Variation in Scots pine needle longevity andnutrient conservation in different habitats andlatitudes

Margus Pensa, Risto Jalkanen, and Valdo Liblik

Abstract: Within-species variation in needle traits is an important characteristic of conifers enabling trees to grow in dif-ferent environments. We compared mean needle age (NA), shoot growth, and nutrient conservation in Scots pine (Pinussylvestris L.) populations in different habitats and latitudes (peatlands and Vaccinium-type stands in Estonia (598N) andLapland (66830’N)). In Vaccinium-type stands, trees with higher NA (mostly in Lapland) had lower shoot length incrementand lower concentration of nitrogen and phosphorus in current-year needles than trees with low NA (mostly in Estonia).However, in peatlands, variation in NA (which was as high as in the Vaccinium-type stands) was weakly or insignificantlyrelated to shoot growth and needle nutrient concentration. Within latitudes, pines with different shoot length incrementsand needle nutrient concentrations tend to have similar NAs. Resorption efficiency and concentration of nitrogen and phos-phorus in senescent needles decreased with the initial concentrations of these nutrients in green needles. Our results dem-onstrate that slow growth and low needle nutrient concentration are not necessarily followed by higher NA and greaternutrient conservation in Scots pine. This is the opposite of the results often obtained in among-species comparisons orwithin species along latitudinal and altitudinal gradients.

Resume : La variation intraspecifique des caracteres des aiguilles est une importante caracteristique des coniferes qui leurpermet de croıtre dans differents environnements. Nous avons compare l’age moyen des aiguilles, la croissance despousses et la conservation des nutriments chez des populations de pin sylvestre (Pinus sylvestris L.) dans differents habi-tats et a differentes latitudes (tourbieres et peuplements a Vaccinium en Estonie (598N) et en Laponie (66830’N)). Dans lespeuplements a Vaccinium, les arbres dont l’age moyen des aiguilles etait plus avance (surtout en Laponie) avaient un plusfaible taux d’elongation des pousses et une plus faible concentration en azote et en phosphore dans les aiguilles de l’anneeque chez les arbres dont l’age moyen des aiguilles etait moins avance (surtout en Estonie). Dans les tourbieres cependant,la variation de l’age moyen des aiguilles (qui etait aussi avance que dans les peuplements a Vaccinium) etait faiblement etnon significativement reliee a la croissance des pousses et a la concentration des nutriments dans les aiguilles. A chaquelatitude, les pins avec differents taux d’elongation des pousses et differentes concentrations des nutriments dans les ai-guilles ont tendance a avoir un age moyen des aiguilles similaire. L’efficacite de resorption et la concentration d’azote etde phosphore dans les aiguilles senescentes ont diminue avec la concentration initiale de ces nutriments dans les aiguillesvivantes. Nos resultats demontrent que la croissance lente et la faible concentration des nutriments dans les aiguilles nesont pas necessairement suivies par un age des aiguilles plus avance et une plus forte conservation des nutriments chez lepin sylvestre. Ceci est contraire aux resultats souvent obtenus dans les comparaisons entre especes ou au sein d’une memeespece le long de gradients latitudinal et altitudinal.

[Traduit par la Redaction]

Introduction

Among a wide spectrum of plant species, it has beenshown that variation in different leaf traits is highly corre-lated, so that there is a trade-off between the persistence offoliage and high photosynthetic assimilation rates (Reich etal. 1992). Thus, plants with short-living leaves have highnutrient concentrations, high growth rates, and low drymass per leaf area, while plants with long-living leaves

have high dry mass per leaf area, low nutrient concentra-tions, and low growth rates (Wright et al. 2004). These in-terrelations of leaf traits may explain the dominance ofplants with long-living leaves in stressful habitats (see Cha-pin 1980; Chabot and Hicks 1982), as slow-growing plantsmay benefit from extended duration of leaves and, thus,from efficient nutrient use under suppressed growth condi-tions (Reich et al. 1997). As regards to within-species varia-tion in leaf traits, it remains controversial whether specieswith high plasticity in their morphological and physiologicalattributes are constrained to the same interrelations betweenleaf traits as has been observed across species. Phenotypicplasticity is an important characteristic of plants, enablingthe adjustment of physiological and structural attributes todifferent combinations of environmental factors, but thequestion of how the reaction norm of one trait is related tothat of another trait needs deeper insight (Nilsen and Orcutt1996).

Received 28 October 2005. Resubmitted 19 October 2006.Accepted 11 January 2007. Published on the NRC ResearchPress Web site at cjfr.nrc.ca on 9 October 2007.

M. Pensa1 and V. Liblik. NE Estonian Department, Institute ofEcology, University of Tallinn, Pargi 15, Johvi 41537, Estonia.R. Jalkanen. Finnish Forest Research Institute, RovaniemiResearch Unit, P.O. Box 16, Rovaniemi FI 96301, Finland.

1Corresponding author (e-mail: margus@ecoviro.johvi.ee).

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A widespread boreal tree species, Scots pine (Pinus syl-vestris L.) grows across an area that extends from the Atlan-tic coast in western Eurasia nearly to the Pacific coast ineastern Eurasia; the southern limit of Scots pine is deter-mined by the aridity of the steppe zone, while the northernlimit extends up to the tundra zone (Richardson 2000).Within the ranges of its distribution, Scots pine grows invery different habitats from dry sand dunes to wet peatlandsand shows high variability in its morphological and physio-logical traits. For example, Pravdin (1964) studied morpho-logical variation of Scots pine across latitudes as well as inan east–west direction and made a distinction between sev-eral intraspecific groups according to needle longevity, nee-dle anatomy and morphology, cone traits, and growth rates.Common garden experiments have shown that variation insome of these characteristics has a genetic background,while variation in other attributes like needle age (NA) isan example of phenotypic plasticity (Oleksyn et al. 1992,1999, 2000; Reich et al. 1996a, 1996b). Natural variabilityin NA of Scots pine, as well as of other pine species, isoften described along climatic gradients (across latitudesand along altitudinal gradients; Ewers and Schmid 1981;Schoettle 1990; Jalkanen et al. 1995). This within-speciesvariability is explained by an increase in environmentalstress, which is accompanied by a decline in photosyntheticand growth rates, since higher leaf age compensates for lowphotosynthesis (Reich et al. 1994; Schoettle and Fahey1994). Thus, it implies that within-species variation in leafage should have the same causes and consequences asamong-species variation described in Reich et al. (1992,1997) and in Wright et al. (2004). As concerns Scots pine,one would expect that populations growing on infertile soilshad higher NA (and lower nutrient concentrations and higherdry mass per needle area) than populations on fertile soils.

In the boreal forest zone, Scots pine is among the few treespecies that grow in nutrient-poor peatlands (ombrotrophicbogs) as well as on nutrient-rich soils where, however, itsgrowth is restricted by competition with other species. Scotspine populations are thus good tools for studying the within-species variation in leaf traits in response to site fertility. Inrecently published literature, only a few studies have directlyaddressed the NA of Scots pine populations growing in peat-lands. Some results show clear differences in NA of Scotspine between peatlands and fertile sites (Niinemets and Luk-janova 2003a, 2003b), while others have reported small dif-ferences (Pensa and Sellin 2002) or that there is nodifference between peatland and fertile sites (Pensa and Sellin2003). In this study, we compared NA, nutrient conservation,and shoot growth of Scots pine populations growing on min-eral soils (in Vaccinium-type stands) and in peatlands at highand mid latitudes. The tested hypotheses were the following:(i) NA of Scots pine is negatively related to shoot growth andis thus greater in habitats where growth is restricted as com-pared with growth-favouring habitats and (ii) NA increaseswith decreasing needle nutrient concentration, which in turnis accompanied by greater nutrient conservation.

Material and methods

Study sites and measurementsWe collected our data during the summer seasons of

2000–2004 in Scots pine stands growing on mineral soils(Vaccinium-type stands sensu Cajander 1926) and in peat-lands (pine bogs characterized by Sphagnum species in theground vegetation layer) in Estonia (598N) and Finnish Lap-land (66830’N). Part of the collected data were used earlierin Pensa and Sellin (2002, 2003) and were reanalysed forthis study. In Vaccinium-type stands, young trees (height1.5–2.5 m, age < 20 years) were growing in plantations, innatural gaps, and at roadsides. All peatland trees (sameheight but age was about 50 years) were natural. It is knownthat the age of Scots pine trees has only a weak (and prob-ably size-related) effect on NA (Pensa et al. 2001). Also,there is evidence that size, and not age per se, is an impor-tant determinant of the developmental stage of trees (e.g.,Mencuccini et al. 2005). Therefore, we considered the simi-larity in heights of the sample trees to be more importantthan the similarity in age.

In total, 28 stands were selected, of which 14 were lo-cated in Estonia and 14 in Lapland (seven stands in peat-lands and seven Vaccinium-type stands). Different standswere sampled in different years, but in each particular stand,all variables were measured in the same year. Each standwas represented by five trees, which were growing withinan approximate area of 100 m2. Since the age of pine nee-dles is affected by light availability (Schoettle and Smith1991; Niinemets et al. 2001), the sample trees were selectedso that all of them were equally exposed to sunlight (therewas not any overstory above the sample trees; the branchesof neighbouring trees were not overlapping). No specialmeasurements of light conditions were carried out in thesampling stands.

Needle age was determined from branches as well as fromstems of the sample trees in all stands. In the middle of thecanopy, two to four branches with no needles on the oldestshoots were selected per sample tree. The survivorship ofneedles on all shoots of a sample branch was determined tothe nearest 10th of needle cohort (i.e., if all needles were at-tached, survivorship was 1, next class was 0.9, and so on; ifno living needles were left on the shoot, then the survivor-ship was 0). The mean survivorship of each needle cohortwas calculated over all branches and stem shoots for eachsample tree. Inclusion of stem shoots ensured that the effectof self-shading was minimized. Mean NA was calculatedfrom the mean survivorships of different needle cohorts

½1� NA ¼Xnc¼1

ðx� xcþ1Þ ðc� 1Þ þ t

12

h i

where xc is mean needle survivorship in cohort c, xc+1 ismean needle survivorship in the next (i.e., 1 year older) nee-dle cohort, and t is the number of months between initiationof new needles and yellowing of the oldest needles (taken as3 months for both Estonia and Lapland). Equation 1 wasadopted from Aalto and Jalkanen (1998) and it is analogousto methods used to estimate the mean life expectancy in po-pulation ecology (e.g., Krebs 1985).

In 10 of 14 stands at both latitudes (five peatlands andfive Vaccinium-type stands), growth rates were characterizedby measuring shoot length increment (length of branchshoots, mm�year–1) on sample branches (the same brancheson which NA was assessed). On each sample branch, the

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length of three to six shoots was measured and a mean shootlength increment was calculated across all sample branchesfor each sample tree.

In 2004, nutrient concentration ([N] and [P]) was deter-mined in different needle cohorts as well as in senescentneedles in 4 of 14 stands at both latitudes (two peatlandstands and two Vaccinium-type stands). In those eightstands, growth rates were characterized only by height incre-ment (length of stem shoots), which was omitted from thisstudy. Because there were too few needles in the samplebranches used for assessments of NA (especially in peat-lands), nutrient concentration was analysed in needles thatwere collected over whole canopies of the sample trees (thesame trees on which NA was assessed). Green needles werecollected over all needle cohorts in August after the end ofshoot elongation and senescent (yellowing) needles from theoldest cohorts in September. In Lapland, senescent needleswere sampled at the beginning of September and in Estoniaat the end of the month. This time lag corresponds to thephenological difference between the two regions. Needleswere kept between 0 and +5 8C after collecting, and nutrientconcentration was assessed as a percentage of dry mass(oven-dried needles, 48 h, 60 8C) in the Laboratory of PlantBiochemistry, Estonian Agricultural University, Tartu, Esto-nia. For nitrogen analyses, the samples were digested by theKjeldahl method and distilled using a Kjeltec 1030 autoana-lyzer (Foss Analytical AB, Sweden). Analysis of phosphoruswas done using the flow injector analysis technique (FIAstar5000, Foss Analytical AB, Sweden). Nutrient conservationwas characterized by measured nutrient resorption efficiency(RE), which was calculated as the difference in nutrient con-centrations between senescent needles and green needles(averaged over all needle cohorts) and expressed as a per-centage. It has been claimed that concentration-based RE val-ues are underestimated because they do not account for leafmass loss during senescence (Van Heerwaarden et al. 2003).However, since we focus on relationships between variables,and not on real values of RE, the usage of concentration-based RE is justified as an index of nutrient conservation(also see Oleksyn et al. 2003).

Data analysisSimple linear regression methods were used to test the re-

lationships between measured variables (NA, shoot lengthincrement, nutrient concentrations, and RE). An analysis ofcovariance (ANCOVA) was used to study whether those re-lationships would differ between latitudes (Estonia versusLapland) or habitats (Vaccinium-type stands versus peat-lands). If the ANCOVA shows that there is a significant in-teraction between grouping variable and covariate, then thegroup with a larger slope has a greater change in the depend-ent variable per unit of change in the covariate, but the meanlevel of the dependent variable cannot be compared amonggroups. If the slope does not differ but the intercept does,then the mean level of dependent variable differs amonggroups, and the difference is constant at any value of covari-ate. Finally, if the covariate is insignificant, the ANCOVAcan still indicate a significant effect of grouping variableson the dependent variable (Quinn and Keough 2002).

All measured variables were tested for homogeneity ofvariances (Levene test) and normality (Kolmogorov–Smirnov

test). Latitude and habitat, as grouping variables, were in-cluded separately into the ANCOVA model. Thus, in thecase of latitude, the model indicated whether within-latitudevariation in the dependent variable was related to the cova-riate and whether this relationship differed between lati-tudes. If habitat was included in the model, within-habitatvariation in the dependent variable was related to the cova-riate at separate levels of habitat. All tests were done at asignificance level of a = 0.05. Computations were carriedout with Systat 11 (SYSTAT Software, Inc., Richmond,California).

ResultsMean NA was related to shoot length increment within

habitats but not within latitudes. However, the relationshipbetween NA and shoot length increment was different be-tween habitat types (a significant habitat by shoot length in-crement interaction term in ANCOVA, F[1,96] = 7.1, P =0.009). While a threefold increase in NA was related to afivefold decrease in shoot lengths in Vaccinium-type stands,the relationship was insignificant in peatlands (Fig. 1). InVaccinium-type stands, the relationship between NA andshoot length increment was caused by the latitudinal varia-tion of both variables (NA was higher, but the shoot lengthincrement was lower in Lapland than in Estonia). In peat-lands, however, trees from both latitudes tended to havesimilar shoot length increments, although NA was different(P < 0.001; Fig. 1).

[N] and [P] in current-year needles decreased with in-creasing NA, but this relationship was weaker in peatlandsthan in Vaccinium-type stands (a significant habitat by NAinteraction in ANCOVA, F[1,35] = 6.19, P = 0.02 for [N]and F[1,36] = 9.08, P = 0.005 for [P]). At a common NA,peatland trees tended to have lower [N] and [P] in current-year needles than the trees sampled in Vaccinium-typestands, but that difference was smaller in Lapland whencompared with Estonia (Fig. 2).

Changes in the REs of nitrogen and phosphorus were notrelated to NA. Rather, the RE of these nutrients increasedwith current-year needle [N] and [P]. This relationship was,nevertheless, significant only at lower [N] and [P] in peat-lands (habitat by [N] interaction, F[1,35] = 4.46, P = 0.04and habitat by [P] interaction, F[1,36] = 42.50, P < 0.001),

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Fig. 1. Relationship between mean needle age and shoot length in-crement in Scots pine (Pinus sylvestris L.) trees in Vaccinium-typestands (R2 = 0.49, P < 0.001, n = 50) and in peatlands (R2 = 0.003,P = 0.3, n = 50). The data were fitted by linear regression (brokenline denotes an insignificant regression); ANCOVA indicated a sig-nificant habitat by shoot length increment interaction (P = 0.009).

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while the slope of the relationship was flat and insignificantat higher [N] and [P] in Vaccinium-type stands (Fig. 3).

Nutrient concentration in senescent needles was morestrongly related to current-year needle [N] and [P] than toRE (Fig. 4). At the same current-year needle [N], peatlandtrees had a higher [N] in senescent needles than the trees inVaccinium-type stands (ANCOVA effect of habitat, F[1,36] =9.5, P = 0.004). In the case of phosphorus, ANCOVAshowed an interaction of current-year needle [P] with habitat(F[1,36] = 5.43, P = 0.03), indicating that the relationship be-tween [P] in current-year needles and that in senescent nee-dles was significant only in Vaccinium-type stands (Fig. 4b).Senescent needle [P] of peatland trees remained close tozero (approximately 0.002%) regardless of the 10-fold in-crease in current-year needle [P].

DiscussionVariation in leaf traits is an important characteristic of

ecological processes that are driving forces for biogeochem-ical cycles in ecosystems (Reich et al. 1992; Wright et al.2004). Studies of leaf traits allow us to gain importantknowledge about the activity of these processes and predictecosystem responses to changing environment. Our researchhas demonstrated that the mean age of Scots pine needles ishigher in pine-dominated boreal forests at the polar circlethan in hemiboreal forests growing 78 southward. This lati-tudinal variation in Scots pine NA agrees with the idea thatgreater leaf age is required to offset higher initial leaf con-structing costs, lower net assimilation rate, and lower carbongain in conditions of restricted growth at higher latitudes

and altitudes (Reich et al. 1994). This idea is supported byobservations that increase in NA of different pine specieswith latitude and altitude is inversely related to annual shootincrement (Schoettle 1990; Schoettle and Smith 1991).However, according to our results, the mean age of Scotspine needles may vary across latitudes without remarkablechanges in shoot length increment (e.g., in peatlands) and,on the other hand, shoot length increment may differ amongtrees within latitude despite similar NAs (e.g., Vaccinium-type stands versus peatlands) (Fig. 1). Thus, we may con-clude that although shoot-level NA and shoot growth areoften correlated in Scots pine (e.g., Pensa and Sellin 2002;Niinemets and Lukjanova 2003b; Pensa and Jalkanen 2005),restricted growth is not necessarily linked to increased ageof Scots pine needles.

The cost–benefit models of leaf age indicate that produc-tion of new leaves is associated with the loss of older leaves(Kikuzawa 1995; Kikuzawa and Ackerly 1999). This bal-ance between leaf production and loss, found also in Scotspine (e.g., Pensa et al. 2001), makes shoot-level leaf ageequal to the number of existing leaves on the shoot dividedby the birth rate of new leaves (Ackerly 1999; Westoby etal. 2002). Thus, the difference in mean NA observed amonglatitudes indicates that the leaf birth rate must be lower and(or) the number of existing needles per shoot axis must behigher in Lapland than in Estonia. As previous studies haveshown, Scots pine does have a low leaf birth rate at higherlatitudes, while the number of needles per shoot axis is ap-

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Fig. 2. Mean needle age in relation to the nutrient concentration incurrent-year needles of Scots pine trees in Vaccinium-type standsand in peatlands. (a) Nitrogen (R2 = 0.36, P = 0.004, n = 19 forVaccinium-type stands and R2 = 0.22, P = 0.02, n = 20 for peatlands);(b) phosphorus (R2 = 0.21, P = 0.03, n = 20 for Vaccinium-typestands and R2 = 0.02, P = 0.3, n = 20 for peatlands). The data werefitted by linear regression (broken line denotes an insignificant re-gression); ANCOVA indicated a significant habitat by nutrient con-centration interaction (P = 0.02 in Fig. 2a and P = 0.005 in Fig. 2b).

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Fig. 3. Resorption efficiency (RE) of nutrients in relation to current-year needle nutrient concentration in Scots pine trees in Vaccinium-type stands and in peatlands. (a) Nitrogen (R2 = 0, P = 0.6, n = 19 forVaccinium-type stands and R2 = 0.29, P = 0.009, n = 20 for peat-lands); (b) phosphorus (R2 = 0, P = 0.4, n = 20 for Vaccinium-typestands and R2 = 0.58, P < 0.001, n = 20 for peatlands). The data werefitted by linear regression (broken lines denote an insignificant re-gression); ANCOVA demonstrated that habitat interacted signifi-cantly with nutrient concentration (P = 0.04 in Fig. 3a and P < 0.001in Fig. 3b).

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proximately the same across latitudes (Pensa and Jalkanen2005; Pensa et al. 2006). In peatlands, where leaf birth rateis also low (as shoot length indicates), trees apparently havea lower number of existing needles on the shoot than thetrees in Vaccinium-type stands; otherwise, the mean NAcould not be similar in these contrasting habitats.

The increase in mean age of Scots pine needles with de-creasing [N] in current-year needles agrees with the resultsof interspecific comparisons (Reich et al. 1992, 1997;Wright et al. 2004) as well as with the observations madeon Scots pine by Oleksyn et al. (2003). This may lead tothe conclusion that latitudinal variation in NA of conifers iscaused by limited nutrient availability, as cold climate vege-tation is often considered to be nitrogen limited (Oleksyn etal. 2003; Wright et al. 2004). However, similar to shootgrowth related variation in mean NA, the comparison ofpeatland trees with the trees growing in Vaccinium-typestands shows that lower nutrient concentration does not nec-essarily cause an increase in the mean age of Scots pine nee-dles (Fig. 2).

In comparison with current-year needles, lower variabilityof nitrogen and phosphorus in senescent needles indicatesthat trees tend to have similar concentrations of these nu-trients in senescent needles. This agrees with Killingbeck’s(1996) statement that plants that minimize the concentrationof limiting nutrients in senescent tissues are favoured by nat-ural selection. Consequently, to achieve that minimum con-centration, trees with higher [N] and [P] need to also havehigher RE, which results in a positive relationship between

current-year needle [N], [P], and RE. However, since REcannot increase infinitely, trees with very high [N] and [P]in current-year needles also have a higher concentration ofthese nutrients in senescent needles. Thus, the trees thathave lower nutrient concentration in current-year needlesalso have higher leaf-level nutrient use efficiency (a recipro-cal of nutrient concentration in senescent needles; Vitousek1982; Aerts and Chapin 2000).

In conclusion, our results indicate that while latitudinalvariation in Scots pine NA is related to shoot growth andgreen needle [N], no such relationships exist within latitude,although shoot length increment and [N] vary by the samedegree within latitudes as between latitudes. Since leaf ageis a ratio of leaf number and leaf birth rate (Ackerly 1999),we propose that Scots pine produces fewer new needles perexisting needles at higher latitudes than at lower latitudes(Pensa and Jalkanen 2005). In peatlands, where leaf birthrate is also low, the trees have apparently fewer needles onshoots than in Vaccinium-type stands, and the ratio of leafnumber to leaf birth rate is, thus, similar in these contrastinghabitats. Regardless of initial [N] and [P] in green needles,Scots pine tends to have similar concentrations of these nu-trients in senescent needles. Because of that, trees with lownutrient concentration in green needles have lower RE thantrees with high nutrient concentration.

AcknowledgmentsIlmart Part is acknowledged for improving the language

of the manuscript. Dr. Ulo Niinemets made valuable com-ments on an earlier version of the manuscript. The researchwas, in part, supported by the EC Environment and ClimateResearch Programme (contract EVK-CT-2002-00136 (PINE)and contract 017008 (GOCE) (Millennium)) and by the Es-tonian Science Foundation (grants 5583 and 6677).

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Chabot, B.F., and Hicks, D.J. 1982. The ecology of leaf life spans.Annu. Rev. Ecol. Syst. 13: 229–259. doi:10.1146/annurev.es.13.110182.001305.

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(a)

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Fig. 4. Nutrient concentration in senescent needles in relation tocurrent-year needle nutrient concentration in Scots pine trees inVaccinium-type stands and in peatlands. (a) Nitrogen (R2 = 0.38,P = 0.003, n = 19 for Vaccinium-type stands and R2 = 0.56, P <0.001, n = 20 for peatlands); (b) phosphorus (R2 = 0.44, P = 0.001,n = 20 for Vaccinium-type stands and R2 = 0, n = 20 for peatlands).The data were fitted by linear regression; ANCOVA demonstratedthat habitat interacted significantly with nutrient concentration (P =0.004 in Fig. 4a and P = 0.03 in Fig. 4b).

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