Science of the Total Environment 444 (2013) 212–223

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Changes in crown architecture as a strategy of mountain birch for survival in habitatsdisturbed by pollution

Vitali Zverev a,b, Mikhail V. Kozlov a, Elena L. Zvereva a,⁎a Section of Ecology, Dept. of Biology, University of Turku, FI-20014 Turku, Finlandb Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences, ul. Vos'mogo Marta 202, Yekaterinburg, 620144, Russia

H I G H L I G H T S

► Birches growing in industrial barrens have compact and dense crowns.► Formation of compact crown is driven by effects of both pollution and microclimate.► Birches from barrens have increased ability to compensate for mechanical damage.► High compensative ability is enabled by increased bud and shoot production.► Compact and dense crowns are adaptive in a harsh environment of industrial barrens.

⁎ Corresponding author. Tel.: +358 2 3335492; fax: +E-mail address: elezve@utu.fi (E.L. Zvereva).

0048-9697/$ – see front matter © 2012 Elsevier B.V. Allhttp://dx.doi.org/10.1016/j.scitotenv.2012.11.084

a b s t r a c t

a r t i c l e i n f o

Article history:Received 29 October 2012Received in revised form 23 November 2012Accepted 26 November 2012Available online 27 December 2012

Keywords:AdaptationClimateCompensatory responsesCrown shapeGrowth habitShoot production

Although trees in polluted areas often exhibitmodified growth habits, the immediate causes of changes in crownarchitecture and their consequences for persistence of plant populations in disturbed habitats are not well un-derstood. We compared individuals of mountain birch, Betula pubescens ssp. czerepanovii, growing in severelydisturbed habitats (industrial barrens) surrounding a nickel–copper smelter in north-western Russia, withbirches growing in unpolluted habitats. They were found to have shorter heights, a shrubby growth habit,lower depth/width and surface/foliar mass ratios of the crown, higher numbers of dead branches and twistedtrunks and higher branching resulting from increased numbers of long shoots and more densely spaced budsthan individuals in unpolluted forests. The increased production of long shoots was enabled by their formationnot only from the axillary buds of previous-year long shoots but also from the apical buds of short shoots.These latter long shoots develop in the inner part of the crown, thus increasing the crown density. Additionally,birches from industrial barrens better compensated for mechanical damage, such as trunk/shoot removal, com-pared to birches from unpolluted forest and mountain tundra habitats, presumably due to the larger number ofbuds formed annually. The specific crown architecture of these birches can be explained by the direct effects ofpollution combinedwith changes inmicroclimate due to pollution-induced forest decline. The seed progenies ofbirches from an industrial barren reared in a benign environment produced higher numbers of long shoots thanseedlings fromother habitats, suggesting that adaptive changes in crown architecture are partially shaped by theselection imposed by long-term pollution impacts. Nearly spherical and compact crowns minimise the impactsof unfavourable environmental conditions on trees and are therefore adaptive. We concluded that the develop-ment of specific crown architecture allowsmountain birch to dominate in habitats that are severely disturbed bypollution.

© 2012 Elsevier B.V. All rights reserved.

1. Introduction

The crown architecture of a tree is the cumulative result of shoot pro-duction and elongation, controlled by genetic and environmentalinteractions on meristem activity in space and time (Tremmel andBazzaz, 1995). The arrangement of leaves within the crown reflects thespatial strategy of the plant for light interception and maximising carbongain (Kawamura, 2010), with obvious consequences for ecosystem

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productivity. Consequently, studies of plant architecture have focused al-most exclusively on light capture by crowns and its potential effect onphotosynthesis (Horn, 1971; Honda and Fisher, 1978; Waller andSteingraeber, 1985). However, links between crown architecture andother crown functions, including, in particular, the minimisation of therisk of damage and the mitigation of high levels of light andtemperature-related stress are not well understood (Pearcy et al., 2005).

Trees growing in heavily polluted habitats generally demonstrate re-tarded vertical growth and changes in growth habit, primarily in crownshape (Halbwachs, 1984; Kryuchkov, 1993; Kozlov et al., 2009). For ex-ample, woody plants (Acer rubrum L., Betula papyrifera Marsh. and

Fig. 1. Shoot types of mountain birch: long shoot (Long) with four axillary buds andtwo short shoots (Short) with one apical bud each.

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Quercus rubra L.) persisting in industrial barrens surrounding non-ferroussmelters in Sudbury often have deadmain stems and abundant sproutingfrom the root collar (James and Courtin, 1985;Winterhalder, 2002). Sim-ilarly, the proportion of low-stature Norway spruce (Picea abies (L.)Karst.) trees with dead upper canopies but with extensive growth ofcreeping lower twigs increased when approaching the smelter atMonchegorsk, Russia (Kozlov, 2001). Two willow species, Salix borealis(Fries.) Nasar. and goat willow, Salix caprea L., have more epicormicshoots in the surroundings of two non-ferrous smelters than inunpolluted forests (Zvereva and Kozlov, 2001). These changes in growthhabit are usually attributed to wind-driven snow abrasion (Arseneaultand Payette, 1997), which may be enhanced by pollutants (Alexeyev,1990), or to an increase in light availability caused by forest decline(Zvereva and Kozlov, 2001). However, we are not aware of any studythat quantitatively describes the crown architecture of trees persistingin habitats that are modified by the long-term impacts of severe pollu-tion.Moreover, both the causalmechanisms behind changes in crown ar-chitecture in trees growing in severely contaminated landscapes and theconsequences of these changes for tree performance remain poorlyknown.

Mountain birch (Betula pubescens ssp. czerepanovii (Orlova) Hämet-Ahti) is the only tree species that is still relatively abundant in the ex-tremely contaminated barren habitats surrounding the nickel–coppersmelter at Monchegorsk in north-western Russia. The growth habit ofthis species is highly variable: it ranges from a tall slender monocormictree in forests to a low-stature polycormic tree with twisted trunks atthe upper tree limits and along sea shores (Kallio et al., 1983;Ermakov, 1986; Torkhov et al., 2005) and to low, prostrate shrubs in in-dustrial barrens (Kryuchkov, 1993; Kozlov et al., 2009). The crown ar-chitecture of the mountain birch is relatively well studied (Kaitaniemiand Ruohomäki, 2003; Renton et al., 2005; Kaitaniemi, 2007), but weare not aware of any architectural analysis performed using birch treesfrom the opposite ends of environmental stress gradients. Therefore,the comparison of mountain birch trees that were able to sustain ex-treme pollution loads with trees growing in benign environmentscould add a new dimension to studies of the genetic and environmentalinfluences on the crown architecture of trees.

A detailed analysis of crown architecture is crucial for understandingthe growth responses of trees to various ecological conditions (Lintunenand Kaitaniemi, 2010). Severely polluted habitats, especially industrialbarrens (bleak open landscapes developed around major polluters dueto the severe long-term impacts of airborne pollutants), offer unique op-portunities for studyingboth theplasticity of crown architecture and theimportance of changes in growth habits for tree survival in unfavourableenvironments. These specific habitats differ from unpolluted forests notonly by the contamination of the soils and ambient air but also by theconsequences of pollution-induced forest dieback, like higher windspeed, thinner and more compact snow cover, lower nutritional qualityof soils and greater temperature extremes (Kozlov and Haukioja, 1997;Lukina and Nikonov, 1999; Kozlov, 2001, 2002; Kozlov and Zvereva,2007). Importantly, most of the mountain birch individuals nowpersisting in industrial barrens are over 50 years old (Zverev, 2009),i.e., these birches had begun to grow in the forests that covered theseareas prior to the early 1960s (Kozlov and Barcan, 2000). Thus, the spe-cific growth habits of these mountain birch individuals have beenformed during the lifetime of one birch generation under increasing im-pacts of both pollution and the harsh environmental conditions associ-ated with the steady decline of primary forest and its replacementwith an industrial barren. This impact was so strong that during a fewdecades, all sensitive genotypes had been eliminated, with only themost resistant individuals ofmountain birch persisting in industrial bar-rens around the two nonferrous smelters located in the Kola Peninsula(Kozlov, 2005; Eränen, 2008). The question then ariseswhether the spe-cific growth habit of thesemountain birches represents an adaptation tosevere environmental stress that allows this species to dominate thebarren landscape.

The goals of the studywere to explore themechanisms of the devel-opment of the specific crown architecture in mountain birches growingin industrial barrens and to examine the adaptive value of the observedcrown modifications for the survival of the birch population in an evo-lutionarily novel habitat created by the long-term impacts of severe pol-lution. We aimed at testing the following hypotheses: (1) the crownarchitecture of birches growing in an industrial barren differs from thecrown architecture of birches growing in unpolluted natural habitats;(2) the development of the specific crown architecture is due to both ef-fects of pollution per se and the effects of pollution-induced changes inmicroclimate (associated with the decline of forest); (3) progenies ofbirches from an industrial barren demonstrate the same modificationsin crown architecture as the trees naturally growing in this habitat;(4) birches that have survived in a polluted environment have a greaterability to compensate for losses of aboveground biomass than birchesfrom unpolluted natural habitats.

2. Materials and methods

2.1. Study species

Mountain birch (B. pubescens ssp. czerepanovii) is the dominant treespecies in the northernmost part of Fennoscandia, in Iceland and insouthern Greenland, where it forms stable climax forests at the treeline. Mountain birch is highly variable in terms of growth habits andleaf morphology, due in part to the hybrid origin of this species (Kallioet al., 1983; Ermakov, 1986). Due to its high ecological importance insubarctic forests, mountain birch has been intensively studied in bothpristine and disturbed environments (Sveinbjörnsson et al., 1996;Wiegolaski, 2005; Zverev, 2009, 2012; Eränen et al., 2009).

Birches produce two different types of shoots (Fig. 1). The mono-podial short shoots bear two to five (usually three) leaves and an api-cal bud that includes primordia for leaves flushing in the subsequentyear. These shoots grow less than 2 mm per year; their primary phys-iological function is photosynthesis. The growth of branches, and ofthe whole birch tree, occurs via the elongation of the sympodial inter-nodes of long shoots. These shoots produce successive single leaveseach supporting one axillary bud. The apical buds of short shoots usu-ally produce short shoots, whereas the axillary buds of long shootsmay produce both long and short shoots. Both types of shoots canbe vegetative and generative. Generative short shoots produce oneto three female catkins and generative long shoots one to five male

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catkins (Kaitaniemi and Ruohomäki, 2003). In the following text,shoot length always refers to vegetative long shoots.

2.2. Study area and study sites

The study was conducted in the Kola Peninsula in north-westernRussia, north of the Arctic Circle. Before the smelter located inMonchegorsk (67° 55′ N, 32° 48′ E) began to operate, the dominanttype of lowland vegetation in the areas south of Monchegorsk was apristine forest formed primarily by Norway spruce with a dense coverof dwarf shrubs dominated by bilberry, Vaccinium myrtillis L., crowber-ry, Empetrum nigrum ssp. hermaphroditum (Hagerup) Böcher, and greenmosses (Bobrova and Kachurin, 1936). The long-term (since 1939) im-pacts of aerial emissions from the nickel–copper smelter, combinedwith logging and fires, resulted in the gradual transformation of the for-ests adjacent to Monchegorsk into an industrial barren with smallpatches of vegetation surrounded by bare landwith the illuvial horizonor even the rock exposed due to intensive soil erosion. The developmentof the industrial barren in our study area began in the early 1960s, andby the early 1990s, it was estimated to cover 200–250 km2, surroundedby 400–500 km2 of dead forests (Kozlov and Zvereva, 2007). For de-tailed descriptions of both the smelter and the impacted area, consultKozlov et al. (2009).

Study sites were randomly selected in three types of habitats:unpolluted forest, mountain tundra and industrial barren (UF, MT andIB, respectively; Fig. 2). Unpolluted forests are formed by Norway spruceand mountain birch with a dense field layer vegetation dominated bycrowberry and bilberry. In the industrial barren that has developedfrom this type of forest, upper canopy trees are absent andwoody plantsare represented by low-stature mountain birch trees located 5–15 mapart with a small admixture of goat willow; field layer vegetation isnearly missing (cover b1%). In subalpine habitats, selected at the uppertree limit of the mountains of Lovozero, Khibiny and Monchetundra(455–615 m a.s.l.), mountain birch trees are located tens to hundreds

Fig. 2. Locations of study sites selected in unpolluted forest (UF1–UF8

of metres apart; field layer vegetation is less dense than in forests butmuch better developed than in industrial barrens. The field layer isformed primarily by crowberry, but bilberry and other dwarf shrubs(Vaccinium vitis-idaea L., Vaccinium uliginosum L., Andromeda polifolia L.and Phyllodoce coerulea (L.) Bab.) are also abundant.

2.3. Crown architecture

In each of the six study sites (IB1, IB4, MT1, MT3, UF6, and UF8;Fig. 2) at the end of July 1995, we cut five to ten birch trees (40 treesin total), randomly selected to represent different size classes, andtransported them to the laboratory. All of the cut trees had basal trunkdiameters b45 mm because the live stems of 98% of the mountainbirch individuals in barren sites did not exceed this value (Zverev,unpublished data). In the laboratory, we recorded the following charac-teristics: basal trunk diameter; tree height (the vertical distance be-tween the ground and the base of the highest leaf); crown depth (thevertical distance between the bases of the lowest and the highest leaf)and width (the first measurement was the maximum horizontal dis-tance between the bases of leaves situated on opposite, relative to thetrunk base, parts of the crown, and the second measurement wasmade in the direction perpendicular to the first one); the number of re-placements of the leading shoot (when, following the death of the apicalbud of the main stem, one of the lateral branches becomes the leader);the basal diameters of all dead branches, including previous-year longshoots arising from live twigs; the numbers of short and long shootsand the numbers of leaves on them; and the lengths of ten long shootsthat were randomly selected from within the crown (or the lengths ofall long shoots, if there were less than ten long shoots on a tree). A ran-dom sample of 10 leaves was dried (at +80 °C for 24 h) and weighed;the total leaf biomass was then calculated by multiplying the numberof leaves by the mean leaf dry weight. The sum of the basal areas of alldead branches served as a measure of branch dying off. Crown shapewas quantified by the ratio between crown depth and the geometric

), mountain tundra (MT1–MT4) and industrial barren (IB1–IB6).

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mean of the twowidth measurements. Crown surface was calculated asdescribed by Zarnoch et al. (2004).

2.4. Branch structure

For a more detailed study of changes in growth pattern, at the endof July 2010 we sampled two first-order branches (lacking deadwoody parts) with basal diameters of ca. 10 mm from oppositesides of the crowns of each of the five birches (height 100–200 cm)from each of two barren and two forest sites (IB2, IB5 and UF2, UF4,respectively; Fig. 2). In the laboratory, we measured basal diameter,branch length (the maximum distance between the base of thebranch and the base of the most distant leaf) and the sum of thelengths of all woody parts, counted the number of buds (both apicaland axillary) and weighed the woody parts of the branch and its fo-liage separately (after drying at +80 °C for 48 h). The ratio betweenthe sum of the lengths of all woody parts and the branch lengthserved as a measure of branching (hereafter, the branching index).

2.5. Annual variation in the production of long shoots

Both the number and the length of long shoots were recordedfrom 1998 to 2011 (data for 2004 were missing) to estimate annualvariations in these characters. In each of the study sites (IB1–IB6and UF1–UF6; Fig. 2) we tagged five mature (20–70 years old) moun-tain birches with growth habits that were typical for the given sites.After the termination of shoot growth (at the end of July), we countedthe long shoots on each tree, measured the lengths of 10 randomlyselected long shoots from different parts of the crown (or the lengthsof all shoots, if there were less than ten long shoots on a tree) and thebasal diameter of the tree trunk(s). The total length of the long shootswas calculated by multiplying the mean tree-specific shoot length bythe number of long shoots on the tree. Monthly mean temperatureand precipitation data based on records for Monchegorsk wereobtained from the archives of the Lapland reserve for the years1998–2004 and from a web-based archive of weather data (www.rp5.ru) for the years 2005–2011.

2.6. Production of long shoots by the progenies of birches from differenthabitats

A commongarden experimentwas established in 2003 in unpollutedwoodlands of northern Norway, comprised of mountain birch seedlingsgrown from seeds that were collected from the high- and low-stressends of multiple stress gradients around the Kola Peninsula. This exper-iment was aimed primarily at the exploration of birch adaptations toheavy metals, wind and drought stress. Details of the protocol and thebasic outcomes of this experiment were described by Eränen et al.(2009). In short, greenhouse-grown seedlings (6 months old) wereplanted in four fenced plots, two of which were located at Skibotndalen(69° 07′N, 20° 45′ E) and another two near Narvik (68° 31′N, 17° 58′ E).In each plot,we planted four seedlings fromeach of thefivemother treesfrom each of the two study sites within each of the three classes of hab-itats. The long shoots were counted and the seedling heights were mea-sured in August of 2004. The analyses performed by Eränen et al. (2009)did not include comparisons between habitats considered in our paper;therefore we re-analysed these data to compare long shoot productionby seedlings grown from seeds collected in industrial barren (IB1, IB5),mountain tundra (MT1, MT4) and unpolluted forest (UF7, UF8) (Fig. 2).

2.7. Regrowth after cutting

In this experiment, we cut birches to simulate the dying off of themain trunk (Fig. 3A), which frequently occurs in mountain birches atthe borders of industrial barrens (Kozlov et al., 2009) and studied thetrees' capacity for regrowth in response to this event. At the end of

July 2000 in each of the six study sites (IB2, IB5, MT1, MT2, UF4, andUF6; Fig. 2), we selected 10 mature birches of similar size (only thosewith a single trunk) and measured their height and basal trunk diame-ter. Then, the treeswere cut, leaving stumps3–8 cm in height. In Augustof 2001 (i.e., the year after cutting), we counted the sprouts that hademerged from each stump and measured their lengths. From 2002 to2004, we counted and measured all long shoots formed by these trees.In the final year of the experiment (2004), we also counted the leaveson these trees; a sample of 10 randomly chosen leaves was dried (at+80 °C for 24 h) and weighed. The total weight of the foliage wasthen calculated by multiplying the mean leaf weight by the number ofleaves.

2.8. Responses to the removal of long shoots

The loss of nearly all current-year long shoots due to frost damagewas repeatedly observed inmountain birches persisting in the industri-al barren (Zverev and Kozlov, unpublished data). Based on these obser-vations, we designed an experiment to explore the growth patterns ofmountain birches the year after the partial or complete loss ofcurrent-year long shoots in populations from different habitats. Ineach of the two barren sites (IB1, IB5; Fig. 2) and two sites in open hab-itats located within unpolluted forests (UF3, UF5; Fig. 2), we selectedfive blocks each consisting of three juvenile birches of similar size andcrown shape. Within each block, one birch was randomly assigned tothe cutting of all current-year long shoots, another to the cutting ofthe upper halves (containing half of the axillary buds) of all current-year long shoots, and the third served as the control. The treatmentswere applied in October 2009. Both before the treatment and the fol-lowing autumn, we counted all long shoots on each tree, measuredtheir lengths and recorded the origin of each shoot (i.e., whether ithad developed from either short or long shoot).

2.9. Statistical analysis

To assess how birch crown architecture varies among habitats, weperformed analyses of covariance (ANCOVAs) (SAS Institute, 2009) foreach measured characteristic. The study site nested within a habitat wasincluded as a randomexplanatory variable, and the covariates differed be-tween the experiments: basal area for trees that were monitored from1998 to 2011 as well as for cut trees and branches, and height for seed-lings in the common garden plantations. Although trees used for long-term monitoring were the same throughout the study, we refrainedfrom using repeated measures analysis of variance (ANOVA), becausethe outcomes of this analysis could be affected by increases in tree sizeand age during the observation period, while ANCOVA with thecurrent-year basal area used as the covariate removed these confoundingeffects. A log, square-root or arcsine transformation was used whenevernecessary to meet the assumptions of normality. The climatic variablethat best explained annual variation in shoot production was identifiedby stepwise regression analysis (SAS REG procedure; SAS Institute,2009) fromdata on themonthlymean temperatures andmonthly precip-itation during the 12 months preceding data collection.

The survival of birch trees after cutting and the production of longshoots after long shoot removal were analysed using logistic regressionand the events/trials syntax (procedure LOGISTIC; SAS Institute, 2009).In the first experiment, the trial was the number of cut trees and theevent was the number of trees that survived by the end of the experi-ment. In the second experiment, the trial was the number of cut longshoots and the event was the number of long shoots produced by thesame tree the year after the treatment. Differences between treesfrom polluted and unpolluted habitats in terms of the proportions oflong shoots originating from short and from long shoots were testednon-parametrically by a Kruskal–Wallis test (procedure FREQ; SASInstitute, 2009).

Fig. 3. The growth habit of mountain birch in an industrial barren: the early (A) and late (B) stages of the formation of a typical compact and dense crown.

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3. Results

3.1. Crown architecture

Birches from the industrial barren, mountain tundra and forest dif-fered inmany crown characteristics (Fig. 4). Trees of similar basal diam-eter in forest sites were three times as tall as those in the barren sites;trees from the mountain tundra had heights intermediate betweenthe first two groups (Fig. 4A). Crown shape was slightly flattened intrees from the industrial barren (oblate ellipsoid: depth/width ratiob1),whereas in forest sites, crown depth was nearly three times greaterthan crown width (prolate ellipsoid); birches from mountain tundraexhibited intermediate crown shapes (depth/width ratio close to 2;Fig. 4B). Both the absolute number of long shoots per tree and their pro-portion in the crown (relative to the total number of both short and longshoots) were highest in the barren sites, lowest in forest sites and inter-mediate in tundra sites (Fig. 4C, D), but the mean length of a long shootdid not differ between habitats (F2, 27=0.24, P=0.89). The foliar bio-mass per unit of crown surface area in barren sites and tundra siteswas twice as high as in forest sites (F2, 34=7.07, P=0.0027), i.e., thecrowns of birches from both industrial barren and mountain tundrawere more compact (Fig. 3B) than the crowns of birches from forests.The number of replacements of the leading shoot was highest in barrensites, intermediate in tundra sites and low to negligible in forest sites(Fig. 4E). The sums of the basal areas of dead branches followed a sim-ilar pattern (Fig. 4F).

3.2. Branch structure

The branches ofmaturemountain birch trees that had been collectedfrom barren and forest sites were of similar size in terms of their totallength and the weight of the woody parts as well as the total numberof shoots, the number and weight of leaves (Table 1, Fig. 5A, B) andthe number of leaves on short shoots (F1, 35=0.56, P=0.46). The num-ber and proportion of long shoots, as well as the proportion of leaves

developed on long shoots, were higher in birches from the barren sites(Table 1, Fig. 5C, D); the branching index in these birches was higherthan in birches from forest sites (Table 1, Fig. 5E). The number of buds,adjusted for branch length, was also higher in birches from the industri-al barren (Table 1, Fig. 5F), indicating that in these trees buds werespaced more densely and the shoots had shorter internodes.

3.3. Annual variation in the production of long shoots

We detected considerable variation in the production of long shoots(Fig. 6A) and their total length (Fig. 6B) among study years (Table 2). Al-though both characteristics varied greatly between study sites, the pro-duction of long shoots was generally higher in the industrial barrenthan in forest sites (Table 2, Fig. 6). However, their total lengths didnot differ between habitats because in the barren sites, the long shootstended to be shorter than in the forest sites (Table 2).

A significant interaction between study year and habitat type(Table 2) prompted us to explore the effects of climate on the differencein the production of long shoots between the barren and forest sites.Stepwise regression analysis demonstrated that the ratio between theleast-square mean number of shoots per tree for the barren and forestsites was best explained by mean temperatures in May (r=0.57, n=13 years, P=0.04): in years withwarmerMay temperatures, the differ-ence between the barren and forest sites was greater. This patternresulted from the marginally significant decrease in shoot productionin forest sites with an increase in mean May temperature (r=−0.50,n=13, P=0.08), whereas in the barren sites, long shoot productionwas independent of any explored climatic variable including May tem-perature (r=0.23, n=13, P=0.45).

3.4. Production of long shoots by the progenies of birches from differenthabitats

In the common garden experiment, seedlings reared from the seedsof birches growing in barren sites produced a higher mean number of

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Fig. 4. Characteristics of the crown architecture of mountain birches from different habitats. Values are back-transformed from least-square means (adjusted for tree basal area)based on two sites within each habitat; bars indicate SE. Different letters indicate values that differ at P=0.05 (Duncan test).

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long shoots compared to the progenies of birches from both mountaintundra and forest sites (Fig. 7). The mean length of long shoots did notdepend on seedling origin (F2, 278=0.58, P=0.56).

3.5. Regrowth after cutting

The majority (83.3%) of the mountain birch trees survived aftercutting; mortality did not differ between habitats (Wald χ2=1.60,df=2, P=0.45). The number of sprouts produced by the cut stumpsthe year after cutting was lower in the barren sites compared toboth mountain tundra and forest sites (Fig. 8A). However, in the bar-ren sites, sprouts were longer than in other habitats (Fig. 8B); as a re-sult, the tree-specific sums of the lengths of all sprouts did not differbetween habitats (F2, 42=0.72, P=0.49). The second year after cut-ting, these sprouts in the barren sites produced three times as manylong shoots as in the other habitats (Fig. 8C), but shoot length didnot differ between habitats (F2, 42=2.66, P=0.08); consequently,the total length of long shoots followed the same pattern as the

number of long shoots. The weight of the foliage produced by treesin the fourth year after the treatment (adjusted for basal areas oftrees prior to cutting) was highest in the barren sites and lowest inforest sites (Fig. 8D).

3.6. Responses to the removal of long shoots

Although removal of long shoots did not affect the length of the longshoots produced the year after the treatment (F1, 51=1.51, P=0.30),the long shoots of damaged birches formed more buds per centimetreof their length (F1, 51=4.83, P=0.03). This effect on bud density didnot differ between the barren and forest sites, as indicated by thenon-significant interaction between habitat and treatment (F1, 51=1.93, P=0.17). However, in terms of the production of long shoots,birch responses to damage differed between the barren and forestsites (Waldχ2=6.05, df=2, P=0.05): a significant decrease in thepro-duction of long shoots the year after damage was observed in forestsites, whereas in the barren sites production remained at the

Table 1Sources of variation and significance test results for the branch characteristics ofmountainbirch.

Character Source of variation df a F P

Total length of woody parts Habitat 1 0.33 0.57Site within habitat 2 4.82 0.01Basal area 1 14.65 0.0005

Branching index(total length of woodyparts/branch length)

Habitat 1 10.10 0.003Site within habitat 2 7.61 0.002Basal area 1 4.81 0.04

Number of long shoots Habitat 1 4.12 0.05Site within habitat 2 0.12 0.88Basal area 1 0.76 0.39

Proportion of long shoots Habitat 1 7.09 0.01Site within habitat 2 0.78 0.47Basal area 1 0.01 0.93

Proportion of leavesproduced by long shoots

Habitat 1 7.50 0.01Site within habitat 2 1.36 0.27Basal area 1 0.0 0.95

Weight of woody parts Habitat 1 2.69 0.11Site within habitat 2 2.52 0.10Basal area 1 98.15 b0.0001

Weight of leaves Habitat 1 0.58 0.45Site within habitat 2 0.64 0.53Basal area 1 21.28 b0.0001

Number of buds Habitat 1 3.95 0.05Site within habitat 2 1.93 0.16Total length of woody parts 1 8.71 0.006

Total number of shoots Habitat 1 0.10 0.75Site within habitat 2 7.10 0.003Total length of woody parts 1 8.15 0.007

Number of leaves Habitat 1 0.18 0.67Site within habitat 2 5.87 0.006Basal area 1 10.12 0.003

a Error df=35 for all characters.

218 V. Zverev et al. / Science of the Total Environment 444 (2013) 212–223

pre-treatment level. The control trees demonstrated a striking differ-ence between the two habitats in the origin of long shoots: in forestsites, all long shoots were produced by the axillary buds of previous-year long shoots, and none of them emerged from short shoot buds(Fig. 9), whereas in the barren sites 45% of the long shoots originatedfrom the apical buds of short shoots (χ2=28.0, df=1, Pb0.0001;Fig. 9). In the treatmentwith the partial removal of long shoots, approx-imately 20% of the long shoots grew from the buds of short shoots evenin forest sites, but in the barren sites the proportion of long shoots orig-inating from short shoots increased to 97% (χ2=41.5, df=1, Pb0.0001;Fig. 9). Long shoots produced by the buds of previous-year short andlong shoots were of the same length (F1, 102=3.01, P=0.09), but longshoots originating from short shoots formed more buds (mean±SE:3.85±0.25 and 3.07±0.17 per shoot, respectively; F1, 102=6.03, P=0.02).

4. Discussion

4.1. Growth habit and crown architecture of mountain birches in industrialbarrens

Our results indicated that mountain birches from the industrial bar-ren differ considerably from birches growing in unpolluted habitats notonly in growth habit but also in numerous characteristics of crown ar-chitecture. Birches from the industrial barrenwere low stature, general-ly polycormic trees with curved trunks and compact, nearly sphericalcrowns. In contrast, birches growing in forests were tall, slender, mostlymonocormic trees with straight trunks and a prolate crown shape.These differences in crown characteristicswere associatedwith changesin the growth patterns of shoots and branches. The compactness of thecrown was explained by high branching, which, in turn, resulted fromthe increased production of long shoots, especially in the inner part ofthe crown. The intensive production of long shoots was, in particular,

enabled by the specific ability of birches from the barren habitats to de-velop long shoots from both the axillary buds of previous-year longshoots, as normally occurs in birches, and the apical buds of short shoots.Additionally, the latter shoots produced more buds per centimetre oftheir length and therefore had shorter internodes; this also contributedto the formation of a denser crown.However, thenumbers of shoots andleaves did not differ between similarly sized branches of birches fromthe industrial barren and forest habitats, indicating that some of theformed buds did not develop into shoots. Although the individual leavesof birches from the barrenwere smaller than the leaves of forest birches(Zverev, 2012), the foliar biomass of similarly sized branches did not dif-fer, presumably because of the greater thickness of leaves from the in-dustrial barren (Lukina and Vasilevskaya, 2012).

As can be observed at the borders of the industrial barren, the forma-tion of a shrubby growth habit usually begins with the death of theupper part of the canopy, followed by the death of the main trunk(Fig. 3A) and the production of multiple branches from dormant budsat the base of the trunk. Morphological studies have demonstratedthat the mountain birch is pre-adapted to the rapid formation of ashrubby (polycormic) crown due to the presence of clusters of budsbelow the ground surface at the base of the tree (Vaarama andValanne, 1973). When the tree is damaged, these buds give rise tosprouts that form additional stems. After the death of the leadingshoot, one of the lateral shoots becomes a leader; this replacement pro-cess, when repeated several times, leads to the formation of a curved(twisted) trunk.

The changes in growth habit observed in mountain birches persistingin severely polluted areas are not exceptional forwoody plants. For exam-ple, the death of theupper part of the canopy is typical for coniferous treesaffected by sulphur dioxide or fluorine-containing emissions (Halbwachs,1984). A decrease in vertical growth is often accompanied by changes incrown shape: mature Scots pines, Pinus sylvestris L., in the vicinity of achemical enterprise near Dzerzhinsk, Russia have had nearly sphericalcrowns (depth/width ratio=1.2), in contrast with the prolate crownsexhibited by the same species in unpolluted forests (depth/widthratio=1.8) (Martynjuk, 2008). Under extremely high levels of pollution,in particular in the industrial barren around Monchegorsk, the death ofthe main trunk and the formation of a shrubby growth habit werereported for Scots pine, Norway spruce and goat willow (Doncheva,1978; Alexeyev and Lyanguzova, 1990; Kozlov, 2001; Yarmishko, 2005);increased branching was found in Scots pine, goat willow and S. borealis(Zvereva and Kozlov, 2001; Yarmishko, 2005). The activation of dormantbuds under severe pollution impacts was also detected in Norway spruce,Siberian larch (Larix sibirica Ledeb.) and (to a lesser extent) Scots pine(Alexeyev and Lyanguzova, 1990; Yarmishko, 2005).

The similarity of crown modifications between several woody plantspecies and between differently polluted areas hints that at least part ofthe changes in crown architecture observed in mountain birches grow-ing in the industrial barren is likely to be caused by pollution. However,in terms of some crown characteristics, these birches are similar tomountain birches from unpolluted habitats with harsh environmentalconditions, such as the mountain tree line (Ermakov, 1986) or theshores of the northern islands (Torkhov et al., 2005). Due to the deathof the primary forest, the microclimate of the industrial barrens is simi-lar to themicroclimates of the unpolluted open habitats in strongwinds,a high level of illumination, larger temperature extremes and thin snowcover (Kozlov and Haukioja, 1997; Kozlov, 2001, 2002; Kozlov andZvereva, 2007). Thus, the growth habit and crown architecture ofbirches from industrial barrens are likely to be shaped by the impactsof both pollution per se and pollution-induced environmental changes.The relative importance of these two groups of factors – pollution andmicroclimate – for the formation of the specific crown architecture ob-served in mountain birches persisting in an industrial barren can beevaluated based on the comparison of these birches with birches grow-ing inmountain tundra, i.e., in an unpolluted habitat that is similar to anindustrial barren in terms of its harsh microclimate.

0

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a

Fig. 5. Characteristics of the branch structure of mountain birches from different habitats. Least-square means (adjusted for branch basal area) are based on two sites within eachhabitat; bars indicate SE. Different letters indicate values that differ at P=0.05.

219V. Zverev et al. / Science of the Total Environment 444 (2013) 212–223

4.2. Causes of changes in crown architecture: pollution versusmicroclimate

We demonstrated that birches growing in mountain tundra slightlyabove the upper tree limit differed considerably from birches growingin forest habitats in terms of crown architecture, including allometric re-lationships, the intensity of the production of long shoots and the fre-quency of changes of the leading shoot. This result is in line withnumerous narrative descriptions of the growth habits of mountainbirches in various open environments (Kallio et al., 1983; Ermakov,1986; Vetchinnikova and Bumagina, 2002). More generally, many treespecies were reported to exhibit a shrubby growth habit under the im-pact of unfavourable environmental conditions such as swamping, lowsnowdepth, high soil acidity, strongwinds, winter frost andmany others(Kryuchkov, 1978; Verwijst, 1988; Telewski, 1995). On the other hand,shrubby, highly branched crowns may develop in trees growing innon-stressful open habitats due to the decreased competition for light

(Messier and Puttonen, 1995; Gruntman et al., 2011). Increased lightavailability weakens apical dominance, thus allowing the intensivegrowth of lateral shoots, and also stimulates the development of addi-tional shoots from dormant buds (Aarssen, 1995). These data, alongwith our results, suggest that the steady increase in habitat opennesscaused by pollution-induced forest decline, associated with changes inmicroclimate, is responsible for a large proportion of the changes in thegrowth habit of mountain birch observed in the industrial barren. How-ever, birches from this habitat differed from birches growing in moun-tain tundra in a number of crown characteristics such as height, thefrequency of changes of the leading shoot, the mortality of branchesand shoots and the production of long shoots. These differences hintthat not only pollution-induced environmental changes, but also the di-rect effects of pollution contribute tomodifications of crown architecturein mountain birch. Direct impacts of airborne pollutants, including thosethat accumulate in soils, were the most likely causes of stunted growth

Fig. 6. Annual variation in the production (A) and total length (B) of long shoots. Least-square means (adjusted for tree basal area) are based on six sites within each habitat;bars indicate SE. For statistics, see Table 2.

0

4

8

12

Long

sho

ot n

umbe

r

b

b

a

Industrial barrenMountain tundraForest

Fig. 7. Production of long shoots in 2 year old seedlings reared in unpolluted sites fromthe seeds of birches originating from different habitats. Least-square means (adjustedfor seedling height) are based on two sites of seed origin within each habitat; bars in-dicate SE. Different letters indicate values that differ at P=0.05 (Duncan test).

220 V. Zverev et al. / Science of the Total Environment 444 (2013) 212–223

and high frequencies of shoot and branch die off in polluted habitats; thedeath of the tree top resulted in a shrubby growth habit (Fig. 3B) and fre-quent changes of the leading shoot.

Another aspect of pollution's impact on crown architecture was re-vealed in the common garden experiment. Growing mountain birchseedlings of different origins in unpolluted habitats revealed that the pro-duction of long shoots, which was linked with many characteristics ofcrown architecture, was higher in seedlings originating from the indus-trial barren compared to seedlings originating from both mountain tun-dra and forest habitats. Similarly, the greenhouse experiment revealed

Table 2Sources of variation and significance test results for the number and tree-specific length oflong shoots and in the resulting total length of long shoots in individually marked maturemountain birches growing in six barren sites and six forest sites (data from 1998 to 2011).

Character Source of variation df a F P

Number of long shoots Year 12 2.39 0.006Habitat 1 19.36 b0.0001Site within habitat 7 8.90 b0.0001Year×habitat 12 2.02 0.02Basal area 1 77.14 b0.0001

Mean length of a long shoot Year 12 5.85 b0.0001Habitat 1 3.46 0.06Site within habitat 7 4.83 b0.0001Year×habitat 12 1.07 0.38Basal area 1 0.18 0.67

Total length of long shootsb Year 12 3.85 b0.0001Habitat 1 0.59 0.44Site within habitat 7 6.44 b0.0001Year×habitat 12 1.99 0.05Basal area 1 45.54 b0.0001

a Error df=340 for all characters.b Tree-specific values calculated by multiplying the number of long shoots by the

mean length of a long shoot.

decreased vertical growth of mountain birch seedlings originating fromthe industrial barren relative to seedlings from unpolluted forests,whereas the height of seedlings from mountain tundra did not differfrom the height of seedlings from forests (Eränen, 2008). Moreover,shrubby tundra birches, when transplanted to the botanical garden situ-ated in the forest zone, after several years formed a crown typical ofbirches growing in forests (Andreev, 1951). These results suggest thatin the industrial barren but not in the mountain tundra, mountainbirches have undergone selection for high production of long shoots,during which phenotypes with low production of long shoots havebeen eliminated by the long-term impacts of pollution. Previous studieshave demonstrated that mountain birch populations from polluted hab-itats around the Monchegorsk and Nikel smelters possess resistance topollution (Kozlov, 2005; Eränen, 2008) and that this resistance may beassociated with the decreased uptake of nickel from contaminated soils(Eränen et al., 2009). In this paper we demonstrated for the first timethat selection imposed by long-term and severe pollution impactscould also act upon the characteristics of growth pattern that are respon-sible for the formation of a specific crown architecture. The indepen-dence of long shoot production from annual climatic fluctuations,discovered for birches in an industrial barren, may appear to be aby-product of this selection. We hypothesise that pollution-resistantmountain birches cannot further increase shoot production even in themost favourable climatic conditions, whereas in unpolluted habitats theproduction of long shoots by birches fluctuates with spring tempera-tures. On the other hand, this independence may result from the abilityof birches growing in the industrial barren to produce additional longshoots from short shoot buds, thus compensating for losses in longshoot production caused by unfavourable climatic conditions.

To conclude, some characteristics of the crown architecture ofmountain birches from habitats disturbed by pollution, in particular,stunted vertical growth and increased branching resulting from the in-creased production of long shoots, have developed due to selectionpressure imposed by the impacts of pollution. However,many of the ob-served changes were caused by the direct impacts of both pollution andunfavourable climatic conditions.

4.3. Consequences of changes in crown architecture: adaptive value andcompensatory responses

Our conclusion that mountain birches persisting in an industrial bar-ren have undergone survival selection for specific characteristics ofcrown architecture suggests that these characteristics, in particular theintensive production of long shoots and, consequently, the formation

0

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iage

(g)

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Fig. 8. Regrowth of mountain birches after cutting. (A)— the number of sprouts emerging from the stump the season after cutting; (B)— the mean length of these sprouts; (C)— thenumber of long shoots produced by each sprout in the second year after cutting; (D) — the dry weight of foliage in the fourth year after cutting. Least-square means (adjusted fortree basal area prior to cutting) are based on two sites within each habitat; bars indicate SE. Different letters indicate values that differ at P=0.05 (Duncan test).

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sho

ots

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by

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t sho

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uds

(%)

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Industrial barrenForest

Fig. 9. The proportion of long shoots originating from the apical buds of short shoots incontrol birches and in birches from which the apical halves of all long shoots were re-moved in the previous year. Means are based on two sites within each habitat, bars in-dicate SE. Different letters indicate values that differ at P=0.05.

221V. Zverev et al. / Science of the Total Environment 444 (2013) 212–223

of a higher number of buds, have an adaptive value for survival in a se-verely polluted, harsh and unpredictable environment. Although manyof the ‘excessive’ buds do not normally produce shoots, as indicated bythe similar numbers of shoots on similarly sized branches from the bar-ren and forest sites, they constitute a reserve. These buds can be activat-ed following damage, thus allowing birches to promptly compensate forbiomass losses. The experimental cutting of trees, as well as the remov-al/damage of long shoots, confirmed this prediction, showing that in theindustrial barren, birches compensated for biomass losses much betterthan in unpolluted forests. This ability is extremely important becausetrunk, branch and shoot damage, often leading to the death of the affect-ed parts of the tree, are frequent events in industrial barrens due to toxicpollutants, frost damage, snow abrasion, browsing and/or severe defoli-ation by herbivores.

Although the conditions of industrial barrens are evidently stressfulfor plants due to the direct effects of airborne pollutants, the harsh mi-croclimate (Kozlov and Haukioja, 1997; Kozlov, 2001, 2002) and thelow nutritional value and toxicity of soils (Lukina and Nikonov, 1999),an increased light availability in barrens (relative to unpolluted forests)may considerably enhance the compensatory responses of plants. Forexample, in the experiments by Hjältén et al. (1993), the removal ofthe top 1 cm of the main stem caused a significant increase in birchgrowth in high light conditions but not in the shade. Similarly, in our ex-periment with trunk removal, regrowth was higher in both of the openhabitats (industrial barren and mountain tundra) than in shady forestsites (Fig. 8D). This effect of high light availability is usually explainedby the weakening of apical dominance (Aarssen, 1995), which allowsthe easier activation of lateral meristems and dormant buds.

In our cutting experiment, birches from the industrial barren dem-onstrated higher levels of compensatory growth than birches frommountain tundra, mostly in terms of the production of long shoots.

This result suggests that, besides high light conditions, there existother factors underlying the higher compensatory growth of birches inthe industrial barren. One of these factors may be the ability to producelarger numbers of buds and, consequently, long shoots observed inbirches from the barren sites.

One of the most important results of our study was the discoveryof increased long shoot production in the progenies of birches from

222 V. Zverev et al. / Science of the Total Environment 444 (2013) 212–223

the industrial barren grown in a benign environment, because thisgrowth pattern ultimately determined nearly all of the specific traitsof crown architecture. Importantly, a specific phenotype of silverbirch with smaller leaves and a shrubby crown architecture, i.e., sim-ilar to the phenotype of mountain birch observed in the industrialbarren, is induced by a few genes (Piispanen et al., 2003). The poten-tial heritability of the growth pattern detected in our study hints atthe existence of such genes in mountain birch; we hypothesise thatthe frequency of these genes has considerably increased in mountainbirch populations from industrial barrens due to the increased surviv-al of this small-leaved shrubby phenotype. However, verification ofthis hypothesis requires additional study.

A very important trait of mountain birches from barren sites is theirability to develop long shoots not only from axillary buds but also fromthe apical buds of short shoots. In polluted habitats, a similar patternwas earlier reported for Siberian larch (Alexeyev and Lyanguzova,1990). In unpolluted habitats, this phenomenonwas observed only in re-sponse to severe damage caused by herbivory (Tenow and Bylund, 2000)and to the removal of the apical halves of all of the long shoots in our ex-periment. In contrast to long shoots growing fromaxillary budswhich aretypically situated on the periphery of the crown, long shoots originatingfrom short shoot buds appear in the inner parts of the crown. As the re-sult, these shoots are better protected from unfavourable environmentalfactors such as wind, extreme temperatures, snow abrasion and acid fog.

On the other hand, the development of nearly half of a tree's longshoots in the inner part of the crown resulted in higher leaf density, con-tributing to the formation of a compact and dense crown (Fig. 3B). Thiscrown structure is also adaptive because its nearly spherical shape min-imises the impacts of unfavourable environmental conditions on a tree.Importantly, many tree species are unable to create compact and densecrowns in polluted habitats; the crowns of the Scots pine, Norwayspruce, beech, Fagus sylvatica L., and several other species becameeven sparser under stress (Alexeyev and Lyanguzova, 1990; Innes,1998; Yarmishko, 2005; Martynjuk, 2008). We therefore conclude thatthemountain birch is better adapted to severely polluted environmentsthanmany other woody species, due in particular to its ability to rapidlychange its growth habit and crown architecture. This ability, resultingfrom both phenotypic plasticity and natural selection driven by pollu-tion, allows this species not only to survive in the extreme conditionsof the industrial barrens but also to become a dominant tree species inthese pollution-disturbed habitats.

5. Conclusions

The analyses of similarities and differences in crown architecture be-tween birches growing in different habitats (industrial barren, moun-tain tundra and undisturbed forest) allowed us to conclude that inindustrial barren the specific crown traits have developed in responseto both changes in microclimate caused by pollution-induced forest de-cline, and direct effects of pollution, andmay be partly shaped by the se-lection imposed by long-term pollution impacts. The latter hypothesis isconfirmed by the differences in key parameters of crown structure be-tween the seed progenies (reared in a benign environment) of birchesfrom an industrial barren and undisturbed forest. The development ofthe specific crown architecture in birches from industrial barrens isunderlied by densely spaced buds and increased production of longshoots, which emerge also from the apical buds of short shoots in theinner part of the crown. This growth pattern creates nearly sphericaland compact crowns that minimise the impacts of unfavourable envi-ronmental conditions on birches persisting in industrial barrens. Forma-tion of a larger number of buds assures better compensative abilities ofthese birches in response to mechanical damage. We conclude that thespecific crown architecture of birches from industrial barrens is adaptiveand allows mountain birch not only to survive, but also to become adominant woody species in habitats that are severely disturbed bypollution.

Acknowledgements

We thank E. Melnikov, M. Inozemtseva and A. Vassiliev for the field-work and laboratory assistance, V. Barcan for providing meteorologicaldata, and P. Rautio for the helpful comments to an earlier draft of themanuscript. The study was supported by the Academy of Finland (pro-jects 201991, 211734, 122133 and 124152), the Maj and Tor NesslingFoundation, the Finnish Cultural Foundation and a strategic researchgrant from the University of Turku.

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