are almost totally made of calcium oxalate, but PART TWO / DISCOVERY AND SPOLIATION OF THE BIOSPHERE their origin is still open to debate. There have been two hypotheses put forward. First, calcium oxalate derives from organic substances used in the past as protective treatments or for esthetic purposes or both; Second, calcium oxalate is secreted by lichens and, incidentally, by bacteria and fungi. Both hypotheses need to be studied further, but it is possible that both are correct, depending on the case in question (Lazzarini and Salvadori, 1989). Bryophytes and Higher Plants In average humidity conditions, the colonization of outdoor monuments usually starts with nitrobacteria, followed by various stages of lichen vegetation or, if humidity conditions allow it, by algal patinas. The growth of mosses, ferns, and higher plants is also delayed because of the need for soil accumulation. In certain conditions, though, this accumulation is fast, such as when dust or stone weathering products are deposited on horizontal surfaces or between stones. Ancient brick structures are typical examples: As soon as roots find their way between bricks, the resulting mechanical effects can be devastating (Caneva and Roccardi, 1991). Many circles of walls in Rome are emblematic in this respect. Typical higher plants found here are pellitories, common throughout Italy, or capers, typical of the Mediterranean part of Italy. Fig trees, ailanthus, ivy, and other trees or bushes make their way between bricks, taking advantage of weak spots in the structure or of the poor resistance of mortar. Their roots also produce chemical alterations by secreting acid substances, but mechanical effects are by far the most dangerous. In some archeological sites, tree roots penetrate in underground cavities, causing irreversible damage to buildings and frescos. In addition to roots, ivy clings to the substratum with its aerial rootlets, producing the detachment of vast portions of superficial layers of construction stones (Caneva and Salvadori, 1989). Occasionally, the presence of higher plants in archeological sites may be useful. In areas where the water table is close to the surface, the flooding of underground buildings is frequent. Planting trees with high evaporation rates is an effective way to lower the water level. Eucalyptuses, for instance, are among the most efficient “biological pumps” known to man. Moreover, a line of trees can be a windbreak, modifying the microclimate, reducing evaporation or direct solar radiation, hindering the wind’s weathering effects, and filtering nitrogen compounds from possible nearby cultivated land. Humble bryophytes (mosses and liverworts), having no roots, are less dangerous. Nevertheless, because they are able to retain large amounts of water (12 liters/m2 or more), they foster biogeochemical deterioration (Fig. 3). Bryophytes also tend to accumulate soil in the form of dust and organic residues. As in any typical primary succession, higher plants thus colonize the substratum. 561 225-A1678 8/6/01 10:38 AM Page 562 PIER LUIGI NIMIS FIGURE 3 Top of the head of a limestone statue in the Villa Manin Park in Passariano (Udine) covered by the nitrophilous lichen Xanthoria calcicola (yellow) and by the moss Grimmia pulvinata (gray) (photo courtesy of S. Del Bianco). ◗ ................................................ in worship practices and religious culture. However, there is very little awareness that in 1 year, one single candle may cause more damage than whole generations of fungi, bacteria, and algae. The gloomy colors of many ancient paintings are not the work of depressed painters but are due to candles lit with the best of intentions; they are certainly not meant to disfigure the object of worship. The stubborn tradition of lighting candles in Italian churches is totally unacceptable today. This problem, complex in many ways, should be a priority for the curie and the Monuments and Fine Arts Offices. In addition to man and his ominous candles, indoor environments host swarming battalions of heterotrophic organisms ready to attack any item made of even minimal quantities of organic matter. Wood, paper, parchments, leather, and cloths are the refectory of legions of bacteria, fungi, and arthropods. Not even paintings or frescos are safe, being composed of delicious specialties such as amid, gums, sugars, glycerin, various types of gelatins, linseed oil, and egg yolk. Ecological Study of Indoor Artwork It may seem that works of art kept in museums, churches, and houses are more protected from biological aggression than outdoor monuments. However, this is true of artwork made of inorganic matter only: The best way to preserve a statue is to keep it in a museum. Any item made of organic matter, if kept outdoors, has a grim and short life compared to a statue; many physical, chemical, and biological agents act synergistically and rapidly destroy it. This is why books, parchments, fabrics, and wooden objects—artwork all or in part made of organic matter—are kept in closed and sheltered places. Thus, some of the ecological factors that allow the growth of damaging organisms may be kept in control. Simply screening off sunlight eliminates all autotrophic organisms, control over temperature and humidity helps limit the growth of bacteria and fungi, and insect aggressions are easily reduced by disinfestation. Nevertheless, even indoors artwork is not perfectly safe: Composite armies of heterotrophic organisms are ready to attack every time control over environmental conditions fails perfection, and a perfect control is far from easy on a broad scale. Before providing a review of the troops responsible for biodeterioration, one of the worst examples of indirect deterioration deserves to be mentioned. It is before anyone’s eyes, in most churches; it may not attract much attention and, paradoxically, it is caused by intelligent and wellmeaning men. It is striking that today most churches of Venice—famous throughout the world for its masterpieces of painting—have endless lines of pitiless candles piously shedding horrible patinas of lampblack on defenseless blackened paintings or, even worse, on newly restored paintings. The tradition of lighting candles is deeply rooted 562 Wood Lignin, cellulose, and hemicellulose are among wood’s principal components. Lignin is the most resistant to biological aggression; its worst enemies are fungi, especially ascomycetes. Also, newly synthesized cellulose is not easily attacked by biological agents, but a long exposure to physical and chemical agents engenders amorphous spots that facilitate aggression by microorganisms. Among the most important are the basidiomycetes Serpula lacrymans, Poria spp., and Coniophora puteana; all have enzymes that convert cellulose in glucose, leaving a brownish residue of nondecomposed lignin (Allsopp and Seal, 1986). Hemicellulose is the least resistant of the three components: It is easily hydrolyzed by bacteria and fungi. Conservation of wood artwork outdoors is a lost battle: The proliferation of bacteria, fungi, and insects is difficult to control effectively and for a long period of time. Indoors, the intensity of microbiological aggressions mostly depends on air humidity. Asco- and deuteromycetes attack wood items kept in humid underground rooms; wood becomes soft if damp and extremely fragile if dry. The humidity of dry wood is in equilibrium with the relative humidity of the surrounding environment; microbiological attacks are relevant only if water content is higher than 20%. Therefore, adequate air-conditioning is the best defense against bacteria and fungi. Insects, however, are still free to attack. Coleopterans, lepidopterans, termites, hymenopterans, and many others can produce much damage to dry wood, not easily attacked by bacteria and fungi. These attacks are carried out with an ingenious biological trick. Most insects, because they are unable to synthesize the enzymes necessary for breaking up lignin and cellulose, host bacteria and fungi (which do produce these enzymes) in their intestine, in VOLUME IV / THE LIVING WORLD 225-A1678 8/6/01 10:38 AM Page 563 ARTISTIC AND HISTORICAL MONUMENTS which the humidity conditions necessary for the growth of such microorganisms is provided. are important differences between fabrics of vegetable derivation (linen and cotton) and fabrics of animal derivation (wool). Paper Cellulose is the principal component of paper, together with lignin, hemicellulose, pectines, various types of wax, tannins, and proteins in different proportions, depending on the type of paper and on the time of fabrication. It is possible that paper fabricated in the Middle Ages was much richer in cellulose, and therefore less prone to biological attacks, than most paper fabricated in recent times (Kowalik, 1980). The principal agents of biodeterioration of paper are bacteria and fungi, and again the level of aggression depends on the water content of substratum. Books kept in dry environments survive longer than those kept in highhumidity conditions. The attacks of fungi and bacteria appear at first as stains or as a discoloration of ink. Stains are differently colored depending on the type of organism and on the type of paper. The discoloration of ink, on the other hand, is due to tannase, an enzyme—synthesized by some fungi of the genera Aspergillus and Penicillium—that catalyzes the hydrolysis of gallotannate. Bindings, which may contain hygroscopic substances, are among the first parts of a book to be damaged. Prolonged growth of fungi and bacteria causes paper to become felt-like and fragile. Its characteristics are altered (e.g., its acidity), fostering the growth of other species of fungi and bacteria more suitable to the new ecological conditions. Even in books kept for centuries in libraries, biologists can study ecological successions similar to those that, in “normal” ecosystems, turn meadows into forests. Books that undergo floods, such as those damaged in the Florence flood in 1966, are a particular case. Pages become cemented in solid blocks and are not easily separated. This is due to the rapid growth of bacteria and fungi that occurs during imbibition. These organisms rapidly degrade cellulose, producing oligosaccharides (with mucus-like properties) which glue the pages together, making the book totally useless. Today in Italy, too many ancient books and papers are kept in ecological conditions that turn them into ecosystems at risk. Even in the rare cases in which rooms are adequately air-conditioned, insects are still dangerous: It is exactly in these conditions that these organisms have their ecological optimum. Among the most dangerous is a devilish little insect that goes by the graceful name of silverfish (Lepisma spp.), commonly found in houses. This small, flat animal can penetrate virtually anywhere; it easily slips inside books, merrily feasting on pages that no one will ever be able to read again. Other insects, instead of eating paper, feed on the fungi and bacteria that live in books, especially close to bindings; their excrements are a rich source of food for saprophagous bacteria and fungi. Similar processes may be observed in the biodeterioration of cloths, although there PART TWO / DISCOVERY AND SPOLIATION OF THE BIOSPHERE Leather and Parchment Although paper is of vegetable derivation, leather and parchment are of animal derivation and therefore have a high protein content. Organisms that decompose such materials must synthesize specific proteolytic enzymes (proteases and peptidases). Italian culture owes some of its most ancient papers to parchment, which is made from sheep or goat skin (the best were made using fetus skins). Parchment is mainly composed of collagen, which is hydrolyzed by specific enzymes (collagenases) synthesized by bacteria of the genus Clostridium (Kowalik, 1980). Collagen, however, is often depolymerized during the processing of parchment; thus, it may be decomposed by nonspecific proteolytic enzymes, synthesized by many bacteria and microfungi. Leather, whose chemical properties are similar to those of collagen, undergoes similar decomposition processes. During processing, though, leather is often treated with tannins, which inhibit biological attacks, especially those of bacteria. As with other materials, insects may still strike; especially dermestids and tineids can banquet on tannintreated leather. Fabrics Ancient fabrics consist of fibers of plant or animal origin, which have different chemical composition. Vegetable fibers mainly consist of cellulose, whereas animal fibers mostly consist of protein compounds such as keratin in wool or sericin in silk. The former are mainly attacked by cellulose-hydrolyzing fungi such as deuteromycetes; the latter can be attacked by many bacteria and fungi, actually more effective in the deterioration of wool than of silk. Again, the control of relative air humidity can prevent part of the damage. The situation is quite different with insects: Everyone is familiar with the damage moths may produce in wool. Therefore, it is not surprising that the preservation of huge arras kept in Italian churches and museums should be quite difficult; obviously, hanging bags full of mothballs is not a solution. Paintings Wood, paper, leather, parchment, and cloth have relatively homogeneous compositions. On the contrary, paintings are composed of a wide variety of materials—so wide, in fact, that their biodeterioration is quite fascinating to biologists. Chemical composition of paintings varies in layers. The undermost layer is often wood—and its biodeterioration is that typical of wood items—but it may also be made of lime or plaster, covered with animal or vegetable glues. Whatever the type of material or biodeterioration process, damage to the base of the painting can be quite serious, 563 225-A1678 8/6/01 10:38 AM Page 564 PIER LUIGI NIMIS FIGURE 4 Detail of fungal attack on a painting on canvas (photo courtesy of O. Salvadori). 564 FIGURE 5 White patina on the frescos of an Etruscan tomb in Tarquinia due to the growth of actinomycetes (reproduced with permission from Caneva et al., 1991). bini et al., 1988). Many murals, situated in damp churches, crypts, caves, and tombs, are disfigured by whitish or grayish patinas of these fungi, which metabolize nitrites and nitrates and reduce sulfates (Fig. 5). ................................................ ◗ resulting in cracks in the painting. Usually, the undermost layer of paintings is a canvas of vegetable nature or, as in the case of watercolors, paper. In these cases, the biodeterioration agents are those typical of fabrics and paper. Canvas is usually covered with colors of mineral derivation, often diluted with animal or vegetable oils, glues, gelatins, etc. Finally, the protective varnishes, which cover paintings and are often renewed throughout the years, are mostly made of organic matter. Therefore, paintings offer a rich and varied menu to many heterotrophic organisms—bacteria, fungi, and, fortunately, few arthropods. A painting is therefore one of the most interesting “artistic ecosystems” among those found indoors. Fungi of the genera Aspergillus, Penicillus, and Trichoderma feed on tempera and color binders; Phoma and Aureobasidium destroy oil colors; Geotrichum feeds on casein binders; and Mucor and Rhizopus attack various types of glues (Ionita, 1971). Therefore, the type of biological aggression depends on the substratum. Also, biodeterioration may concern all the different layers of paintings or be limited to the color layer, depending on the type of colors and diluents used. Usually, the undermost layers of paintings are those at risk of biodeterioration, although many species of organisms also attack colors, damaging them irreversibly (Fig. 4). Bacteria and fungi are mainly active in conditions of high air humidity levels, whereas insects prefer dry environments and tend to limit their attacks to the parts in wood and paper of paintings (the base or the frame). Frescos and other inorganic types of murals are a special case because they are attacked by actinomycetes (Giaco- Ecological Study of Submerged Artwork Italian coasts conceal a huge historic and artistic patrimony. In the course of centuries, hundreds of ships have sunk with their precious loads, and only recently has Italy started to discover this treasure of historical heritage. To study biodeterioration processes in an aquatic environment, a close examination of marine ecology is necesary, and this is beyond the scope of this article. Therefore, what follows is only a brief account of such processes. It is obvious that almost all organic matter left for long periods of time under water has a short life. Books, parchments, and cloths, once under water, are lost forever. The only exception is wood, especially that of ship hulls. In a terrestrial environment, lignin is mainly attacked by bacteria, fungi, and insects. Millions of years of evolution have brought about organisms able to decompose wood in the environment in which this is frequent—the terrestrial environment. In an aquatic environment, especially at great depths, wood is rare; in natural conditions, wood at sea mostly floats. Even under water, some bacteria and fungi are able to decompose wood, although less effectively than in a terrestrial environment. Aquatic bacteria and fungi are both aerobic and anaerobic; various species produce different types of damage, such as superficial erosion, cavitation, and the formation of small holes. Occasionally, especially in shallow water, submerged wood may become covered in algal colonies, which do not much alter their substratum. Greater damage is caused by animals. The sea may not be populated by insects, but their absence is amply compen- VOLUME IV / THE LIVING WORLD 225-A1678 8/6/01 10:38 AM Page 565 ARTISTIC AND HISTORICAL MONUMENTS sated by the abundant presence of mollusks and crustaceans, which may cause serious damage to submerged artwork. Mollusks involved in biodeterioration are mainly of the genera Teredo, Bankia, and Martesia; they dig deep holes in wood structures. Crustaceans are mostly isopod genera, and they cause wood to become extremely fragile. Most of these organisms, however, are active only when wood is close to surface. In the past, these animals were sailors’ nightmares because the hulls of ships were made of wood. Wrecks, kept at greater depths by the weight of their loads, are infrequent items in marine ecosystems and therefore less prone to biological aggression. Even artwork made of stone is subject to biological attacks in marine environments. The biodeterioration produced by mollusks is the most devastating. These organisms can perforate rock, digging holes as deep as 10 cm, through mechanical action or by secreting acid substances. Roman columns near Pozzuoli are a well-known example of this phenomenon. Because the area is subject to bradyseism, these columns have been alternatively above and under water through the centuries. Through the holes left in the columns by marine organisms, it is possible to reconstruct the raising and lowering movements of the ground through time. Other organisms, such as some species of calcareous algae, thickly encrust with calcium carbonate the surfaces of submerged objects. FIGURE 6 A limestone statue in the Villa Manin Park in Passariano (Udine) covered with various communities of nitrophilous lichens (photo courtesy of E. Rui). ◗ ................................................ What Can Be Done? Works of art and historical papers are small but nonetheless complicated ecosystems. Control and prevention of biodeterioration must consider a wide variety of organisms, which attack different parts of works of art, and each of these organisms has a different ecological optimum. Restoration and preservation must not only aim at eliminating potentially harmful organisms but also at controlling the ecological factors that may foster recolonization. Outdoor Restoration Eliminating organisms from statues, walls, and basrelieves should satisfy esthetic criteria, but a close preliminary ecological and biological study of the object of restoration should also be undertaken. Three factors should be attentively considered: species, the causes of their growth, and the damage they produced. Many monuments, for instance, are covered with fungi, lichens, and other nitrophilous organisms. Simply eliminating them without identifying the source of nitrogen compounds is useless: The same organisms will grow back in just a few years (Fig. 6). Simple measures such as coverings or canalization and deviation of rainwater can be taken if a monument is exposed to rain (or to rainwater from gutters) and if the growth of biodeterioration agents arises from water availability. PART TWO / DISCOVERY AND SPOLIATION OF THE BIOSPHERE When nitrogen compounds are brought by the wind from nearby cultivated land, a line of trees may be planted as a windbreak. If eutrophication is due to guano deposits, the bird population should be brought under control or structures that prevent birds from alighting on monuments should be constructed. In some cases, however, nothing can be done to prevent damage. In many parks of Italian villas, statues are covered with colonies of nitrophilous lichens because of guano deposited by birds. Usually, birds are attractions in parks, so it is obviously impossible to eliminate them, and fair venuses and nymphs cannot be burdened with disturbing crowns of thorns. In these cases, removing the lichens would only be a temporary remedy; moreover, biological patinas may only be removed through mechanical action, per se damaging to stone surfaces. It is best to accept that the idea of contrasting nature with candid marble statues was queer from the start. Once placed in a park, statues become part of that ecosystem, and biological patinas should be accepted as a natural consequence of it. This may not please art critics, but it may teach man that he cannot always bend Nature to his will, and it may teach art critics the importance of ecology, an almost ignored discipline in the eighteenth century. Should a statue have an extremely high artistic value, the best thing to do is put the original in a museum and leave the park with a copy. Organisms are usually eliminated with the use of bio- 565 225-A1678 8/6/01 10:38 AM Page 566 PIER LUIGI NIMIS cides. These compounds are a heterogeneous class of chemical agents, and none are specifically meant or sold for restoration purposes; the restoration market is so poor that the cost of producing them would be much too high. Biocides in use mainly come from two fields: medical science (disinfectants such as quaternary ammonium salts) and agronomy (herbicides). When in contact with the target organism, these substances either inhibit photosynthesis (as urea derivatives do) or interfere with other metabolic processes. In choosing between these substances, characteristics such as efficacy, interactions with the substratum, and toxicological properties must be considered. Efficacy (i.e., the level of action against biodeterioration agents) should be relevant at minimal doses, for an ample range of susceptible organisms, and of long duration. Biocides must not interfere chemically or physically with the substratum; they must not react with certain components of stone (the worst case possible) or alter the appearance of monuments by changing their color (yellowing or whitening) or brightness. All bio- cides, in different measure, are toxic. Therefore, both restoration operators and the environment are at risk. Washing off of water-soluble biocides can result in unwanted toxic effects on insects, plants, and animals. Moreover, biocides can modify the ecosystem, fostering colonization by more aggressive or nonsusceptible organisms. In my opinion, biocides are often misused, especially for eliminating microorganisms on outdoor monuments. This misuse is the result of transferring to autotrophic organisms in open-air ecosystems the restoration techniques correctly used for heterotrophic organisms in sheltered environments. Many algal, lichen, and bryophyte patinas are easily removed by mechanical means without the help of potentially toxic substances, whose use should be avoided in areas visited by tourists. Moreover, mechanical removal is necessary even after the use of biocides. In some cases, the use of biocides is extremely damaging, as in the case of endolithic lichens (Fig. 7) living on limestone monuments (Tretiach, 1998). When killed, the lichen, deeply rooted in FIGURE 7 (a) Thallus and fruiting bodies (orange) of the endolithic lichen Petractis clausa. (b) A polished section of the same lichen in which the symbiotic cyanobacteria colonies (green) and the areas of solution of the calcareous substratum (indicated by arrows) are visible. (c) Detail of the polished section, stained with Schiff reagent to reveal the fungal hyphae, aggregated in balls in the areas of substratum solution (photos courtesy of O. Salvadori and M. Tretiach). 566 VOLUME IV / THE LIVING WORLD 225-A1678 8/6/01 10:38 AM Page 567 ARTISTIC AND HISTORICAL MONUMENTS the stone substratum, causes the exfoliation of the outermost layer (lithocortex) that detaches in small scales, leaving the underlying stone surface exposed. This surface, however, is extremely porous because of the penetration of the fungal hyphae, leaving the monument defenseless against the aggression of physical, chemical, and biological agents (such as rain, wind, atmospheric pollutants, and organisms). It is worth asking whether it is always appropriate to remove organisms from monuments. Until a few years ago, the answer would have been affirmative in any situation or condition. Originally, any monument was certainly free of biological colonization of any kind. Bringing it back to its original state through restoration was seen as a priority by restoration experts. Today, the growing importance of the biologist’s point of view has partially changed this state of things. Columns, statues, and historical buildings can offer allochthonous substrata for fungi, plants, and animals that would otherwise be absent from the area. Many archeological sites in Latium, the Italian region with Rome, have monuments made from exotic materials from distant regions of the Roman Empire. Today, such monuments host a remarkably rich and diverse lichenic flora. Moreover, many of the more than 500 lichen species known to live in Latium are found only on ancient monuments (Nimis et al., 1987). Sardinia’s nuraghi, with their subcylindrical shape and the consequent great variety of microclimatic conditions, host a great number of rare lichen species. Italy is a signatory of the Rio Biological Diversity Treaty, and this involves severe restrictions on a global scale. The high biodiversity of many archeological and monumental areas is per se a richness worthy of preservation, which indicates the artistic and historical value of a site. The cultural importance of biological diversity is a relatively new concept and not always a priority in artistic and monumental site management. A preliminary study of the importance of organisms from a biological point of view is absolutely necessary when planning interventions aimed at the removal of these organisms from such sites. This, of course, may engender conflicts between biologists and the Monuments and Fine Arts Office. Guidelines for the resolution of such conflicts are still a debated and urgent matter. However, collaboration between biologists and art historians may also produce otherwise unthinkable historical valorization of the biological component of archeological sites. For instance, many of Sardinia’s nuraghi, especially those built with basalt, are covered with a red-orange lichen, Xanthoria calcicola, whose color inspires even the names of some nuraghi, for example, nuraghe ruju (“red nuraghe”). This lichen causes no relevant damage to the stone substratum so that its removal would be absurd even from a cultural point of view, especially if the nuraghe is named after the lichen. Another example is the north wall of a Roman temple in Ostia Antica. This brick wall is completely covered with a thick carpet of a hanging gray lichen, Roccella phycopsis. This lichen does not produce relevant esthetic PART TWO / DISCOVERY AND SPOLIATION OF THE BIOSPHERE or mechanical damage—the wall is gray rather than reddish—but someone may have the brilliant idea of removing the “mold” from the wall. However, Roccella is far from being a mold: It was the product Romans mainly used for extracting purple dye. This dye is of an inferior quality to “royal purple” extracted from Murex shells (it is less resistant to light), but it was also much less expensive. Ships loaded with Roccella sailed the Mediterranean from Sardinia, the Balearic Islands, and African coasts to Ostia. Many islands depended economically on this lichen and numerous traces of this commerce are still found in toponymy. The use and commerce of Roccella was so much revived in the Renaissance that the lichen was named after a Florentine family of merchants. Therefore, instead of getting rid of the mold, it would be far more interesting to inform the visitor on the routes of Roman Roccella trade and on the dying properties of the lichen. This is only one of many cases in which scientific culture and arts and humanities should, for the good of Italian heritage, go hand in hand. Indoor Restoration As discussed previously, indoor ecosystems usually have no primary producers: The main biodeterioration agents are bacteria, fungi, and insects. The ideal growth conditions for bacteria and fungi are high relative humidity, high temperatures, and scarce ventilation. Some species are favored by strong light, whereas others need substrata rich in nitrogen compounds (dirt, dust, substances used in restoration, etc.). Bacteria and fungi propagate by spores or conidia. Biologists studying the organic matter content of air also study the propagule content of air in indoor environments, such as libraries and archive collections. These studies are important for evaluating potential risks both for books and papers and for the public or people working at these institutions. In fact, the propagules of many species are a hazard for health. High humidity of indoor environments is one of the most damaging biodeterioration factors because it favors the growth of fungi and bacteria. Some of the most ancient and important documents of human culture, such as Egyptian papyri or the famous Qumran manuscripts, were preserved by the dry climate of the subdesert areas where they rested for millennia. Italy’s climate is very different from those of Palestine or Egypt. Being a narrow peninsula cooking in a bain-marie—the Mediterranean—the control of air humidity is a priority even indoors. Paper, parchment, and wood are all hygroscopic to some degree, and as such their conservation requires a careful control on temperature and relative humidity through air-conditioning. Relative humidity can also be controlled through the use of hygroscopic substances. In addition to natural air humidity, another problem must be considered. Italian archeological sites and museums are among the most visited worldwide, and the presence of visitors may increase both temperature and relative humidity indoors. Moreover, the “micro- 567 225-A1678 8/6/01 10:38 AM Page 568 PIER LUIGI NIMIS climatic needs” of visitors often differ from those necessary to prevent biodeterioration. The microclimate of cathedrals, crypts, museums, libraries, and art galleries deserves further study from the ecological standpoint. These environments host a variety of microclimates. In some churches, “nave breezes” or “cupola breezes” could be measured, just like sea and coast breezes are measured. Buildings could be studied to determine the areas with more frequent temperature inversions in which, therefore, water condenses more easily. This would avoid the conservation of paintings in places in which the microclimatic conditions allow water condensation, which is particularly dangerous for the back of a painting. Studying these factors is essential to planning careful biological control. Usually, acceptable temperatures are expected to vary between 18 and 20°C, whereas relative humidity should be between 50 and 65% (Gallo, 1985). To date, the efforts that Italy has devoted to the preservation of a heritage that belongs to humanity are not sufficient. Nearly the totality of churches in Italy are still not monitored for biological deterioration agents, and the same can be said of proper air-conditioning. Moreover, candles still burn undeterred. In some environments, such as caves, crypts, catacombs, and other underground rooms, microclimatic factors are almost impossible to keep under control, especially when these environments host visitors daily. Lighting conditions have a major influence on biodeterioration, both directly and indirectly. Organic matter is degraded by light and this makes environments more susceptible to biological attacks. In particularly humid environments, artificial light may foster the growth of algal patinas (Fig. 8). To reduce damage caused by light, the time of exposure can be shortened and the intensity of light diminished by the use of filters to eliminate ultraviolet radiation and reduce red and infrared wavelengths. On the contrary, algal patinas that grow by artificial light may be controlled by ultraviolet irradiation without the use of biocides, but only when substrates are not damaged by it (stone, mortar, and FIGURE 8 Proliferation of green algae in patinas under artificial light in an underground room of the Domus Aurea in Rome (reproduced with permission from Caneva et al., 1991). 568 bricks). Often, however, the needs of visitors are the same of biodeterioration agents. Even when lighting problems are solved, most insects and many fungi are still active biodeterioration agents, able to grow in complete obscurity. The use of fungicides or insecticides cannot be avoided, but, apart from being toxic to man, the efficacy of these substances is limited in time. Control over some insects, especially those that feed on wood, is particularly difficult. Contrarily to what many think, termites are not at all rare in some parts of Italy. These animals grow and feed inside wood, rarely eating their way to the surface like other insects do. This makes damage difficult to discover at an early stage: Roof beams and other wooden objects can be turned to crumbs before anyone is aware of what’s going on inside the wood. Sometimes, the conservation of the immense patrimony that Italy has inherited may seem a Sisyphean toil. Nevertheless, Italians must devote all efforts to this task: This patrimony belongs to the whole of humanity. Acknowledgments I thank Prof. G. Caneva, Dr. M. Castello, Dr. E. Rui, Dr. O. Salvatori, Dr. N. Skert and Dr. M. Tretiach, who have kindly helped with constructive criticism of the paper or have supplied material for it. References Cited ALLSOPP, D., and SEAL, K. J. (1986). Introduction to Biodeterioration. Arnold, London. CANEVA, G., and ROCCARDI, A. (1991). Harmful flora in the conservation of Roman monuments. In Int. Congr. Biodet. Cultural Property, Lucknow, 212 –218. CANEVA, G., and SALVADORI, O. (1989). Sistematica e sinsistematica delle comunità vegetali nella pianificazione di interventi di restauri. In Il Cantiere della Conoscenza, il Cantiere del Restauro: Atti del Convegno di Studi. Bressanone, 27–30 Giugno 1989 (G. Biscontin, M. Dal Colle, and S. Volpin, Eds.), pp. 325 – 335. Libreria Progetto, Padova. CANEVA, G., et al. (1991). Biology in the Conservation of Works of Art. ICCROM, Rome. GALLO, F. (1985). Biological Factors in the Deterioration of Paper. ICCROM, Rome. GARTY, J. (1990). Influence of epilithic microorganisms on the surface temperature of building walls. Can. J. Bot. 68, 1349 – 1353. GIACOBINI, C., DE CICCO, M. A., TIGLIÈ, I., and ACCARDO, G. (1988). Actynomycetes and biodeterioration in the field of fine art. In Biodeterioration 7: Selected Papers Presented at the Seventh International Biodeterioration Symposium. Cambridge, UK, 6 –11 September 1987 (D. R. Houghton, R. N. Smith, and H. O. W. Eggins, Eds.), pp. 418 – 423. Elsevier, London. IONITA, I. (1971). Contribution to the study of the biodeterioration of the works of art and of historic monuments. II. Species of fungi isolated from oil tempera and paintings. Rev. Roum. Biol. Botanique 16, 377–381. KOWALIK, R. (1980). Microbiodeterioration of library materials. Part. I. Restaurator 4, 99 –114. VOLUME IV / THE LIVING WORLD 225-A1678 8/6/01 10:38 AM Page 569 ARTISTIC AND HISTORICAL MONUMENTS LAZZARINI, L., and SALVADORI, O. (1989). A reassessment of the formation of the patina called “scialbatura.’’ Stud. Conserv. 34, 20 –26. NIMIS, P. L., and MONTE, M. (1988). Lichens and monuments. Stud. Geobot. 8, 1–133. NIMIS, P. L., MONTE, M., and TRETIACH, M. (1987). Flora e vegetazione lichenica di aree archeologiche del Lazio. Stud. Geobot. 7, 3 –161. PINNA, D., et al. (1998). Plant Biosyst. 132, 183 –195. SEAWARD, M. R. D. (1988). Lichen damage to ancient monuments: A case study. Lichenologist 10, 291–295. TRETIACH, M. (1998). Ecophysiology of calcicolous endolithic lichens. Giorn. Bot. Ital. 129, 159 –184. PART TWO / DISCOVERY AND SPOLIATION OF THE BIOSPHERE General References CANEVA, G., NUGARI, M. P., and SALVADORI, O. (1994). La Biologia nel Restauro. Nardini, Firenze. CANEVA, G., NUGARI, M. P., PINNA D., and SALVADORI, O. (1996). Il Controllo del Degrado Biologico, i Biocidi nel Restauro dei Materiali Lapidei. Nardini, Firenze. GALLO, F. (1992). Il Biodeterioramento di Libri e Documenti, 5th ed. Centro di Studi per la Conservazione della Carta, Rome. LIOTTA, G. (1991). Gli Insetti e i Danni del Legno: Problemi di Restauro. Nardini, Firenze. MANDRIOLI, P., and CANEVA, G. (Eds.) (1998). Aerobiologia e Beni Culturali. Metodologia e Tecniche di Misura. Nardini, Firenze. NIMIS, P. L., PINNA, D., and SALVADORI, O. (1992). Licheni e Conservazione dei Monumenti. CLUEB, Bologna. 569 225-A1678 8/6/01 10:38 AM Page 570