Lichens on branches of Siberian fir (Abies sibirica Ledeb.) as indicators of atmospheric pollution in forests

ISSN 1062-3590, Biology Bulletin, 2008, Vol. 35, No. 4, pp. 411–421. © Pleiades Publishing, Inc., 2008.Original Russian Text © T.N. Otnyukova, O. P. Sekretenko, 2008, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2008, No. 4, pp. 479–490.

411

INTRODUCTION

The impact of acid pollutants (sulfur dioxide, acidrains, etc.) on lichens is considered in many publica-tions (Skye, 1968; Hawksworth and Rose, 1970; Le-Blanc and DeSloover, 1970; LeBlanc and Rao, 1973;Richardson, 1988; etc.). Less abundant are data on theresponse of lichens to nonacid pollutants such as limeand cement dust, ash, fertilizer dust, and ammonia(Barkman, 1958; Gilbert, 1976; Nilson and Martin,1982; Van Herk, 1999, 2001).

In the 1970s and 1980s, some pollution-sensitivelichen species appeared again in their former habitats(Henderson-Sellers and Seaward, 1979; Rose andHawksworth, 1981; Showman, 1981; Hawksworth andMcManus, 1989). Changes in the species diversity oflichens no longer show direct dependence on the sulfurdioxide content in the atmosphere (Rose and Hawk-sworth, 1981), in contrast to the situation described bythe same authors previously (Hawksworth and Rose,1970). This is due to a general decrease in atmosphericSO

2

concentrations in many regions of the world(Hawksworth and McManus, 1989; Seaward, 1993,1997). Low concentrations of SO

2

in the atmosphere donot lead to changes in the pH of tree bark (Van Dobbenand de Bakker, 1996; Van Dobben and ter Braak, 1998,1999; Van Herk, 1999, 2001), and the epiphytic lichencover is restored due not only to the return of some pre-viously extinct acidophytic species (Showman, 1981)but also to the advent of nitrophytic species, with theabundance of the latter increasing at a higher rate thanthat of the former (De Bakker, 1989; Van Dobben andde Bakker, 1996; Van Dobben and ter Braak, 1998,1999).

Lichens are highly sensitive to a wide spectrum ofnatural and anthropogenic factors. Their growth ontrees depends on both microclimatic conditions(humidity, illumination, the state of the atmosphere)and specific features of the substrate (surface micro-structure, chemical parameters, and pH) (

Lichen Eco-logy

, 1977).

Tree species can be divided into groups with acidbark (birch, oak, spruce, etc.) and subneutral bark (pop-lar, elm, etc.), with bark pH ranging in nature from 3.1to 4.5 and from 4.7 to 7.1, respectively (Barkman,1958; Skye, 1968; Nilson and Martin, 1982).

In polluted areas, bark pH in the same tree speciesmay vary widely, with the difference between the high-est and lowest pH values reaching several units. Underacid pollution, for example, bark pH in deciduous spe-cies (

Fraxinus

sp.,

Ulmus

sp.,

Acer

sp.,

Populus

sp.)decreases from 4.7–7.1 to 3.0 (Skye, 1968). Con-versely, dust pollution leads to an increase in bark pHfrom 3.2 to 5.8 in pine and from 3.9 to 7.1 in birch (Nil-son and Martin, 1982), and bark pH in

Quercus

sp.under conditions of pollution with ammonia increasesfrom 4.5 to 6.5 (Van Herk, 1999, 2001). Extremely low(pH < 3) or extremely high (pH > 8) pH values of thesubstrate, ambient water, and thalli have equally toxiceffects on lichens (Türk and Wirth, 1975; Nilson andMartin, 1982).

In studies with lichens used as indicators of pollu-tion, they are usually examined on tree stems at breastheight, approximately 1.5 m above ground. Recently, itwas proposed to study lichen communities on lowertree branches, as they are more sensitive to changes inthe air environment than the communities growing on

Lichens on Branches of Siberian Fir (

Abies sibirica

Ledeb.) as Indicators of Atmospheric Pollution in Forests

T. N. Otnyukova

a,b

and O. P. Sekretenko

a

a

Sukachev Institute of Forest, Siberian Branch, Russian Academy of Sciences, Akademgorodok, Krasnoyarsk, 660036 Russia e-mail: [email protected]

b

Siberian Federal University, Svobodnyi pr. 79, Krasnoyarsk, 660041 Russia

Received July 23, 2007

Abstract

—The abundance distribution of different ecological groups of lichens depending on bark pH has beenstudied on 1- to 24-year shoots of Siberian fir in the mountains of southern Siberia. Along with acidophyticlichens commonly found on the Siberian fir (

Usnea

sp.,

Bryoria

sp., etc.), its young shoots are also colonizedby nitrophytic species (

Physcia tenella, Melanelia exasperatula

, etc.), which is evidence for the increasing pHof shoot bark. The proportion of thalli of nitrophytic lichen species shows a significant positive correlation withthe pH of the upper (dusted) bark layer and is greater in the Eastern Sayan (at bark pH averaging 5.4) than inthe Western Sayan (pH 4.7). The trends revealed in this study may be used for indication of pollution and eco-logical monitoring of forest ecosystems.

DOI:

10.1134/S1062359008040146

ECOLOGY

412

BIOLOGY BULLETIN

Vol. 35

No. 4

2008

OTNYUKOVA, SEKRETENKO

tree stems (Wolseley and Pryor, 1999; Wolseley et al.,2006). This is explained by the fact that young branchesannually provide lichens with a fresh substrate, with pHof the bark depending on its chemical properties and thecomposition of pollutants settling on the surface,whereas the pH of stem bark is determined by a com-plex of diverse pollutants accumulated over many years(Wolseley ey al., 2006). To reveal the effects of alkalinedust and ammonia, epiphytic lichens are studied ontrees with acid bark (Gilbert, 1976; Nilson and Martin,1982; Van Dobben and ter Braak, 1998, 1999, VanHerk, 1999, 2001; Wolseley and Pryor, 1999; Wolseleyet al., 2006).

As the properties of tree bark change under theeffect of pollution, the flora of epiphytic lichens alsochanges, which allows the use of lichens as indicatorsof the state of the air environment.

The purpose of this study was to reveal general dis-tribution trends and indicator properties of ecologicalgroups and species of lichens differing in preference forsubstrate pH on branches of Siberian fir (

Abies sibirica

Ledeb.) in forest ecosystems in the mountains of south-ern Siberia.

MATERIALS AND METHODS

According to forest zoning of eastern Siberianmountains, the study areas lie in the Eastern Sayan andNorthern Altai–Sayan forest provinces of the Altai–Sayan forest region (

Tipy lesov…

, 1980).

Eastern Sayan province

. Test plots were estab-lished in northwestern spurs of the Eastern Sayan,within the Stolby State Nature Reserve, which isincluded in the green belt of the city of Krasnoyarsk.The region has low-mountain topography with eleva-tions ranging from 200 to 800 m a.s.l. River valleys liebelow 400 m, and summits of watershed ridges riseabove 700 m. The climate is mild continental. Averagemonthly temperatures range from

–16.2°ë

in Januaryto

16.8°ë

in July; annual precipitation is 680 mm(

Trudy…

, 1958; Andreeva, 2005). Characteristics of theplots were as follows: plot 1 (middle mountains, 700–800 m), summits of watershed ridges in the dark taiga(fir) belt 25–35 km southwest of Krasnoyarsk; plot 2(low mountains. 500–550 m), the lower part of a water-shed ridge in the herbaceous pine–larch forest belt 10–15 km southwest of Krasnoyarsk.

Northern Altai–Sayan province

. Test plots wereestablished in the system of ridges on the northern mac-roslope of the Western Sayan. The region has mountaintopography, with watersheds rising to 1300–1500 mand valleys lying at 400–800 a.s.l. The climate is coolor cold, with the annual amount of precipitation chang-ing with elevation from 500 to 1500 mm. Monthly aver-age temperatures range from

–19.9°ë

in January to

15.3°ë

in July in low mountain areas and from –19.0 to

12.3°ë

in high mountain areas, respectively (

Tipylesov…

, 1980). Test plots were as follows: plot 3 (high

mountains, 1300–1400 m), the subgoltsy–subalpineopen forest belt on the northern macroslope of theOiskii Ridge; plot 4 (low mountains, 500 m), the darkconifer forest belt on the lower northern macroslope ofthe Kulumys Ridge facing the Tanzybei Depression.With respect to the sources of industrial pollution, theplots were located 350–400 km south of Krasnoyarskand 80–100 km west of Sayanogorsk.

Shoots of

A. sibirica

were collected at 13 samplingsites in the Eastern Sayan and 3 sites in the WesternSayan in August and September 2001–2003. Sampleswere taken from the vegetative and male generativecrown layers (2–8 and 15–22 m above ground, respec-tively, depending on tree height and location of lowerbranches). Each shoot of a certain age (1, 2, 3, …,24 years) was examined under a binocular lens to cal-culate the numbers of all lichen species and measuretheir thalli. To reveal the dynamics of lichen abundance,the shoots were divided into fragments at three-yearage intervals (1–3, 4–6, 7–9, …, 21–24 years).

To measure pH, the upper 1-mm bark layer withdust deposits was scraped off from each 24-year shootwithout dividing it into fragments. Bark samples fromshoots collected at the same site and from the samecrown layer were pooled into one or several samples,and 1-g aliquots of the pooled samples were placed in20 ml freshly distilled water. After 2 h, water pH in theunfiltered suspension was measured with a pH-410 pH-millivoltmeter (Akvilon, Russia).

Statistical data processing

. The results obtainedwere processed by methods of descriptive statistics.Since the Kolmogorov–Smirnov test showed that thedistribution of test characters differed from the normalpattern, relationships between them were analyzed withthe Spearman rank correlation coefficient, and charac-ter values under different conditions were comparedusing nonparametric Kruskal–Wallis ANOVA for ranks(Orlov, 2004). Correlations between bark pH and thenumerical ratio of the thalli of ecologically differentlichen groups were analyzed by the bootstrap method(Efron, 1988; Wilcox, 2003). In the material collectedat the same site, bark samples were taken from the sameshoots on which lichens were counted. Therefore, ourstatistical model assumed that every pH value recordedat the same site and in the same crown layer is equallyprobable for each shoot. Data sets generated in this waywere processed by the bootstrap method with 800 iter-ations to obtain bootstrap estimates for regression linesand their 95% confidence intervals. The Spearman rankcorrelation coefficients and their significance weredetermined by the same method. Calculations weremade with the STATISTICA and MATLAB programpackages.

Sources of pollution in the study region

. In thenorthwestern spurs of the Eastern Sayan, the mainsources of air pollution are the nonferrous metal,energy, chemical construction materials, and automo-tive transport industries in Krasnoyarsk. According to

BIOLOGY BULLETIN

Vol. 35

No. 4

2008

LICHENS ON BRANCHES OF SIBERIAN FIR 413

official data on Krasnoyarsk krai, pollutant emissionsinto the atmosphere between 1992 and 1996 amountedto 174–199 thousand metric tons, with their composi-tion being as follows: dust particles, 30–23%; CO

2

49–42%;

SO

2

19–17%;

NO

2

, 8–7%; HF, 1.0–0.9%; Cl

2

andHCl, 0.08–0.06%; and NH

3

, 0.05–0.03% (

O sostoya-nii…

, 1997, 2002). A tendency toward a decrease inpollution level is observed. The concentration of SO

2

averages 0.002–0.003 mg/m

3

(

O sostoyanii...

, 1997,2001), which is many times lower than the correspond-ing MAC (0.05 mg/m

3

). According to zoning based onlichen indication, such a low SO

2

concentration corre-sponds to the unpolluted zone (LeBlanc et al., 1972;Trass, 1985). The average concentrations of NH

3

varywithin a range of 0.01–0.03 mg/m

3

, being also lowerthan the corresponding MAC (0.04 mg/m

3

), whereas itsmaximum concentrations may exceed it by a factor offive (

O sostoyanii…

, 1997, 2002). At concentrations of0.013–0.035 mg/m

3

NH

3

in the atmosphere, acido-phytic lichens disappear, whereas nitrophytic lichensgain dominance (Van Herk, 1999, 2001).

Conditions on the northern macroslope of the West-ern Sayan are more favorable, as major sources ofindustrial pollution are absent. There are several vil-lages and a road maintenance depot with an asphaltplant in the Tanzybei Depression, and a highway passesthrough the system of mountain ridges. Long-distancewestern transfer of pollutants is possible from the Say-anogorsk Aluminum Plant.

RESULTS

Species diversity and ecological groups oflichens

. The list of lichens growing on

A. sibirica

proved to comprise 23 taxa, which were classified intothree ecological groups with respect to preference forcertain pH of the bark (Table 1). Many aspects of rele-vant terminology are subject to discussion (VanDobben and ter Braak, 1998; Van Herk, 1999, 2001;Wolseley et al., 2006). However, our classification ofepiphytic lichen species into the acidophytic, indiffer-ent, and nitrophytic groups is based on factual data andagrees with published data. It reflects preferences oflichen species for certain pH ranges under natural con-ditions (Barkman, 1958; Hällingbäck

, 1995

) and theirresponses to an increase in bark pH under the impact ofpollution (Nilson and Martin, 1982; Van Herk, 1999,2001; Wolseley et al., 2006) and eutrophication causedby dust deposition (Nilson and Martin, 1982; Barkman,1958).

Acidophytic species (

Bryoria

sp.,

Usnea

sp.) innature grow mainly on trees with weakly acid bark suchas conifers and birch, in which bark pH varies within arelatively narrow range (pH 4.0–5.0) (Hällingbäck,1995). These lichens negatively respond to an increasein bark pH upon pollution (Van Dobben and ter Braak,1998; Van Herk, 1999, 2001; Wolseley et al., 2006).

Directly opposite to epiphytic acidophytes is thegroup of species that positively respond to an increasein substrate pH under anthropogenic conditions. Thisgroup is referred to as nitrophytic, since nitrophytes(species of the genus

Physcia, Candelariella vitellina

,etc.) absolutely prevail in it (Van Herk, 1999, 2001). Innature, representatives of this group (e.g.,

Physciatenella, Ph. dubia, Ph. aipolia

, and

Melanelia exasper-atula

) grow on different substrate types at pH 5.0–7.0(Hällingbäck, 1995) and show a favorable response toan increase in bark pH upon pollution (Gilbert, 1976;Nilson and Martin, 1982; Van Herk, 1999, 2001; Ker-mit and Gauslaa, 2001).

The indifferent group considered in this study com-prises the species (

Hypogymnia physodes, Parmeliasulcata

, etc.) that grow with equal success both on poor,acid and reach, subneutral bark at pH 4.0–6.0 (Hälling-bäck, 1995) as well as on other types of woody sub-strates. These species show no distinct response tochanges in the pH of the substrate (phorophyte) uponpollution.

Lichen species found on

A. sibirica

shoots belongednot only to the acidophytic (

Usnea

sp.,

Bryoria

sp.) andindifferent (

H. physodes, P. sulcata

) groups but also tothe nitrophytic group. Among nitrophytes,

M. exasper-atula

and

Ph. tenella

dominated on young shoots, with

Ph. aipolia, C. vitellina

, and, less frequently,

Ph. adscendens

and

Ph. dubia

prevailing on oldershoots. At stem bases, only acidophytic and indifferentspecies occurred (Table 1). The prevalence of acido-phytic and indifferent lichens at stem bases vs. nitro-phytic lichens prevailing on shoots correlated withrespective values of bark pH: 4.3–4.7 vs. 4.7, 5.4(Table 1).

Abundance distribution of epiphytic lichens on

A. sibirica

shoots depending on bark pH.

Pooled dataobtained in the Western and Eastern Sayan were used toestimate the dependence of abundance of different eco-logical groups of lichens on bark pH. The regressionlines obtained by means of bootstrap modeling indicatethat a rise of bark pH from 4.3 to 6.3 was accompaniedby an increase in the proportion of nitrophytic lichens(on average, from 10 to 90%), whereas the proportionof acidophytes decreasing from 70% almost to zero(Fig. 1). Calculations showed that shoot bark pH

5.4

±

0.1

was the threshold value, with acidophytic and indif-ferent species being dominant (accounting for morethan 50% of all lichens) at lower pH and nitrophyticlichens prevailing at higher pH. Calculated values ofthe Spearman correlation coefficient

ρ

also showed adirect correlation between bark pH and the proportionof thalli for lichens of the nitrophytic group (

ρ

= 0.51)and an inverse correlation for lichens of the acidophyticgroup (

ρ

= –0.60). The bootstrap method showed thatboth coefficients were statistically significant at

p

< 0.01.

(1) Eastern and Western Sayan.

On average, barkpH on

A. sibirica

shoots was higher in the Eastern

414

BIOLOGY BULLETIN

Vol. 35

No. 4

2008


Sayan (pH ~5.4) than in the Western Sayan (pH ~4.7)(Table 2). According to the Kruskal–Wallis test, the dif-ference was significant at

p

< 0.0001.

Differences in the total number of lichen thalli andin the proportions of lichen thalli of different ecologicalgroups correlated with differences in bark pH. Theabsolute number of thalli per shoot of the same ageaveraged 64 in the Eastern Sayan vs. 106 in the WesternSayan, with variation limits being similar: from 0 to242 and from 0 to 246, respectively.

In the Eastern Sayan, where bark pH on

A. sibirica

shoots was higher, the thalli of nitrophytic lichens pre-vailed (~60%), with the proportion of acidophyticlichens being less than half this value (~25%). In theWestern Sayan, conversely, lichens of the acidophyticgroups were dominant (~60%), and the proportion ofnitrophytic species was only about 10%. The response

of indifferent lichens to changes in bark pH was similarto that of acidophytic species, with the abundance oftheir thalli being higher in the Western Sayan (at lowerbark pH) than in the Eastern Sayan.

(2) Altitudinal belts.

The average numbers of thalliper shoot of the same age in altitudinal belts of the East-ern Sayan were 1.5–2 times smaller than in the WesternSayan: 61–67 vs. 93–120, respectively. In each region,significant differences (

p

< 0.001) in

A. sibirica

barkpH between altitudinal belts were revealed (Table 3),with pH values being higher in the low than in the mid-dle and high mountain belts.

In correspondence with bark pH values, the propor-tions of lichen thalli of different ecological groups alsodiffered depending on elevation. These differenceswere more distinct in the Eastern Sayan: nitrophyticlichens were absolutely dominant in the lower moun-

Table 1.

Species composition of lichens on young shoots (1–24 years) and stem bases of Siberian fir (“Abies sibirica” Le-deb.) trees in the Eastern and Western Sayan

ParameterSpecies composition

Eastern Sayan Western Sayan

Ecological group shoots stem base shoots stem base

Acidophytes

Bryoria

sp.

+ + + +

Cetrelia cetrarioides

– –

+ +

Hypogymnia vitata

–

+ + +

Lecanora symmicta

–

+

–

+

Melanelia olivacea

– –

+ +

Parmelia squarrosa

– – –

+

Pertusaria amara

–

+ – +Platismatia glauca – – – +Pseudevernia furfuracea – – + +Ramalina thrausta – + – –

Vulpicida pinastri – + + +Usnea sp. + + + +

Indifferent species Evernia mesomorpha + + + +Hypogymnia physodes + + + +H. tubulosa – + + +Parmelia sulcata + + + +Ramalina dilacerata + + + +

Nitrophytes Candellariella vitellina + – + –

Melanelia exasperatula + – + –

Physcia aipolia + – + –

P. adscendens + – – –

P. dubia + – – –

P. tenella + – + –

Bark pH 5.4 ± 0.02 4.3 ± 0.05 4.7 ± 0.03 4.1 ± 0.00

Note: Plus and minus signs indicate the presence of absence of a given species, respectively.

BIOLOGY BULLETIN Vol. 35 No. 4 2008


tain belt, but their proportion decreased to only 26% inthe middle belt, where the average bark pH was0.7 units lower, with the proportion of acidophyticlichens increasing to 60% (Table 3).

Low values of bark pH are not typical of A. sibiricain the Western Sayan, since lichens growing on itsshoots always included a certain proportion of nitro-phytic species (8–11%), although most of them wereacidophytic (68–71%).

Compared to lichens of acidophytic and nitrophyticgroups, indifferent species were less responsive tochanges in bark pH. Nevertheless, their abundance hada distinct tendency to decrease at higher pH of shootbark.

(3) Vertical gradient along tree height. Bark pHon shoots from the upper generative (male) crown layer(15–22 m above ground) proved to be more acid than inthe lower vegetative layer, at a height of 4–8 m(Table 4). As lower pH of A. sibirica bark is more favor-able for lichen growth, the total number of thalli wasgreater in the upper than in the lower layer, especiallyin the Western Sayan.

However, no significant differences between thegenerative and vegetative crown layers was revealedwith respect to abundance ratio of the three ecologicalgroups of lichens.

Abundance distribution of lichen thalli of differ-ent ecological groups depending on the age ofA. sibirica shoots. We revealed general trends in thedynamics of lichen thalli abundance depending onshoot age, in which four stages were identified: settling,growth (an increase in the number of thalli), stabiliza-tion of abundance, and decline. On 24-year branches,the first three stages were observed in the middle andlower mountain belts of the Western Sayan and in themiddle belt of the Eastern Sayan, and all four stageswere observed in the low mountain belt of the EasternSayan.

The pioneer lichens settling the bark appeared ontwo- to three-year shoots and were never detected onone-year shoots.1

The stage of increase in lichen thalli abundance con-tinued until the shoots reached an age of 10–12 years.Then followed the stage of stabilization, but its coursediffered depending on the altitudinal belt. In the uppermountain belts of the Eastern and Western Sayan, theabundance of thalli proved to remain high over a longperiod of time, on shoots of all ages studied (up to

1 As the count of lichens involved measurements of every thallus, itwas found that the pioneer lichens found on two-year (the EasternSayan) or three-year shoots (the Western Sayan) had a size ofabout 0.05–0.1 mm, which was the minimum detectable under abinocular lens. The stage of growth (increase in abundance) wascharacterized by the presence of uneven-sized thalli with theabsolute prevalence of minute and small thalli, in correspondencewith shoot age. At the stage of stabilization of lichen abundance,the minute thalli were already absent or occurred sporadically(unpublished data).

24 years), without any age-related decrease. In thelower mountain belt, this stage was poorly manifested,with the total abundance of thalli sharply decreasing on16- to 18-year (the Eastern Sayan) or 19- to 24-year(the Western Sayan) fragments of branches.

In the upper mountain belts (the middle mountainbelt of the Eastern Sayan and the high mountain belt ofthe Western Sayan), the abundance of lichen thalli ofacidophytic and indifferent uniformly increased fromyear to year, whereas that of nitrophytic speciesdecreased on older shoots (Figs. 3a, 4a). In the lowermountain belts of the Eastern and Western Sayan, theabundance of all groups, irrespective of ecologicalgroup, proved to decrease with an increase in shoot age.

Changes in the abundance of lichen thalli of differ-ent ecological groups depending on shoot age in themiddle mountain belt of the Eastern Sayan (Fig. 3c) andin both belts of the Western Sayan (Figs. 4c, 4d) had asimilar pattern. As the age of shoots increased, a ten-dency toward dominance of acidophytic species anddecreasing abundance of nitrophytic species could bedetected. Low-mountain areas in the northwesternspurs of the Eastern Sayan sharply differed from uppermountain belts of the Western and Eastern Sayan in theprevalence of nitrophytic lichens on shoots of all agegroups (Fig. 3d). It is noteworthy that the behavior ofindifferent species varied insignificantly.

Prop

ortio

n of

thal

li, %

80

100

60

40

20

0

4.2 4.4 4.6 4.8 5.0 5.2 5.4 5.6 5.8 6.0 6.2

80

100

60

40

20

0

(b)

(‡)

Bark pH

Fig. 1. Proportions of thalli of (a) nitrophytic and (b) acido-phytic lichen species on Siberian fir branches as a functionof bark pH. Solid and broken lines show bootstrap estimatesof empirical regression lines and their 95% confidenceintervals, respectively. Triangles indicate scattering fieldscorresponding to one of bootstrap samples.

416



DISCUSSION

As follows from the results of our studies on forestecosystems in the mountains of southern Siberia (theEastern and Western Sayan), branches of A. sibirica arepopulated not only by acidophytic and indifferentlichens characteristic of this tree species but also bynitrophytic lichens (Table 1). In the latter group,Ph. tenella is dominant in the Eastern Sayan andM. exasperatula is dominant in the Western Sayan.

Among six nitrophytic lichens listed in Table 1, thespecies previously found on fir include Ph. aipolia(Sedel’nikova, 2001, Urbanaviciene, 2001) and

M. exasperatula (Urbanaviciene, 2001). Physciatenella in Cisbaikalia sporadically occurs on stones(Makryi, 1990) and is not frequent on poplar trees(Urbanaviciene and Urbanavicius, 1999); in the SayanMountains, it grown mainly on the bark of deciduoustree species (Sedel’nikova, 2001). In Europe, the occur-rence of the above nitrophytic species on trees with theinitially acid bark, such as Quercus and Fraxinus, gen-erally coincides with the presence of nearby sources ofammonia, such as livestock farms and other agriculturalenterprises (Van Herk, 1999, 2001; Wolseley et al.,2006). The same nitrophytic species grow also underconditions of dust pollution (e.g., on dust-coveredbases of tree stems) (Gilbert, 1976; Nilson and Martin,1982). Dust and ammonia promote the spread of nitro-phytic lichens by increasing the pH of the substrate(Gilbert, 1976; Van Herk, 1999, 2001).

The authors who were the first to find nitrophyticlichens (namely, M. exasperatula) on the bark of darkconifers in forest ecosystems (McCune et al., 2000;Kermit and Gauslaa, 2001; Urbanaviciene, 2001) didnot regard this finding as related to atmospheric pollu-tion. The occurrence of this species in the upper part oftree crown was attributed to deposition of bird feces onbranches (McCune et al., 2000), lower humidity andhigher illumination (Urbanaviciene, 2001), and higherbark pH supposedly accounted for by Ca2+ cations(Kermit and Gauslaa, 2001).

The results of our studies show that the settling oflichens on A. sibirica branches on the northwesternspurs of the Eastern Sayan may be explained by pollu-tion by emissions from industries located 15–35 kmsoutheast of Krasnoyarsk. The content of dust particlesin the total volume of these emissions reaches 30%(O sostoyanii…, 1997, 2002; Gosudarstvennyidoklad…, 2003), and ammonia concentrations recordedin the city are several times higher than the threshold

Table 2. Bark pH and proportions of lichen thalli of differ-ent ecological groups on Siberian fir (Abies sibirica Ledeb.)branches in the Eastern and Western Sayan

Parameter Eastern Sayan Western Sayan

Number of pH measure-ments

212 82

Bark pH 4.49–6.32 5.40 ± 0.02

4.29–5.43 4.70 ± 0.03

Number of branches exam-ined

121 45

Number of lichen thalli per 18-year branch

0–242(64) 0–246(106)

NITR, % 59 10

ACID, % 27 56

IND, % 14 34

Note: Differences in bark pH between the two regions are signifi-cant at p < 0.0001. Here and in Tables 2 and 4, NITR, ACID,and IND designate nitrophytic, acidophytic, and indifferentspecies groups, respectively. Figures in parentheses showaverage values; figures above and below the line show therange of values and the mean with standard deviation,respectively.

Table 3. Bark pH and proportions of of lichen thalli of different ecological groups on Siberian fir (Abies sibirica Ledeb.)branches in different altitudinal vegetation belts of the Eastern and Western Sayan

ParameterEastern Sayan Western Sayan

low mountain belt middle mountain belt low mountain belt middle mountain belt

Number of pH measurements 104 108 11 71

Bark pH 5.10–6.32 5.72 ± 0.03

4.49–5.74 5.01 ± 0.03

4.40–5.43 4.86 ± 0.10

4.29–4.92 4.67 ± 0.02

Number of branches examined 79 42 23 22


70 61 114 97

NITR, % 93 26 11 8

ACID, % 4 60 68 71

IND, % 3 14 21 21

Note: Differences in bark pH between vegetation belts of the Eastern and Western Sayan are significant at p < 0.001.



concentration sufficient for the growth of nitrophyticlichens. Extrapolating these results to remote mountainregions of southern Siberia, we conclude that the spreadof nitrophytic lichen species in the Western Sayan mayalso be explained by dust and ammonia (from regionalsources or due to long-distance atmospheric transfer).

There is ample published evidence for the globalatmospheric transfer of pollutants (Zagryaznenievozdukha…, 1988). The variety of substances involvedin this process includes ammonia (Charlson and Rodhe,1982; Ammonia emissions…, 1992).

In the atmosphere, ammonia is the dominant alka-line component that neutralizes a major part of acidcomponents such as sulfur dioxide and nitrogen oxides(Ammonia emissions…, 1992). Even a slight shift in the

balance of N ; N and S due to either a

decrease in S or increase in N leads to changesin rainwater pH (Charlson and Rodhe, 1982). Analyz-ing factors determining this parameter, these authorsconcluded that the cessation of SO2 and NOx emissionsagainst the background of continuing NH3 emissionswould result in a higher rainwater pH (Charlson andRodhe, 1982). On the global scale, the pH of precipita-tion has indeed increased from 4.1–4.6 in the 1970s(Charlson and Rodhe, 1982), to pH 6.0–7.0 or evenhigher in recent years (O sostoyanii…, 1997, 2002).

H3+ H4

+ O42–

O42– H4

+

According to the model of atmospheric transport of

NHx (NH3 + N ) (Asman and Jaarsveld, 1992),

approximately 44% NH3 and 14% (N )aerosol fall withdry precipitation and 42% NHx falls with wet precipita-tion. The fallout of NH3 with dry precipitation takes

H4+

H4+

Table 4. Bark pH and proportions of lichen thalli of different ecological groups on branches of the male generative and veg-etative crown layers of Siberian fir (Abies sibirica Ledeb.) in the Eastern and Western Sayan

Parameter

Eastern Sayan Western Sayan

low mountain belt middle mountain belt low mountain belt middle mountain belt

Crown layer

VEG GEN VEG GEN VEG GEN VEG GEN

Number of pH mea-surements

41 63 44 64 4 7 25 46

Bark pH 5.59–6.32 5.91 ± 0.03

5.10–6.20 5.59 ± 0.04

4.60–5.74 5.18 ± 0.05

4.49–5.45 4.90 ± 0.03

5.00–5.43 5.22 ± 0.10

4.40–4.84 4.66 ± 0.07

4.62–4.92 4.80 ± 0.02

4.29–4.92 4.66 ± 0.02

Number of branches examined

44 35 21 21 9 14 13 9


57 85 58 64 14 178 71 135

NITR, % 98 94 27 25 9 12 8 7

ACID, % 1 4 59 61 73 65 69 73

IND, % 1 2 14 14 18 23 23 20

Note: Differences in bark pH between crown layers are significant at p < 0.001. VEG and GEN designate vegetative and generative crownlayers.

Num

ber

of th

alli

1–3 4–6 7–9 10–12 13–15 16–18 19–21 22–24

40

50

30

20

10

0

Age of branch fragments, years

1 2 3 4

Fig. 2. Changes in the total numbers of lichen thalli depend-ing on the age of Siberian fir branches in (1) the middle and(2) low mountain belts of the Eastern Sayan and in (3) thehigh and (4) low mountain belts of the Western Sayan.

418



place at relatively short distances (100–1000 m) fromthe pollution source, whereas the wet fallout of

N )aerosol may occur farther than 100 km from thesource (Asman and Jaarsveld, 1992).

Thus, these data show that the growth of nitrophyticlichen species on dark conifer tree species in remoteforest ecosystems may be explained by atmosphericpollution with alkaline components, such as alkalinedust and ammonia.

As noted by many researchers, the shift of domi-nance from acidophytic to acidophobic (in our case,nitrophytic) species upon an increase in bark pH takesplace more rapidly than a general decrease in the num-ber of species in the epiphytic lichen cover. Visually,the group of nitrophytic species numerically prevailsover the acidophytic group, especially under conditionsof pollution with ammonia: as the pH of the substratebecomes higher, a relatively small number of nitro-phytic species rapidly increase in abundance (VanDobben and ter Braak, 1998, 1999; Van Herk, 1999,2001).

Virtually the same picture is observed in the EasternSayan: upon pH rise by 0.7 units, the numbers of thalliin nitrophytic lichen species increases severalfold. Thesensitivity of these species to changes in substrate pH is

H4+

so high that an increase in their abundance (at theexpense of acidophytic lichens) may be detected evenupon pH rise by no more than 0.2–0.3 units (Tables 3, 4;Figs. 1).

Considering the abundance dynamics of lichenthalli on A. sibirica branches of different ages, we cannote significant differences in the behavior of speciestypical of the fir bark (acidophytic and indifferentlichens) and species “alien” to it (nitrophytic lichens).As the branches grow older, the abundance of acido-phytic and indifferent species gradually increases andstabilizes at a certain level, whereas that of nitrophyticspecies initially increases, reaching a certain peak, andthen begins to decrease (Fig. 3, 4).

Lichens indicate the boundary between the periph-eral and central parts of the tree crown. In the WesternSayan, the thalli of nitrophytic lichens on branchesolder than 17–18 years either decrease in abundance (inthe high mountain belt) or disappear (in the low moun-tain belt) (Figs. 4a, 4b). On the northwestern spurs ofthe Eastern Sayan, this differentiation between theperipheral and central parts of the crown begins whenthe branches reach the age of 17 years (in the middlemountain belt) or 14 years (in the lower mountain belt)(Figs. 3a, 3b).

Num

ber

of th

alli

1–3 4–6 7–9 10–12 13–15 16–18 19–21 22–24

8

12

6

4

2

0


1 2 310

1–3 4–6 7–9 10–12 13–15 16–18

8

12

6420

10

1416182022

(‡)

(b)

Num

eric

al r

atio

of

thal

li, %

3 6 9 12 15 18 21 24

80

100

60

40

20

0

Age of shoots, years3 6 9 12 15 18

80

100

60

40

20

0

(c)

(d)

Middle mountain belt

Low mountain belt

Num

ber

of th

alli

Num

eric

al r

atio

of

thal

li, %

Fig. 3. Numbers (a, b) and proportions of thalli (c, d) of lichens belonging to different ecological groups with respect to preferencefor bark pH on Siberian fir branches in the Eastern Sayan. Ecological groups: (1) acidophytic, (2) indifferent, and (3) nitrophyticspecies (here and in Fig. 4).



It is noteworthy that, in more heavily polluted areas,nitrophytic lichen species can grow along the wholebranch length as well as at the stem base, as wasdescribed for Quercus sp. and Fraxinus sp. trees inagricultural regions (Wolseley et al., 2006).

Similarity in the distribution of nitrophytic lichenson A. sibirica branches in forest ecosystems of theWestern and Eastern Sayan may be accounted for bytrends in the fallout of suspended particles, turbulenceof air flows, and substrate structure. The conical shapeof fir crowns promotes the development of turbulencedue to which the bulk of atmospheric fallout settles onthe tree top and peripheral shoots, rather than on theinner part of the crown and the stem. Moreover, settledparticles accumulate in greater amounts on small thanon large branches (White and Turner, 1970) and onrough than on smooth surfaces (Little, 1977). Hence, itmay be concluded that bark pH on peripheral A. sibi-rica branches is mainly determined by the externalenvironment, whereas that on the internal segments ofbranches largely depends on the flow of rainwaterthrough the crown, which levels off the influence ofexternal environmental factors.

Thus, the dynamics of lichen growth on young A.sibirica shoots is a sensitive indicator of changes in thequality of air environment in forest ecosystems. Regu-

lar studies on lichens of different ecological groupswith regard to bark pH on A. sibirica twigs are instru-mental for monitoring the ecological state of forest eco-systems both near the sources of pollution and inremote areas.

REFERENCES

Air Pollution and Plant Life, Treshow, M., Ed., New York:Wiley, 1984. Translated under the title Zagryaznenievozdukha i zhizn' rastenii, Leningrad: Gidrometeoizdat,1988.Ammonia Emissions in Europe: Emission Coefficients andAbatement Costs. Proc. IIASA Workshop, February 4–6,1991, Laxenburg, Austria, Ed. Klaassen, G., Laxenburg:IIASA, 1992.Andreeva, E.B., On Climatic Characterization of the StolbyReserve, Mater. n.-prakt. konf., posv. 80-letiyu Goszapoved-nika “Stolby”: “Mnogoletnie nablyudeniya OOPT, istoriya,sovremennoe sostoyanie, perspektivy”, Krasnoyarsk, 14–17sentyabrya 2005 g. (Proc. Sci.–Pract. Conf. “Long-TermObservations of Specially Protected Nature Areas: History,Current State, and Prospects,” Krasnoyarsk, September14−17, 2005), Kel’beshekov, B.K., Ed., Krasnoyarsk, 2005,pp. 67–71.Asman, W.A.H and Jaarsveld, H.A, Ammonia Emission ofUse in Atmospheric Transport Models, in Ammonia Emissionsin Europe: Emission Coefficients and Abatement Costs. Proc.

Num

ber

of th

alli

1–3 4–6 7–9 10–12 13–1516–1819–2122–24

20

30

15

10

5

0


1 2 325

1–3 4–6 7–9 10–12 13–1516–18

10

20

5

0

15

25

30

35

(‡)

(b)

Num

eric

al r

atio

of

thal

li, %

3 6 9 12 15 18 21 24

80

100

60

40

20

0

Age of shoots, years3 6 9 12 15 18

80

100

60

40

20

0

(c)

(d)

Middle mountain belt

Low mountain belt

19–21 22–24 21 24

Num

ber

of th

alli

Num

eric

al r

atio

of

thal

li, %

Fig. 4. Numbers of thalli (a, b) and proportions of thalli (c, d) of lichens belonging to different ecological groups with respect topreference for bark pH on Siberian fir branches in the Western Sayan.

420



IIASA Workshop, February 4–6, 1991, Laxenburg, Austria,Ed. Klaassen, G., Laxenburg: IIASA, 1992, pp. 3–15.Barkman, J.J., Phytosociology and Ecology of CryptogamicEpiphytes, Assen: van Cornum, 1958.Charlson, R.J. and Rodhe, H., Factors Controlling the Acid-ity of Natural Rainwater, Nature, 1982, vol. 295, pp. 683–685.De Bakker, A.J., Effects of Ammonia Emission on EpiphyticLichen Vegetation, Acta Bot. Neerl., 1989, vol. 38, pp. 337–342.Efron, B., Netraditsionnye metody mnogomernogo statis-ticheskogo analiza (Unconventional Methods of MultivariateStatistical Analysis), Moscow: Finansy i Statistika, 1988.Gilbert, O.L., An Alkaline Dust Effect on Epiphytic Lichens,Lichenologist, 1976, vol. 8, pp. 173–178.Gosudarstvennyi doklad o sostoyanii i okhrane okruzhay-ushchei prirodnoi sredy Krasnoyarskogo kraya v 1996 godu(State Report on the State of the Environment in KrasnoyarskKrai in 2001), Moscow: NIA-Priroda, 2003.Hällingbäck, T., Ekologisk katalog över lavar (The Lichensof Sweden and Their Ecology), Uppsala: ArtDatabanken,1995.Hawksworth, D.L. and McManus, P.M., Lichen Recoloniza-tion in London under Conditions of Rapidly Falling SulphurDioxide Levels and the Concept of Zone Skipping, Bot. J.Linn. Soc., 1989, vol. 100, pp. 99–109.Hawksworth, D.L. and Rose, F., Qualitative Scale for Esti-mating Sulphur Dioxide Air Pollution in England and WalesUsing Epiphytic Lichens, Nature, 1970, vol.227, pp. 145–148.Henderson-Sellers, A. and Seaward, M.R.D., MonitoringLichen Reinvasion of Ameliorating Environments, Environ.Pollut., 1979, vol. 19, pp. 207–213.Kermit, T. and Gauslaa, Y., The Vertical Gradient of Bark pHof Twigs and Macrolichens in a Picea abies Canopy NotAffected by Acid Rain, Lichenologist, 2001, vol. 33, no. 4,pp. 353–359.LeBlanc, F. and DeSloover, J., Relation between Industrial-ization and the Distribution and Growth of Epiphytic Lichensand Mosses in Montreal, Can. J. Bot., 1970, vol. 48,pp. 1485–1496.LeBlanc, F. and Rao, D.N., Effects of Sulphur Dioxide onLichen and Moss Transplants, Ecology, 1973, vol. 54,pp. 612–617.LeBlanc, F., Rao, D.N., and Comeau, G., The Epiphytic Veg-etation of Populus balsamifera and Its Significance As an AirPollution Indicator in Sudbury, Ontario, Can. J. Bot., 1972,vol. 50, pp. 519–528.Lichen Ecology, Seaward, M.R.D., Ed., London: Academic,1977.Little, P., Deposition of 2.75, 5.0 and 8.5 μm Particles toPlant and Soil Surface, Environ. Pollut., 1977, vol. 12,pp. 293–305.Makryi, T.V., Lishainiki Baikal’skogo khrebta (Lichens of theBaikal Ridge), Novosibirsk: Nauka, 1990.McCune, B., Rosentreter, R., Ponzetti, J.M., and Shaw, D.C.,Epiphyte Habitats in an Old Conifer Forest in Western Wash-ington, USA, Bryologist, 2000, vol. 96, pp. 405–411.Nilson, E.M. and Martin, L.N., Epiphytic Lichens underConditions of Acid and Alkaline Pollution, in Vzaimodeistvielesnykh ekosistem i atmosfernykh zagryaznitelei (Interaction

of Forest Ecosystems and Atmospheric Pollutants), part 2,Tallinn: Tartu. Univ., 1982, pp. 88–100.O sostoyanii okruzhayushchei prirodnoi sredy Krasno-yarskogo kraya v 1996 godu (Ezhegodnyi doklad) (AnnualReport on the State of Natural Environment in KrasnoyarskKrai in 1996), Krasnoyarsk: GU MPR Rossii po Krasno-yarskomu Krayu, 1997 (manuscript).O sostoyanii i okhrane okruzhayushchei sredy Krasno-yarskogo kraya v 2001 godu (Gosudarstvennyi doklad)(State Report on the State and Protection of Natural Environ-ment in Krasnoyarsk Krai in 2001), Krasnoyarsk: GU MPRRossii po Krasnoyarskomu Krayu, 2002 (manuscript).Orlov, A.I., Prikladnaya statistika (Applied Statistics), Mos-cow: Ekzamen, 2004.Richardson, D.H.S., Understanding the Pollution Sensitivityof Lichens, Bot. J. Lin. Soc., 1988, vol. 96, pp. 31–43.Rose, C.I. and Hawksworth, D.L., Lichen Recolonization inLondon’s Cleaner Air, Nature, 1981, vol. 289, pp. 289–292.Seaward, M.R.D., Lichens and Sulphur Dioxide Air Pollu-tion: Field Studies, Environ. Rev., 1993, vol. 1, pp. 73–91.Seaward, M.R.D., Urban Deserts Bloom: A Lichen Renais-sance, Bibl. Lichenol., 1997, vol. 67, pp. 297–309.Sedel’nikova, N.V., Lishainiki Zapadnogo i VostochnogoSayana (Lichens of the Western and Eastern Sayan Moun-tains), Novosibirsk: Sib. Otd. Ross. Akad. Nauk, 2001.Showman, R.E., Lichen Recolonization Following Air Qual-ity Improvement, Bryologist, 1981, vol. 84, pp. 492–497.Skye, E., Lichens and Air Pollution, Acta Phytogeogr. Suec.,1968, vol. 52, pp. 1–123.Tipy lesov gor Yuzhnoi Sibiri (Forest Types in the Mountainsof Southern Siberia), Novosibirsk: Nauka, 1980.Trass, Kh.Kh., Classes of Lichen Poleotolerance and Ecolog-ical Monitoring, in Problemy ekologicheskogo monitoringa imodelirovaniya ekosistem (Problems in Ecological Monitor-ing and Ecosystem Modeling), Izrael’, Yu.A., Ed., Lenin-grad: Gidrometeoizdat, 1985, vol. 7, pp. 122–137.Trudy Gosudarstvennogo zapovednika “Stolby” (Proceed-ings of the Stolby State Nature Reserve), issue 2, Krasno-yarsk: Krasnoyarsk. Knizhn. Izd., 1958.Türk, R. and Wirth, V., The pH Dependence of SO2 Damageto Lichens, Oecologia, 1975, vol. 19, pp. 285–291.Urbanaviciene, I.N., Ecology of Epiphytic Lichens Growingon Abies sibirica in Southern Cisbaikalia, Bot. Zh., 2001,vol. 86, no. 9, pp. 80–90.Urbanaviciene, I.N. and Urbanavicius, G.P., Lichens of theBaikal Reserve, in Flora i fauna zapovednikov (Flora andFauna of Nature Reserves), issue 68, Golubkova, N.S., Ed.,Moscow: IPEE RAN, 1998.Van Dobben, H.F. and de Bakker, A.J., Re-Mapping Epi-phytic Lichen Biodiversity in the Netherlands: The Effects ofDecreasing SO2 and Increasing NH3, Acta Bot. Neerl., 1996,vol. 45, pp. 55–71.Van Dobben, H.F. and ter Braak, C.J.F., Effects of Atmo-spheric NH3 on Epiphytic Lichens in the Netherlands: ThePitfalls of Biological Monitoring, Atm. Environ., 1998,vol. 32, no. 3, pp. 551–557.Van Dobben, H.F. and ter Braak, C.J.F., Ranking of Epi-phytic Lichen Sensitivity to Air Pollution Using SurveyData: A Comparison of Indicator Scales, Lichenologist,1999, vol. 31, pp. 27–39.



Van Herk, C.M., Mapping of Ammonia Pollution with Epi-phytic Lichens in the Netherlands, Lichenologist, 1999,vol. 31, pp. 9–20.Van Herk, C.M., Bark pH and Susceptibility to Toxic Air Pol-lution As Independent Causes of Changes in EpiphyticLichen Composition in Space and Time, Lichenologist,2001, vol. 33, pp. 419–441.White, E.J. and Turner, F., A Method of Estimating Incomeof Nutrients in a Catch of Airborne Particles by a WoodlandCanopy, J. Appl. Ecol., 1970, vol. 7, pp. 441–461.

Wilcox, R.R., Applying Contemporary Statistical Tech-niques, New York: Academic, 2003.Wolseley, P.A. and Pryor, K.V., The Potential of EpiphyticTwig Communities on Quercus petraea in a Welsh WoodlandSite (Tycanol) for Evaluating Environmental Changes,Lichenologist, 1999, vol. 31, pp. 41–61.Wolseley, P.A., James, P.W., Theobald, M.R., and Sutton,M.A., Detecting Changes in Epiphytic Lichen Communitiesat Sites Affected by Atmospheric Ammonia from Agricul-tural Sources, Lichenologist, 2006, vol. 38, pp. 161–176.

Documents

Lichens on branches of Siberian fir (Abies sibirica Ledeb.) as indicators of atmospheric pollution in forests