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The Science of the Total Environment 167 (1995) 255-271

Role of fungi in the deterioration of wall paintings

K.L. Garg*, Kamal K. Jain, AK. Mishra


National Research Laboratory for Conservation (NRLC), E /3, Aliganj, Lucknow-226020, India

Abstract

Wall painting wasone of the earliestforms of art all over the world. On account of a variety of factors, thesewall
paintings undergo deterioration. Growth of fungi over these has been considereda major factor in their decay by
many workers and attempts have been made to understand the mechanismof decay as well as to find suitable
fungicidesfor their control. This paper summarizesthe presentstate of knowledgewith regard to the role of fungi in
the deterioration of wall paintings.

Keywords: Wall paintings; Fungal deterioration; Wall paintings;Control of fungal growth

1. Introduction
the aesthetics and stability of the other. There-
The tradition of wall painting is very old, dating fore, it becomes imperative to take proper mea-
back to prehistoric times. These wall paintings sures for the conservation of wall paintings as
which are valuable not only as works of art but well as taking steps for the conservation of the
also as a source of invaluable information about historic buildings.
the contemporary society, occupy a place of pride The wall paintings, generally classified as tem-
in the repertory of any nation’s cultural heritage, pera, secco or fresco depending upon the tech-
and hence hardly need any justification for their nique of execution, possess a layered structure
preservation. These murals are also an integral consisting of support, ground and the paint layer.
part of the structure of the building where these These constituents of wall paintings undergo de-
are present (Fig. 1). Not only from the point of terioration physically, chemically or biologically
view of aesthetics or art history but also from the (Mora et al., 1984; Subbaraman, 1992). Although
point of view of conservation these paintings are generally factors like moisture, salts, atmospheric
considered a part of these historic structures pollution, etc. have been held responsible for the
(Mora et al., 1984), and as such any decay of the deterioration of wall paintings in most cases, many
wall paintings or the structure is bound to affect workers believe that the growth of biological
agencies like fungi is also responsible to a large
extent for the decay of murals (Tonolo and Gia-
*Corresponding author. cobini, 1963; Wazny, 1965; Roznerska, 1967; Ku-

0048-9697/95/$09.50 0 1995 Elsevier Science BV. All rights reserved.


SSDZ 0048-9697(95)04587-D
256 K L. Garg et al. /Science of the Total Environment I67 (1995) 255-271

Fig. 1. The wall paintings are an integral part of a historic building as evident in this old fort at Nagaur, India.

ritzyna, 1968; Ionita, 1973; Krumbein and Lange, by these factors. It is well known that microorgan-
1978; Strzelczyk, 1979, 1981; Bianchi et al., 1980; isms such as fungi grow rapidly in an environment
Saiz-Jimenez and Samson, 1981; Jeffries, 1986, where relative humidity is more than 65%. In the
1991; Hirte et al., 1987; Sorlini et al., 1987; case of wall paintings, the relative humidity re-
Agrawal et al., 1988, 1989, 1991; Sampo and quirements suitable for fungal growth may be
Mosca, 1989; Karpovich-Tate and Rebricova, fulfilled by atmospheric humidity e.g. in the rainy
1991; Rebricova, 1993; Garg and Dhawan, 1994; season when the humidity is generally very high
Garg et al., 1993). Consequently, several studies and the growth of fungi is greater (Tilak et al.,
done over the years by many workers have not 1970, 1972; Strzelczyk, 1981; Tilak, 1986, 1991;
only tried to explain the role played by the fungi Agrawal et al., 1988, 1991). In many cases, the
in the deterioration of wall paintings but have
dampness in the wall is responsible for meeting
also endeavoured to find suitable fungicides for
the humidity requirements (Fig. 2). According to
their control.
Strzelczyk (19811, the spores of most of the fungal
The paper reviews the current state of
forms are capable of utilizing condensation mois-
knowledge in this important area.
ture. Under conditions of high relative humidity
(75-95%), the spores germinate into mycelium. If
2. Factors conducive to fungal growth on wall the humidity conditions remain unchanged, devel-
paintings oping hyphae produce further spores within 48-72
h, dominating the surface of paintings.
Relative humidity, temperature and availability Generally, a temperature range of 20-35°C is
of nutrition are the three most important factors considered optimum for the growth of most
which are considered responsible for mould species of fungi but there are species which are
growth over any type of material. The growth of capable of withstanding a much wider range of
fungi over wall paintings is also governed largely temperature.
KL. Gurget al. /Science of the Total Environment 167 (1995) 255-271 257

Fig. 2. The moisture traveling through the walls or roof is an important factor for the growth of fungi. In this extreme case, the
plaster containing the paintings has fallen off (Nagaur fort, India).

The nutritional requirements of growing fungal nizers of moist frescoes and building materials
forms are met by the presence of organic com- and thus represented the first supply of organic
pounds either in the ground or the paint layer of matter there. Karpovich-Tate and Rebricova
the paintings. Since most of the fungi are depen- (1991) subscribed to this hypothesis. In such cases,
dent upon the organic compounds present in the the death and lysis of such bacteria would pro-
binding media as a source of nutrition, it is mote the growth of fungi. It is already known that
believed that the paintings done in the fresco some fungi could utilize the cell walls of
technique where lime is the medium used for the chemolithotrophic bacteria as the only source of
binding of the pigments should not be attacked by nutrition (Heinen and Lauwers, 1980).
fungi. However, there are many examples where Karpovich-Tate and Rebricova (1991) concluded
fungal growth has been reported from frescoes that, although fungi could use organic substances
(Bianchi et al., 1980; Saiz-Jimenez and Samson, in dust accumulating on the rough surfaces of
1981; Sorlini et al., 1987; Sampo and Mosca, 1989; wall paintings and those in the binding medium of
Karpovich-Tate and Rebricova, 1991; Rebricova, paints and restoration adjunct materials (egg-yolk
1993). It is believed that in the case of frescoes, emulsion) as well as in plaster (cellulose, starch,
the nutritional requirements are met by the pres- milk), it is the trophic interrelationship that plays
ence of organic compounds in the dust layer the main role within microbial communities on
which has accumulated over the paintings. In fact, frescoes, plaster and brick. It has been reported
these dust and dirt particles are not only capable by Sorlini et al. (1987) that materials used in the
of retaining moisture on the surface of the paint- paintings such as casein or Rabbit’s foot gelatin
ings which in turn helps in the growth of fungal allows abundant fungal growth whereas pigments
spores but also attract fungal spores (Tilak et al., like limonite, haematite and malachite when
1970; Tilak, 1991). Saiz-Jimenez and Samson added to Rabbit’s foot gelatin inhibited the fun-
(1981) believed that bacteria were the first colo- gal growth totally or partially.
258 KL. Garg et al. /Science of the Total Environment I67 (1995) 255-271

Since fungi are heterotrophic microorganisms, especially for the species like Cladospotium
the availability of light is not essential for their sphaerospermum, Engyodontium album and As-
growth and hence they are found growing pro- pergillus versicolor. Tresner and Hayer (1971) re-
fusely even in dark comers. According to some ported that Penicillium and Aspergillus species
workers (Bassi and Giacobini, 1973), the growth were outstandingly more resistant to sodium chlo-
of fungi is also dependent upon some other fac- ride than other fungal species.
tors like the nature of the painting constituents, Several workers (Bassi and Chiatante, 1976;
the adaptability and the life span of microflora as Sorlini et al., 1982; Agrawal et al., 1988) have
well as the antagonism between fungi of different reported the presence of bat and pigeon excreta
species. For example, the tolerance of many fun- on wall paintings and these may also provide
gal species to harsh environments is also con- nutrition for the proliferation of fungi.
sidered a factor for the survival of certain fungi
on wall paintings (Saiz-Jimenez and Samson, 3. Fungal flora on wall paintings
1981). Similarly, there are some fungal species
such as Aureobasidiumpullulans which have been Since all the conditions required for the growth
found unable to colonise on the paint films in the of fungi are met easily in the case of wall paint-
absence of other fungal forms like Aspergillus, ings, the problem of fungal growth on wall paint-
Mucor, Altemaria and Cladosporium (Winters et ings is widespread as attested by reports from
different countries like Italy, Japan, Bulgaria,
al., 1976). It is suggested that cellulase from As-
Spain, Romania, Poland, Switzerland, England,
pergillus and Alternaria aids in the initial colonisa-
Russia, Germany, India, etc. The fungal species
tion of these fungi due to hydrolysis of hydroxy
observed by various workers on wall paintings
ethyl cellulose present within the paint film. Ac-
have been reported in Table 1. It may be inferred
cording to Rebricova (1991, 1993), the formation
from this table that although a wide variety of
of different microbial communities on the surface
fungal forms may be present on the wall paint-
of wall paintings depends upon the painting tech- ings, a few forms namely, species of Aspergillus,
niques as well as the climatic conditions. Penicillium, Cladosporium, Altemaria, Curvularia,
Another factor which plays a vital role in the Dreschlera, Chaetomium, Fusarium, Trichodemta,
development of fungi is the dispersal of fungal Gliomastk, Aureobasidium, etc. are more common
spores. Mostly it is through air. However, many in their distribution. In temperate climates, fungi
times the spores may reach the surface through like Aureobasidium pullulans, Cladosporium
the persons visiting the wall painting sites (Emote herbatum and species of Alternaria, Penicillium
and Emoto, 1974; Agrawal et al., 1988, 1991). In and Aspetgillus have been found to be common
some instances, the materials used for the conser- on exterior paint surfaces.
vation treatment are the source of fungal growth
(Sorlini et al., 1982, 1987; Sampo and Mosca, 4. Effects of fungal growth on wall paintings
1989; Hammer and Lux, 1990; Karpovich-Tate
and Rebricova, 1991). The growth of fungi on wall paintings manifests
Environmental pollution has also been con- itself most commonly by discolouration or deteri-
sidered as a contributing factor for fungal growth oration of the surface. The fungi may produce
by Saiz-Jimenez and Samson (1981). According to variously coloured superficial stains which may
them, the existence of hydrocarbons and volatile seriously impair the chromatic and aesthetic ap-
organic compounds in the atmosphere, emitted by peal of the paintings (Figs. 3,4). For example,
the neighbouring oil refineries and cellulose pulp Emoto and Emoto (1974) reported black, green
plants can deposit on the paintings and form a and red stains on wall paintings from ancient
layer of organic compounds able to support the tombs in Japan as a result of fungal growth.
growth of microorganisms. Saiz-Jimenez and Similarly stains of other colours have also been
Samson (1981) are also of the view that saline reported by several workers (Gargani, 1968;
deposits may provide a suitable habitat for fungi, Ionita, 1973; Bassi and Giacobini, 1973; Arai,
K L. Garg et al. /Science of the Total Environment 167 (1995) 255-271 259

Table 1
Fungi isolated from deteriorated wall paintings

No. Fungi Location References

1. Aspetgillus sp., Cephalosporium sp., Frescoes of ancient Tonolo and Giacobini (1963)
Penicillium sp., Dematiaceous hyphomycetes Ostia; church of
St. Khment in Rome;
frescoes of Sinorelli
2. Aspergillus sp., Cephalosporium acremonium, Wall paintings in Wazny (1965)
Mucor mucedo, Oospora crustacea, Polish palaces and
Penicillium sp., Plicaria muralis, Roman catholic
Pullularia pullulans, Pyronema domesticum, churches
Bhizopus nigricans, Sporom’chum roseum,
Stemphylium sp., Torula murorum
3. Altemaria sp., Aspet@llus candidus, Wall paintings of Voronina (1966)
Cephalosporium coremioides, temples of Tsminda-
Circinella conica, Cladospotium atroseptum, Nikolazi and
C. epiphyllum, Fusarium sp., Tsalindzhikha in
Penicillium paxilli, P. puberulum, Georgia, USSR
Sporom’chum bombycinum, Trichoderma roseum,
Mycelia sterilia
4. Cladospotium epiphyllum, Mucor sp., Pozhaisky monastery Voronina (1966)
Sporomchum bombycinum, Mycelia sterilia wall paintings
in Lithunia
5. Asperg&s sp., Gliocladium sp., Frescoes in Florence Gargani (1972)
Mucor sp., Penicillium citrinum,
P. commune, P. camemberti, P. decumbens,
P. frequentans, P. putpurogenum,
P. rest&urn, Stemphylium sp.
6. Aspetgillus versicolor, Bispora meruellii, Wall paintings Kuritzyna (1968)
B. pusilla, Cephalosporium acremonium, Novogorod, Kostroma,
Cladosporium cladosporiokies, C. elatum, Vladimir, Moscow,
C.sphaerospermum, Fusidium viride, USSR
Penicillium meleagrinum,
Plicatia muralis, Sporom’chum gorlenkoanum,
Stemphylium ilicis, Verticillium lateritium
7. Aspetgillus sp., Camposporium sp., Aeroflora of Ajanta Tilak et al. (1970);
Cladosporium sp., Curvularia sp., caves, India Tilak (1991)
Haplosporella, sp., Helminthosporium sp.,
Nigrospora sp., Pithomyces sp.,
Pseudototula sp.,
8. Altemaria sp., Aspergillus sp., Aeroflora of Ellora Tilak et al. (1970);
Cladospotium sp., Curvularia sp., caves, India Tilak (1991)
Helminthosporium sp., Nigrospora sp.,
Pithomyces sp.
9. Altemaria tenuis, Altematia sp., Polychromed wall Emoto (1971)
AspergiNus fimigatus, A. otyzae, A. sydowi, painting panels in
A. versicolor, A. wentii, the main Hall of
Aureobasidium pullulans, Cladosporium herbarum, Horyuji Temple, Japan
Curvularia sp., Nigrospora sphaerica,
Paecilomyces vartotii, Papularia sphaerosperma,
Papulatia sp., Penicillium crustosum,
P. frequentarts, P. multicolor, P. rest&us,
P. rubrum, P. spinulosum, Pestalotia sp.,
Bhodotorula gelatinis, Sporom’chum sp.,
Stemphylium sp., Ttichodenna viride,
Tritiratium album, Zygosporium echinulatum,
Z. parasiticurn
260 KL. Gatget al. /Science of the Total Environment 167 (1995) 255-271

Table 1 ( Continued)

No Fungi Location References


-
10. Altemaria tenuis, Aspergillus amstelodami, Paintings from 14-17th Savulescu and Ionita (1971)
A. niger, A. versicolo~ Botryom’chum centuries in monasteries
artogriseum, B. piluliferum, Chaetomium murorum, of Northern Moldavia,
C. globosum, C. indicum, Circinella sydowi, Voronet, Sucevita,
Cladosporium herbarum, Cunninghamelk echinulata, Humor, Arbore, Patraati,
Geotrichum candidum, Mucor spinosus, Varatec, Agapia, Putna,
Penicillium lilacinum, Scopulariopsis brevicaulis, the Cozia monastery
Stachybottis atra, S. cylindrospora, the princely church
Stemphylium Perrfonne, Torula herbarum, at Curtea de Arges
Trichodenna viride
11. Altematia sp., Chaetomium sp. Murals of church of St. Slavova (1972)
Petka Samardzhiyska, St.
Panteleymon in village of
Boyan, Church of Holy
Archangel in village of
Arbanasi, Bulgaria
12. Cladospotium cladosporioides, Frescoes in cathedrals, Bassi and Giacobini (1973);
C. sphaerospennum, Cladosporium sp. tombs, and burial vaults, Giacobini et al. (1991)
Italy
13. Aspergillus echinulatus, A. niger, A. repens, Wall paintings of Ionita (19731
Chaetomium herbarum, Scopulatiopsis brevicaulis, 14-17th cent. from Northern
Stemphylium macrosporoideum, S. piriforme Moldavia (Humor, Sucevita
Voronet, Arbore, Patrauti,
Parhauti, Varatech, Moldavita)
14. Altemaria altemata, Cladospotium sp., Wall paintings of Ozuka Emoto and Emoto (1974)
C. herbamm, Epicoccum putpurascens, tomb (Fukuoka), Chibusan
Gliochsdium roseum, G. virens, Gliomastix sp., tomb (Kumamoto), Japan
Pencillium sp., P. citreo-viride, P. citrinum,
P. janthinellum, P. oxalicum, P. purpurogenum,
Trichoakna viride, Verticillium sp.
15. Acremonium roseum, Aspergillus echinulatus, Wall paintings, Romania Istudor et al. (1976)
Penicillium chrysogenum, Stemphylium piriforme
16. Filamentous fungi Paintings of Etruscan tombs, Curri (1979)
Belfry in Arezzo, Italy
17. Micromycetes Frescoes of the Ragione Sorlini et al. (1979)
Palace in Milan, Italy
18. Penicillium chermisinum, P. implicatum, Paintings of Roman Smyk (19791
Sporotrichum grisellum, Trichodenna viride Catholic Church in Dembna
Podgolyanskom, Poland
19. Cladosporium cladosporioides, Penicillium Paintings of burial vault Bianchi et al. (1980)
lanoso-coeruleum of St. Sebastian in Pavia,
Italy
20. Altemaria altemata, Acremonium charticola, Wall paintings of the Saiz-Jimenez and Samson (1981)
Arthrinium state of Apiospora montagnei, monastery of Santa Maria
Aspergillus versicolor, Bottytis cinerea, de la Rabida, Huelva, Spain
Chaetomium elatum, Chaetomium sp., Chtdosporium
sphaerospermum, Cunninghamella echinulata,
Engyodontium album, Penicillium brevi-compactum,
P. chtysogenum, P. citrinum, P. decumbens,
P. frequentarts, P. nigrkans, P. raciborski,
P. verrucosum var. &opium, Phoma glomerata
21. Micromycetes Wall paintings of the Hadjivulcheva and Gesheva (19821
church of St. Panteleymon
in the village of Boyan,
Bulgaria
K. L. Garg et al. / Science of the Total Environment 167 (1995) 255-271 261

Table 1 ( Continued)

No. Fungi Location References

22. AspetgUus sp., Cephalosporium sp., Wall paintings of Sorlini et al. (1982)
Ciadosporium sp., Epicoccum sp., Penicillium sp., Palazzo della Ragione
Scopulariopsis sp. in Milan, Italy
23. Aspergilrus niger, Cladospotium cladospotioides, Wall paintings of the Crippa (1983)
C. cucumerinum, Epicoccum purpurascens, Old Churches of Pavia,
Fusarikm o~spomm, PeniciNium fresuentans, Italy
P. oxalicum
24. Aspe rgillus glaucus Wall paintings in the Raschle (1983)
Swiss Baroque monastery church,
Switzerland
25. Cladosporium sp., Doratomyces sp., Fusarium sp., Paintings of Takamatsu- Arai (1984)
Mucor sp., Penicillium sp., Trichoderma sp., zuka tumulus, Japan
Verticillium sp.
26. Alternaria sp., Aspergillus sp., Cladosporium Mural paintings of Arai (1984)
sp., Penicillium sp., Pestalotia sp., Torazuka tumulus,
Trichodenna sp. Japan
27. Phialophora sp. Nakata-Oketsu tumulus, Arai (1984)
Japan
28. Trichodema sp. Hayama-Oketsu tumulus, Arai (1984)
Japan
29. Beauueria alba Wall paintings in Jeffries (1986,199l)
Canterbury cathedral,
England
30. Micromycetes Wall paintings from the Lyalikova and Petushkova (1986)
17th Century in the church
of John Bogoslov in Rostov,
USSR
31. Altemaria sp., Aschersonia sp., Aspergillus sp., Wall paintings of Hirte et al. (1987)
Chaetomium sp., Mucor sp., Penicillium sp., Sans Souci Palace, Germany
Stemphylium sp., Trichodenna sp.
32. Altemaria sp., Aureobasidium puilulans, Wall paintings of the Rebricova et al. (1987);
Chaetomium sp., Cladospotium cladosporioides, Trinity cathedral in Rebricova (1991,1993)
C. sphaerospermum, Sremphylium botryosum Aleksandrov, USSR
33. Aspergillus repens, A. versicolor, Bo*tis Wall paintings of the Rebricova et al. (1987);
cinerea, Cladosporium cladosporioides, Pantelimonovsky Rebricova (1991, 1993)
Mycelia sterilia, Penicillium chrysogenum, cathedral in New Athon,
P. verrucosum var. cyclopium, Stemphylium sp., USSR
Tritirachium album
34. Acremonium charticola, Cladosporium Wall paintings of the Rebricova et al. (1987);
sphaerospermum, Sporom‘chum sp. George cathedral in Rebricova (1991,1993)
Novgorod, USSR
35. Acrothecium sp., AspergiNus niger, Gambara’s Frescoes, Sorlini et al. (1987)
AspergiNrrs sp. (3) Brescia, Italy
36. Acremonium indicum, Alfernaria alternata, Wall paintings of Agrawal et al. (1988, 1991);
Aspergillusjlavus, A. nidulans, A. niger, Ajanta Caves, India Dhawan et al. (1991);
A. terreus, A. versicolor, Cladospotium Garg and Dhawan (1994)
cladospon’oides, C. herbarum, Curvularia Garg et al. (1991)
lunata, C. pallescens, Chaeromium globosum,
Drechslera australiensis, D. hawaiiensis,
Emericella nidulans, Epicoccum n&rum,
Fusarium oxVsporum, F. solani, Macrophomina
phaseolina, Memnoniella echinata,
Mycelia sterilia, Paecilomyces variotii,
Rhizopus nigricans, Srachyborrys atra,
Trichoderma halzianum
262 K.L. Gang et al. /Science of the Total Environment 167 (1995) 255-271

Table 1 ( Continued)

No. Fungi Location References


37. Aspe@lus versicoloc Beauvetia sp., Paintings of the Rebricova and Karpovich (1988);
Botrytis cinerea, Chaetomium globosum, cathedral of Birth Rebricova (1991,1993)
Cladosporium sphaerospennum, Epicoccum nignon, of the Holy Virgin
Geomyces pannorum, Penicillium chtysogenum, in Russia
P. cyclopium, P. verrucosum, Sporomchum sp.,
Verticillium htmellicola, V lecanii
38. Acremonium charticola, A. terricola, Paintings of the Rebricova (1988,1991,1993)
Altemaria sp., Aspergillus sydowi, cathedral of Birth of
A. versicolor, Aureobasidium pullulans, Holy Virgin (16th
Candida sp., Cladosporium cladosporioides, Cent.) in Ferapontovo,
C. sphaerospermum, Hyalodendron sp., Russia
Mycelia sterilia, Trichoderma viride,
Tritirachium album
39. Micromycctes Paintings of the cathedral Lyalikova and Petushkova (1988);
of Birth of the Holy Virgin Petushkova et al. (1989)
(16th cent.) in Ferapontovo,
USSR
40. Aspergillus flavus, A. sydowi, A. wrsicolor, 15th Cent. frescoes of Sampo and Mosca (1989)
Asper$lus sp., Bohyth cinerea, Ognissanty church in
Cladospotium cladosporioides, C. sphaerospennum, Florence, Italy
Coniothytium cerealis, Engyodontium sp.,
Oidiodendron cerealis, Penicillium brevicompactum,
P. chrysogenum, P. meleagrmum, P. notatum,
P. purpurogenum, P. rugulosum, P. variabile,
Bhodotonda sp., Tilletiopsis sp.,
Trichoderma hatzianum, Mycelium sterile moniliaceum,
Mycelium sterile dematiaceum
41. Acrodontium cratertfonne, Beaucmia bassiana, Wall paintings of the cathedral Karpovich-Tate and Rebricova (1991)
Cladosporium sphaerospermum, Fusidium viride, of the Nativity of the Virgin
Geomyces pannorum, Penicillium sp., in the Pafnutii-Borovskii
Phialophora sp.,Tritirachium album, monastery, USSR
Vertkillium lamellicola
42. Acremonium sp., Aspergillus versicolor, Wall paintings of the church Rebricova (1991,1993)
Cladosporium herbarum, C. sphaerospermum, of Precursor in Yaroslav and
Hyalodendron sp., Penicillium verrucosum the church of Assumption of
var. cyclopium, Tritirachium album the Holy Virgin in Meletovo,
USSR

1984, 1985; Agrawal et al., 1988). Fungal growth the cause of blisters and craters (Tonolo and
may also result in serious alterations in the paint- Giacobini, 1963; Kuritzyna, 1968). According to
ings through hyphal penetration or deterioration Kowalik (1984), who observed the fruiting bodies
of the substrate resulting in the detachment of of fungi Phoma sp. and Aureobasidium sp. under-
fragments (Giacobini and Lacerna, 1965; Ionita, neath the pigment layer they concluded that such
1973; Strzelczyk, 1981). According to Gargani a condition may result in the rupture of the
(19681, who studied the vigorous attack of fungal pigment layer in the form of small blisters
growth on the surface of wall paintings in Flo- (Whiteley, 1972). According to Tonolo and Gia-
rence after a flood, the spreading of fungal hy- cobini (19631, abundant sub-surface growth of
phae was responsible for the powdering of the fungi greatly contributes to loosening of the bind-
weakened pigment layer. The growth of fruiting ing medium between the pigment and its support.
bodies of fungi like perithecia, pycnidia and Karpovich-Tate and Rebricova (1991) associated
stroma under the surface has been reported to be the growth of fungi with the formation of a com-
K.L. Garg et al. /Science of the Total Environment 167 (1995) 255-271 263

pact yellowish-white coating on the restored fres- environmental conditions, any of the two
coes in the Cathedral of Pafnutii-Borovskii. The processes could be predominant and the decay
growth of fungi may also damage the different may proceed either from the surface to the subs-
constituents of the paintings by the chemical ac- trate or vice versa, depending upon the localiza-
tion of its various secretions. According to Strzel- tion of the fungi.
czyk (1981), the extracellular enzymes, enabling
the hyphae to penetrate inside the paintings, cause
5.1. Physical decay
deterioration of all components of the object.
This type of decay of the wall paintings is
mainly due to the physical action of the growth of
5. Mechanism of decay of wall paintings by fungal fungal hyphae or the fruiting bodies either on or
action below the surface. According to Wazny and Rud-
niewsky (1972), the fungal hyphae growing inside
The decay of wall paintings by fungal action the paint layer caused dislodging of the various
may be both physical as well as chemical in na- layers. A similar effect may be brought about by
ture. Generally, both these processes occur simul- fungal fruiting structures, which are frequently
taneously. Although depending upon the kind of formed under the surface of the painting layer. If
the substrate and the fungal form as well as the the growth is over the surface, it results in the
formation of filaments, which on spreading over
the surface mask the colour and design of the
paintings.

5.2. Chemical decay


Besides physical damage to the paintings, the
fungi are also responsible for chemical decay of
the wall paintings through their metabolites ei-
ther by assimilation or dissimilation processes. In
the assimilation process, the fungi use the con-
stituents of wall paintings as a carbon source
through enzyme production, whereas in the dis-
similation process, the decay is mainly by the
excretion of waste products or secretion of
metabolic intermediates including acids and pig-
ments which can damage, stain or disfigure the
surface. The diffusion of metabolic products
between cells and the surrounding environment is
facilitated rapidly on account of the high surface
to volume ratio of fungi. The chemical deteriora-
tion of wall paintings on account of fungi may
proceed in either of the following ways:
Acid production. During metabolic activity, fungi
give out acids like gluconic, citric, oxalic, malic,
succinic, itaconic, etc. in varying amounts
(Gomez-Alar&n and de la Torre, 1994). These
acids are capable of reacting with the various wall
painting constituents either by solubilization of
Fig. 3. In this wall painting at Nagaur fort (India), the fungal the cations or by chelation with metal ions pre-
growth is visible in the form of black stains. sent in the pigments. Many a time, the acids given
264 K.L. Garg et al. /Science of the Total Environment 167 (1995) 255-271

Fig. 4. The growth of fungi over the paintings is responsible for the covering of painting designs.

out by the fungi produce salts, for example, oxalic The extracellular enzymes play an important role
acid may react with the calcium ions to produce in this process. These enzymes transform complex
whewellite and wedellite minerals. The formation molecules such as protein, cellulose, hemicellu-
of salts like oxalates of calcium, iron, magnesium, lose, lignin, etc. into simple ones that are water
etc. was also confirmed by the experiments car- soluble. The enzymatic activity results in the loos-
ried out by G6mez-Alar&n and de la Torre (1994) ening, cracking or falling of the paint layer. It also
using acidogenic fungi in conjunction with sand- destroys the binder present in the paint layer,
stone, limestone and granite. plant residues in the plaster as well as restoration
The carbon dioxide, produced by all aerobic materials (Rebricova, 1991, 1993). Extracellular
organisms including fungi as a result of respira- enzymes also enable hyphae to penetrate inside
tion, may change in an aqueous/humid environ- the paint layer.
ment to carbonic acid. This carbonic acid is capa- Pigment formation. As a consequence of their
ble of dissolving the calcium and magnesium car- metabolic activity, many fungi produce organic
bonates of the plaster layer to form calcium and pigments of different colours (green, grey, blue,
magnesium bicarbonates which are readily solu- purple, violet, etc.). These pigments, belonging to
ble in water. In addition to direct attack on wall different classes of compounds like an-
paintings, the production of acids favours the thraquinones, xanthones or carotenes, are charac-
growth of acidophillic fungal species as secondary teristic of different species but the colour of the
growth, thus hastening the decay process. stain depends not only upon the chemical compo-
Enzyme production. The fungi, producing dif- sition of the pigment but also on other factors
ferent types of enzymes, are also capable of af- like the composition of painting constituents,
fecting the paintings through the activity of their presence of other microbial species or environ-
enzymes (O’Neil, 1986; Rebricova, 1991, 1993). mental conditions. The release of pigments on
The enzymes, which are protein molecules of high the substrate or the presence of fungi containing
specific activity, perform their catalytic activity by pigments causes the appearance of different
combining with the various painting components. coloured stains or patches on wall paintings
K.L. Garg et al. /Science of the Total Environment 167 (1995) 255-271 265

(Giacobini and Lacerna, 1965; Gargani, 1968; the wall paintings is considered useful if these
Ionita, 1973; Bassi and Giacobini, 1973; Emoto chemicals are capable of inhibiting the fungal
and Emoto, 1974; Arai, 1984, 198.5; Agrawal et growth effectively without having a negative ef-
al., 1988). Once formed, these stains are almost fect on the painting materials. Unfortunately, in
impossible to remove from the surface of the most cases, the conventional paint fungicides do
paintings. not always prove effective or they have side ef-
fects (Kaplan, 1968; Pauli, 19721. Thus, the search
6. Control of fungal growth on wall paintings for a better and more suitable fungicide is still
continuing.
As mentioned earlier, the growth of fungi, which Another problem generally encountered in the
has been recognized as an important factor in the use of fungicides is the method of application
deterioration of wall paintings, especially in tropi- without leaving areas of wall paintings untreated,
cal countries, requires proper preventive and con- as even a few fungal spores are enough to repro-
trol measures for safeguarding the priceless mu- duce new colonies.
rals. The control measures include modification The following three methods are commonly
of the factors which are responsible for the growth used for the application of fungicides on wall
of different fungal forms and the removal of paintings:
already existing fungal species. 1. Injection method: This method is used to kill
Since moisture is the most vital factor which the fungal growth that is located below the sur-
facilitates fungal growth, the control of biodeteri- face or in the substrate.
oration of wall paintings could be achieved by 2. Spray method: This method is particularly
proper ventilation of the area and by taking suit- suitable for covering large areas. However, the
able measures to avoid moisture condensation on penetration of fungicidal solution to deeper areas
the surface. Such optimization of temperature is difficult to ensure (Pauli, 1972).
and moisture was successfully carried out by Re- 3. Brushing method: To ensure a better contact
bricova (1991, 1993) at the Cathedral of Birth of between the affected surface and the fungicide,
the Holy Virgin in Ferapontovo. In some cases, this method seems to be quite effective. However,
the use of hydrophobic materials to avoid con- the method is time consuming and requires at
densation has also been suggested but in many least two or three treatments.
cases the use of such materials may prove Generally, the fungicides which are available
counter-productive, especially when the source of on the market are aimed to be effective on plant
moisture is from the substrate. Air conditioning parasites, while their activity on saprophytes such
of the area has also been recommended as a step as common fungi has not been tested in most
to control the environmental conditions. In order cases. Therefore, Bianchi et al. (1980) suggested
to eliminate another important source of mois- that before applying a biocide on wall paintings, it
ture, i.e. wall humidity, use of epoxy resins as a should be first tested in vitro on fungi samples
damp proof course has also been made (Saiz- obtained from wall paintings. In fact, an ideal
Jimenez and Samson, 1981; Rebricova, 1991, fungicide for use on wall paintings should possess
1993). However, in many cases, the modification the following characteristics (Strzelczyk, 1981): (1)
of environmental conditions, which requires regu- It should have a high fungitoxic value so that it
lar monitoring, may not be easy besides being a can be used in low concentrations; (2) It should
costly proposition. Although modification of cli- not affect any component of the wall paintings i.e.
matic conditions may be helpful in reducing fur- the fastness of pigments, the binders, the glues in
ther growth of fungi, one of the biggest problems the ground and the plaster; (3) It should have low
faced by the conservators is to kill the already volatility to ensure a prolonged protective effect
existing growth. A variety of chemicals, commonly on wall paintings; (4) It should not be liable to
termed biocides (fungicides), have been used for ageing or associated with the formation of nox-
the purpose. The use of biocides for protecting ious decay products; (5) It should not loose its
266 RL. Gag et al. /Science of the Total Environment 167 (1995) 255-271

fungitoxic properties by combining with con- present in excess increased the fungal resistance
stituents of the wall paintings treated; (6) It should of lime plaster containing organic additives. An-
have low toxicity to man. other method suggested for the prevention of
The chemicals that have been used by conser- fungi is the protection of biologically nonresistant
vation scientists for the control of fungal growth materials (Rebricova, 1993). For example, in Po-
either in vitro or in situ have been reported in land for the protection of PVS dispersions used in
Table 2. However, some workers are of the view the restoration of wall paintings, sterinol (QAC),
that the wall paintings should be first treated with tributyl tin oxide (TBTO) and phenylmer-
a suitable disinfectant. But only a rather limited cuthiomethyl were recommended (Koneczny and
choice of suitable disinfectants is available. This Strelczyk, 1983). Similarly, in Russia natural glues
is due to their short-term effect. According to such as hen’s egg yolk, sturgeon glue, leather glue
Tonolo and Giacobini (19631, the wall paintings and synthetic glues based on vinyl acetate,
should be first disinfected with ethylene oxide and organo-silicon compounds and acrylic dispersions
then kept in a nitrogen atmosphere. Saiz-Jimenez were used for strengthening the paint layer as
and Samson (1981) have reported that ethylene synthetic polymers were found to be superior to
oxide and methyl bromide are effective against natural polymers against biological growth (Re-
selected isolates of fungi in vitro. Hueck-van-der bricova, 1991, 1993; Karpovich-Tate and Rebri-
Plas (1966) recommended p-chloro-m-cresol for cova, 1991).
disinfecting paints, glues and binders. Payne
(1963) found p-chloro-m-cresol and phenyl mer- 7. Methodology used for the study of fungi on wall
curic acetate to be effective only for a limited paintings
duration as disinfectant but still superior to nys-
tatin (antibiotic used by Gargani (1968) for de-
In order to identify the various fungal forms
stroying heterotrophic microorganisms on fres-
growing over the surface and to select a proper
coes in Florence). However, Strzelczyk (1981) re-
biocide for conservation treatment, it is important
commended the use of 0.3% p-chloro-m-cresol to carry out scientific investigations. The method-
and 0.1% phenylmercuric acetate in ethanol, for ology involves not only the identification of da-
disinfecting mural paintings, based on his labora- mage causing fungal flora but also the effect of
tory work. various fungicides on these forms as well as paint-
To check the growth of fungi on wall paintings, ing materials. In addition to the fungal species
the disinfecting effect of the fungicide is not growing over the surface, it is also necessary to
sufficient, as a rule, for even if the cause of the carry out, wherever possible, quantitative analyses
growth of fungi was leakage that has been re- in order to ensure correct interpretation of re-
moved, the process of drying of massive guarding sults as there may be many species which though
structures is sufficiently long. Therefore, fungi- present on the surface of the wall paintings or in
cides providing protection for a long time are the environment, might be dormant and thus not
preferable (Rebricova, 1991, 1993). In this con- responsible directly for the decay of wall paint-
nection, the selection of a solvent and method of ings. According to Strzelczyk (1981), out of a wide
application of biocide solution is important. variety of fungi observed over the wall paintings
Since most of the fungicides do not have a only a few develop and damage the paintings. He
long-term effect, one of the approaches is to confirmed his findings by comparing the fungal
make use of biologically resistant conservation flora identified directly under the microscope with
materials. For example, some workers have stud- the fungi observed on the culture media inocu-
ied the fungal resistance of materials like gypsum, lated with the samples overgrown with fungi. Some
lime, polyvinyl acetate, carboxymethyl cellulose, workers have employed non-destructive tech-
casein, gelatin, egg albumin, etc. (Raschle et al., niques like cotton swab and paper stick methods
1989; Rebricova, 1991, 1993; Karpovich-Tate and for sample collection from murals (Agrawal et al.,
Rebricova, 1991). It was noted that lime when 1988; Caneva et al., 1991).
KL. Gag et al. /Science of the Total Environment 167 (1995) 255-271 267

Table 2
Biocides used for the control of fungi on wall paintings

Biocide Effective concentration Reference Remarks

Bavistin 100 ppm Bianchi et al. (1980) Tested in vitro,


(Carbendaziml in distilled highly effective;
water tested in situ
also; yearly treatment
recommended
2. 3enlate 100 ppm in 50% Bianchi et al. (1980) As above
(Benomyl) ethanol
3. Catamine-A 2% soln. Kuritzyna (19681 Tested in vitro
4. Cational- 2% soln. Kuritzyna (1968) As above
5. Cetyl pyridinium Kuritzyna (1968) As above
bromide
6. Cetyl pyridinium 1% in ethanol Kuritzyna (19681; As above
chloride or in distilled water Agrawal et al. (1991)
7. Dichlorofluanide Raschle (19831 Tested in situ
8. Florasan 100 ppm in distilled Bianchi et al. As in No. 1
(Imazalil) water. (1980)
9. Organo-tin In 70% isopropanol Raschle (1983) Tested in situ and
compounds found most suitable
10. Orthophenylphenol 0.02% in ethanol Agrawal et al. Tested in vitro
or in distilled (1991); Dhawan et al.
(1991)
11. Parachloro-m (1) O.l-0.3% Jeffries (1986,1991); Disinfections are of
-cresol ethanol Hueck-van-der Plas limited duration
(1966); Strzelczyk
(1981)
(210.02% in ethanol or Agrawal et al. (1991); Tested in vitro
in distilled water Dhawan et al. (1991)
12. Parachloro-m 0.3% + 0.1% Strzelczyk (1981); No adverse effect
-cresol + Phenyl ethanol Jeffries (1986,1991) on murals
mercuric acetate
13. Phenyl mercuric (1) 0.1% in alcohol Jeffries (1986,1991); Highly fungitoxic. No
acetate Strzelczyk (1979, 1981) noxious effect on
murals
(2) 0.001% Agrawal et al. (1991) Tested in vitro
in alcohol
14. Prevent01 R-90 0.05% in ethanol or Agrawal et al. (1991) Tested in vitro
(Benzalkonium distilled water
-chloride)
15. Quatemary Raschle (19831; Tested in situ
ammonium Kuritzyna (1968)
compounds
16. Quaternary - Raschle (1983) Tested in situ
ammonium
compounds +
organo-tin
compounds
17. Sodium- 0.1% in ethanol Agrawal et al. (1991) Tested in vitro
pentachloro or in distilled
phenate water
18. Ethylene oxide - Saiz-Jimenez and Tested in vitro;
Samson (1981) effective
Methylbromide As above As above
19. Desogen 2.5 mg/cm’ Sorlini et al. (1982) In situ spray, highly
(aqueous spray) effective, colourless
268 KL. Garg et al. /Science of the Total Environment 167 (1995) 255-271

Table 2 ( Continued)

No. Biocide Effective concentration Reference Remarks

20. Organo-tin - Rebricova (1988) Field trials directly


compound and on lower painting
Methacid layers. Effective
up to 2 years
21. Prevent01 R-80 1% aqueous solution Nugari et al. (1991) Tested in situ on
previously mechanically
cleaned patches
Vancide-51 As above As above As above
TBTO (Tributyl- As above As above As above
tin oxide)
Prevent01 As above As above As above
R-80 + TBTO (1:l)
22. Sodium penta- 1% Agrawal et al. (1991); Tested on replicas.
chlorophenate Garg et al. (1991); Effective up to 2.5 years
Dhawan et al. (1992)
Phenylmercuric 0.1% As above Tested on replicas.
acetate Effective up to 1 year
Zinc DDC 1% As above Tested on replicas.
Causes whitening and
effective up to 1 year
p-Chloro-m 0.5% As above Tested on replicas.
cresol Effective only up to
1 month
Prevent01 R-90 0.5% As above As above
0-Phenyl 10.5% As above As above
phenol

The collection of samples, a prerequisite for 1991). However, in order to avoid the discrepancy
any type of investigation, varies with the nature of as a result of the presence of dormant fungal
the deterioration, e.g. superficial powder, crusts, species, many workers consider the method of
flakes, etc. The samples are collected with the direct microscopic examination of fungal flora as
help of sterilized tools (scalpels, brushes, swabs, a better choice.
paper sticks, etc.) in sterilized cases. Where it is To carry out a quantitative estimation of fungal
not possible to analyze the samples immediately, contamination of the wall paintings, use is made
these are preserved at 4°C until such time as they of a number of quick tests which make it possible
can be analysed in the laboratory. Many workers to obtain reliable results. For example, fungal
(Gargani, 1968; Agrawal et al., 1988) have pro- contamination is determined by measuring the
posed the sampling of fungal growth directly from amount of adenosine triphosphate (ATP) and
the wall paintings with the help of sticky tape. components of the cellular wall and membrane
The sticky tape directly removes the powdered lipids and also by the activity of the glycolysis
paint together with fungal fruiting bodies. In this ferments. In order to detect viable and metaboli-
way, direct identification of fungi becomes much cally active cells, use is made of fluorescent dyes
easier. These samples are then cultured in the as well as the indirect immunofluorescence
laboratory for further investigations with the help method, scanning electron microscopy and meth-
of either a stereomicroscope, transmission elec- ods based on the variation of electrical resistance
tron microscope or scanning electron microscope of the substrate in the development of fungi (Mc-
(Gargani, 1968; Bassi and Giacobini, 1973; Carthy, 1989). But these methods are used infre-
Bianchi et al., 1980; Strzelczyk, 1981; Saiz-Jimenez quently as they require a relatively large amount
and Samson, 1981; Rebricova, 1984, 1988; Kar- of sample from the priceless wall paintings.
povich-Tate and Rebricova, 1991; Giacobini et al., After the identification of fungal flora present
K.L. Garg et al. /Science of the Total Environment 167 (199.5) 255-271 269

Agrawal, O.P., S. Dhawan, K.L. Garg, F. Shaheen, N. Pathak


and A. Misra, 1988. Study of Biodeterioration of the Ajanta
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Bianchi, A., M. Favali, N. Barbieri and M. Bassi, 1980. The
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Building Mycology. E & FN Spon, London, pp. 239-259.
to Shri Anil R. Singh for providing the pho-
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