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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.
◗
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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-
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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.
◗
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Biodeterioration of Works of Art
558
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◗
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
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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-
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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
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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.
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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).
◗
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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
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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,
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FIGURE 4 Detail of fungal attack on a painting on canvas
(photo courtesy of O. Salvadori).
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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).
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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-
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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).
◗
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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-
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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).
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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-
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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.
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LIOTTA, G. (1991). Gli Insetti e i Danni del Legno: Problemi di
Restauro. Nardini, Firenze.
MANDRIOLI, P., and CANEVA, G. (Eds.) (1998). Aerobiologia e
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NIMIS, P. L., PINNA, D., and SALVADORI, O. (1992). Licheni e Conservazione dei Monumenti. CLUEB, Bologna.
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