International Biodeterioration 28 ( 1991 ) 187-207
The Biodeterioration of Stone: a Review of Deterioration Mechanisms, Conservation Case
Histories, and Treatment
P. S. Griffin
New York University, Institute of Fine Arts, Conservation Center. New York.
New York 10021, USA
N. I n d i c t o r
Chemistry Dept. Brooklyn College & The Graduate Center. CUNY. Brooklyn.
New York I 1210. USA
&
R. J. Koestler*
The Metropolitan Museum of Art, New York. New York 10028-0198. USA
A BSTRA C T
Several aspects of the biodeterioration of stone are reviewed, including general deterioration mechanisms, deterioration attributed to specific biological os?ganisms, conservation case histories, and treatment options. The literature is cited with emphasis on historic monuments.
INTRODUCTION
Biodeterioration is physical and/or chemical damage effected by biological organisms on an object of historic, artistic, or economic
*To whom correspondence should be addressed.
187
International Biodeterioration 0265-3036/91/$03.50 © 1991 Elsevier Science Publishers Ltd, England. Printed in Great Britain.
188 P S. Griffin. ~ Indictor. R. J. Koestler
importance. Biophysical deterioration is mechanical damage exacted upon the substrate due to surface detachment resulting in superficial losses, or penetration and exerted pressure during growth resulting in increased porosity,. Biochemical deterioration is the direct action by biological organisms" metabolic processes on the substrate. This involves the exudation of organic acids which can etch or solubilize stone, the exudation of organic chelating agents which sequester metallic cations from stone, or the conversion of inorganic substances by redox reactions which form inorganic acids that etch stone and contribute to salt formation. Aerobic organisms produce respiratory, carbon dioxide which becomes carbonic acid and contributes to dissolution of the stone and soluble salt formation.
The biodeterioration of building materials results in the uptake of calcium or other ions, leaving the surface eroded and exposed to water and frost attacks (Bech-Andersen & Christensen, 1983). The inter- relationship between biodegradation and other environmental degra- dative processes has been noted Krumbein (1968), Krumbein & Altmann (1973), and Krumbein & Lange (1978). Biodeterioration when coupled with other environmentally induced degradation is usually synergistic:
the presence of the one makes deterioration by the other all the more effective, Biodeterioration is typically a secondary degradation process which begins after some degree of deterioration has occurred as the result of other causes. This damage can take the form of a rougher surface, a soil-like powder on the surface, or the deposition of inorganic or organic matter. Biodeterioration may be enhanced or subdued by other environmental conditions. A deteriorated monument usually exhibits several types of deterioration processes operating in tandem, making it difficult to attribute damage specifically to a single cause.
Several articles have been published which provide general reviews of the biodeterioration of stone, including Caneva & Salvadori (1989).
Eckhardt (1978), Hueck-van der Plas (1968), Krumbein (1988a, b), Krumbein & Dyer (1985), Pochon & Jaton (1968), Stambolov & van Asperen de Boer (1976) and Tiano (1987).
BACTERIA
Bacteria are found on exposed surfaces, and attack stone chemically.
Under experimental conditions bacterial activity, on stone substrates has been associated with lower pH and metabolic acid formation (Duffet al., 1963; Lepidi & Schippa, 1972a, b; Eckhardt, 1978: Lewis et al., 1985, 1987:
Bock et al., 1988: Lewis et al., 1988a, b: Meincke. 1988: Wolters et al., 1988).
A physical deterioration mechanism has recently been postulated for
B i o d e t e r i o r a t i o n o f s t o n e - - a r e v i e w 189
cyanobacteria and algal films involving lifting of microbial films containing adherent mineral grains in periods of dryness (Ortega-Calvo et al., 1991).
Autotrophic bacteria derive energy from light and chemical redox reactions. Sulphur-oxidizing bacteria convert hydrogen sulphide to sulphuric acid (Lepidi & Schippa, 1972a). The metabolic states of sulphur-oxidizing bacteria from deteriorated stone have been studied experimentally (Sila & Tarantino, 1981), as well as sulphuric acid production (Lepidi & Schippa. 1972a, b. and Lewis e t a l . , 1985. 1988a, b).
gypsum formation (Koestler et al.. 1985) and weight loss of stone dueto solubilized cations (Lewis et al., 1985. 1988a, b). Bacteria in the nitrogen cycle oxidize ammonia to nitrite, and nitrite to nitrate, resulting in nitric acid formation, dissolution of the stone, and soluble salts. Several studies have demonstrated the presence of nitrifying bacteria on deteriorated stone (Lewis, 1985: Meincke et al., 1988: and Wolters et al., 1988). Acid formation and stone dissolution have been demonstrated experimentally (Bock et al., 1988). Other autotrophic bacteria include those that oxidize iron. manganese, and calcium which contribute to dissolution of cations from the stone and surface staining (Koestler & Santoro. 1988: and Wolters et al.. 1988),
Heterotrophic bacteria derive enemy from existing organic substances on the substrate, and also play a role in stone degradation. The presence of heterotrophic bacteria on decayed stone has been well established (Lewi,,~ et al.. i 985: Eckhardt, 1988: Lewis et al., ! 988a. b: and Mav& Lewis.
1988). The deterioration mechanism involves the evolution of chelating agents and organic acids that form salts or complexes with cations from within the stone's matrix (Duff et al., 1963: and Caneva & Salvadori.
1989). Heterotrophic bacteria were found in larger populations on decayed stone, and produced weight loss on limestone and calcareous sandstone in the laboratory due to acid production and solubilized calcium (Lewis et al., 1988b). Deterioration by bacterial metabolic acids has been shown to result in the dissolution of calcium, magnesium, and manganese cations, and the formation of converted silica compounds and iron oxides from the remaining rock structure (Duff et al.. 1963).
Heterotrophic bacteria have also been associated with staining {Realini et al.. 1985).
FUNGI
Fungi on stone are heterotrophic and require the presence of organic material on the substrate prior to growth. Once established they degrade stone mechanically and chemically. Fungal hyphae can penetrate
190 P S. Griffin. N. Indictor. R. J. Koestler
deeply into stone (Koestler
et al.,1985). Fungi produce a variety of inorganic and organic acids (Caneva & Salvadori. 1989). Organic acids such as oxalic, lactic and gluconic function as chelating agents and can demineralize a variety of stone substrates in which calcium, silicon, iron.
manganese or magnesium are leached. Chemical degradation of stone by fungi has been demonstrated experimentally (Silverman & Munoz.
1970: Eckhardt, 1978: Koestler
et al..1985: Jones & Pemberton, 1987:
Eckhardt, 1988: and Kuroczkin
et al.,1988). Fungal acid production has been studied using strains isolated from decaying monuments (Silverman
& Munoz, 1970: Eckhardt, 1978, 1988: Kuroczkin, 1988: and Petersen.
1988). Solubility of cations differs according to the substrates and the cations leached (Silverman & Munoz. 1970). The dissolution, recrystall- ization and redeposition of calcite by fungi have been studied (Jones &
Pemberton, 1987). Hyphal penetration along etched channels and etching of grains of calcite and dolomite have also been demonstrated (Koestler
et al.,1985). Fungi have also been shown to oxidize manganese in the laboratory, causing staining (Petersen
et al.,1988a, b), and have been associated with deteriorated stone
in situexhibiting a powdery, surface (Realini
et al.,1985).
ALGAE
Algae are often the first biodeteriorant to inhabit stone because their primary requirement is light. Unlike fungi and most bacteria, algal infestation is usually readily recognizable through patina formation of distinctive hues. These patinas are usually epilithic associations of algae, but granular, pigmented surface products, as a result of algal activity.
have also been cited (Pietrini
et al.,1985).
Stone degradation by algae occurs by mechanical (Ortega-Calvo
et al.,1991) and chemical action. Deterioration includes increased water retention due to algal films which can exacerbate damage by freeze-thaw cycling, and mineral dissolution by organic acids or chelating agents.
Endolithic algae actively dissolve carbonates to enable penetration into the substrate. The type of microcavity created is species-specific, and related to light requirements (Caneva & Salvadori. 1989).
The deterioration of stone by algae has been reviewed by Caneva and Salvadori (1989), and Garg
et al.(1988), and studied by Grant and Bravery (1985a, b), among others. Instances of algal fouling of stone monuments include those cited by Paleni & Curri. 1972: Trotet
et al.,1972; Lefevre, 1974; Bell, 1984.
B i o d e t e r i o r a t i o n o f s t o n e - - a r e v i e w 191
LICHENS
Lichens are a self-sufficient association of fungi and algae or cyano- bacteria. Both lichens and algal-fungal protolichenous symbiotic associations are associated with stone deterioration. Some articles have reviewed the characteristics of lichens and their deleterious effects on stone (Florian, 1985: Jones & Wilson, 1985: Lallemant & Deruelle. 1987:
Garg et al., 1988). Several instances of lichen activity on stone substrates have been cited, including Monte (1991): Giacobini and Bettini, (1978):
Giacobini et al. (1985) and Bech-Andersen and Christensen (1983).
Lichens cause stone degradation mechanically and chemically.
Mechanical weathering involves growth of the hyphae into the stone and periodic detachment of the thallus related to fluctuations in humidity, resulting in the loss of adherent mineral fragments. Chemical degradation includes the production of carbonic acid. oxalic acid. and water-soluble organic chelating agents. The role of such chelating agents, primarily polyphenolic compounds, was reviewed by Jones and Wilson (1985).
Their role in stone deterioration is established but less well studied than the role of oxalic acid in stone weathering. Carbonic acid is produced when carbon dioxide from respiration is dissolved in water held by the thallus. Deterioration involves depletion of basic cations such as calcium, magnesium, and silica, and accumulation of aluminum and iron. Carbonic acid is a potent weathering agent over long periods of time (Jones & Wilson, 1985).
OXALATE FORMATION
Oxaliic acid is produced by the fungal half of the lichen. The accumulation of oxalic acid increases with the age of the lichen and is more prevalent in calcium-loving species. A close relationship between the fbrmation of calcium oxalate monohydrate, calcium oxalate dihydrate, magnesium oxalate dihydrate, and manganese oxalate dihydrate, and the composition of the substrate has been established (Ascaso & Galvan. 1976: Ornella & Andreina, 1981: Ascaso et al., 1982:
and Jones et al., 1988). The deterioration of calcitic and dolomitic limesllone by lichens has been studied (Ascaso et al., 1982): dihydrate formation was found to be related to water content of the stone. Minerals are chemically affected differentially (Ascaso et al., 1982: Bech-Andersen
& Christensen, 1983).
Oxalate formation may result in a surface patina as well as in chemical
192 P. S. Gr(['fin. N. Indictor. R. J. Koestler
weathering of the stone. Discoloration by patinas are most pronounced on light-colored stones. It is believed that some cases of'scialbatura', a brownish, reddish or yellowish patina whose occurrence has been established on marble buildings and monuments over a widespread portion of Italy. represent the formation of calcium oxalate mono- hydrate (whewellite) and calcium oxalate dihydrate (weddellite) due to lichen activity (Del Monte & Sabbioni. 1987: Del Monte et al.. 1987).
Other instances of pigmented calcium oxalate films have been attributed to past decorative or preservative treatments (Charola et al., 1986:
Agrawal et al.. 1987: and Lazzarini & Salvadori, 1989). or conversion of atmospheric hydrocarbons to oxalic acid (Lazzarini & Salvadori, 1989).
MOSSES AND HIGHER PLANTS
Mosses and higher plants exhibit chemical degradative effects on stone similar to lichen effects. Mechanical damage to stone by mosses is less threatening than for higher plants: they possess rhyzines rather than roots, and require a surface layer of soil before they can grow. Growth at mortar joins, however, can cause problems for the overall structure. Acid production and chelation of cations is caused by higher plant forms:
however, the deleterious effects are less pronounced than for lower organisms which exhibit higher acidity at penetrating appendages.
Bech-Andersen (1986) and Tiano (1987) discuss the deterioration mechanisms of mosses and higher plants. Caneva & Altieri (1988) have surveyed the literature on the biodeterioration of stone by higher plant forms. Oxalic acid formation results in the formation of extracellular whewellite in plant tissues. A study of the effect of ivy, on stone determined that the production ofwhewellite was a cosmetic problem for light-colored stones but not deleterious (Lewin & Charola, 1981):
however, the initial calcium source was not considered.
CASE HISTORIES
Incidences ofbiological deterioration of archaeological monuments and works of art in stone are cited by many authors in tropical locations as well as western, industrialized countries (Agarossi et al.. 1985, 1988;
Agrawal et al., 1986, 1987; Andersson, 1985; Bassi & Giacobini, 1973:
Bech-Andersen, 1986; Bech-Andersen & Christensen, 1983; Bell, 1984;
Benassi et al., 1974: Blanc et al., 1981; Bock et al., 1988; Charola &
Lazzarini, 1987, 1988; Charola et al., 1986: Ciarallo, 1985: Curd, 1974:
B i o d e t e H o r a t i o n o f s t o n e ~ a r e v i e w 193
Curri & Paleni, 1976: Del Monte & Sabbioni, 1987: Del Monte
et al.,1987:
Dragovich, 1981: Eckhardt, 1978, 1985. 1988: Franchi
et al..1978:
Gehrmann
et al.,1988: Ghigonetto. 1985: Giacobini
et al.,1985:
Gugliandolo & Maugeri. 1988: Hale. 1975: Hueck-van der Plas. 1968:
Hyvert, 1973: Ionita, 1971: Jaton, 1973: Jaton & Orial, 1976: Kertesz &
Attila-Nemeth, 1985: Krumbein & Lange, 1978: Kuroczkin
et al..1988:
Lal. 1978: Lailemant & Deruelle. 1987: Lazzarini & Salvadori, 1989:
Lefevre, 1974: Lelikova & Tomashevich. 1975: Lepidi & Schippa, 1972:
Lewin & Charola, 1981: Lewis
et al.,1985, 1988a, b: Monte, 1991:
NisJhiura, 1986: Ornella & Andreina, 1981: Ortega & Martin, 1988: Ortega
etal.,
1988: Paleni & Curri. 1972: Benassi
etal.,1976a: Pallecchi & Pinna, 1988: Pietrini
etal.,1985: Realini
etal..1985: Riederer, 1984, 1986: Sadirin, 1988: Sharma, 1978: Sharma
et al.,1985: Siswowiyanto, 1981: Soediman, 1973: Somavilla
et al.,1978: Subbaraman, 1985: Taylor & May, 1991:
Tiano, 1987;
T u d o r e t a l . ,1990: Vero
etal.,1976: Voute. 1973). Much ofthe conservation literature relies upon surface changes such as encrustations or diiscoloration, as indicators of biological growth. Often the biological organisms responsible for surface changes are not further specified or identified. Few authors attribute physical or chemical damage to biodeterioration.
ENUMERATION AND CHARACTERIZATION OF MICROORGANISMS
Scientific techniques that have been used recently in the study of the deteritoration ofstone by biological organisms can be found in references Bassi & Giacobini (1973), Krumbein & Altmann (1973), Benassi
et al.(1976a. b), Galizzi
et al.(1976), Curri & Paleni (1981 ). Ornella & Andreina
(1981 ), Bell (1984), Koestler
et al.(1985), Bech-Andersen (1986). Eckha rdt
(1988), Gugliandolo & Maugeri (1988), Kuroczkin
et al,(1988), and
Lazzarini & Salvadori (1989). These methods include microscopy such
as scanning electron microscopy (SEM) and polarizing light microscopy
(PLM): fluorescent microscopy: qualitative identification of organic and
inorganic chemical species using techniques such as energy dispersive
spectroscopy (EDS), X-ray diffraction (XRD). thin-layer chromatography
(TLC), gas chromatography-mass spectroscopy (GC-MS), and infrared
spectroscopy (IR): and adaptation of biochemical culturing, counting
and histochemical techniques used to quantify, identify and establish
the presence of biological organisms. Knowledge of the types of species
present and their activity is important in evaluating potential damage
and appropriate treatment.
194 P S. Griffin. N. Indictor. R. J. Koesth'r
T R E A T M ENT
Several authors discuss the treatment of stone affected by biological organisms as general reviews, a n d in a case history context. Caneva a n d Salvadori (1989), R i c h a r d s o n (1973, 1976, 1988), and T i a n o (1978, 1982, 1987) review the treatment o f cultural property: the practical aspects o f the protection of building materials has also been reviewed (Hugo &
Russell, 1982).
In general, the conservation approach to the treatment of stone m o n u m e n t s affected by biodeterioration is characterized by extremes.
The most c o m m o n a p p r o a c h can be characterized as a non-intervention approach, and derives from the perception that other causes of deterioration such as soluble salt migration and freeze-thaw cycling are primary causes o f degradation. Biodeterioration is typically seen as only a cosmetic problem: it is noted chiefly as a difference in a p p e a r a n c e from unaffected stone. This approach reflects a m i s u n d e r s t a n d i n g of the nature of biodeterioration a n d its synergistic effect on other degradative processes.
Treatment involves solving problems posed by the deterioration caused by other physical processes. This approach does not address the problem of biodeterioration, and mav indeed exacerbate it. Aqueous treatments used to clean stone or remove soluble salts are not necessarily effective in removing biological growth, a n d could result in an increase in growth as a result of the wetted stone (Warscheid et al.. 1988).
Consolidation treatments may provide new nutrients for biological growth, ultimately rendering the consolidation ineffective, and leading to further deterioration (Nugari & Priori, 1985: Koestler & Santoro, 1988:
Koestler et al., 1988: Salvadori & Nugari, I988).
Indirect treatment involves the alteration of e n v i r o n m e n t a l factors to make growth unfavorable, such as reducing contact with water, a n d lowering a m b i e n t h u m i d i t y or temperature, or light levels. Effecting e n v i r o n m e n t a l changes has been established as effective means to control biological growth on m a n y substrates (Hopton, 1988: Ley, 1988:
Van der Molen et al., 1980). Although not all r e c o m m e n d e d practices are applicable to exterior stone m o n u m e n t s , biological growths on stone have been controlled in part by c h a n g i n g e n v i r o n m e n t a l conditions.
primarily access to moisture (Lefevre, 1974: C h a r o l a et al., 1986: Del Monte et al., 1987).
Direct treatments affect the life cycle of the biodeteriorant. These may involve cleaning to remove obvious biological remains, treatment with a biostat or biocide to inhibit a n d or eradicate future growth, a n d the application of a moisture barrier or consolidant.
Biodetelqoration o f s t o n e - a review 195
Several case histories involving direct treatment of biodeterioration have been reported for monuments in India (Lal, 1978: Sharma, 1978:
Sharma et al., 1985). primarily using 2-5% ammonia to clean, zinc flurosilicate to inhibit growth, and polyvinyl acetate (PVA) as a moisture barrier. Methods were chosen based on availability and expense, and were reported successful in field usage.
At Borobadur (Siswowiyanto, 1981), biological growths were treated using AC 322 (a variation of AB 57, the "Mora" poultice, Mora et al.. 1984) to clean, and a quaternary a m m o n i u m salt compound to inhibit growth.
Treatment provided temporary inhibition, and periodic maintenance was/is required. Earlier treatments performed at the temple complex also exhibited short-term effects (Hyvert, 1973: Sharma et al., 1985: Warscheid et al., 1988a, b).
Richardson (1973, 1976, 1988) has researched the control of algae and lichens on stone for over 20 years in laboratory tests and field usage.
primarily using a combination of quaternary ammonium and organotin compounds, with periodic maintenance treatments using q u a t e r n a ~ ammonium salts. Prior cleaning of the stone surface is not necessary for most biological films; natural weathering processes remove the dead biological material resulting in cleaned stone. His research has also included borates. PolyborTR, a mixture of borates and boric acid, has been used in the field by Richardson without observed damage. Sodium borates such as Borax have also often been used for cleaning as well as biocidal properties, but can lead to soluble salt formation in urban atmospheres. Borax and Chlorox were used in tandem to control growths on Mayan ruins by Hale (1975).
SonTte studies indicated that no biocide was uniformly effective on all organisms and on all stone substrates (Lloyd, 1971: Richardson, 1973, 1976, 1988; Tiano, 1979; Grant & Bravery, 1981a, b; Bravery. 1982: Hugo
& Rus,;ell, 1982: Emmel et al., 1988). A review of available biocides and recommended usage was compiled by Allsopp and Allsopp (Allsopp &
Allsopp, 1983). Grant and Bravery, among others have provided a model for laboratory testing of the effectiveness of biocides on different organisms and substrates (1981a, b, 1985a, b, 1987). More work needs to be done on testing of biocides on different substrates, and within the framework of other conservation treatments to avoid interactions between subsequently used materials (Tudor, 1990). Quaternary ammonium compounds have been shown to contribute to the degadation of lime mortars and hardened Portland cement (Fearn, 1978). Other potential problems are treatments including biocides or chemical cleaning solutions that introduce materials which can form soluble salts, or consolidation or water-repellent treatments which utilize materials
196 P S. Gr([lqn. N. Indictor. R. J Koe~th,r
which provide nutrients for biological growth. Several recent studies indicate that many materials c o m m o n l y used to waterproof or consolidate stone increased the potential for biological growth (Koestler & Santoro, 1988: Koestler et al., 1988: Nugari & Priori, 1985: Salvadori & Nugari, 1988).
C O N C L U S I O N
The potential for d a m a g e to stone substrates by biological organisms has been d e m o n s t r a t e d by observations in the field and experiments in the laboratory. It is difficult, however, to quantify and attribute observed deterioration o n m o n u m e n t s specifically to biological organisms rather than to other e n v i r o n m e n t a l factors, The type of organism present may affect observed d a m a g e and treatment options. Indirect and direct treatments have been used with success to reduce the deleterious effects of biological organisms. If direct treatment is used, the chosen materials should be evaluated to determine possible chemical changes to stone.
a n d potential reactivity with other materials from previous, current, or future treatments. In addition, materials used in the treatment should be evaluated to determine their prohibitory or promotional effect on the biological organisms which are present.
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