research article bog recovery in northeastern estonia after … · 2010. 1. 8. · research article...

R E S E A R C H A R T I C L E

Bog Recovery in Northeastern Estonia after theReduction of Atmospheric Pollutant InputJaanus Paal,1 Kai Vellak,1 Jaan Liira,1 and Edgar Karofeld1,2

AbstractThe restoration of wetland ecosystems is one of the flag-ships of modern conservation ecology, and the developmentof methodologies is vital to the enhancement of biodiver-sity. Bogs in northeastern Estonia have been under inten-sive pressure from alkaline fly ash pollution emitted by oilshale–heated power plants since the 1950s. In the vicin-ity of pollution sources, the input of alkaline fly ash hasincreased the ash content in mosses and raised the pHvalue of bog water, which had caused the replacement ofSphagnum mosses by other bryophytes and the invasionof eutrophic plants by the 1980s. The results of our study

show that in recent decades, after the reduction in atmo-spheric input by power plants, the ash content in mosseshas fallen, bog water pH is lower, and bog-specific plantspecies have begun to return to the bogs that were mod-erately polluted in recent decades. However, historicallyheavily polluted bogs show little signs of self-restoration,and their vegetation is still threatened by continuing degra-dation. Based on the wide gradient of pollution intensity,we suggested a list of indicators that can be used to evaluatebog degradation rates and restoration success.

Key words: alkaline pollution, atmospheric input, bog veg-etation, CCA, GRM, recovery, Sphagnum .

Introduction

Air pollution crossing state borders and also affecting natureprotection areas has been of serious international concern fordecades. The sensitivity and buffering capacity against airpollution and the speed of recovery differs between ecosys-tems. Ombrotrophic bogs (raised bogs, EU Natura 2000 sitescodes 7110, 7120; Paal 2007) are remarkable habitats: theyare fed solely by precipitation, are built from living plantsand their partially decayed remains, and have acidic surfacewaters that are poor in minerals and nutrients. Bogs have verylow ecological buffering capacity, and therefore the responsesof these ecosystems to atmospheric pollution are more dra-matic than those observed in many other ecosystems (Adams& Preston 1992; Goubet et al. 2006). The disappearance ofSphagnum mosses caused by increased atmospheric input wasfirst described over 200 years ago in Great Britain (after Tallis1964; Adams & Preston 1992). Later, similar changes in bogplant cover were described over much wider areas in West-ern Europe (Tallis 1973; Bragg & Tallis 2001) and northernAmerica (Gignac & Beckett 1986; Glooschenko 1989).

Bogs in northeastern (NE) Estonia have been under increas-ing pressure from atmospheric pollution from power plants

1 Institute of Ecology and Earth Sciences, University of Tartu, 40 Lai Street, Tartu,51005 Estonia2 Address correspondence to Edgar Karofeld, email [email protected]

© 2009 Society for Ecological Restoration Internationaldoi: 10.1111/j.1526-100X.2009.00608.x

since the 1950s. Remarkable changes in bog geochemistry andvegetation composition have been recorded in this industrialregion since the 1980s (Punning 1994). Whereas the high SO2concentration in air and increased atmospheric input have beenshown to be the main cause of the disappearance of Sphagnummosses in bogs in other industrial areas (Ferguson & Lee 1980;Press et al. 1986), changes in NE Estonian bogs are morelikely caused by highly alkaline (pH of water solution approx-imately 12), calcium-rich fly ash from power plants heatedby local oil shale. In the 1980s the oil shale–based powerplants and the chemical industry emitted into the atmospheremore than 400,000 t of pollutants, mainly SO2 (approximately218,000 t) and oil shale fly ash (approximately 193,000 t)(Liblik & Kundel 1995). The changes in the geochemistryand vegetation of the bogs in NE Estonia in the near vicin-ity of the Ahtme, Balti, or Eesti power plants (launched in1951, 1959, and 1969, respectively) have been described inthe 1980s (Karofeld 1987, 1994; Punning et al. 1987, 1989).In those bogs, there was a substantial increase in pH valuesand the content of various chemicals (e.g., Ca2+, HCO−3 ) inbog water and in the upper layers of peat (Punning et al. 1987,1989; Karofeld 1994, 1996). The increased ash content in thesurviving Sphagnum mosses was particularly remarkable. Inthe most polluted bogs, the total disappearance of Sphagnummosses and the appearance of plant species typical of morenutrient rich and/or alkaline habitats were recorded (Karofeld1994, 1996; Liblik et al. 2003), as well as the increased radialgrowth of Scots pine (Karofeld 1994; Pensa et al. 2004, 2007;Ots & Reisner 2007; Kaasik et al. 2008). The majority of these

Restoration Ecology 1

Bog Recovery in Northeastern Estonia

air polluted bogs in NE Estonia belongs to Estonia’s largestprotected mire complexes in the Puhatu, Agusalu, and Kurtnaprotected areas. Therefore, there is a justified concern abouttheir poor condition, and interest in the success of the restora-tion of their original natural state.

In recent decades, the emission of pollutants from powerplants has been reduced dozens of times due to the decreasedproduction of electricity and the installation of improveddust catching filters (Liiv & Kaasik 2004; Liblik & Maalma2005). The first signs of the natural recovery of vegetationin these bogs have already been documented, namely thereappearance of Sphagnum mosses and the increase in theircoverage (Karofeld 1996). The reduction in the radial growthof Scots pines (Kaasik et al. 2008) and the decrease in thecontent of heavy metals in mosses (Liiv & Kaasik 2004)have also been documented. However, it is unclear whetherthe atmospheric input of pollutants to bogs has been reducedsufficiently for bog system recovering, and how much timesuch a self-restoration process would take. Most of theexisting knowledge of bog flora recovery is based on bogrestoration work from mire areas that were drained, mined,or converted to agricultural fields (Roderfeld 1993; Graf et al.2008; Wagner et al. 2008), and we have remarkably littleexperience regarding the self-restoration of bogs that arechanging in response to decreases in the effects of atmosphericpollution rather than recovering from an altered hydrologicregime. At the same time, atmospheric pollution input is oneof the main threats to European mires (Bobbink et al. 1998;Turetsky & Louis 2006).

The current study addresses the following questions:(1) What is the present state of the raised bog ecosystemsin the region of alkaline pollution in NE Estonia? (2) Howsuccessful was the natural recovery of raised bog ecosystemsin the last two decades after the decreased input intensity of(alkaline) pollutants? and (3) Can we define indicators that canbe used as targets for the assessment of bog recovery? For thatpurpose, we aim to compare the present state of geochemistryand vegetation in bogs of the intensive pollution region withthe records from earlier decades and to reference bogs in anintact condition.

Methods

Because little historical data were recorded, we selected bogsites for the study that would maximize our options for reveal-ing the changes that have followed the significant reduction inthe emission of pollutants during recent decades. At the end ofthe summer in the years 2006–2008, we studied the changesin geochemistry and plant cover in 11 NE Estonian hollow-ridge bogs located at various distances from atmospheric pol-luters (mainly oil shale–operated electric power plants) andnot affected by drainage or other direct anthropogenic impacts(Fig. 1). Liivjärve, Niinsaare, Kõrgesoo, Mustaladva, and Kri-vasoo bogs are located in the region of the most intensiveatmospheric deposition loads of fly ash. Kasesoo, Fjodorisoo,and Heinasoo bogs were selected as representatives of inter-mediate or relatively low deposition loads, taking into accountthe data available from the 1980s to the 1990s (Kaasik 1996;Kaasik & Sõukand 2000). The Männikjärve and Laukasoo

Figure 1. Location of studied bogs (⊗ denotes polluted bogs; • denotes intact bogs) and the greatest air pollution sources (PP—power plants) in NEEstonia.

2 Restoration Ecology


bogs in central Estonia and Meenikunno bog in southeasternEstonia were studied as intact reference bogs characteristic toeastern Estonia (Masing 1984; Paal 2005). In addition, the his-torical geochemical data of two other intact bogs (Nigula andKoitjärve) were used as supporting supplements of historicalgeochemical background. In these bogs, the bog water pH (3.8for Nigula and 4.1 for Koitjärve) and ash content of Sphag-num mosses in Nigula bog were measured in 1990 (Karofeld1994).

Data Sampling

In every studied bog a circular 0.1 ha sample plot wasestablished for analysis, where the average height of treeswas estimated visually and the relative height of hummocksabove lawns was measured (Fig. 2). The total coverage ofthe tree, shrub, and field layer, as well as hummocks wasestimated. The list of vascular plant and bryophyte species wascreated for each circular sample plot. The cover percentageof each bryophyte species was also recorded separately onhummocks and lawns at 10 randomly located 20 × 20 cmsample squares. The nomenclature for vascular plant speciesfollows Leht (2007), and for bryophytes, Ingerpuu et al.(1998).

The pH and electric conductivity of bog water weremeasured in situ under 10 hummocks and 10 lawns in aperforated plastic tube using the WTW MultiLine P4 UniversalMeter. Conductivity estimates were corrected according topH (Sjörs 1950). Samples from the topmost 10–15 cm ofSphagnum mosses (five from hummocks and five from lawns)were taken to determine the ash content (%) from dry weight.Litter and vascular plant remains were removed from samplesbefore they were dried at 60◦C for constant dry weight andthen ashed at 450◦C for 4.5 hours in the laboratory of theEstonian University of Life Sciences.

Data Processing

Several key references (Kannukene & Kask 1982; Kask1982; Ingerpuu et al. 1998; Leht 2007) were used to identifythe habitat preferences of the plant species and to separatetypical bog species from the species that usually grow inother habitats. Ecological indicator values of soil reactionand nutrient content (Ellenberg et al. 1991) were calculatedas cover weighted averages for vascular plant and bryophytespecies separately.

As pollution is the pooled effect of distances from thesources and prevailing winds, in the analyses, the estimated

Figure 2. Overall view of formerly polluted Niinsaare bog study plot with increased tree cover and higher Pinus sylvestris, and Triophorum alpinum andRynchospora alba dominating in the field layer. This figure appears in color in the online version of the article.



deposition load was used as a factor variable (Kaasik 1996;Kaasik & Sõukand 2000). The geochemical dataset wasseparated into three groups: (1) historical observations in bogsof the polluted region from the 1980s and early 1990s;(2) present day observations in bogs of the polluted regionfrom 2006 to 2008; and (3) observations made in various years(from 1990 to 2008) in regions where atmospheric input is atnear-natural level (intact bogs). For the following analyses,ash content and electric conductivity were log-transformed toobtain the normality of residual distribution and the linearityof the relationship with other variables.

Principal component analysis (PCA) was performed toexamine the correlations among the characteristics of bogwater chemistry and vegetation structural parameters in obser-vations from 2006 to 2008 (i.e., using data of bog groups 2and 3 in a dataset). Bog vegetation structure was characterizedby the average height and proportional area of hummocks, bythe coverage and species number of field and moss layers, andby the ratio of typical bog plant species in total species con-tent. Biochemical variables, the pollution intensity estimatesof two moments in time—deposition load of Ca2+ in 1979and 1999 (Kaasik 1996; Kaasik & Sõukand 2000)—and theaverage height of the tree layer were entered as active vari-ables, whereas parameters describing vegetation structure andthe ecological indicator values of species were treated as pas-sive variables.

The analysis of variance (ANOVA) was applied to evaluatethe significance of changes in the environmental characteristicsof bogs in the polluted region, and to compare these changeswith the respective estimates in intact bogs. The generalregression model (GRM) was built to determine the criticallist of factors affecting the proportion of bog-specific species,using a two-way stepwise procedure.

For the joint ordination of species data and environmentalfactors, canonical correspondence analysis (CCA; Ter Braak& Šmilauer 2002) was used with default settings.

Results

Environmental Conditions and Correlates

The first two principal axes of PCA pooled 82.3% of totalvariability in environmental variables and some general char-acteristics of vegetation structure (the first axis 57.6% and thesecond axis 24.8%). Analysis of correlation structure revealedthat calcium deposition load in two contrasting periods (1979and 1999) was quite closely correlated (Fig. 3). As expected,ash content in Sphagnum mosses and bog water pH valuesare both positively correlated with calcium deposition loads,although at the same time ash content and water pH are weaklycorrelated (Fig. 3). The electric conductivity of bog water isthe only variable that is strongly related to the second principalcomponent and nearly perpendicular to the vectors of deposi-tion loads and bog water pH. It appears that the height of thetree layer can somehow affect the ash content in Sphagnummosses and bog water conductivity, as the vector of tree heightis directed between the two of them.

Figure 3. The diagram of PCA, illustrating the correlation structureamong environmental variables and some characteristics of vegetationstructure. Definitions of environmental variables used in the PCA:Dep.load’79 and Dep.load’99—Ca2+ deposition loads in 1979 and 1999according to Kaasik (1996) and Kaasik and Sõukand (2000);Pine.Height—average height of Scotch pines Pinus sylvestris in treelayer; Conduct.—bog water conductivity (log-transformed); Ash%—ashcontent in Sphagnum mosses (log-transformed), Water pH—bog waterpH. Vegetation traits—supplementary variables in PCA, characterizingvegetation structure: Hummock A%—the proportional area ofhummocks in a bog; Hummock H—the average height of hummocks;Bryo.Cover%—the average total cover of mosses in plots;Vasc.Cover%—the average total cover of vascular plants in plots;#Sp.Bryo—number of bryophyte species; #Sp.Vasc—number ofvascular plant species; Bog-Vasc%—percent of bog-specific vascularplant species; Bog-Bryo%—percent of bog-specific bryophytes;Ind.Fert.Vasc—ecological indicator value for soil fertility estimated forvascular plants; Ind.pH Bryo—ecological indicator value for pHestimated for bryophytes; Ind.pH Vasc—ecological indicator value forpH estimated for vascular plants.

The correlation of passive variables to principal componentsshows that species ecological indicator values of pH (calcu-lated separately for vascular plants and bryophytes) as well asthe indicator values of soil nutrient content (calculated onlyfor vascular plant species) are positively correlated to pollu-tion gradient. The bryophytes’ ecological indicator value ofpH shows a more linear relationship to directly measured bogwater pH than in the case of vascular plants. The expectedresult is that the number of species of vascular plants andbryophytes is positively correlated to gradients of depositionload and bog water pH. At the same time, the area of hum-mocks and total bryophyte cover shows a negative correlationto calcium deposition load and bog water pH. Finally, thestrong negative response of the proportion of bog-specific



vascular plants and bryophyte species to pollution is partic-ularly notable.

Changes in the Ash Content of Sphagnum Mosses, Bog WaterpH Value, and Electric Conductivity

The ash content of Sphagnum mosses has significantlydecreased during the past 18 years in bogs in the pollutedregion (F2;14 = 27.5;p = 0.00001; Fig. 4A), but has not yetreached the level of intact bogs. The pH value of bog water hasalso decreased to some extent, but this alteration is still not sig-nificant (Fig. 4B): the statistical test result (F2;14 = 28.77;p =0.00001) indicates only differences among bogs of the pollutedregion and bogs in intact conditions. Bog water conductiv-ity estimates are only available for the present day period of2006–2008, and therefore we cannot test for changes duringself-restoration (between bog groups 1 and 2). Surprisingly,in contrast to other indicators, within the dataset from 2006to 2008 we did not find significant differences in bog waterconductivity among intact bogs (group 3) and bogs from thepolluted region (group 2).

A detailed examination of changes by each separate bogreveals that the ash content of Sphagnum mosses and bogwater pH have considerably changed toward the intact statein Krivasoo bog near the Eesti Power Plant (Fig. 5). Thedecrease in the ash content in the three other bogs of the pol-luted region—Kõrgesoo, Liivjärve, and Mustaladva—is alsonotable; however, similar improvements cannot be observedin the bog water pH level of these bogs (Fig. 5).

Vegetation

The vegetation of bogs in the polluted zone differs from thatin intact bogs. Total bryophyte cover increases from bogs thatare close to polluters toward bogs in intact conditions, whereasthe total cover of vascular plants fluctuates quite randomly,and does not show as a clear trend (Table 1). In bogs thatare located in the vicinity of polluters (Kõrgesoo, Liivjärve,Niinsaare), the number of vascular plant species is up toor even greater than three times the amount in intact bogs,but the species richness of bryophytes shows no significantdifferences. At the same time, very remarkable differencesappear in the proportion of bog-specific species, which isstrikingly lower in polluted bogs (Table 1).

According to the results of the GRM analysis, bog waterpH is the major predictor of “purity” in the plant speciescomposition of bogs (Table 2). In bogs closer to polluters,we recorded calciphilous bryophytes such as Catoscopiumnigritum, Helodium blandowii, Sphagnum subsecundum, andS. platyphyllum (Fig. 6). In the most polluted Kõrgesooand Liivjärve bogs, the proportion of bog-specific bryophytespecies is only 25–31%, whereas in bogs with improvedenvironmental conditions (Niinsaare, Mustaladva, and Kriva-soo), the proportion of bog-specific species reaches 50–84%(Table 1). The same tendency can be observed in the case ofvascular plant species. In contrast to bog-specific bryophytespecies, however, the proportion of bog-specific vascular plant

(A)

(B)

Figure 4. The ash content of Sphagnum mosses (A) and bog water pH(B) in polluted regions in 1990 and from 2006 to 2008, and in thecontrol group of intact bogs over the period 1990–2008.Newman–Keuls multiple comparison test results are presented as labelson the graph. Bars denote 95% confidence intervals for the mean.

species also depends on the history of pollution intensity, theaverage height of pine trees, and the height of hummocks(Table 2). There is a clearly visible reduction in the total num-ber of vascular plant species, which can be correlated with theincreasing distance from polluters (decreased deposition load).On Liivjärve, Kõrgesoo, and Niinsaare bogs, 43–53 species ofvascular plants were recorded, whereas in bogs about another10 km further from pollutants (Mustaladva, Krivasoo, andKasesoo), the corresponding number (8–19 species) is com-parable with that in natural bogs (Table 1). In bogs situatedin the vicinity of the polluters, we found several species thatare more characteristic of the more nutrient rich and calcare-ous sub-neutral wet meadows or rich fens, such as Carexflava, Dactylorhiza incarnata, Epipactis palustris, Gymnode-nia conopsea, Schoenus ferrugineus, and Pinguicula vulgaris(Fig. 6).

In comparison with the historical data published by Karofeld(1994) about the vegetation in Liivjärve and Niinsaare bogs,



(A)

(B)

Figure 5. Changes in ash content of Sphagnum mosses (A) and in bog water pH (B) in bogs of the pollution zone in the time period 1990 to 2008. Thedeposition load of Ca2+ for each bog is taken according to the survey year of ash content and water pH: for the survey from 1990, the deposition loadestimates from 1992 (Kaasik 1996) were used, and for survey data from 2006 to 2008, the deposition load estimates from 1999 (Kaasik & Sõukand2000) were used. Dotted lines have been drawn as a smoothed trend line to illustrate the relationships among variables within particular years.

we discovered that in light of the remarkable decrease in thenumber of species in these bogs (123 in Liivjärve and 91 inNiinsaare recorded in the late 1980s and early 1990s, and 58and 43 species in 2007, respectively), we recorded in these twobogs 22 new vascular plant species, 12 of which are classifiedas calciphilous and nitrophilous species (after Ellenberg et al.1991). Among bryophytes, especially the number of Sphagnumspecies has increased. Whereas in the mid-1980s a total of nineSphagnum species were recorded in Liivjärve and Niinsaarebogs (Karofeld 1987, 1994), in 2007 we registered 14 speciesof that genera from these bogs. Newly emerged speciessuch as meso-eutrophic S. capillifolium, oligo-mesotrophicS. angustifolium, and oligotrophic S. tenellum indicate the

restoration of environmental conditions that are more suitablefor typical bog species.

CCA ordination of vascular plants and bryophytes (Fig. 6)revealed the still existing relationship between gradients ofpollution intensity (calcium deposition load) and vegetationcomposition, with a clearly visible graduation from heav-ily polluted bogs (Kõrgesoo and Liivjärve) over presentlyrecovering bogs (Niinsaare and Mustaladva) and the nearlyrecovered Krivasoo bog to bogs in natural conditions. Thisself-restorational succession is correlated to changes in bogenvironment: the succession begins with conditions of highdeposition load, high pH, and conductivity values of bog waterin the presently heavily polluted Kõrgesoo bog, continued with



Tab

le1.

Ave

rage

estim

ates

ofen

viro

nmen

tal

vari

able

san

dve

geta

tion

char

acte

rist

ics.

Bog

Type

Dep

osit

ion

Loa

dC

ondu

ctC

orre

cted

Wat

erA

shP

ine

Hum

moc

kH

umm

ock

Num

ber

ofB

og-S

peci

ficC

over

(%)

Env

iron

men

tal

(μSc

m−1

)C

ondu

ctpH

(%)

Hei

ght

Are

aH

eigh

tSp

ecie

sSp

ecie

s(%

)In

dica

tor

Valu

es(m

)(%

)(c

m)

1979

1992

1999

Vas

c.B

ryo.

Vas

c.B

ryo.

Vas

c.B

ryo.

pHpH

Fert

Vas

cB

ryo

Vas

c

Kõr

geso

oPo

llute

d19

1510

98.1

98.0

5.7

2.8

440

2053

2836

2550

552.

255.

511.

87L

iivj

ärve

Pollu

ted

258

810

910

8.9

5.4

3.1

2.5

425

5832

3431

3041

3.20

6.05

2.16

Nii

nsaa

rePo

llut

ed22

75

82.7

82.5

5.2

2.7

420

3243

2033

5060

601.

534.

261.

34M

usta

ladv

aPo

llute

d17

94

74.7

74.2

4.8

2.9

2.5

1030

1917

6376

5085

1.72

1.68

1.38

Kri

vaso

oPo

llute

d15

105

147.

114

3.0

3.9

4.8

285

3510

2590

8416

871.

711.

821.

22K

ases

ooIn

tact

106

212

6.4

119.

13.

72.

32.

575

248

1788

100

1795

1.26

1.31

1.06

Fjod

oris

ooIn

tact

65

394

.387

.83.

71.

62

7030

915

7810

013

951.

971.

701.

12H

eina

soo

Inta

ct4

22

151.

513

8.6

3.4

2.1

690

198

575

100

1996

1.92

2.02

1.30

Män

nikj

ärve

Inta

ct0

00

63.3

59.6

41.

31.

555

2213

1892

100

6093

1.22

1.23

1.21

Lau

kaso

oIn

tact

00

098

.595

.64.

11.

51.

240

2215

2087

100

4091

1.45

1.24

1.16

Mee

niku

nno

Inta

ct0

00

83.8

74.6

3.6

1.8

1.6

9728

822

8886

1891

1.74

1.13

1.15

Con

duct

.,bo

gw

ater

cond

uctiv

ity;

Vas

c.,

vasc

ular

plan

ts;

Bry

o.,

bryo

phyt

es;

Fer

t,so

ilfe

rtili

ty.



the decrease in water conductivity in Liivjärve and Niinsaarebog, followed by the reduction of pH value and the presentday deposition load in Mustaladva bog, and finally ends in therecovered Krivasoo and Kasesoo bogs (Fig. 5, Table 1). Thewater conductivity fluctuation between different bogs couldalso be caused by local chance factors and may not followsuch clear trends as water pH and ash content in these bogs.

Discussion

Raised bogs are organic landforms that cover large continentalareas, and locally play an important role as fresh waterreservoirs, and globally as major carbon sinks (Gorham 1991).These are nutrient-poor natural ecosystems that are formedmostly by the growth and biomass accumulation of Sphagnummosses, the keystone species (Andrus 1986). Due to thelack of minerals in bogs and the very low ash content ofSphagnum, the pH of bog water is regulated by the metabolismof Sphagnum mosses and organic acids released from thedecaying plants to be about 3–4 units (Clymo 1984; Gagnon& Glime 1992; Siegel et al. 2006).

The increased value of water pH in polluted bogs iscaused by the two-way impact of alkaline fly ash and nutrientinput—first through its increasing pH and second, due tothe direct and indirect lethal effects of ash on Sphagnummosses, the system has lost its buffering capacity. Underconditions of alkaline pollution, Sphagnum species can partlycompensate for the alkalization of bog water up to a certainlevel. For most Sphagnum species it is lower than 5.5 pHunits (Andrus 1986; Succow & Joosten 2001), but exceedingthat level, they die, and the further alkalization of bog waterwill accelerate, supported by increased competition of otherbryophyte species and vascular plants adapted to neutral oralkaline soil conditions and improved nutrient levels. Newlyformed bryophyte-grass peat also isolates Sphagnum peatfrom bog surface water, thus its effect on bog water acidityis minimized. Such successional degradation processes havebeen theoretically explained as catastrophic shifts betweenmore stable states after long-term resilience to disturbances(Scheffer & Carpenter 2003), and have also been observed inmire communities in the upland hills of the United Kingdom(Bragg & Clymo 1995; Bragg & Tallis 2001), bog-agriculturalfield ecotones in Poland (Krunk et al. 2003), raised bogcommunities in Sweden (Johnson & Damman 1991), andpeatlands in Minnesota (Glaser et al. 1990), where changedhydrological regime, liming, and increased pollution havebroken the ecosystem stability threshold and caused the decayof peat, increased peat erosion, and the rapid degradation ofthe ombrotrophic ecosystem into transitional mire-like system.

During the period of the highest air pollution loads, from1970 to 1990, the water pH in the most polluted bogs ofKõrgesoo, Liivjärve, and Niinsaare reached values of 5.3–6.7.The Ca2+ content (the main compound of oil shale fly ash)in bog water in Kõrgesoo bog was then circa 37 mg L−1 incomparison with less than 0.05 mg L−1 in the intact Nigulabog (Karofeld 1994). Eventually, in several bogs, Sphagnum

species became completely extinct and were replaced byspecies characteristic to more nutrient rich habitats.

Currently, after air pollution emission loads have beenreduced (Liiv & Kaasik 2004), the ash content in the mosslayer of the most polluted bogs decreased by almost 2–4times (e.g., in Kõrgesoo it has changed from 10.6–15.2to 2.1–4.0% and in Liivjärve from 7.9–9.0 to 2.8–3.6%).However, the atmospheric input in this historically pollutedarea is still high and, especially in the neighborhood of thebiggest polluter—Eesti Power Plant, the ash content in bogswithin the impact zone is still higher than in intact bogselsewhere in Estonia, where its average content is from 1.3to 2%.

We did not find a significant correlation between bogwater electric conductivity, bog microtopography, and distancefrom a polluter (Karofeld et al. 2007). In addition to otherfactors, this could be caused by extra local reasons such asthe upward movement of more mineral rich water from themore decomposed fen peat layer (Glaser et al. 1990; Siegelet al. 1995; Lamers et al. 1999; Ilomets et al. 2004) or birddroppings (Tomassen 2005).

Nevertheless, following the modest reduction in oil shale flyash input, Sphagnum species have already began to reappearin previously degraded bogs, particularly in Niinsaare andLiivjärve bogs. Recently, newly established Sphagnum coverwas recorded even in the Kõrgesoo bog, which is situated nearto the two major power plants and has, therefore, the highestloads of ash input (Karofeld 1996; Kaasik & Sõukand 2000).Sphagnum mosses reappear first on bog hummocks and poolbanks fed solely by precipitation, and thus these microhabitatsbecome suitable for Sphagna earlier than lawns that arestill affected by the outwash from mineral rich peat layersformed in periods with heavy air pollution loads (Karofeldet al. 2007). Once they have reappeared, Sphagnum speciesthemselves cause the lowering of bog water pH toward thelevel that is characteristic for natural bogs, and facilitate theestablishment of other typical bog species. As we have found,the water pH in the bogs of marginal areas within the pollutedregion has decreased by 0.5–1 units, except for the absenceof changes in the most intensively polluted Kõrgesoo bog.Such a change has given rise to the processes of communityrecovery and recolonization of bog-specific bryophyte andvascular plant species. This can be seen from the increasedproportion of bog-specific plant species along the water pHgradient. The tendency toward improved floristic compositionis also reflected by altered bryophyte species preferences forsoil pH and reduced requirements for nutrient availability bymosses and vascular plants. Positive changes in bog vegetationare also reflected by the total cover of bryophytes. At the sametime, one cannot detect such correlations among environmentalvariables and the species richness of both plant groups and thecoverage of vascular plants, which can easily lead to biasedconclusions about bog recovery.

As we found a negative relationship between the propor-tion of vascular plant species typical for bogs and tree standheight, we assume that bog self-restoration processes might behalted by the intensified growth of Scots pines that occurred



(A)

(B)

Figure 6. Ordination of sample areas, vascular plant (A) and bryophyte (B) species, and pollution characteristics by CCA axes 1 and 2. Circles mark thebogs located in the most polluted region, diamonds correspond to the bogs in less polluted zone or in intact areas. Other notations are as in Fig. 3. Fullnames of plant species abbreviations are given in Appendix.



Table 2. GRM analysis results estimating the predictors of the proportion of bog-specific species among vascular plants (BogVasc%) and bryophytes(BogBryo%).

BogVasc% BogBryo%(adjR2 = 0.94;p = 0.0001) (adjR2 = 0.86;p < 0.0001)

Slope Beta p Slope Beta pEstimate Estimate

Intercept 301.66 0.0002 219.25 0.0001pH −37.87 −1.29 0.0004 −32.98 −0.94 0.0001Pollution zone −13.47 −0.59 0.0329Height of pines −8.07 −0.48 0.0020Hummock height −1.78 −0.39 0.0241

during the period of intensive pollutant input (Karofeld 1994;Pensa et al. 2007; Kaasik et al. 2008). The enhanced tree layerwill probably influence the course of vegetation successionvia (1) decreasing light availability, as the majority of typicalbog species in North Europe prefer open habitats (Hájek et al.2009); (2) creating efficient traps for atmospheric depositionboth directly (by creating additional surface areas to trap par-ticulates and precipitation) and indirectly (increased roughnessof canopy upper surface reduces wind); and (3) influencingwater regime via increased evapotranspiration (Fenton & Berg-eron 2006). At the same time, pine needle litter could helprestore the natural acidity of bog water.

We studied various aspects of the bog ecosystem to revealpotential indicators for the evaluation of recovery processes.Geochemical indicators have been widely used in many stud-ies (Bragazza et al. 2003; Liblik et al. 2003), whereas thecomposition and structure of vegetation have received lessattention. However, when considering habitat quality and veg-etation structure, the latter has received increasing attention inrecent decades because of improved analytical instrumentation(Aaviksoo et al. 1994; Liira et al. 2007; Ejrnaes et al. 2008).One simple and informative indicator shown here is the per-centage of bog-specific plant species in the total number ofspecies. The observed indicators of bog ecosystem recoveryand the relationships among them point to strong causal andstatistical correlations, and they seem to be biogeographicallyrobust. These are some of the basic requirements for successfulindicators (Brooks & Kennedy 2004; Kohv & Liira 2005). Wehave demonstrated that several geochemical indicators, suchas water pH, but also ash content, and several compositionalindicators of typical bog vegetation are promising variables tobe included in the monitoring methods.

In the current study, we did not examine the potential effectsof landscape, which might affect self-recovery, as dispersallimitation and dispersal distance are important factors evenfor species propagating with spores (Jüriado et al. 2006). Thequestion of how one can explain the rapid reestablishment ofhabitat-demanding species in severely damaged bog commu-nities (Hughes & Barber 2003), however, remains still open tostudy (e.g., are there any type refugia in the landscape or withinthese bogs itself, or that they have a long-lasting seed bank).Some typical bog plants were probably never killed completelyat a site, so their populations rebounded quickly once the pH

of the surface waters reequilibrated to their natural range. Reg-ular monitoring of the self-restoration of these bogs in parallelwith reference sites over longer periods should provide thereal insight into the natural way in which bog communitiesare restored, and whether current observations have succeededin pointing to proper indicators and authentic processes.

Conclusions

After the installation of improved dust catching filters, reducedpower production, and therefore decreased alkaline ash emis-sions in recent decades, there are signs of natural recovery inthe formerly air polluted and degraded bogs of NE Estonia.Geochemical variables, however, indicate that bogs locatedclose to power plants still exceed their threshold of environ-mental buffering capacity, and that these bogs are subject toan ongoing risk of large-scale changes in ecosystem qualityand vegetation structure. In heavily polluted bogs, fewer bog-specific vascular plant and bryophyte species can be found,and the moss layer is also very fragmented—the ecosystemreminds a lot the transitional mire. In bogs with improved envi-ronmental conditions, however, there are signs that these bogsmay recover naturally, as the number and share of species thatare characteristic of intact bog communities has increased afterthe reduction of air pollution that took place since the 1990s.In order to enhance the speed of self-restoration, even moredrastic air protection measures should be taken, and intensivemonitoring of its status should be performed so as to detectpotential stagnation in the bog recovery process.

Implications for Practice

The following suggestions for restoration practice could bepointed out:

• Most essential is to reduce the atmospheric input ofpollutants. Some bog-specific species can persist in thecommunity or nearby refugia, and are able to recovernaturally after decades of pollution. Therefore, for therestoration of raised bog ecosystems after the cessationof pollution input, natural self-restoration should bepreferred and the transplantation of Sphagnum mosses



and/or vascular plant species is not necessary. For that,low-cost and long-term passive conservation activitiesshould be planned.

• The temptation to preserve alkaline pollution inducedhigher species richness of bog communities, and rare nonbog–specific plant species is unreasonable because underconditions of continuous pollution, the future degradationof a bog ecosystem can lead to unpredictable results.

• We suggest that the bog water pH, bryophyte coverage,and the number or proportion of habitat-specific plantspecies can be used as efficient indicators to monitor theself-restoration succession. The usually exploited indica-tors of bog restoration such as electrical conductivity andthe total number of species appeared to be less efficientindicators.

Acknowledgments

We are grateful to Nele Ingerpuu and Mare Toom for theirassistance with the fieldwork and in identifying some criticalplant species. Alexander Harding is thanked for revision ofEnglish language. This study was financed by the EstonianState Nature Conservation Centre of Ida-Virumaa County,target-financing projects SF0182732s06, SF0182639s04, andSF0180012s09, Estonian Science Foundation grant 7387, andthe Centre of Excellence FIBIR.

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Appendix. List of bryophytes and vascular plant species used in an ordination of sample areas and plants.

Abbreviation Species FamilyBryophytes

Ane ping Aneura pinguis AneuraceaeAul palu Aulacomnium palustre AulacomniaceaeBry pseu Bryum pseudotriquetrum BryaceaeCal giga Calliergon giganteum AmblystegiaceaeCal rich Calliergon richardsonii AmblystegiaceaeCal cusp Calliergonella cuspidata AmblystegiaceaeCam stel Campylium stellatum AmblystegiaceaeCat nigr Catoscopium nigritum CatoscopiaceaeCep conn Cephalozia connivens CephaloziaceaeCep loit Cephalozia loitlesbergeri CephaloziaceaeCep lunu Cephalozia lunulifolia CephaloziaceaeCep plen Cephalozia pleniceps CephaloziaceaeCin styg Cinclidium stygium MniaceaeCla flui Cladopodiella fluitans CephaloziaceaeCli dend Climacium dendroides ClimaciaceaeDic berg Dicranum bergeri DicranaceaeDic bonj Dicranum bonjeanii DicranaceaeDic poly Dicranum polysetum DicranaceaeDic scop Dicranum scoparium DicranaceaeDre coss Drepanocladus cossonii AmblystegiaceaeDre revo Drepanocladus revolvens AmblystegiaceaeFis adia Fissidens adianthoides FissidentaceaeGym infl Gymnocolea inflata LophoziaceaeHel blan Helodium blandowii ThuidiaceaeHyl sple Hylocomium splendens HypnaceaeLop hete Lophocolea heterophylla GeocalycaceaeKur pauc Kurzia pauciflora LepidoziaceaeMyl anom Mylia anomala JungermanniaceaePal squa Paludella squarrosa MeesiaceaePle schr Pleurozium schreberi HypnaceaePoh nuta Pohlia nutans BryaceaePoh spha Pohlia sphagnicola BryaceaePol comm Polytrichum commune PolytrichaceaePol juni Polytrichum juniperinum PolytrichaceaePol stri Polytrichum strictum PolytrichaceaeRhy triq Rhytidiadelphus triquetrus HypnaceaeRic cham Riccardia chamedryfolia AneuraceaeSan unci Sanionia uncinata AmblystegiaceaeSph angu Sphagnum angustifolium SphagnaceaeSph balt Sphagnum balticum SphagnaceaeSph capi Sphagnum capillifolium SphagnaceaeSph cent Sphagnum centrale SphagnaceaeSph cusp Sphagnum cuspidatum SphagnaceaeSph fall Sphagnum fallax SphagnaceaeSph flex Sphagnum flexuosum SphagnaceaeSph fusc Sphagnum fuscum SphagnaceaeSph mage Sphagnum magellanicum SphagnaceaeSph maju Sphagnum majus SphagnaceaeSph plat Sphagnum platyphyllum SphagnaceaeSph rube Sphagnum rubellum SphagnaceaeSph squa Sphagnum squarrosum SphagnaceaeSph subf Sphagnum subfulvum SphagnaceaeSph subn Sphagnum subnitens SphagnaceaeSph subs Sphagnum subsecundum SphagnaceaeSph tene Sphagnum tenellum SphagnaceaeSph tere Sphagnum teres SphagnaceaeSph warn Sphagnum warnstorfii SphagnaceaeThu reco Thuidium recognitum Thuidiaceae



Appendix. (Continued ).

Abbreviation Species FamilyBryophytes

Thu phil Thuidium philibertii ThuidiaceaeTom nite Tomentypnum nitens BrachytheciaceaeWar exan Warnstorfia exannulata Amblystegiaceae

Vascular plants

And poli Andromeda polifolia EricaceaeAng sylv Angelica sylvestris ApiaceaeCal epi Calamagrostis epigeios PoaceaeCal cane Calamagrostis canescens PoaceaeCar lasi Carex lasiocarpa CyperaceaeCar limo Carex limosa CyperaceaeCar rost Carex rostrata CyperaceaeCha caly Chamaedaphne calyculata EricaceaeCir arve Cirsium arvense AsteraceaeCir hete Cirsium heterophyllum AsteraceaeDac fuch Dactylorhiza fuchsii OrchidaceaeDac macu Dactylorhiza maculata OrchidaceaeDro angl Drosera anglica DroseraceaeDro inte Drosera intermedia DroseraceaeDro rotu Drosera rotundifolia DroseraceaeEmp nigr Empetrum nigrum EmpetraceaeEpi angu Epilobium angustifolium OnagraceaeEri vagi Eriophorum vaginatum CyperaceaeEup cann Eupatorium cannabinum AsteraceaeFes rubr Festuca rubra PoaceaeFra vesc Fragaria vesca RosaceaeGal albu Galium album RubiaceaeGal ulig Galium uliginosum RubiaceaeGym cono Gymnadenia conopsea OrchidaceaeHam palu Hammarbya paludosa OrchidaceaeHie umbe Hieracium umbellatum AsteraceaeJun nodo Juncus nodulosus JuncaceaeLed palu Ledum palustre EricaceaeLyc euro Lycopus europaeus LamiaceaeMel prat Melampyrum pratense ScrophulariaceaeMen trif Menyanthes trifoliata MenyanthaceaeMol caer Molinia caerulea PoaceaeOxy micr Oxycoccus microcarpus VacciniaceaeOxy palu Oxycoccus palustris VacciniaceaePin vulg Pinguicula vulgaris LentibulariaceaePla bifo Platanthera bifolia OrchidaceaePoa angu Poa angustifolia PoaceaePol amar Polygala amarella PolygalaceaePot erec Potentilla erecta RosaceaePyr rotu Pyrola rotundifolia PyrolaceaeRhy alba Rhynchospora alba CyperaceaeRhy fusc Rhynchospora fusca CyperaceaeRub cham Rubus chamaemorus RosaceaeRub idae Rubus idaeus RosaceaeSch ferr Schoenus ferrugineus CyperaceaeSuc prat Succisa pratensis DipsacaceaeTri caes Trichophorum cespitosum CyperaceaeTri palu Triglochin palustre JuncaginaceaeTyp angu Typha angustifolia TyphaceaeUtr mino Utricularia minor LentibulariaceaeVac ulig Vaccinium uliginosum VacciniaceaeVal offi Valeriana officinalis ValerianaceaeVio palu Viola palustris Violaceae


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