artistic and historical monuments: threatened ecosystems

PART TWO / DISCOVERY AND SPOLIATION OF THE BIOSPHERE 557

SECTION II / MAN AND THE ENVIRONMENT

PIER LUIGI NIMIS

Department of BiologyUniversity of TriesteTrieste, Italy

Artistic andHistoricalMonuments:ThreatenedEcosystems

Italy has the largest heritage worldwide in historicalmonuments, ancient books, parchments, paintings,sculptures, ancient tapestries, and textiles. Some arekept outdoors, some indoors, and others even underwater; their preservation is a responsibility of allItalians to mankind. These works of art are attackedby many organisms, and the biologist regards themas outright ecosystems. Open-air monuments mostlyhost photosynthetic organisms, such as cyanobacteria,algae, lichens, mosses, and higher plants, whereasthose stored indoors are attacked by heterotrophicorganisms, such as bacteria, fungi, and insects.Biology can help their conservation and restoration inthat it can identify such organisms and the ecologicalconditions that allow their growth. This knowledgeallows the biologist to judge the effectiveness ofrestoring treatments. Much has been done and muchmore still remains to be done.

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Works of Art as Ecosystems

The richness and variety of Italian artistic heritage is un-equalled worldwide. All Italians are responsible for its con-servation. However, it is not an easy task: Physical, chemi-cal, and biological agents attack any item. Often, changesthus produced are irreversible. Living beings play an im-portant part in this process; an ancient illumination in a li-brary, a Roman statue in an archeological site, and a frescoor a painting in a church are all under aggression. Many or-ganisms may destroy them or change them enough to maskthe artist’s idea. Thus, the biologist’s knowledge can preventthese works of art from disappearing.

Illuminations, statues, and paintings can be viewed ina biological light: They are ecosystems, with primary pro-

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ducers, decomposers, and predators, like any African plainseen in many television documentaries. An imaginary docu-mentary titled “The Statue Ecosystem” would unveil a newand remote world in which no acacias grow and in whichno elephants, hyenas, lions, or hunting dogs dwell. Instead,this ecosystem includes primordial cyanobacteria; weirdcolonies of algae (the sea is not the only place in whichthey live), attacked by squadrons of sneaky fungi; unearthlylichen landscapes; and tiny moss forests, inhabited by hor-rible creatures that human eyes have rarely seen—every-thing from sleepy herbivorous tardigrades to ferociouspredator carabids.

Therefore, a statue is in itself an environment in whichall ecological phenomena can be observed: competition,host–parasite and prey–predator relationships, and succes-

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558 VOLUME IV / THE LIVING WORLD

sions. It is also the substratum for the complex reactions ofbiogeochemical cycles, such as nitrogen, carbon, and sulfurcycles.

Restoration ecology is a recent field of study in whichmuch still remains to be done. Italy holds a prominent po-sition in this field, if not in others. The available knowledgeis based on the work of many biologists, who work for pres-tigious institutions that study the decay and conservationof works of art. Examples of such institutions are the Isti-tuto Centrale per il Restauro (Central Institute of Resto-ration), the Istituto per la Patologia del Libro (Institute forBook Pathologies), the Istituto per la Ricerca sul Legno(Institute for Wood Research), various centers of the Con-siglio Nazionale delle Ricerche (National Council for Sci-entific Research), the Monuments and Fine Arts Officeresearch laboratories in Bologna and Venice, university de-partments, and other research centers. This article aims toobserve statues, churches, illuminations, and parchmentsfrom the biologist’s point of view; thus, the material tracesof our cultural roots will become tiny, complex, and fragileecosystems, threatened with destruction by the same lawsof nature that generated them through human intelligence.

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Biodeterioration of Works of Art

Biodeterioration is the name biologists give to the damagethat biological agents produce on various materials. Twotypes of organisms are involved: autotrophic and heterotro-phic. The former—cyanobacteria, algae, lichens, mosses,and vascular plants—draw energy from sunlight throughphotosynthesis; thus, they do not use the substratum as anenergy source but as a mere support or, at most, as a sourceof micronutrients or water or both. Therefore, these organ-isms can grow on inorganic substrata, such as monuments,stained-glass windows, or metal objects, when these are ex-posed to sunlight. On the other hand, heterotrophic organ-isms classified as decomposers (such as bacteria and fungi),herbivores, and predators (usually snails and insects) drawenergy by decomposing organic molecules. These organ-isms live on organic matter (other organisms, paper, wood,parchment, and some types of paint) used as a direct sourceof energy irrespective of the lighting conditions; this makesthem the primary biodeterioration agents for works of artkept indoors.

Heterotrophic organisms often produce irreversibledamage when they feed directly on artwork made of or-ganic matter, whereas they are less involved in the bio-deterioration of outdoor monuments. Autotrophic organ-isms, on the other hand, can cause both reversible andirreversible damage. For example, the color changes thatalgal patinas cause on church façades are easily restored—when not associated with physical or chemical damage—by removing the algae.

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Both hetero- and autotrophic organisms mainly bringabout two types of biodeterioration: (i) physical actions(disintegration), such as the effect of tree roots on marblemonuments, physical disruption of rock by lichens, andholes dug by insects in wood, and (ii) chemical actions (de-composition), such as the irreversible alterations that fungicause to fabrics, paper, and wood, the chromatic changesdue to fungal and bacterial pigments, and the solution ofcalcareous rocks by endolithic cyanobacteria and lichens.

Biodeterioration can be both direct and indirect. Theformer is caused by organisms that permanently use a par-ticular substratum for support or nourishment, such as thedestruction of books by fungi and bacteria or the perfora-tion of submerged columns by mollusks. Indirect biodeter-ioration is caused by organisms whose ecology is not tied toa particular substratum; examples are guano deposits onstatues and monuments that, incidentally, can give rise todirect biodeterioration by other organisms or chemical andphysical alterations. At the extreme, even human vandal-ism can be considered indirect biodeterioration.

There is a marked ecological difference between worksof art kept outdoors and those kept indoors. The former areattacked primarily by autotrophic organisms, which growon inorganic materials (stone, glass, and metal). The latter,made entirely or in part of organic material (paper, parch-ment, wood, glue, and paint), host heterotrophic organisms.Outdoor monuments are the substratum for complete min-iature ecosystems, inclusive of primary producers (photo-synthetic organisms); on the contrary, indoor artwork is a“halved ecosystem” in which decomposers prevail.

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Ecological Study of Outdoor Monuments

The use of inorganic constructing materials, such as stone,bricks, and mortar, throughout its history has left Italy withan amazing architectural heritage that endures throughtime. Other cultures, such as those of the Far East, havingbuilt their monuments in wood, are left with a much moredeteriorated or recent memory of the past, mainly becauseof the action of biological agents. Nevertheless, Italian mon-uments are still prone to physical, chemical, and biologicaldeterioration because they are mostly made of calcareousrock such as marble. Glass, of siliceous nature, is anotherlithic substratum, but it is not subject to colonization bymicroecosystems, except when air humidity levels are high.This condition is rare in Italy, but the stained-glass windowsof French churches, for example, exposed to humid Atlan-tic winds, are attacked by fungi, lichens, and algae that dis-color them or make them irreversibly opaque.

Monuments built in stone are mainly colonized byphotosynthetic organisms—cyanobacteria, algae, lichens,mosses, and vascular plants—that use the substratumuniquely as a support to reach light, their primary source of

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ARTISTIC AND HISTORICAL MONUMENTS

energy. Sometimes, though, the colonization of stone sur-faces starts with chemoautotrophic organisms, such as par-ticular types of bacteria, which are able to draw energyfrom inorganic substances without light. These organismsprepare the substratum for the development of various se-ries of biological successions. Heterotrophic organisms ar-rive later because they need to feed on the organic sub-stances that autotrophic organisms have produced. Theseorganisms are less important in the biodeterioration oflithic substrata and they will be discussed only with regardto organic substrata preserved indoors.

As in any ecosystem, biological colonization of monu-ments depends on a variety of factors, such as exposure, sub-stratum, and the availability of nitrogen compounds. Study-ing the ecology of the communities that invade monumentscan help identify the factors that favored their growth, thuscontributing to the planning of strategies for restorationand preservation.

BacteriaBacteria that colonize monuments are mainly autotro-

phic, such as sulfur and nitro- and cyanobacteria; the alter-ations that they cause are of a chemical nature. Nonphoto-synthetic sulfur bacteria convert limestone into gypsum(especially in sulfur dioxide-polluted areas), irreversiblycovering the surfaces of statues and capitals with horribleblack crusts. Nitrobacteria cause less damage, although theycan alter lithic substrata by producing sulfuric and nitric ac-ids. Nitrifying bacteria are the first to colonize stone sur-faces; they mainly produce nitrates, which often foster thegrowth of other microorganisms including lichens. Cyano-bacteria were among the first prokaryotic organisms to col-onize land; they have chlorophyll and play an importantrole in the deterioration of stone surfaces, especially cal-careous ones. Some even penetrate beneath the surface,producing typical erosion phenomena; others become en-crusted in thick calcium carbonate secretions, deformingtheir substratum. Free from competitors, many coccal cy-anobacteria cover in dark patinas large vertical areas ex-posed to sunlight, such as walls facing south. In additionto the esthetic damage, these dark patinas, in the Mediter-ranean area, cause the temperature to increase by up to8°C higher than that of the noncolonized, lighter-coloredsurfaces, facilitating further physical deterioration (Garty,1990). Cyanobacteria need water in a liquid state to carryout photosynthesis. In their search for the long-lost andnearly lunar world they conquered alone, cyanobacteria col-onize hot, arid, and sunny surfaces, with water flowing overthem for brief periods; all these conditions can be found onany vertical surface facing south and washed down by rain.Cyanobacteria cells, enclosed in gelatinous secretions, canretain water for long periods, thus delaying desiccation ofthe stone surface and favoring chemical alterations, such asthe solution of calcium carbonate. Nitrifying bacteria, like

cyanobacteria, are able to fix atmospheric nitrogen, enrich-ing the surface of statues and bas-relieves with nutrients forfurther harmful colonizing organisms.

AlgaeThe algae living on works of art are green algae, ances-

tors of higher plants. They are simple, unicellular, or thread-like organisms with few defenses against desiccation. Algalpatinas, frequent on monuments, are among the first to col-onize stone and glass surfaces after bacteria, but only damp,shady surfaces allow them to grow and cause damage. Typi-cal places are usually the base of monuments or surfacesfacing north. However, algae produce only chromatic alter-ations, coloring the substratum green or red-orange (if thealgae are of the genus Trentpohlia). These patinas can beeasily 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 themost superficial layer and is usually repaired easily; on thecontrary, on stained-glass windows, small chemical alter-ations can result in irreversible esthetic damage.

LichensLichens are a symbiotic association between algae or

cyanobacteria and fungi. These organisms are certainlythe most conspicuous and important colonizers of outdoormonuments, including both glass and lead surfaces of an-cient stained-glass windows; only heavy pollution can pre-vent their growth. The most noticeable effects of lichen col-onization are of a chromatic nature: Italian archeologicalsites and parks are populated by mythological heroes, ve-nuses, nymphs, and horses whose noses are Caloplaca red,whose heads are Candelariella yellow, and whose bodies areAspicilia gray. The north façade of the Orvieto duomo is anexample of the esthetic damage produced by lichens. Theduomo was built with dark basalt and light-colored lime-stone in alternate bands. The dark bands are colonized bylight-colored species, whereas the light-colored bands hostorange or dark species (Nimis and Monte, 1988). The resultis bizarre and may not be that unpleasant, but it is certainlyfar from what the artist had in mind (Fig. 1).

However, threat due to lichens may be much more se-vere: They can produce much worse damage, such as majoralterations of stone surfaces through biogeophysical andbiogeochemical processes. Biogeophysical alterations arecaused by the penetration of fungal hyphae (the thin fila-ments that make up the fungus) beneath the stone surfaceand by the contraction and expansion of the lichen sub-sequent to desiccation and rehydration (Seaward, 1988).These contraction–expansion cycles are due to the lichencontent in gelatinous and mucilaginous substances, whosevolume strongly depends on water content. These move-

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a

bFIGURE 1 (a) The south façade of the Orvieto duomo notcolonized by lichens, with the typical alternate bands of darkbasalt and light-colored limestone. (b) The north façade of theOrvieto duomo: three bands, two made of basalt and the cen-tral one of limestone, extensively colonized by lichens.

FIGURE 2 Scanning electron micrograph of the endolithicthallus of the lichen Verrucaria baldensis in calcareous rock,partially decalcified in acetic acid. The penetration of the fun-gal hyphae in the rock is evident (reproduced with permissionfrom Pinna et al., 1998).

ments result in the lifting of the marginal part of the lichenand in a “peeling” effect on the stone surface, with the de-tachment of superficial layers. The depth of penetration ofthe hyphae depends on the composition of the substratum,the type of lichen (foliose or crustose, epilithic or endo-lithic), and the species. The symbiotic algae rarely pene-trate deeper than 2 mm and can usually be found less than1 mm from the stone surface; the fungal hyphae may pene-trate up to 15 mm in very porous carbonate rocks, althoughthese too usually penetrate no more than 2 or 3 mm. Thehyphae can at times penetrate through the mineral crystals,but more often, especially in siliceous rocks, it is much eas-ier for them to dig their way between the crystals.

Endolithic lichens are a particular case: Their growth

takes place entirely inside rocks, usually calcareous ones,and they are often invisible to the naked eye because theircolor is identical to that of the rock (Fig. 2). Their fruit-ing bodies, however, protrude on the surface, leaving small

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hollows as they fall; this effect is called pitting. The smallholes, measuring 0.2–2 mm across, are a typical weak spotfor chemical aggressions, such as the solution of calciumcarbonate in water or the penetration of pollutants. Littlewas known of these organisms before the studies carriedout by Tretiach (1998). Some of the findings are truly un-expected: The amount of chlorophyll per unit area enclosedin rock may be the same as that found in tree leaves, butthe primary productivity of an endolithic lichen is definitelysmaller. The growth of these lichens is often very slow—not more than a fraction of a millimeter per year. Strange asit may seem, many statues, bas-relieves, or cathedral wallslive, breath, and carry out photosynthesis; they contain asmuch chlorophyll as the trees in the parks in which they aresituated.

The chemical alterations lichens produce are due tothree substances they secrete: carbon dioxide, lichen com-pounds with complex properties, and oxalic acid. Carbondioxide, produced through respiration, when in an aqueousenvironment produces an acid solution that, although weak,can solubilize relatively insoluble salts such as calcium andmagnesium carbonates in limestone, dolomite, a variety ofmarbles, and plasters that contain carbonates. All these areconverted into much more soluble bicarbonates. This pro-cess is common to all organisms, and in the case of lichensit is not particularly relevant to biodeterioration.

Many of the organic compounds secreted by lichens,commonly called lichen acids, have complex properties dueto polar chemical groups that can chelate metallic cationsby donating electron pairs. Lichens produce a variety ofchelating substances in large amounts, and they often takeon rusty colors due to iron accumulation, especially on si-liceous rocks. Oxalic acid is one of the most active acids inmetal deterioration and in cation exchange. Different li-chen species have different oxalate production capacities;moreover, the type of oxalate produced depends on the cat-ions available in the environment—that is, on the mineralcomposition of the substratum. Calcium oxalate is found inlichens in two different crystals: whewellite and weddellite.When secreted, calcium oxalate forms an extracellular in-soluble deposit. Species obliged by their physiology to liveon calcareous substrata have much higher calcium oxalatelevels than species living on siliceous substrata. Lichen pro-duction of calcium oxalate has given rise to heated debateamong restoration ecology experts. The difference betweena “new” stone surface and the “age patinas” that cover an-cient artwork is evident: Many restorations have been crit-icized for removing these patinas. When thus restored,churches, bas-relieves, and statues take on an almost mod-ern appearance, as if they were made of plaster. Many per-ceive this type of restoration as artificial compared to thepassing of time. The vast yellowish or brownish films (timepatinas) are almost totally made of calcium oxalate, but

their origin is still open to debate. There have been two hy-potheses put forward. First, calcium oxalate derives fromorganic substances used in the past as protective treatmentsor for esthetic purposes or both; Second, calcium oxalate issecreted by lichens and, incidentally, by bacteria and fungi.Both hypotheses need to be studied further, but it is pos-sible that both are correct, depending on the case in ques-tion (Lazzarini and Salvadori, 1989).

Bryophytes and Higher PlantsIn average humidity conditions, the colonization of out-

door monuments usually starts with nitrobacteria, followedby various stages of lichen vegetation or, if humidity condi-tions allow it, by algal patinas. The growth of mosses, ferns,and higher plants is also delayed because of the need forsoil accumulation. In certain conditions, though, this accu-mulation is fast, such as when dust or stone weatheringproducts are deposited on horizontal surfaces or betweenstones. Ancient brick structures are typical examples: Assoon as roots find their way between bricks, the resultingmechanical effects can be devastating (Caneva and Roc-cardi, 1991).

Many circles of walls in Rome are emblematic in this re-spect. Typical higher plants found here are pellitories, com-mon throughout Italy, or capers, typical of the Mediterra-nean part of Italy. Fig trees, ailanthus, ivy, and other treesor bushes make their way between bricks, taking advantageof weak spots in the structure or of the poor resistance ofmortar. Their roots also produce chemical alterations bysecreting acid substances, but mechanical effects are byfar the most dangerous. In some archeological sites, treeroots penetrate in underground cavities, causing irrevers-ible damage to buildings and frescos. In addition to roots,ivy clings to the substratum with its aerial rootlets, produc-ing the detachment of vast portions of superficial layers ofconstruction stones (Caneva and Salvadori, 1989). Occa-sionally, the presence of higher plants in archeological sitesmay be useful. In areas where the water table is close to thesurface, the flooding of underground buildings is frequent.Planting trees with high evaporation rates is an effectiveway to lower the water level. Eucalyptuses, for instance, areamong the most efficient “biological pumps” known to man.Moreover, a line of trees can be a windbreak, modifying themicroclimate, reducing evaporation or direct solar radia-tion, hindering the wind’s weathering effects, and filteringnitrogen compounds from possible nearby cultivated land.

Humble bryophytes (mosses and liverworts), having noroots, are less dangerous. Nevertheless, because they areable to retain large amounts of water (12 liters/m2 or more),they foster biogeochemical deterioration (Fig. 3). Bryo-phytes also tend to accumulate soil in the form of dustand organic residues. As in any typical primary succession,higher plants thus colonize the substratum.

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FIGURE 3 Top of the head of a limestone statue in the VillaManin Park in Passariano (Udine) covered by the nitrophilouslichen Xanthoria calcicola (yellow) and by the moss Grimmiapulvinata (gray) (photo courtesy of S. Del Bianco).

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Ecological Study of Indoor Artwork

It may seem that works of art kept in museums, churches,and houses are more protected from biological aggressionthan outdoor monuments. However, this is true of artworkmade of inorganic matter only: The best way to preserve astatue is to keep it in a museum. Any item made of organicmatter, if kept outdoors, has a grim and short life comparedto a statue; many physical, chemical, and biological agentsact synergistically and rapidly destroy it. This is why books,parchments, fabrics, and wooden objects—artwork all or inpart made of organic matter—are kept in closed and shel-tered places. Thus, some of the ecological factors that allowthe growth of damaging organisms may be kept in control.Simply screening off sunlight eliminates all autotrophic or-ganisms, control over temperature and humidity helps limitthe growth of bacteria and fungi, and insect aggressions areeasily reduced by disinfestation. Nevertheless, even indoorsartwork is not perfectly safe: Composite armies of hetero-trophic organisms are ready to attack every time controlover environmental conditions fails perfection, and a per-fect control is far from easy on a broad scale.

Before providing a review of the troops responsible forbiodeterioration, one of the worst examples of indirectdeterioration deserves to be mentioned. It is before any-one’s eyes, in most churches; it may not attract much atten-tion and, paradoxically, it is caused by intelligent and well-meaning men. It is striking that today most churches ofVenice—famous throughout the world for its masterpiecesof painting—have endless lines of pitiless candles pi-ously shedding horrible patinas of lampblack on defense-less blackened paintings or, even worse, on newly restoredpaintings. The tradition of lighting candles is deeply rooted

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in worship practices and religious culture. However, thereis very little awareness that in 1 year, one single candle maycause more damage than whole generations of fungi, bac-teria, and algae. The gloomy colors of many ancient paint-ings are not the work of depressed painters but are due tocandles lit with the best of intentions; they are certainly notmeant to disfigure the object of worship. The stubborn tra-dition of lighting candles in Italian churches is totally un-acceptable today. This problem, complex in many ways,should be a priority for the curie and the Monuments andFine Arts Offices.

In addition to man and his ominous candles, indoor en-vironments host swarming battalions of heterotrophic or-ganisms ready to attack any item made of even minimalquantities of organic matter. Wood, paper, parchments,leather, and cloths are the refectory of legions of bacteria,fungi, and arthropods. Not even paintings or frescos aresafe, being composed of delicious specialties such as amid,gums, sugars, glycerin, various types of gelatins, linseed oil,and egg yolk.

WoodLignin, cellulose, and hemicellulose are among wood’s

principal components. Lignin is the most resistant to bio-logical aggression; its worst enemies are fungi, especiallyascomycetes. Also, newly synthesized cellulose is not easilyattacked by biological agents, but a long exposure to phys-ical and chemical agents engenders amorphous spots thatfacilitate aggression by microorganisms. Among the mostimportant are the basidiomycetes Serpula lacrymans, Poriaspp., and Coniophora puteana; all have enzymes that con-vert cellulose in glucose, leaving a brownish residue of non-decomposed lignin (Allsopp and Seal, 1986). Hemicelluloseis the least resistant of the three components: It is easily hy-drolyzed by bacteria and fungi.

Conservation of wood artwork outdoors is a lost battle:The proliferation of bacteria, fungi, and insects is difficultto control effectively and for a long period of time. Indoors,the intensity of microbiological aggressions mostly dependson air humidity. Asco- and deuteromycetes attack wooditems kept in humid underground rooms; wood becomessoft if damp and extremely fragile if dry. The humidity ofdry wood is in equilibrium with the relative humidity of thesurrounding environment; microbiological attacks are rel-evant only if water content is higher than 20%. Therefore,adequate air-conditioning is the best defense against bac-teria and fungi. Insects, however, are still free to attack.Coleopterans, lepidopterans, termites, hymenopterans, andmany others can produce much damage to dry wood, noteasily attacked by bacteria and fungi. These attacks are car-ried out with an ingenious biological trick. Most insects, be-cause they are unable to synthesize the enzymes necessaryfor breaking up lignin and cellulose, host bacteria and fungi(which do produce these enzymes) in their intestine, in

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which the humidity conditions necessary for the growth ofsuch microorganisms is provided.

PaperCellulose is the principal component of paper, together

with lignin, hemicellulose, pectines, various types of wax,tannins, and proteins in different proportions, dependingon the type of paper and on the time of fabrication. It is pos-sible that paper fabricated in the Middle Ages was muchricher in cellulose, and therefore less prone to biological at-tacks, than most paper fabricated in recent times (Kowalik,1980).

The principal agents of biodeterioration of paper arebacteria and fungi, and again the level of aggression de-pends on the water content of substratum. Books kept indry environments survive longer than those kept in high-humidity conditions. The attacks of fungi and bacteria ap-pear at first as stains or as a discoloration of ink. Stains aredifferently colored depending on the type of organism andon the type of paper. The discoloration of ink, on the otherhand, is due to tannase, an enzyme—synthesized by somefungi of the genera Aspergillus and Penicillium—that cat-alyzes the hydrolysis of gallotannate. Bindings, which maycontain hygroscopic substances, are among the first parts ofa book to be damaged. Prolonged growth of fungi and bac-teria causes paper to become felt-like and fragile. Its char-acteristics are altered (e.g., its acidity), fostering the growthof other species of fungi and bacteria more suitable to thenew ecological conditions. Even in books kept for centuriesin libraries, biologists can study ecological successions sim-ilar to those that, in “normal” ecosystems, turn meadowsinto forests. Books that undergo floods, such as those dam-aged in the Florence flood in 1966, are a particular case.Pages become cemented in solid blocks and are not easilyseparated. This is due to the rapid growth of bacteria andfungi that occurs during imbibition. These organisms rap-idly degrade cellulose, producing oligosaccharides (withmucus-like properties) which glue the pages together, mak-ing the book totally useless.

Today in Italy, too many ancient books and papers arekept in ecological conditions that turn them into ecosystemsat risk. Even in the rare cases in which rooms are adequatelyair-conditioned, insects are still dangerous: It is exactly inthese conditions that these organisms have their ecologicaloptimum. Among the most dangerous is a devilish little in-sect that goes by the graceful name of silverfish (Lepismaspp.), commonly found in houses. This small, flat animal canpenetrate virtually anywhere; it easily slips inside books,merrily feasting on pages that no one will ever be able toread again. Other insects, instead of eating paper, feed onthe fungi and bacteria that live in books, especially closeto bindings; their excrements are a rich source of food forsaprophagous bacteria and fungi. Similar processes may beobserved in the biodeterioration of cloths, although there

are important differences between fabrics of vegetable der-ivation (linen and cotton) and fabrics of animal derivation(wool).

Leather and ParchmentAlthough paper is of vegetable derivation, leather and

parchment are of animal derivation and therefore have ahigh protein content. Organisms that decompose such ma-terials must synthesize specific proteolytic enzymes (prote-ases and peptidases). Italian culture owes some of its mostancient papers to parchment, which is made from sheepor goat skin (the best were made using fetus skins). Parch-ment is mainly composed of collagen, which is hydrolyzedby specific enzymes (collagenases) synthesized by bacteriaof the genus Clostridium (Kowalik, 1980). Collagen, how-ever, is often depolymerized during the processing of parch-ment; thus, it may be decomposed by nonspecific proteolyticenzymes, synthesized by many bacteria and microfungi.Leather, whose chemical properties are similar to those ofcollagen, undergoes similar decomposition processes. Dur-ing processing, though, leather is often treated with tan-nins, which inhibit biological attacks, especially those ofbacteria. As with other materials, insects may still strike;especially dermestids and tineids can banquet on tannin-treated leather.

FabricsAncient fabrics consist of fibers of plant or animal ori-

gin, which have different chemical composition. Vegetablefibers mainly consist of cellulose, whereas animal fibersmostly consist of protein compounds such as keratin in woolor sericin in silk. The former are mainly attacked by cellu-lose-hydrolyzing fungi such as deuteromycetes; the lattercan be attacked by many bacteria and fungi, actually moreeffective in the deterioration of wool than of silk. Again,the control of relative air humidity can prevent part of thedamage. The situation is quite different with insects: Every-one is familiar with the damage moths may produce in wool.Therefore, it is not surprising that the preservation of hugearras kept in Italian churches and museums should be quitedifficult; obviously, hanging bags full of mothballs is not asolution.

PaintingsWood, paper, leather, parchment, and cloth have rela-

tively homogeneous compositions. On the contrary, paint-ings are composed of a wide variety of materials—so wide,in fact, that their biodeterioration is quite fascinating to bi-ologists. Chemical composition of paintings varies in layers.The undermost layer is often wood—and its biodeteriora-tion is that typical of wood items—but it may also be madeof 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,

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FIGURE 5 White patina on the frescos of an Etruscan tombin Tarquinia due to the growth of actinomycetes (reproducedwith permission from Caneva et al., 1991).

FIGURE 4 Detail of fungal attack on a painting on canvas(photo courtesy of O. Salvadori).

resulting in cracks in the painting. Usually, the undermostlayer of paintings is a canvas of vegetable nature or, as inthe case of watercolors, paper. In these cases, the biodeteri-oration agents are those typical of fabrics and paper. Can-vas is usually covered with colors of mineral derivation, of-ten diluted with animal or vegetable oils, glues, gelatins, etc.Finally, the protective varnishes, which cover paintings andare often renewed throughout the years, are mostly made oforganic matter. Therefore, paintings offer a rich and variedmenu to many heterotrophic organisms—bacteria, fungi,and, fortunately, few arthropods. A painting is thereforeone of the most interesting “artistic ecosystems” amongthose found indoors. Fungi of the genera Aspergillus, Peni-cillus, and Trichoderma feed on tempera and color binders;Phoma and Aureobasidium destroy oil colors; Geotrichumfeeds on casein binders; and Mucor and Rhizopus attackvarious types of glues (Ionita, 1971). Therefore, the type ofbiological aggression depends on the substratum. Also, bio-deterioration may concern all the different layers of paint-ings or be limited to the color layer, depending on the typeof colors and diluents used. Usually, the undermost layersof paintings are those at risk of biodeterioration, althoughmany species of organisms also attack colors, damagingthem irreversibly (Fig. 4). Bacteria and fungi are mainlyactive in conditions of high air humidity levels, whereasinsects prefer dry environments and tend to limit their at-tacks to the parts in wood and paper of paintings (the baseor the frame).

Frescos and other inorganic types of murals are a specialcase because they are attacked by actinomycetes (Giaco-

bini et al., 1988). Many murals, situated in damp churches,crypts, caves, and tombs, are disfigured by whitish or gray-ish patinas of these fungi, which metabolize nitrites and ni-trates and reduce sulfates (Fig. 5).

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Ecological Study of Submerged Artwork

Italian coasts conceal a huge historic and artistic patrimony.In the course of centuries, hundreds of ships have sunk withtheir precious loads, and only recently has Italy started todiscover this treasure of historical heritage. To study bio-deterioration processes in an aquatic environment, a closeexamination of marine ecology is necesary, and this is be-yond the scope of this article. Therefore, what follows isonly a brief account of such processes.

It is obvious that almost all organic matter left for longperiods of time under water has a short life. Books, parch-ments, and cloths, once under water, are lost forever. Theonly exception is wood, especially that of ship hulls. In aterrestrial environment, lignin is mainly attacked by bacte-ria, fungi, and insects. Millions of years of evolution havebrought about organisms able to decompose wood in theenvironment in which this is frequent—the terrestrial en-vironment. In an aquatic environment, especially at greatdepths, wood is rare; in natural conditions, wood at seamostly floats. Even under water, some bacteria and fungiare able to decompose wood, although less effectively thanin a terrestrial environment. Aquatic bacteria and fungi areboth aerobic and anaerobic; various species produce differ-ent types of damage, such as superficial erosion, cavitation,and the formation of small holes. Occasionally, especiallyin shallow water, submerged wood may become coveredin algal colonies, which do not much alter their substratum.Greater damage is caused by animals. The sea may not bepopulated by insects, but their absence is amply compen-

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FIGURE 6 A limestone statue in the Villa Manin Park in Pas-sariano (Udine) covered with various communities of nitro-philous lichens (photo courtesy of E. Rui).

sated by the abundant presence of mollusks and crusta-ceans, which may cause serious damage to submerged art-work. Mollusks involved in biodeterioration are mainly ofthe genera Teredo, Bankia, and Martesia; they dig deepholes in wood structures. Crustaceans are mostly isopodgenera, and they cause wood to become extremely fragile.Most of these organisms, however, are active only whenwood is close to surface. In the past, these animals weresailors’ nightmares because the hulls of ships were made ofwood. Wrecks, kept at greater depths by the weight of theirloads, are infrequent items in marine ecosystems and there-fore less prone to biological aggression.

Even artwork made of stone is subject to biological at-tacks in marine environments. The biodeterioration pro-duced by mollusks is the most devastating. These organismscan perforate rock, digging holes as deep as 10 cm, throughmechanical action or by secreting acid substances. Romancolumns near Pozzuoli are a well-known example of thisphenomenon. Because the area is subject to bradyseism,these columns have been alternatively above and under wa-ter through the centuries. Through the holes left in the col-umns by marine organisms, it is possible to reconstructthe raising and lowering movements of the ground throughtime. Other organisms, such as some species of calcareousalgae, thickly encrust with calcium carbonate the surfacesof submerged objects.

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What Can Be Done?

Works of art and historical papers are small but nonethe-less complicated ecosystems. Control and prevention of bio-deterioration must consider a wide variety of organisms,which attack different parts of works of art, and each ofthese organisms has a different ecological optimum. Resto-ration and preservation must not only aim at eliminatingpotentially harmful organisms but also at controlling theecological factors that may foster recolonization.

Outdoor RestorationEliminating organisms from statues, walls, and bas-

relieves should satisfy esthetic criteria, but a close prelimi-nary ecological and biological study of the object of resto-ration should also be undertaken. Three factors should beattentively considered: species, the causes of their growth,and the damage they produced. Many monuments, for in-stance, are covered with fungi, lichens, and other nitro-philous organisms. Simply eliminating them without iden-tifying the source of nitrogen compounds is useless: Thesame organisms will grow back in just a few years (Fig. 6).

Simple measures such as coverings or canalization anddeviation of rainwater can be taken if a monument is ex-posed to rain (or to rainwater from gutters) and if the growthof biodeterioration agents arises from water availability.

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When nitrogen compounds are brought by the wind fromnearby cultivated land, a line of trees may be planted asa windbreak. If eutrophication is due to guano deposits,the bird population should be brought under control orstructures that prevent birds from alighting on monumentsshould be constructed. In some cases, however, nothing canbe done to prevent damage. In many parks of Italian villas,statues are covered with colonies of nitrophilous lichensbecause of guano deposited by birds. Usually, birds are at-tractions in parks, so it is obviously impossible to eliminatethem, and fair venuses and nymphs cannot be burdenedwith disturbing crowns of thorns. In these cases, removingthe lichens would only be a temporary remedy; moreover,biological patinas may only be removed through mechani-cal action, per se damaging to stone surfaces. It is best to ac-cept that the idea of contrasting nature with candid marblestatues was queer from the start. Once placed in a park,statues become part of that ecosystem, and biological pa-tinas should be accepted as a natural consequence of it.This may not please art critics, but it may teach man that hecannot always bend Nature to his will, and it may teach artcritics the importance of ecology, an almost ignored disci-pline in the eighteenth century. Should a statue have an ex-tremely high artistic value, the best thing to do is put theoriginal in a museum and leave the park with a copy.

Organisms are usually eliminated with the use of bio-

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FIGURE 7 (a) Thallus and fruiting bodies (orange) of the endolithic lichen Petractis clausa. (b) A polished sec-tion of the same lichen in which the symbiotic cyanobacteria colonies (green) and the areas of solution of the cal-careous substratum (indicated by arrows) are visible. (c) Detail of the polished section, stained with Schiff re-agent to reveal the fungal hyphae, aggregated in balls in the areas of substratum solution (photos courtesy ofO. Salvadori and M. Tretiach).

cides. These compounds are a heterogeneous class of chem-ical agents, and none are specifically meant or sold for res-toration purposes; the restoration market is so poor that thecost of producing them would be much too high. Biocidesin use mainly come from two fields: medical science (disin-fectants such as quaternary ammonium salts) and agron-omy (herbicides). When in contact with the target organ-ism, these substances either inhibit photosynthesis (as ureaderivatives do) or interfere with other metabolic processes.In choosing between these substances, characteristics suchas efficacy, interactions with the substratum, and toxicolog-ical properties must be considered. Efficacy (i.e., the levelof action against biodeterioration agents) should be rele-vant at minimal doses, for an ample range of susceptible or-ganisms, and of long duration. Biocides must not interferechemically or physically with the substratum; they must notreact with certain components of stone (the worst case pos-sible) or alter the appearance of monuments by changingtheir color (yellowing or whitening) or brightness. All bio-

cides, in different measure, are toxic. Therefore, both resto-ration operators and the environment are at risk. Washingoff of water-soluble biocides can result in unwanted toxiceffects on insects, plants, and animals. Moreover, biocidescan modify the ecosystem, fostering colonization by moreaggressive or nonsusceptible organisms.

In my opinion, biocides are often misused, especially foreliminating microorganisms on outdoor monuments. Thismisuse is the result of transferring to autotrophic organ-isms in open-air ecosystems the restoration techniques cor-rectly used for heterotrophic organisms in sheltered envi-ronments. Many algal, lichen, and bryophyte patinas areeasily removed by mechanical means without the help ofpotentially toxic substances, whose use should be avoidedin areas visited by tourists. Moreover, mechanical removalis necessary even after the use of biocides. In some cases,the use of biocides is extremely damaging, as in the case ofendolithic lichens (Fig. 7) living on limestone monuments(Tretiach, 1998). When killed, the lichen, deeply rooted in

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the stone substratum, causes the exfoliation of the outer-most layer (lithocortex) that detaches in small scales, leavingthe underlying stone surface exposed. This surface, how-ever, is extremely porous because of the penetration of thefungal hyphae, leaving the monument defenseless againstthe 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 re-move organisms from monuments. Until a few years ago,the answer would have been affirmative in any situation orcondition. Originally, any monument was certainly free ofbiological colonization of any kind. Bringing it back to itsoriginal state through restoration was seen as a priority byrestoration experts. Today, the growing importance of thebiologist’s point of view has partially changed this state ofthings. Columns, statues, and historical buildings can offerallochthonous substrata for fungi, plants, and animals thatwould otherwise be absent from the area. Many archeologi-cal sites in Latium, the Italian region with Rome, have mon-uments made from exotic materials from distant regions ofthe Roman Empire. Today, such monuments host a remark-ably rich and diverse lichenic flora. Moreover, many of themore than 500 lichen species known to live in Latium arefound only on ancient monuments (Nimis et al., 1987). Sar-dinia’s nuraghi, with their subcylindrical shape and the con-sequent great variety of microclimatic conditions, host agreat number of rare lichen species.

Italy is a signatory of the Rio Biological Diversity Treaty,and this involves severe restrictions on a global scale. Thehigh biodiversity of many archeological and monumentalareas is per se a richness worthy of preservation, which in-dicates the artistic and historical value of a site. The cul-tural importance of biological diversity is a relatively newconcept and not always a priority in artistic and monumen-tal site management. A preliminary study of the impor-tance of organisms from a biological point of view is abso-lutely necessary when planning interventions aimed at theremoval of these organisms from such sites. This, of course,may engender conflicts between biologists and the Monu-ments and Fine Arts Office. Guidelines for the resolutionof such conflicts are still a debated and urgent matter. How-ever, collaboration between biologists and art historiansmay also produce otherwise unthinkable historical valoriza-tion of the biological component of archeological sites. Forinstance, many of Sardinia’s nuraghi, especially those builtwith basalt, are covered with a red-orange lichen, Xanthoriacalcicola, whose color inspires even the names of some nu-raghi, for example, nuraghe ruju (“red nuraghe”). This li-chen causes no relevant damage to the stone substratumso that its removal would be absurd even from a culturalpoint of view, especially if the nuraghe is named after thelichen. Another example is the north wall of a Romantemple in Ostia Antica. This brick wall is completely cov-ered with a thick carpet of a hanging gray lichen, Roccellaphycopsis. This lichen does not produce relevant esthetic

or mechanical damage—the wall is gray rather than red-dish—but someone may have the brilliant idea of remov-ing the “mold” from the wall. However, Roccella is far frombeing a mold: It was the product Romans mainly used forextracting purple dye. This dye is of an inferior quality to“royal purple” extracted from Murex shells (it is less re-sistant to light), but it was also much less expensive. Shipsloaded with Roccella sailed the Mediterranean from Sar-dinia, the Balearic Islands, and African coasts to Ostia.Many islands depended economically on this lichen and nu-merous traces of this commerce are still found in toponymy.The use and commerce of Roccella was so much revived inthe Renaissance that the lichen was named after a Floren-tine family of merchants. Therefore, instead of getting ridof the mold, it would be far more interesting to inform thevisitor on the routes of Roman Roccella trade and on the dy-ing properties of the lichen. This is only one of many casesin which scientific culture and arts and humanities should,for the good of Italian heritage, go hand in hand.

Indoor RestorationAs discussed previously, indoor ecosystems usually have

no primary producers: The main biodeterioration agentsare bacteria, fungi, and insects. The ideal growth conditionsfor bacteria and fungi are high relative humidity, high tem-peratures, and scarce ventilation. Some species are favoredby strong light, whereas others need substrata rich in nitro-gen compounds (dirt, dust, substances used in restoration,etc.). Bacteria and fungi propagate by spores or conidia. Bi-ologists studying the organic matter content of air also studythe propagule content of air in indoor environments, such aslibraries and archive collections. These studies are impor-tant for evaluating potential risks both for books and pa-pers and for the public or people working at these institu-tions. In fact, the propagules of many species are a hazardfor health.

High humidity of indoor environments is one of themost damaging biodeterioration factors because it favorsthe growth of fungi and bacteria. Some of the most ancientand important documents of human culture, such as Egyp-tian papyri or the famous Qumran manuscripts, were pre-served by the dry climate of the subdesert areas wherethey rested for millennia. Italy’s climate is very differentfrom those of Palestine or Egypt. Being a narrow peninsulacooking in a bain-marie—the Mediterranean—the controlof air humidity is a priority even indoors. Paper, parchment,and wood are all hygroscopic to some degree, and as suchtheir conservation requires a careful control on tempera-ture and relative humidity through air-conditioning. Rela-tive humidity can also be controlled through the use of hy-groscopic substances. In addition to natural air humidity,another problem must be considered. Italian archeologicalsites and museums are among the most visited worldwide,and the presence of visitors may increase both tempera-ture and relative humidity indoors. Moreover, the “micro-

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FIGURE 8 Proliferation of green algae in patinas under ar-tificial light in an underground room of the Domus Aurea inRome (reproduced with permission from Caneva et al., 1991).

climatic needs” of visitors often differ from those necessaryto prevent biodeterioration. The microclimate of cathe-drals, crypts, museums, libraries, and art galleries deservesfurther study from the ecological standpoint. These envi-ronments host a variety of microclimates. In some churches,“nave breezes” or “cupola breezes” could be measured, justlike sea and coast breezes are measured. Buildings could bestudied to determine the areas with more frequent temper-ature inversions in which, therefore, water condenses moreeasily. This would avoid the conservation of paintings inplaces in which the microclimatic conditions allow watercondensation, which is particularly dangerous for the backof a painting. Studying these factors is essential to planningcareful biological control. Usually, acceptable temperaturesare expected to vary between 18 and 20°C, whereas relativehumidity should be between 50 and 65% (Gallo, 1985).

To date, the efforts that Italy has devoted to the preser-vation of a heritage that belongs to humanity are not suf-ficient. Nearly the totality of churches in Italy are still notmonitored for biological deterioration agents, and the samecan be said of proper air-conditioning. Moreover, candlesstill burn undeterred. In some environments, such as caves,crypts, catacombs, and other underground rooms, micro-climatic factors are almost impossible to keep under con-trol, especially when these environments host visitors daily.Lighting conditions have a major influence on biodeteri-oration, both directly and indirectly. Organic matter isdegraded by light and this makes environments more sus-ceptible to biological attacks. In particularly humid envi-ronments, artificial light may foster the growth of algal pa-tinas (Fig. 8).

To reduce damage caused by light, the time of exposurecan be shortened and the intensity of light diminished bythe use of filters to eliminate ultraviolet radiation and re-duce red and infrared wavelengths. On the contrary, algalpatinas that grow by artificial light may be controlled by ul-traviolet irradiation without the use of biocides, but onlywhen substrates are not damaged by it (stone, mortar, and

bricks). Often, however, the needs of visitors are the sameof biodeterioration agents.

Even when lighting problems are solved, most insectsand many fungi are still active biodeterioration agents, ableto grow in complete obscurity. The use of fungicides or in-secticides cannot be avoided, but, apart from being toxic toman, the efficacy of these substances is limited in time. Con-trol over some insects, especially those that feed on wood,is particularly difficult. Contrarily to what many think, ter-mites are not at all rare in some parts of Italy. These ani-mals grow and feed inside wood, rarely eating their way tothe surface like other insects do. This makes damage diffi-cult to discover at an early stage: Roof beams and otherwooden objects can be turned to crumbs before anyone isaware of what’s going on inside the wood. Sometimes, theconservation of the immense patrimony that Italy has in-herited may seem a Sisyphean toil. Nevertheless, Italiansmust devote all efforts to this task: This patrimony belongsto the whole of humanity.

Acknowledgments

I thank Prof. G. Caneva, Dr. M. Castello, Dr. E. Rui, Dr. O. Salva-tori, Dr. N. Skert and Dr. M. Tretiach, who have kindly helped withconstructive criticism of the paper or have supplied material for it.

References Cited

ALLSOPP, D., and SEAL, K. J. (1986). Introduction to Biodeterio-ration. Arnold, London.

CANEVA, G., and ROCCARDI, A. (1991). Harmful flora in the con-servation of Roman monuments. In Int. Congr. Biodet. Cul-tural Property, Lucknow, 212–218.

CANEVA, G., and SALVADORI, O. (1989). Sistematica e sinsistema-tica delle comunità vegetali nella pianificazione di interventidi restauri. In Il Cantiere della Conoscenza, il Cantiere del Re-stauro: Atti del Convegno di Studi. Bressanone, 27–30 Giugno1989 (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 ofArt. ICCROM, Rome.

GALLO, F. (1985). Biological Factors in the Deterioration of Paper.ICCROM, Rome.

GARTY, J. (1990). Influence of epilithic microorganisms on thesurface 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 fineart. In Biodeterioration 7: Selected Papers Presented at the Sev-enth International Biodeterioration Symposium. Cambridge,UK, 6–11 September 1987 (D. R. Houghton, R. N. Smith, andH. O. W. Eggins, Eds.), pp. 418– 423. Elsevier, London.

IONITA, I. (1971). Contribution to the study of the biodeteriora-tion of the works of art and of historic monuments. II. Speciesof 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.

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General References

CANEVA, G., NUGARI, M. P., and SALVADORI, O. (1994). La Bio-logia nel Restauro. Nardini, Firenze.

CANEVA, G., NUGARI, M. P., PINNA D., and SALVADORI, O. (1996).Il Controllo del Degrado Biologico, i Biocidi nel Restauro deiMateriali Lapidei. Nardini, Firenze.

GALLO, F. (1992). Il Biodeterioramento di Libri e Documenti, 5thed. Centro di Studi per la Conservazione della Carta, Rome.

LIOTTA, G. (1991). Gli Insetti e i Danni del Legno: Problemi diRestauro. Nardini, Firenze.

MANDRIOLI, P., and CANEVA, G. (Eds.) (1998). Aerobiologia eBeni Culturali. Metodologia e Tecniche di Misura. Nardini,Firenze.

NIMIS, P. L., PINNA, D., and SALVADORI, O. (1992). Licheni e Con-servazione dei Monumenti. CLUEB, Bologna.

LAZZARINI, L., and SALVADORI, O. (1989). A reassessment of theformation 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 vege-tazione lichenica di aree archeologiche del Lazio. Stud. Geo-bot. 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 li-

chens. Giorn. Bot. Ital. 129, 159–184.

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artistic and historical monuments: threatened ecosystems

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