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International Biodeterioration & Biodegradation 55 (2005) 131–139

A comparative study of the major microbial biomass of biolms onexteriors of buildings in Europe and Latin America

Christine C. Gaylarde a, , Peter M. Gaylarde b

a Department of Biophysics, Federal University of Rio Grande do Sul (UFRGS), Campus do Vale, Porto Alegre - RS, 91500-970, Brazil b Prac - a Julio Bozzano 51/1, Porto Alegre - RS, Brazil

Received 9 May 2004; received in revised form 22 September 2004; accepted 29 September 2004

Abstract

Microorganisms in biolms on building surfaces include algae, bacteria and fungi and cause discolouration and degradation, butdenitive information about preferences of microbial groups for given building substrates and how this is affected by environmentalconditions is lacking. Major biomass in 230 biolms from buildings in seven Latin American and six European countries wasanalysed. Substrates included composites (cement, mortar, concrete, brick), painted surfaces and dimensional stone. Cyanobacteria,mostly coccoid types, were most frequently present as major biomass in LA, followed by fungi, whereas in Europe algae were mostcommon, followed by cyanobacteria. Algae were more frequent than other groups on all substrates in Europe. Fungi, particularlyuncommon as major biomass on stone, were more frequent on paint than on all other substrates (40% cf. 12%). Actinomycetes(frequently streptomycetes) were detected occasionally as major biomass, mainly on stone; climatic differences may explain therelative prevalence of this group in Europe.r 2004 Published by Elsevier Ltd.

Keywords: Actinomycetes; Algae; Biolms; Buildings; Cyanobacteria; Fungi; Paint; Stone

1. Introduction

The importance of microbial biolms in the deteriora-tion and degradation of historic and modern buildingexteriors, a process commonly referred to as ‘‘weath-ering’’, is well recognized ( Gaylarde and Morton, 1999,2002 ). There have been a number of studies on themicroorganisms present on building surfaces ( Ortega-Calvo et al., 1991; Garcia de Miguel et al., 1995; Hirsch

et al., 1995; Ortega-Morales et al., 2000; Tomaselli et al.,2000; Crispim et al., 2003 ). Biolms on building fac - adescontain algae, cyanobacteria, heterotrophic bacteria,fungi, protozoa and a variety of small animals andplants. Fungi, algae and cyanobacteria are particularlyadapted to survive UV exposure and repeated drying

and rehydration ( Potts, 1994; Yancey et al., 1982 ) andmight be expected to be the major groups in biolms onexposed surfaces. Many of the cyanobacteria, actino-mycetes and fungi produce pigments, leading to thetypical discolouration seen on poorly maintained build-ings ( Fig. 1 ), in addition to their degradation ( Ortega-Calvo et al., 1991; May et al., 1993; Ortega-Moraleset al., 2000 ).

Guillitte and Dreesen (1995) suggested that the

bioreceptivity of building materials was highly variable.They postulated that it was controlled mainly by surfaceroughness, initial porosity and the mineralogical natureof the substrate. The other factors controlling coloniza-tion are clearly environmental. It has been stated thatalgae cause more problems than fungi on paintedsurfaces in Southeast Asia ( Frazier and Downey,1995 ), while in two recent studies on colonization of paint lms in Brazil and Norway, the major organismsisolated were fungi ( Shirakawa et al., 2002; English

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www.elsevier.com/locate/ibiod

0964-8305/$- see front matter r 2004 Published by Elsevier Ltd.doi:10.1016/j.ibiod.2004.10.001

Corresponding author. Tel. : +555133166026; fax:+5551 33166029.

E-mail address: [email protected] (C.C. Gaylarde).

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et al., 2003 ), agreeing with much earlier work in theUSA ( Goll et al., 1952 ). Rindi et al. (1999) commentedon the unexpectedly high numbers of green algae of theorder Prasiolales on cement and bricks (articial‘‘composites’’), as opposed to stone, in Galway, Ireland,but the predominance of cyanobacteria over green algae

on these substrates had previously been reported byJohn (1988) . There are, then, no denitive answers in theliterature to the question of possible preference of particular microbial groups for given building substratesand how this is affected by important environmentalconditions such as humidity and temperature. Onefactor that has prevented answering of these questionsthrough a statistical meta-analysis of the published datais the wide range of methodologies used by differentworkers. Most rely on the use of culture techniques, withcolonies of the various microbial groups being countedon (relatively) specic media. Such culture dependentstudies obviously produce a skewed result, since themedia used are selective and many organisms cannot beisolated in culture. Thus, enumeration of organisms byculture on these media may not reect the actualbiomass present on the original substrate.

After many years of studying the microorganismspresent on building surfaces in a variety of locations,using direct microscope observations of the biolms, wefelt that it was important to carry out a statisticalanalysis of our set of data to try to resolve the matter.

2. Materials and methods

2.1. Sampling sites and method

Over 1500 samples of biolms have been taken fromvertical surfaces of modern and historic buildings inEurope and Latin America (LA) using the adhesive tapemethod ( Sarkany and Gaylarde, 1968; Gaylarde andGaylarde, 1998; Shirakawa et al., 2002 ). Of these, 230freshly acquired samples were included in a majorbiomass survey. Countries included in the survey areNorthern Argentina, Bolivia, Brazil, Colombia, Equa-

dor, Mexico and Peru in Latin America (LA) and CzechRepublic, England, France, Italy, Poland, Portugal andSpain in Europe. Substrates sampled include composites(cement, mortar, concrete, brick), painted surfaces(generally over concrete or mortar) and dimensionalstone of both calcareous and siliceous types. All thesurfaces showed visible discolouration, generally grey/

black, but occasionally brown, orange, red or green inappearance; lichens were not sampled. The lower, splashzone area (generally less than 20 cm above ground level)was avoided; samples were normally taken between oneand two metres above the ground. Where the biolmhad a macroscopically different appearance on the same

substrate, samples (10–15cm of adhesive tape) weretaken from these differing regions. This was oftenindicative of different exposure conditions, such asinsolation or water availability. Examples are shown inFig. 1 . For thick, mature biolms, the tape removedonly the upper layer. Successive strips did not differ withrespect to the major biomass present and so only thisupper layer has been used in the analysis, i.e. samplenumbers were not articially increased by using thesame site more than once.

2.2. Microbiological analysis

Samples (0 : 6 cm 2) were cut from 10–15cm tape stripsand placed directly on a nutrient poor (oligotrophic)medium, as recommended by Hirsch et al. (1995) andWarscheid et al. (1995) . The agar medium used wassolid Modied Knop’s Medium (MKM), which con-tained (gL 1) KNO 3 1: 25 ; KH 2PO 4 1: 25 ; MgSO 4 7H 2O 2 : 5; Fe 2 ðSO 4Þ3 0: 004 ; sodium citrate, 0 : 3 andCaCl 2 2H 2O 0 : 036 ; to which was added 1 mL micro-nutrient mixture, containing (g L 1) H 3BO 3 ; 2: 86 ;MnCl 2 4H 2O 1 : 81 ; ZnSO 4 7H 2O 0 : 222 ; Na 2MoO 4 2H 2O 0 : 39 ; CuSO 4 5H 2O 0 : 079 and CoCl 2

6H 2O 0 : 045 (Gaylarde and Gaylarde, 1998 ). Plates wereincubated at 25 C in an illuminated BOD incubator andwere examined microscopically after 1–4 h at magnica-tions up to 312 to visualize rehydrated microorgan-isms in situ, and then after further incubation. Eithertwo or three replicate samples (0 : 6 cm 2) were examinedfor each rehydrated tape strip. Observations were alsomade at 1250 where necessary; these were notincubated further, as they had been contaminated byimmersion oil. The major biomass was noted at theinitial observation, with the exception of actinomycetes,which were recorded after growth for 24–48 h, when

they could be readily differentiated from other bacteria.Major biomass was dened as the most prevalent groupof organisms visible in the biolm over the whole0 : 6 cm 2 : The major biomass (algae, cyanobacteria, fungi,or actinomycetes) at each site was recorded and the totalnumber of sites containing each specic major biomasswas calculated. If two groups, e.g. fungi and algae, were

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Fig. 1. Some of the buildings sampled: (a) a rough-cast painted wall in Florianopolis, Brazil. Note grey biolms in areas unprotected from rain; (b)the limestone plinth of a lead statue of Queen Charlotte in London, UK. A green biolm is present in the water-runoff area; (c) marble tomb in Sa õJoa õ del Rei, Brazil, with thin black crust. Sloping surfaces are more heavily colonized than vertical ones; (d) degraded sandstone pillar on Sevillecathedral, Spain. A hard black crust, mainly sloughed off lower down, is seen on the upper regions.

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the most common and were approx. equal in prevalence,a score of one-half was given to each. Although manymicroorganisms were identied to genus or species level,these identications are not specically reported hereand the methods used are therefore not included.

2.3. Statistical analysis

Results (original untransformed data) were analysedby the w2 test with Yate’s correction, accepting a value of 1% as showing signicant difference between variables,unless otherwise stated.

3. Results

Cyanobacteria, algae and fungi, with other bacteria,protozoa and small animals, were present in the

biolms. In some cases, the biolm was extremely mixedor was so clumped that it was impossible to determinethe major biomass. Just 219 samples yielded results thatallowed the comparison of major microbial biomassespresent on the various substrates and in the two climaticregions. The locations that were included in this nalanalysis are shown in the legend to Fig. 2 ; there are 27different sites in LA and 15 in Europe. Occasionally,when rehydrated samples were examined at 1250 to

conrm microbial identities, coccoid or bacilliform non-photosynthetic bacteria were found as the majorbiomass in thin biolms, but they have not beenincluded in the analysis, as this was not routine. Hencefour main classes of biomass were included in theanalysis, viz. cyanobacteria, algae, fungi and lamen-tous actinomycetes.

3.1. Biolms in different climatic areas

Fig. 2 shows that cyanobacteria were most frequentlypresent as the major biomass in LA, followed by fungi,

whereas in Europe algae were most common, followedby cyanobacteria. The dominance of cyanobacteria andfungi in LA compared to Europe and of algae in Europecompared to LA were all signicant at 1%.

3.2. Biolms on different substrates

The results for stone and composites were basicallysimilar ( Fig. 3 ) and are taken together as ‘‘mineralsubstrates’’. The most common major biomass on thesesurfaces was composed of cyanobacteria in LA andalgae in Europe ( Fig. 3 ). In LA the subsection II coccoid

colonial organisms were most frequently found and weresometimes present as almost a monoculture (see Fig. 4 ).Deeply pigmented coccoid cyanobacterial cells were alsopresent in LA samples ( Figs. 5 and 6 ), especially (but notexclusively) when the buildings were situated at altitudesover 1000 m ( Fig. 5 ).

Fungi were found infrequently as the major biomasson stone. They occurred more frequently as such onpaint than on other substrates (40% cf. 12%) ( Fig. 3 ).Algal major biomasses were also signicantly higher forpaint, as compared with mineral substrates, in LA(Table 1 ), but there was no signicant difference overallbetween the occurrence of either algae or fungi as major

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0

10

20

30

40

50

60

70

Europe Latin America

T o

t a l N o .

S i t e s

ActinomycetesFungiAlgaeCyanobacteria

Fig. 2. Total number of sites where each microbial group was detectedas major biomass on buildings in Europe and Latin America. N ¼ 66for Europe and 153 for Latin America. Sampling locations: (1)Europe —London, Morcombelake, Boscombe, Bath (England); Seville,Carmona, Italica (Spain); Aquileia, Padua, Trieste, Venice (Italy);Lodz (Poland); Prague (Czech Republic); Blaye (France); (2) LatinAmerica . Ouro Preto, Mariana, Sa õ Joa õ del Rei, Olinda, Recife,Salvador, Brası ĺia, Bonito, Porto Alegre, Atlantida, Sa õ Paulo,Floriano ṕolis (Brazil); Tucuman (Northern Argentina); Cartagena,Bogota ´ (Colombia); Quito, Banhos (Equador); Coroico (Bolivia);Cuzco, Aguas Calientes, Machu Picchu (Peru); Cancun, PuertoMorelles, Mayan buildings of the Yucatan Peninsula (Mexico).

0

5

10

15

20

25

30

35

40

45

Paint Composites Stone

T o

t a l N o .

S i t e s

ActinomycetesFungiAlgaeCyanobacteria

Fig. 3. Comparison of total number of sites at which each of thevarious groups of microorganisms was the major biomass in biolmson paint ðN ¼ 103Þ; stone ðN ¼ 68Þ and composites ðN ¼ 48Þ:



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biomass on painted surfaces in the two regions.Actinomycetes were occasionally detected as majorbiomass in thin biolms; they were signicantly morecommon on stone and more frequent, though notstatistically signicantly different, in Europe than LA(Figs. 2 and 3).

Table 1 shows the percentages of biolms in which

each of the four groups of microorganisms was presentas major biomass on each substrate in Europe and LA.

3.3. Specic microbial types detected

Although no detailed analysis of the genera andspecies present in the biolms is presented here,morphological comparisons can be made. Coccoidphototrophs most frequently formed the major biomassin the majority of cases. It is of interest to note thatwhen the major biomass seen was lamentous cyano-

bacteria, these were always present as very shortlaments with thick pigmented sheaths. They were mostfrequently members of the Scytonemataceae, but alsoincluded members of the Microchaetaceae and Rivular-aceae. Cyanobacteria of the Oscillatoriales and theNostocaceae were generally seen in clearly lamentousform only after extended culture. The main lamentousalgae detected as major biomass were the Trentepoh-liales, which often grew in a coccoid colonial form withonly a few short laments (see Fig. 7 ). This group wasalways the major lamentous algal biomass in LA, butmuch more variety was seen in Europe, where the genusKlebsormidium was also frequent. Note that red staining

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Fig. 4. Subsection II cyanobacteria detected as almost sole biomass onthe surface of an unpainted concrete building in Porto Alegre, Brazil.Some cells show a brown pigmentation, sometimes extending to thecapsules. The biolm appeared green to the naked eye.

Fig. 5. Subsection I cyanobacteria detected in a black biolm on apainted church in Minas Gerais, Brazil. Cells, capsules and matrix areall deep blue. The contrast of the photograph was decreasedelectronically, using the gamma function, to allow visualization of cells within the matrix.

Fig. 6. Two microcolonies of Subsection I and/or II cyanobacteria.Although further incubation could dene the subsection, and possiblythe genus, these in situ photos do not allow such identication. Samplefrom a grey biolm on a Mayan limestone building in the Yucatan,Mexico.

Table 1Presence of each microbial group as major biomass on the differentsubstrates in Europe and Latin America (LA), given as a percentage of all major biomasses detected on that substrate

Site Actinomycetes * Fungi Algae ** Cyanobacteria *

Paint/Europe 8.3 20.8 54.2 16.7Minerals/Europe 12.9 5.6 46.3 35.2Paint/LA 1.1 42.3 31.3 25.3Minerals/LA 3.2 17.7 12.9 66.1

Statistical analysis ( w2) was carried out on the raw data as separate4 2 tables comparing each microbial group with all others jointly.

* Signicantly different at the 5% level.** Signicantly different at the 1% level.



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was not always indicative of the presence of Trente-pohliales (see Fig. 8 ).

Some of the biolms were almost monocultures and,except in one case where only Aspergillus candidus wasdetected on a varnished stone surface in Salvador,Bahia, these contained only coccoid cyanobacteria of

subsections I or II ( Fig. 4 shows a subsection II biolm).One of the sites sampled differed from all the rest inbeing a copper-stained area of a limestone monument inLondon, on which only actinomycetes ( Streptomyces )and Myxococcus were detected.

4. Discussion

We have previously reported that the major groups of microorganisms in these terrestrial biolms are cyano-bacteria, algae and fungi, with other bacteria, protozoaand small animals also present ( Gaylarde and Gaylarde,

2000; Crispim et al., 2003 ). This result is conrmed bythe inclusion of a larger number of samples.

The highly signicant predominance of algae as majorbiomass organisms on all substrates in Europe, ascompared with LA ( Fig. 3 ), was unexpected, althoughthis group of phototrophs has been stated to be of major

importance on stone monuments on the wet west coastof Great Britain ( Richardson, 1995 ) and on granitemonuments in NW Spain ( Rifon-Lastra and Noguerol-Seoane, 2001 ) and the Ukraine ( Darienko and Hoff-mann, 2003 ). The Trentepohliales, detected as majorlamentous algal biomass in both regions, have pre-viously been reported as important colonizers of buildings, either painted or unpainted, in Singaporeand Western Ireland ( Wee and Lee, 1980; Rindi andGuiry, 2002 ). Algae are more frequent on moist than ondry sites ( Gillatt and Tracey, 1987 ) and it could be thathigher average temperatures in the Latin Americancountries included in our survey reduced the time forwhich external building surfaces remained wet (aparameter known to engineers as ‘‘time of wetness’’and of recognized importance for degradation of materials). Relative humidity of the air is also animportant factor in the growth and survival of micro-organisms and the areas of LA included in this surveyare almost all from regions with a mean annualhumidity 4 70% ; a value much greater than that foundin most sites sampled in Europe. However, highhumidity is not essential for the survival of allmicroorganisms. Adhikary and Satapathy (1996)showed that the predominant organism on the rock

surfaces of temples in the Indian state of Orissa, thecyanobacterium Tolypothrix byssoidea , retained lowlevels of activity, as indicated by triphenyl tetrazoliumchloride hydrolysis, even under extremely arid andhot conditions. Its thick brownish sheath probablyoffered protection from desiccation, as well as from highlight intensity.

The lack of inuence of the chemical composition of stone materials on their microbial colonization haspreviously been suggested by Tiano et al. (1995) . In ourcase, major biolm components, cyanobacteria in LAand algae in Europe ( Fig. 3 ), depended on climate and

not substrate. The dominance of cyanobacteria onstone has previously been recorded by us in LA(Ortega-Morales et al., 2000; Gaylarde et al., 2001 )and studied elsewhere by other authors ( John, 1988;Urzi and Realini, 1998; Tomaselli et al., 2000; Ascasoet al., 2002 ).

Cyanobacteria are known to be resistant to high solarirradiation and frequently have densely pigmented cellsand/or sheaths ( Garcia-Pichel et al., 1992, 1993; Roy etal., 1997 ). This obviously acts in their favour in thetropical and sub-tropical countries of LA studied here.We found many such dark pigmented cyanobacteria insamples taken at altitudes over 1000m within the tropics

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Fig. 7. Fungal laments and the alga Trentepohlia in a brown biolmon a painted surface in Porto Alegre.

Fig. 8. An algal biolm on paint in Northern Argentina. Filamentousand coccoid algae are seen. The biolm was red in colour.



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(an example is shown in Fig. 5 ), but they were much lesscommon in lower areas outside the tropics, such as inPorto Alegre, Brazil. Nevertheless, cyanobacteria re-mained the dominant biomass, probably because of their ability to resist high temperatures and dehydration.The thick, pigmented sheaths may also provide protec-

tion to grazing organisms; arthropods, as detected bytheir faecal pellets, are more common in our tropicalsamples than in samples from other environments.Pigmentation in fungi is known to be protective;melanization of the cell walls confers resistance tohydrolytic enzymes (such as those released as exoen-zymes by bacteria and some arthropods) as well as tofree radicals ( Bloomeld and Alexander, 1967; Jacob-son, 2000 ). Mites, slime moulds, rotifers and gastropodsare the most important grazers affecting biolmstructure and composition on walls.

The ability of microorganisms to remain metaboli-cally active under conditions of low water activity isgenerally related to the presence of osmotic protectants(osmolytes) within the cells; there are many types of substance used as osmolytes by different groups of organisms. Osmolytes protect against desiccation andhigh salt concentrations, common conditions on drywalls. Two fungal genera frequently observed on paint,Aureobasidium and Cladosporium (Drescher, 1958;Shirakawa et al., 2002; Saad et al., 2003; Gorbushinaet al., 2004 ), are found in natural salterns with a salinityof 30% and are important contaminants of frozen andsalted food-stuffs ( Atapattu and Samarajeewa, 1990;Gunde-Cimerman et al., 2000 ). In laboratory experi-

ments (not described), we found that the wall-inhabitingorganisms tolerant to the highest salt levels were acyanobacterium ( Gloeocapsa ) and the two fungal generacited above, growing at a sodium chloride concentrationof 20%. We have also detected algae that are obligatehalophiles (minimum 7% NaCl), whereas all cyanobac-teria and fungi detected were able to grow also withoutthe addition of salts.

The infrequency of fungi as major biomass organismson stone, seen in Fig. 3 , has previously been reported byGarcia-Valle ś et al. (2000) , who used both directmicroscope techniques and culture methods to study

microorganisms present on marble surfaces in Turkey.Various types of patina were studied and in no casewas the major microbial biomass fungal. In contrast,painted surfaces most commonly contained a majorbiomass composed of fungi ( 40%) in the currentsurvey ( Fig. 3 ). Observations on microbial succession onnewly painted walls in LA have shown that fungi arepredominant in the rst 2 years after repainting(Gaylarde et al., 2004 ). Given sufcient organic carbon,fungi grow much faster than the autotrophs and it seemslikely that more readily available organic substrate is thereason for this predominance on paint. Previous studieshave suggested that algae colonize painted surfaces

before cyanobacteria ( Gaylarde and Gaylarde, 1999 )and the relative proportions of these three groups of microorganisms on paint in this current study closelyfollow the suggested colonization sequence, with fungibeing followed rst by algae and then by cyanobacteria.Painted surfaces are renewed more frequently than stone

and composites, and the relationship between majorbiomass and colonization sequence would thus beretained. Of the cyanobacteria, subsection I organismsare most frequently observed on paint (421 of 844cyanobacterial identications, Fig. 5 ; Gaylarde andGaylarde, 2000 ), rather than subsection II, as seen onminerals ( Fig. 4 ).

The low numbers of actinomycetes detected overallare almost certainly due to the biolms being sampledon external surfaces; we have detected many moremembers of this microbial group on internal walls,especially of stone and composites, and they are veryfrequently present in large numbers in endolithicsamples. Giacobini et al. (1995) reported the isolationand identication of actinomycetes from many frescoesin underground historic sites in Italy and we havedetected this group as important endolithic organisms invarious stone buildings in LA. In both situations, thecells are protected from extremes of temperature, UVradiation and desiccation. Climatic differences wouldexplain why this group is more prevalent in the moremoderate environments of Europe and, indeed, actino-mycetes have previously been detected on external stonesurfaces in Europe. Warscheid et al. (1995) reportedthem in 3 of 12 samples taken from stone buildings in

Germany; actinomycetes were, apparently, not themajor biomass, although this is difcult to afrmdenitively because of the methods used for quantica-tion (colony counts on articial media). Palla et al.(2002) reported that the actinomycete genus Nocardiawas particularly prevalent in degraded sandstonemonuments in Italy and these were detected bymolecular techniques without isolation. Gonza ĺez et al.(2003) identied a large number of actinomycetes onnatural rocks in Spain, the majority being of the genusStreptomyces ; this is in agreement with our unpublishedobservations on actinomycete genera seen in both

Europe and LA. The literature, along with the resultsof our analysis ( Fig. 3 ), suggests that actinomycetes aremore common on stone surfaces. Although theseorganisms were detected in many of our samples frompaint and concrete, they were very rarely the majorbiomass.

The results show that biolms on painted and non-painted materials differ in their composition, fungi beingmore prevalent overall on paint. Climatic conditions caninuence the colonization pattern, algae being morecommon in biolms on all substrates sampled in Europethan in LA. The identication of fungi as the principalbiomass on painted surfaces, both in Europe and LA,

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has important implications for the coatings industry,suggesting that, as previously stated but not consistentlyproven by empirical and reliable data, fungicides areimportant components of paint formulations. However,many of the paint lms sampled doubtless contained afungicide and the results may indicate the failure of

these biocides in use. The duration of modern antifungalbiocide activity in external paint lms is short com-pared to the lifetime of the lm itself ( Gaylarde et al.,2004 ); leaching by rain, oxidation and degradationby photochemical processes play a part in this, butleaching is likely to be the most important mechanism.One of the challenges for the biocides industry isthe development of paint lm fungicides that havelow leach rates and good in-lm stability, togetherwith rapid degradation once released into the environ-ment.

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