Available online at www.sciencedirect.com

Biomass and Bioenergy 27 (2004) 9–19

Growth and production of a short rotation coppice culture ofpoplar I. Clonal di"erences in leaf characteristics in relation

to biomass productionA. Pellis∗, I. Laureysens, R. Ceulemans

Department of Biology, University of Antwerp (UA), Universiteitsplein 1, B-2610 Wilrijk, Belgium

Abstract

Seventeen di"erent poplar (Populus) clones were studied during the +rst growing season of the second rotation of ahigh-density coppice culture. In August 2001, total leaf area (tLA), number of leaves and speci+c leaf area (SLA) weredetermined for 15 shoots per clone. Above-ground woody biomass production and leaf area index (LAI) were estimatedby using allometric relationships and an up-scaling approach. Signi+cant clonal variation was observed in LAI, biomassproduction, tLA and number of leaves per basal shoot area. Biomass production ranged from 3 to 8 Mg ha−1 y−1 and LAIranged from 2 to 6 m2 m−2. The LAI, tLA per shoot, and SLA were the most important determinants of above-groundwoody biomass production. The production of many small leaves was shown to give a similar biomass production as theproduction of few but large leaves.? 2003 Elsevier Ltd. All rights reserved.

Keywords: Populus spp.; Speci+c leaf area; Leaf weight ratio

1. Introduction

In short rotation forestry (SRF) fast growing hard-woods of good coppicing ability are used in carefullytended plantations to produce woody biomass [1,2].SRF systems, particularly coppice systems, are of in-terest for three principal reasons: as an alternativeuse for the land taken out of agricultural production[3]; as a feedstock for energy and industry [1]; andas a means to sequester carbon dioxide [4]. Further-more, they have a positive impact on biodiversity, nu-trient capture and carbon circulation in the soil-plant

∗ Corresponding author. Tel.: +32-3-820-22-72; fax: +32-3-820-22-71.

E-mail address: an.pellis@ua.ac.be (A. Pellis).

atmosphere system, especially on former agriculturalland, and they protect the soil from water and winderosion [5–7]. Management objectives are aimed atobtaining a maximum output (i.e. woody biomass)with a minimum input (i.e. fertilization, site prepa-ration, etc.) [2,8]. Major improvements in productiv-ity among economically important species have beenachieved through breeding, genetic selection and de-velopment of more e@cient management techniques[9].

Poplar (Populus) species and their hybrids are inthe forefront of SRF trees because of their vigoroussprouting after cutting, their ease of propagation andtheir suitability for a variety of wood +ber products[10,11]. Final biomass yields that can be achievedby poplar under optimal conditions (favourable

0961-9534/$ - see front matter ? 2003 Elsevier Ltd. All rights reserved.doi:10.1016/j.biombioe.2003.11.001

10 A. Pellis et al. / Biomass and Bioenergy 27 (2004) 9–19

climate, irrigation, fertilization) are in the order of20–25 Mg ha−1 y−1 [12–14]. Under normal +eldconditions, annual yields of 10–15 Mg ha−1 y−1 aremore realistic [1,15].

The expansion of their photosynthetic surface area,i.e. leaf area, a"ects the growth and productivity oftrees, whether in agricultural or natural settings [16].Signi+cant clonal and species di"erences in variousleaf characteristics have already been reported, suchas in size and number of leaves [16], leaf area [17,18],leaf form and leaf production rate [19]. The timingof bud burst in spring, the pattern of cell formationand expansion in the growing leaves, the rate of leafexpansion, and the duration and e@ciency of photo-synthetic activity throughout the growing season alla"ect the amount of carbon that can be +xed, and ul-timately the size of a tree [16]. Rapid development ofleaf area and canopy closure are essential for the suc-cessful establishment and growth of SRF poplar plan-tations [20]. Rapid juvenile growth of selected poplarspecies can achieve the most e@cient use of land, bycombining close plant spacing, coppicing, and shortrotation cycles. The net result of these cultural man-agement practices is a rapid development of a largeleaf surface, and consequently an increased biomassproductivity [21].

The most commonly used parameter to express leafarea in stands is the leaf area index (LAI), which ex-presses total leaf area (tLA) of a plant canopy per unitland area it covers [22]. Leaf area duration, the inte-gral of LAI over the growing season, is another im-portant factor in crop growth [22]. High LAIs must becarried throughout the period when the environmentis favourable for tree growth. Leaf area duration inpoplar can be signi+cantly inEuenced by foliage dis-eases, particularly Melampsora rust, which can causeheavy defoliation [22–24]. Also water and nutrientlevels a"ect leaf production. Any restriction in watersupply reduces leaf area [25], and nitrogen fertilizationa"ects both the number of leaves and their size [26].

Because of the strong relationship between thequantity of radiation absorbed by the foliage and thebiomass production of SRF, the objectives of thepresent paper were:

(1) to examine clonal di"erences in leaf character-istics and leaf morphology for di"erent poplarspecies;

(2) to establish useful allometric relationships topredict above-ground woody biomass productionand LAI;

(3) to relate leaf characteristics and leaf morphologyto above-ground woody biomass production.

2. Materials and methods

2.1. Plant material and plantation layout

Seventeen di"erent poplar (Populus) clones, be-longing to six di"erent parentages, i.e. P. nigra L.(N) clone Wolterson; P. trichocarpa T. & G. (T)clones Columbia River, Fritzi Pauley and Trichobel;P. trichocarpa × P. deltoides Marsh. (T×D) clonesBeauprJe, Boelare, Hazendans, Hoogvorst, Raspaljeand Unal; P. deltoides × P. trichocarpa (D × T)clones IBW1, IBW2 and IBW3; P. deltoides × P.nigra (D × N) clones Gaver, Gibecq and Primo; andP. trichocarpa × P. balsamifera L. (T × B) cloneBalsam Spire were examined at an existing short ro-tation coppice plantation in Boom (51◦05′N; 4◦22′E;5 m above sea level) in the province of Antwerp(Belgium). The plantation is situated on an old wastedisposal site, covered with a 2 m thick layer of sand,clay and mixed rubble. The soil is characterized bya high bulk density, a heavy clay-loam texture, highCa-levels and a high pH. Bulk density ranges between1.22 and 1:62 g cm−3, pH ranges between 7.3 and8.1. The upper soil horizons contain between 0.8%and 1.8% organic matter. The nutrient and mineralreserves are extremely high in comparison with forestsoils, but moderate in comparison with agriculturalsoils.

In 1996, more than 6000, 25 cm long unrooted hard-wood cuttings were planted in a randomized mono-clonal block design with three replicate plots per clone(except for clone Hoogvorst with six replicate plotsand clones Raspalje and IBW1 with only two replicateplots). Within the rows, the plant distance was 0:9 mwith alternating inter-row distances of 0.75 and 1:5 m,resulting in a total plant density of 10,000 trees perha. Each monoclonal plot had a double border row,leaving 36 assessment trees in the centre of each plot[27]. For a more detailed description of the plantationand the clonal material the reader is referred to Lau-reysens et al. [28] and Casella and Ceulemans [29].

A. Pellis et al. / Biomass and Bioenergy 27 (2004) 9–19 11

2.2. Plantation management regime

To ensure good establishment, irrigation was ap-plied at the onset of the +rst growing season. No fer-tilization or irrigation was applied for the duration ofthe trial. Both mechanical and chemical weed controltechniques were applied. Mechanical weeding with atrimmer was done frequently during the +rst and thesecond growing season. On three occasions, in June1996, June 1997 and May 2001, herbicides (a mix-ture of glyphosate at 3:2 kg ha−1 and oxadiazon at9:0 kg ha−1) were applied because mechanical controlalone was ine"ective. These herbicides were appliedusing a spraying device with a hood-covered nozzleto minimize impact on the trees. The cuttings that didnot establish in 1996 were replaced in the spring of1997 with new 25 cm long hardwood cuttings (40 cmfor the clones with a mortality rate higher than 10%).These ‘beatings’ were included in the biomass produc-tion estimates. At the end of the +rst growing season(1996), all trees were cut back to a height of 5 cmto create a coppice system with an average numberof two to ten shoots per stool. In the present study,a shoot was de+ned as the composition of the stemwith its branches and leaves. And, a stool was com-posed of a stump with its shoots. In January 2001, theplantation was cut back again at a height of 5 cm. Allthe measurements in this study were made in 2001 on1-year-old shoots on 6-year-old roots.

2.3. Destructive measurements

In August and September 2001, the thinnest, thethickest and three random shoots per replicate plotwere harvested. The harvested shoots originated fromthe inner row of the double border row. The selectedshoots were cut at 5 cm above soil level. Before theshoots were cut, height and shoot diameter at 22 cmabove soil level were measured [30]. The diameterswere measured to the nearest 0:01 cm, with a digitalcalliper (Mitutoyo, type CD-15DC, UK). All leavesof each shoot were removed and brought to the labora-tory for analysis. Individual leaf area, leaf length andleaf width were measured for all leaves with a laserarea meter (CID Inc. type CI-203, USA). Dry mass ofstems (i.e. shoots without leaves), and of 20 randomlychosen leaves per shoot were determined after dryingthe leaves at 60◦C, and the stems at 75◦C in a forced

air oven for four days until constant dry mass wasreached. For each clone, an allometric power equationwas calculated: between individual leaf area and indi-vidual leaf dry mass (n = 20 leaves), between shootdiameter and tLA per shoot (n = 5 shoots), betweenshoot diameter and total leaf dry mass (n= 5 shoots),and between shoot diameter and stem dry mass (n= 5shoots).

For most clones, the data from all replicate plotswere pooled to calculate the allometric power equa-tions. However, for clones Gibecq and ColumbiaRiver, the allometric relation was calculated for eachreplicate plot separately, because of a low determi-nation coe@cient of the combined allometric rela-tion when all replicates were pooled. LAI could notbe calculated for clone Hazendans, because of thenon-signi+cant allometric power equation betweenshoot diameter and tLA per shoot (n = 5 shoots). Atthe end of the growing season, the diameters of allshoots of the 36 assessment trees were measured at22 cm [28].

2.4. Leaf characteristics and derived ratio’s

Using the allometric relationships of tLA, the in-dividual stem dry mass and an inventory of all shootdiameters (of the 36 assessment trees), both LAI andabove-ground woody biomass production were deter-mined. The allometric relation between shoot diameterand tLA per shoot was used to estimate the tLA (at theend of August) of each replicate plot. LAI was calcu-lated as the tLA of the 36 assessment trees of the repli-cate plot per unit ground area (36 m2) of the replicateplot. Biomass production was scaled-up to dry massper ha and per year, using the measured shoot diame-ters of the 36 assessment trees and the allometric rela-tion between shoot diameter and shoot dry mass. Leafarea ratio (LAR) was calculated as tLA divided bythe individual shoot dry mass, while speci+c leaf area(SLA) was calculated as individual leaf area dividedby individual leaf dry mass. Leaf weight ratio (LWR)was calculated as total leaf dry mass (per shoot) di-vided by shoot dry mass. Note that root biomass wasnot included in the calculations of LAR and LWR.Number of leaves per shoot basal area (NBA) wascalculated by dividing the number of leaves per shootby the basal area of the shoot. The di"erent ratio’s de-rived from leaf area and dry mass measurements are

12 A. Pellis et al. / Biomass and Bioenergy 27 (2004) 9–19

Table 1De+nitions and units of di"erent ratio’s calculated in this study

Ratio De+nition Units

Leaf area ratio (LAR) Total leaf area (per shoot) cm2 g−1

per unit shoot dry massLeaf weight ratio (LWR) Total leaf dry mass (per shoot) as a %

proportion of shoot dry massSpeci+c leaf area (SLA) Individual leaf area per individual leaf dry mass cm2 g−1

Number of leaves per shoot Number of leaves per unit shoot basal area cm−2

basal area (NBA)

summarized in Table 1. The variation of individualleaf size within a shoot was expressed as a coe@cientof variation (CV) (leaf area variation). All leaf char-acteristics and derived ratio’s were calculated as meanvalues of three replicate plots (=15 shoots) per clone.

2.5. Nitrogen analyses

Ten mature leaves from the upper portion of thecanopy were randomly per replicate plot collected fornitrogen (N) analysis. Following drying, samples wereground to a +ne powder and analysed for N by a dy-namic Flush Combustion Method with the NC 2100Soil Autoanalyser (Carlo Erba, Italy). Each samplewas analysed twice; the detection limit of the instru-ment was 0.01%. Nitrogen concentrations were cal-culated on a mass basis and were expressed as a per-centage of dry mass.

2.6. Statistical analysis

Di"erences in leaf characteristics among cloneswere tested, using analysis of variance (ANOVA).The analysis was performed with the SAS statisticalsoftware package (SA System 6.12, SAS instituteInc., Cary, NC) using the mixed procedure [31]. Arandomized complete block design was applied, withclone as a +xed factor and replicate as a random fac-tor. Least squares means were pairwise compared forclones/parentages, and were considered signi+cantwhen the P-value of the ANOVA t-test was ¡ 0:05.The normal distribution of the data was veri+ed withthe Shaphiro-Wilk statistic (proc univariate in SAS).The signi+cance of the interaction clone × plot wastested with the likelihood ratio test. With StatMost

2.50 (DataMost Corporation, Salt Lake City, USA),the correlations among leaf characteristics and nitro-gen content of the leaves were tested with a Pearsonrank correlation test. Correlations were consideredsigni+cant from the P¡ 0:05 level on.

3. Results

3.1. Leaf level

Leaf length, leaf width and leaf area reEected thediverse leaf morphologies (i.e. lanceolate, round, ob-long, deltoid or heart-shaped) among clones belong-ing to di"erent parentages (Fig. 1). Leaves could belonger than wide, wider than long or equal in bothdimensions. Mean leaf length ranged between 7 cmfor clone Wolterson and 16 cm for clone Hazendans;mean leaf width ranged from 7 cm for clones Wolter-son and Fritzi Pauley, to 13 cm for clone Hazendans.The leaf area of Wolterson was the smallest of anyclone and signi+cantly smaller than the leaf area ofother clones. Clones Hazendans and Hoogvorst hadthe highest mean individual leaf area, i.e. averaging176 and 174 cm2, respectively, which was signi+-cantly higher than the mean individual leaf area of allother clones (Fig. 2). Leaf dimensions di"ered sig-ni+cantly among the di"erent parentage groups. TheT×D parentage group had signi+cantly larger leavesthan all other parentage groups, resulting from a sig-ni+cantly higher leaf length, leaf width and leaf area.A low CV, ranging from 4% for the D × T parentagegroup to 27% for the T×D parentage group, indicatedthe limited variation of individual leaf area amongclones within the same parentage groups (data not

A. Pellis et al. / Biomass and Bioenergy 27 (2004) 9–19 13

Fig. 1. Photographs of individual leaves of six Populus clonesused in this study (Wolterson, Fritzi Pauley, Raspalje, IBW1,Gaver, Balsam Spire) belonging to di"erent parentage groups. N:P. nigra, T: P. trichocarpa, D: P. deltoides, B: P. balsamifera.

Fig. 2. Mean individual leaf area (cm2) of all leaves of 17 di"erentpoplar clones in the +rst growing season of the second coppicerotation. Mean values of three replicates and their standard errorbars are presented. BA: Balsam Spire, BE: BeauprJe, BO: Boelare,HA: Hazendans, HO: Hoogvorst, RA: Raspalje, UN: Unal, CO:Columbia River, FR: Fritzi Pauley, TR: Trichobel, GA: Gaver,GI: Gibecq, PR: Primo, I1: IBW1, I2: IBW2, I3: IBW3, WO:Wolterson. N: P. nigra, T: P. trichocarpa, D: P. deltoides, B: P.balsamifera.

shown). The variation of individual leaf area withina shoot, expressed as a CV, ranged between 37%for clone IBW3 and 86% for clone Columbia River(Table 2).

SLA was not signi+cantly di"erent among clones,and ranged between 160 and 211 cm2 g−1 (Table 2).SLA was signi+cantly correlated with the nitrogencontent of the leaves (r = 0:372). Nitrogen contentwas similar for all clones, averaging 3%.

3.2. Shoot level

tLA per shoot di"ered signi+cantly among clones,ranging from 3324 cm2 for clone Balsam Spire to6589 cm2 for clone Hazendans (Fig. 3). The tLA wassigni+cantly correlated with the mean individual LA(r=0:391) and with the number of leaves (r=0:490).The NBA di"ered signi+cantly among clones, rang-ing from 15 cm−2 for clone Hoogvorst to 65 cm−2

for clone Wolterson (Fig. 3). This means that theclone with the smallest leaves (clone Wolterson) hadfour times as many leaves per unit basal area thanthe clone with the largest leaves (i.e. Hoogvorst).Individual LA and NBA were negatively correlated(r=−0:749). Furthermore, NBA was negatively cor-related with SLA (r = −0:306) (Table 3).

LAR was not signi+cantly di"erent among clones,and ranged from 47 cm2 g−1 for clone Balsam Spireto 84 cm2 g−1 for clone IBW1. LWR was also notsigni+cantly di"erent among clones, ranging between31% for clone Balsam Spire and 44% for clone IBW2(Table 2). LAR was signi+cantly correlated with LWR(r= 0:686) and with SLA (r= 0:273); LWR was sig-ni+cantly correlated with tLA (r=−0:358), with SLA(r = −0:341), and with LAI (r = −0:556) (Table 3).

3.3. Allometric relationships

Allometric relationships were established betweenshoot diameter (mm) and stem dry mass (g), and be-tween shoot diameter (mm) and shoot tLA (m2) toobtain woody biomass production and LAI, respec-tively (Fig. 4). For both allometric relationships andfor nearly all clones, the power function (y = axb)yielded the best +t regarding correlation coe@cients(r). Correlation coe@cients (r) of the allometric re-lationship between shoot diameter and stem dry massranged between 0.869 (n= 15) and 0.999 (n= 10) forFritzi Pauley and Hazendans, respectively. Correlationcoe@cients (r) of the allometric relationship betweenshoot diameter and shoot tLA ranged between 0.613(n = 10) and 0.980 (n = 15) for IBW2 and Primo,

14 A. Pellis et al. / Biomass and Bioenergy 27 (2004) 9–19

Table 2Speci+c leaf area (SLA), leaf area ratio (LAR), leaf weight ratio (LWR) and leaf area variation within a shoot in the +rst year aftercoppicing (2001) of 17 poplar clones in a short rotation coppice culture established in April 1996

Parentage Clone SLA LAR LWR Leaf area variation(cm2 g−1) (cm2 g−1) (%) CV (%)

T × B Balsam Spire 173 (7.6) 47 (2.0) 31 (1.2) 58

T × D BeauprJe 169 (12.9) 65 (8.1) 42 (4.1) 80Boelare 197 (8.7) 74 (1.1) 41 (4.0) 62Hazendans 181 (12.0) 67 (1.1) 40 (1.4) 47Hoogvorst 209 (7.4) 57 (1.8) 32 (1.0) 58Raspalje 174 (15.3) 71 (0.3) 39 (5.1) 72Unal 202 (18.9) 63 (7.5) 36 (3.2) 82

D × T IBW1 211 (6.5) 84 (11.3) 42 (3.6) 61IBW2 197 (17.3) 74 (8.0) 44 (3.1) 65IBW3 178 (17.3) 71 (6.9) 41 (1.1) 37

D × N Gaver 209 (8.8) 62 (2.1) 32 (1.0) 70Gibecq 166 (13.0) 54 (3.0) 35 (1.0) 57Primo 196 (8.2) 59 (1.8) 32 (1.4) 73

T Columbia River 203 (14.6) 65 (0.7) 39 (4.1) 86Fritzi Pauley 160 (17.2) 56 (5.0) 40 (4.1) 68Trichobel 184 (29.8) 55 (2.3) 36 (2.7) 78

N Wolterson 172 (23.9) 53 (0.9) 32 (2.3) 62

The stand was coppiced in December 1996 and January 2001. For SLA, LAR and LWR mean values with standard error (SE) of threereplicates are presented. T: P. trichocarpa, B: P. balsamifera, D: P. deltoides, N: P. nigra, CV = coe@cient of variation for leaf area.

respectively. For clone Hazendans the latter relation-ship was too weak (r ¡ 0:05) and no LAI could becalculated.

3.4. Canopy level

LAI was determined by using the allometric rela-tionships for tLA and an inventory of all shoot di-ameters (of the 36 assessment trees) (Fig. 4). Themean LAI di"ered signi+cantly among clones, rangingfrom 2.1 for clone IBW2 to 5.8 for clone Primo. Thelowest LAI values were achieved by clones IBW2,Boelare, IBW1, and Gibecq, with LAI values rang-ing between 2.1 and 2.7. Clones IBW3, BeauprJe, Bal-sam Spire, Unal, Fritzi Pauley, Trichobel and Raspaljehad intermediate LAI values ranging between 3.2 and4.3. High LAI values, ranging between 4.9 and 5.8,were achieved by clones Hoogvorst, Columbia River,Wolterson and Primo. The signi+cantly lowest valueswere observed for clones IBW2 and Boelare, i.e. 2.1

and 2.2, respectively (Fig. 5). The LAI was negativelycorrelated with LAR (r = −0:307) and with LWR(r=−0:556), and positively with tLA (r=0:344) andwith total above-ground biomass (r=0:914) (Table 3).

Above-ground biomass production was deter-mined, using the allometric relationship of individualstem dry mass and an inventory of all shoot diam-eters (of the 36 assessment trees) (Fig. 4). Meanabove-ground woody biomass production ranged from2:9 Mg ha−1 y−1 for clone IBW2 to 8:3 Mg ha−1 y−1

for clones Wolterson and Primo. Low biomass yieldswere achieved by clones IBW2, Boelare, IBW1,Gibecq, IBW3, Raspalje, BeauprJe, Fritzi Pauley, Tri-chobel and Columbia River, with productions rangingbetween 2.9 and 5:2 Mg ha−1 y−1. Clones IBW3,Raspalje and BeauprJe had a similar productivity of4:1 Mg ha−1 y−1 each. Clones Balsam Spire, Unal,Gaver, Hoogvorst, Hazendans, Primo and Woltersonachieved the highest biomass productions, rangingfrom 6.0 to 8:3 Mg ha−1 y−1.

A. Pellis et al. / Biomass and Bioenergy 27 (2004) 9–19 15

Fig. 3. Total leaf area per shoot (103 cm2) and number ofleaves per unit basal area (NBA; [cm−2]) of 17 di"erent poplarclones in the +rst growing season of the second coppice ro-tation. Mean values of three replicates and standard error barsare presented. BA: Balsam Spire, BE: BeauprJe, BO: Boelare,HA: Hazendans, HO: Hoogvorst, RA: Raspalje, UN: Unal, CO:Columbia River, FR: Fritzi Pauley, TR: Trichobel, GA: Gaver,GI: Gibecq, PR: Primo, I1: IBW1, I2: IBW2, I3: IBW3, WO:Wolterson. N: P. nigra, T: P. trichocarpa, D: P. deltoides, B: P.balsamifera.

Table 3Pearson rank correlation coe@cients of total leaf area (tLA), mean individual leaf area (individual LA), speci+c leaf area (SLA), leaf areaindex (LAI), above-ground woody biomass production, number of leaves per unit basal area (NBA), leaf weight ratio (LWR) and leafarea ratio (LAR)

Individual LA SLA NBA LAI Biomass LAR LWR(cm2) (cm2 g−1) (cm−2) (m2 m−2) (Mg ha−1 y−1) (cm2 g−1) (%)

tLA (cm2) 0:391∗∗ 0:423∗∗ −0:255 0:344∗ 0:361∗∗ −0:152 −0:358∗∗Individual LA (cm2) −0:314∗ −0:749∗∗∗ 0.014 0.154 0.219 −0:043SLA (cm2 g−1) −0:306∗ 0.279 0:295∗ 0:273∗ −0:341∗NBA (cm−2) 0.009 −0:054 −0:101 0.072LAI (m2 m−2) 0:914∗∗∗ −0:307∗ −0:556∗∗∗Biomass (Mg ha−1 y−1) −0:319∗ −0:583∗∗∗LAR (cm2 g−1) 0:686∗∗∗

Levels of signi+cance (P-values) are indicated as: ∗P¡ 0:05; ∗∗P6 0:01; ∗∗∗P6 0:001.

4. Discussion

Within poplars and willows, a high genotypic vari-ation in above-ground biomass production has beenreported [32]. Under temperate conditions and siteswithout extreme nutrient and water stress, the an-nual “working maximum” of above-ground biomassincrement of closely spaced poplars, grown for ro-tations of 4–5 years, generally has not exceeded10–12 Mg ha−1 in the +rst rotation after planting[15,33,34]. At the end of the +rst year after the sec-ond coppice, the best performing clones in this studywere Wolterson (N) and Primo (D × N) with a meanbiomass production of 8 Mg ha−1 y−1. In this study,biomass production was signi+cantly correlated withleaf area index (LAI), total leaf area (tLA) per shoot,and speci+c leaf area (SLA). A similar strong re-lation between biomass and LAI has been found innumerous other studies, e.g [35,36]. Most natural,mature forests have an LAI ranging between 2 and7 [37]. In comparison, SRF can already develop anLAI of 3–4 during the establishment year [20,38]and up to 11 in fully developed canopies [20]. Incoppice culture, even higher values can be reached.Coppicing results in several shoots per stool with ahigh growth rate and a rapid leaf area development,leading to fast crown closure and e@cient utilizationof space. In the present study, LAI values rangedbetween 2.1 and 5.8. The lower values were found inreplicate plots with a high cutting and stool mortality,resulting in a low stool density [39]. The high LAI

16 A. Pellis et al. / Biomass and Bioenergy 27 (2004) 9–19

Fig. 4. Allometric power equation between shoot diameter andtotal leaf area per shoot (upper panel), and between shoot diameterand stem dry mass (lower panel) for clone Wolterson during thesecond coppice rotation.

value of 5.8, the +rst year after coppicing, observedfor clones Primo (D × N) and Wolterson (N), andof 5 for clones Gaver (D × N), Hoogvorst (T × D)and Columbia River (T) demonstrates the potential ofthis SRF coppice culture for good biomass produc-tion. Although we did not validate our upscaled LAIestimates with +eld measurements using e.g., a leafcanopy analyser, Ceulemans et al. [40] and Casellaand Ceulemans [29] already showed that LAI valuescan be accurately estimated from height and diametermeasurements using allometric relationships.

In a study from Taylor et al. [41] and Ridge etal. [17] leaf size was found to be a good indicatorof biomass productivity in fast growing trees. Theyconcluded that high photosynthetic rates coupled tofast development of leaf area at cell, leaf and canopyscales all contribute to rapid accumulation of woodybiomass, but that leaf area traits may be of greater im-portance than those of photosynthesis. Also other stud-ies con+rmed that in Populus, tree leaf area develop-ment and individual leaf size are linked to productiv-ity [17,42,43]. Based on these studies, we expected agood correlation between LAI and individual leaf area,and between woody biomass and individual leaf area.However, leaf size alone, instead of LAI, is not a goodindicator of biomass production. High LAI values, andthus high biomass production, can be obtained by ahigh leaf area density (lots of smaller leaves) and/ora high individual leaf area (fewer larger leaves). In

Fig. 5. Leaf area index (m2 m−2) and above-ground woodybiomass production (Mg ha−1 y−1) of 17 di"erent poplar clonesat the end of the +rst growing season of the second coppice ro-tation. Mean values of three replicates and standard error barsare presented. BA: Balsam Spire, BE: BeauprJe, BO: Boelare,HA: Hazendans, HO: Hoogvorst, RA: Raspalje, UN: Unal, CO:Columbia River, FR: Fritzi Pauley, TR: Trichobel, GA: Gaver,GI: Gibecq, PR: Primo, I1: IBW1, I2: IBW2, I3: IBW3, WO:Wolterson. N: P. nigra, T: P. trichocarpa, D: P. deltoides, B: P.balsamifera.

the current study, the correlation between LAI and thenumber of leaves, expressed on a basal area basis, thecorrelation between LAI and individual leaf area andthe correlation between woody biomass and individ-ual leaf area were not signi+cant. There are two possi-ble reasons for the lack of correlation. The +rst reasonmight be the infection with Melampsora rust, causingearly defoliation and the absence of a signi+cant corre-lation between LAI and individual leaf area. The leafrust Melampsora is without any doubt the most dam-aging pathogen to SRF plantations [44]. In the presentstudy, Melampsora larici-populina, as a limiting fac-tor to productivity, attacked the entire D × T parent-age group and some clones of the T × D parentage

A. Pellis et al. / Biomass and Bioenergy 27 (2004) 9–19 17

group, mainly Boelare and BeauprJe. Because of early(middle of August) leaf fall, the allometric relations ofthose clones were not as strong as allometric relationswhen less or no rust attack was present. The second,more acceptable reason, might be the opposing strate-gies of some high productive clones, i.e. Woltersonand Primo characterized by many small leaves, ver-sus clones Hoogvorst and Hazendans characterized byfewer but larger leaves.

Besides the di"erences of individual leaf areaamong clones, we also found di"erences of indi-vidual leaf area within a shoot of the same clone,expressed as a coe@cient of variation and rangingbetween 37% and 86%. As for many broadleaved‘shade-intolerant’ trees, poplar shows a morphologi-cal light adaptation response, i.e. sun exposed leavesexhibit smaller leaf areas and smaller SLA valuesthan shade leaves from the inner part of the tree or atthe lower canopy level [29]. During the +rst growingseason, a light pro+le develops within the canopyof a tree, resulting in a distribution of SLA withinthe canopy in the following growing seasons. In thisstudy above-ground woody biomass production wascorrelated with SLA, rather than with individual leafarea.

Nitrogen stress can reduce the individual leaf areaand the number of leaves, inEuencing the LAI and+nally the biomass production. SLA is sensitive tothe amount of light and to the nitrogen content of thesoil [45]. In the present study a signi+cant, positivecorrelation between SLA and nitrogen content of theleaves was found. The nitrogen content of the leavesin this study was about 3% on a dry weight basis,well within the range of 2.1–3.9% nitrogen content ofPopulus leaves (under fertilized conditions) reportedearlier [21]. Therefore nitrogen was probably not alimiting factor in our study.

We conclude that LAI was the primary determinant,and tLA and SLA were the second drivers (correlatedwith LAI) of biomass production in this study. More-over two di"erent growth strategies were observed, i.e.clones with many small leaves per shoot and cloneswith fewer large leaves per shoot, resulting in a sim-ilar biomass production. As shown in this study, var-ious genetically controlled leaf characteristics deter-mine biomass production in SRF; however abiotic andexternal biotic factors such as leaf rust attacks are alsoimportant.

Acknowledgements

This study is being supported by a research contractof the Province of Antwerp. The project has been car-ried out in close co-operation with Eta-com B., sup-plying the grounds and part of the infrastructure, andwith the logistic support of the city council of Boom.All plant materials were kindly provided by the Insti-tute for Forestry and Game Management (Geraards-bergen) and by the Forest Research, Forestry Com-mission (UK). We gratefully acknowledge F., E. andH. Pellis for help with the harvest, L. D’A"nay andT. Indeherberge for help with the +eld measurements,as well as A. Mattheeussen and N. Calluy for the ni-trogen analyses.

References

[1] Hansen EA. Poplar woody biomass yields: a look to thefuture. Biomass and Bioenergy 1991;1:1–7.

[2] Deraedt W, Ceulemans R. Clonal variability in biomassproduction and conversion e@ciency of poplar during theestablishment year of a short rotation coppice plantation.Biomass and Bioenergy 1998;15:391–8.

[3] Ranney JW, Wright LL, Layton PA. Hardwood energy crops:the technology of intensive culture. Forestry 1987;85:17–28.

[4] Hall DO, House JI. Trees and biomass energy: carbonstorage and/or fossil fuel substitution? Biomass and Bioenergy1994;6:11–30.

[5] Gordon JC. The productive potential of woody plants. IowaState Journal of Research 1975;49:267–74.

[6] Isebrands JG, Karnosky DF. Environmental bene+ts of poplarculture. In: Dickmann DI, Isebrands JG, Eckenwalder JE,Richardson J, editors. Poplar culture in North America.Ottawa: NRC Research Press; 2001. p. 207–18.

[7] Perttu KL. Ecological, biological balances and conservation.Biomass and Bioenergy 1995;9:107–16.

[8] Ledin S, Willebrand E. Handbook on how to grow shortrotation forests. Uppsala: Swedish University of AgriculturalSciences, Department of Short Rotation Forestry; 1996.

[9] Bradshaw Jr HD, Strauss SH. Breeding strategies for the 21stcentury: domestication of poplar. In: Dickmann DI, IsebrandsJG, Eckenwalder JE, Richardson J, editors. Poplar culture inNorth America. Part B. Otawwa: NRC Research Press; 2001.p. 383–94.

[10] Gordon JC, Promnitz LC. Photosynthetic and enzymaticcriteria for the early selection of fast-growing Populus clones.In: Cannell MGR, Last FT, editors. Tree physiology and yieldimprovement. New York: Academic Press; 1976. p. 79–97.

[11] Dickmann DI, Nguyen PV, Pregitzer KS. E"ects of irrigationand coppicing on above-ground growth, physiology, and +neroot-dynamics of two +eld-grown hybrid poplar clones. ForestEcology and Management 1996;80:163–74.

18 A. Pellis et al. / Biomass and Bioenergy 27 (2004) 9–19

[12] Heilman PE, Stettler RF. Genetic variation and productivityof Populus trichocarpa T. & G. and its hybrids. II. Biomassproduction in a 4-year plantation. Canadian Journal of ForestResearch 1985;15:384–8.

[13] Heilman PE, Ekuan G, Fogle D. Above- and below-groundbiomass and +ne roots of 4-year-old hybrids of Populustrichocarpa × Populus deltoides and parental species inshort-rotation culture. Canadian Journal of Forest Research1994;24:1186–92.

[14] Scarascia-Mugnozza GE, Ceulemans R, Heilman PE,Isebrands JG, Stettler RF, Hinckley TM. Productionphysiology and morphology of Populus species and theirhybrids grown under short rotation. II. Biomass componentsand harvest index of hybrid and parental species clones.Canadian Journal of Forest Research 1997;27:285–94.

[15] Cannell MGR, Smith RI. Yields of minirotation closelyspaced hardwoods in temperate regions: review and appraisal.Forest Science 1980;26:415–28.

[16] Van Volkenburgh E, Taylor G. Leaf growth physiology.In: Stettler RF, Bradshaw Jr HD, Heilman PE, HinckleyTM, editors. Biology of Populus and its implications formanagement and conservation. Ottawa: NRC Research Press;1996. p. 283–99.

[17] Ridge CR, Hinckley TM, Stettler RE, Van Volkenburgh E.Leaf growth characteristics of fast-growing poplar hybridsPopulus trichocarpa × P. deltoides. Tree Physiology1986;1:209–16.

[18] Barigah TS, Saugier B, Mousseau M, Guittet J, CeulemansR. Photosynthesis, leaf area and productivity of 5 poplarclones during their establishment year. Annales des SciencesForestiWeres 1994;51:613–25.

[19] Isebrands JG, Promnitz LC, Dawson DH. Leaf areadevelopment in short rotation intensive cultured Populusplots. Proceedings of TAPPI Forest Biology Wood ChemicalConference, Wisconsin, June 20–22, 1977. p. 201–10.

[20] Heilman PE, Hinckley TM, Roberts DA, Ceulemans R.Production physiology. In: Stettler RF, Bradshaw Jr HD,Heilman PE, Hinckley TM, editors. Biology of Populus andits implications for management and conservation. Ottawa:NRC Research Press; 1996. p. 459–89.

[21] Larson PR, Isebrands JG. Some physiological applicationsfor intensive culture. Technical Report NC-21, US ForestService, North Central Station, 1976. p. 117.

[22] Dickmann DI. Physiological determinants of poplar growthunder intensive culture. In: Fayle DCF, Zsu"a L, AndersonHW. editors. Management and utilization in Canada. ForestResearch Information Paper No. 102. Brockville: OntarioMinistry of Natural Resources; 1979. p. 12.1–.12.

[23] Christersson L, Ramstedt M, Forsberg J. Pests, diseases andinjuries in intensive short-rotation forestry. In: Mitchell CP,Ford-Robertson JB, Hinckley T, Sennerby-Forsse, editors.Ecophysiology of short rotation forest crops, Oxford: ElsevierApplied Science; 1992. p. 185–215.

[24] Mitchell CP, Stevens EA, Watters MP. Short-rotationforestry—operations, productivity and costs based onexperience gained in the UK. Forest Ecology andManagement 1999;121:123–36.

[25] Kira T. Primary production of forests. In: Cooper JP, editor.Photosynthesis and productivity in di"erent environments.Cambridge: Cambridge University Press; 1975. p. 5–40.

[26] Madgwick HAI. Mensuration of forest biomass. In: YoungHE, editor. Oslo biomass studies. Orono: University of Maine;1976. p. 13–27.

[27] Zavitkovski J. Small plots with unplanted plot border candistort data in biomass production studies. Canadian Journalof Forest Research 1981;11:9–12.

[28] Laureysens I, Deraedt W, Indeherberge T, Ceulemans R.Population dynamics in a six-year-old coppice culture ofpoplar. I. Clonal di"erences in stool mortality, shoot dynamicsand shoot diameter distribution in relation to biomassproduction. Biomass and Bioenergy 2003;24:81–95.

[29] Casella E, Ceulemans R. Spatial distribution of leafmorphological and physiological characteristics in relationto local radiation regime within the canopies of 3-year-oldPopulus clones in coppice culture. Tree Physiology2002;22:1277–88.

[30] Pontailler J-Y, Ceulemans R, Guittet J, Mau M. Linear andnon-linear functions of volume index to estimate woodybiomass in high density young poplar stands. Annales desSciences ForestiWeres 1997;54:335–45.

[31] Littell RC, Milliken GA, Stroup WW, Wol+nger RD. SASSystem for Mixed Models. Cary, NC, USA: SAS InstituteInc.; 1996.

[32] Ceulemans R, Deraedt W. Production physiology and growthpotential of poplars under short-rotation forestry culture.Forest Ecology and Management 1999;121:9–23.

[33] Makeschin F, Rehfuess KE, RZusch I, SchZorry R.Anbau von Pappeln und Weiden im Kurzumtriebauf ehemaligem Acker: StandZortliche Voraussetzungen,NZahrsto"versorgung, Wuchsleistung und bodenZokologischeWirkungen. ForstwissenschaEiches Centralblatt 1989;108:125–43.

[34] Ho"mann-Schielle C, Jug A, Makeschin F, Rehfuess KE.Short rotation plantations of balsam poplar, aspen and willowson former arable land in the Federal Republic of Germany.I. Site-growth relationships. Forest Ecology and Management1999;121:41–55.

[35] Linder S. Potential and actual production in Australian foreststands. In: Landsberg JJ, Parsons W, editors. Research forforest management. Melbourne, Australia: CSIRO; 1985.p. 11–35.

[36] Zavitkovski J, Isebrands JG, Dawson DH. Productivity andutilization potential of short-rotation Populus in the LakeStates. In: Thielges BA, Land SBJ, editors. Proceedings ofSymposium on Eastern Cottonwood and Related Species.Baton Rouge: Louisiana State University; 1976. p. 392–401.

[37] Satoo T. A synthesis of studies by the harvest method:Primary production relations in the temperate deciduousforests of Japan. In: Reichle DE, editor. Analysis of temperatedeciduous forest ecosystems. Berlin: Springer; 1970.p. 55–72.

[38] Anderson HW. Biomass production of hybrid poplar grown inminirotation. In: Fayle DCF, Zsu"a L, Anderson HW, editors.

A. Pellis et al. / Biomass and Bioenergy 27 (2004) 9–19 19

Poplar research, management and utilization in Canada.Maple, ON: Ontario Research Centre, Ministry of NaturalResources; 1997, 1979. 13pp.

[39] Laureysens I, Bogaert J, Blust R, Ceulemans R. Biomassproduction of 17 poplar clones grown in a short-rotationculture in relation to soil characteristics. Forest Ecology andManagement 2004, in press.

[40] Ceulemans R, Pontailler J-Y, Mau F, Guittet J. Leafallometry in young poplar stands: reliability of leaf area indexestimation, site and clone e"ects. Biomass and Bioenergy1993;4:315–21.

[41] Taylor G, Beckett KP, Robinson KM, Stiles K, Rae AM.Identifying QTL for yield in UK biomass poplar. Aspects ofApplied Biology 2001;65:173–82.

[42] Dunlap JM, Stettler RF. Genetic variation and productivityof Populus trichocarpa and its hybrids. X. Trait correlationsin young black cottonwood from four river valleys inWashington. Trees-Structure and Function 1998;13:28–39.

[43] Wu R, Stettler RF. Developmental quantitative geneticsof growth in Populus. Theoretical and Applied Genetics1998;97:1110–19.

[44] Royle DJ, Hunter T, Pei MH. Evaluation of the biology andimportance of diseases and pests in willow plantations: LongAshton Research Station, 1992, ETSU B 1258.

[45] Larocque GR. Performance and morphological response ofthe hybrid poplar DN-74 (Populus deltoides × nigra) underdi"erent spacings on a 4-year rotation. Annals of ForestScience 1998;56:275–87.