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Available at www.sciencedirect.com
B I O M A S S A N D B I O E N E R G Y ] ( ] ] ] ] ) ] ] ] – ] ] ]
0961-9534/$ - see frodoi:10.1016/j.biomb
�Corresponding auE-mail address:
Please cite this aculture of popj.biombioe.2007.1
http://www.elsevier.com/locate/biombioe
Growth and production of a short-rotation coppice cultureof poplar—IV: Fine root characteristics of five poplar clones
N. Al Afasa, N. Marronb, C. Zavallonia, R. Ceulemansa,�
aDepartment of Biology, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, BelgiumbUMR 1137, INRA-UHP Ecologie et Ecophysiologie Forestieres, F-54280 Champenoux, France
a r t i c l e i n f o
Article history:
Received 10 April 2007
Received in revised form
14 November 2007
Accepted 15 November 2007
Keywords:
Fine root biomass
Root length
Genotype
Root area index
Nitrogen concentration
Leaf area index
Populus spp.
R
nt matter & 2007 Elsevieioe.2007.11.007
thor. Tel.: +32 3820 2256; fReinhart.Ceulemans@ua.
rticle as: Al Afas N, Marlar—IV: Fine root c1.007
RECTED PROOFa b s t r a c t
Below-ground characteristics of five Populus clones, belonging to different species and
parentages, were studied during the second growing season of the third rotation of a high-
density coppice culture. Size (length, area and volume), biomass, nitrogen and carbon
concentrations of three classes of fine roots (diameter classes of 0–1, 1–2 and 2–5 mm) were
determined for four different soil layers. Fine root biomass varied significantly among
clones and among soil layers. Clone Primo (Populus deltoides� Populus nigra) had the highest
root biomass and the longest fine roots, while clone Hazendans (Populus trichocarpa� P.
deltoides) had the lowest root biomass and shortest fine roots. The topsoil layer (0–5 cm) was
very rich in fine roots; the fine root biomass and distribution of all clones decreased with
increasing soil depth. Fine root area index (diameter classes of 0–1 and 1–2 mm) varied
among clones, with higher values for clones Wolterson and Primo (3.6 and 3.7,
respectively), while clones Hazendans and Columbia River had lower values (1.7 and 2.2,
respectively). The absence of a significant correlation between fine root traits and above-
ground biomass leads to the conclusion that above-ground biomass was not a reliable
indicator of below-ground biomass in poplar, probably because of the age of the plantation
in our study (stump age of 10 years). Fine root area index was positively correlated with leaf
area index for all clones and at all soil depths, i.e., clones with a high fine root area index
also had a high leaf area index. We conclude that leaf area index can be an indicator of root
area.
& 2007 Elsevier Ltd. All rights reserved.
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UNCO1. Introduction
Roots are a large and metabolically active fraction of total tree
biomass [1,2]. Among all roots, fine roots represent only a
small fraction of total tree biomass, but fine root production
and turnover are significant components of the carbon
turnover (up to 40%) [3]. In most ecosystems, a major portion
of carbon fixed through photosynthesis is allocated to the
production and maintenance of fine roots, and therefore they
represent a major sink of carbon [4]. Additionally, fine roots
are an extremely important component of tree root systems,
r Ltd. All rights reserved.
ax: +32 3820 2271.ac.be (R. Ceulemans).
ron N, Zavalloni C, Ceulharacteristics of five
as they are the main links between the plant and the soil,
allowing water and nutrient uptake. At a larger scale, fine
roots also play a crucial role for nutrient, carbon and energy
cycling in forest ecosystems. The fast turnover rate and the
short life span of fine roots enable a great flexibility to
changing soil environmental conditions [5]. However, sam-
pling and quantification of fine roots are more time consum-
ing than those of other compartments of the tree, and the
methods are usually less precise [6]. Moreover, the root
system is known to be very dependent on environmental
conditions and on genetic background. The tight dependence
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emans R. Growth and production of a short-rotation coppicepoplar.... Biomass and Bioenergy (2007), doi:10.1016/
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Table 1 – Soil characteristics of the experimental short-rotation coppice plantation of poplar
Soil characteristics
pH 7.7 (0.001)
OM (%) 1.25 (0.001)
N (mg/100 g) 122.5 (2.5)
P (mg/100 g) 16.4 (2.1)
Bulk density (g cm�3) 1.46 (0.02)
Mean (standard error) soil pH, organic matter (OM), total nitrogen
(N), plant available phosphorus (P) and bulk density are presented.
B I O M A S S A N D B I O E N E R G Y ] ( ] ] ] ] ) ] ] ] – ] ] ]2
RRECT
of fine roots on a variety of abiotic and biotic factors, as well
as on the edaphic composition and soil depth, makes the
analysis of this below-ground compartment even more
difficult [7]. Differences in standing biomass of roots among
different tree species are frequently observed. Although we
have some general knowledge of the vertical distribution and
seasonal dynamics of fine roots of trees, information on fine
root growth and development is still needed for many tree
species. Thus, fine roots remain one of the least accessible,
but most important, study areas in terrestrial ecosystems [8].
Poplars are among the fastest growing trees at temperate
latitudes and are of considerable commercial importance [9].
Above-ground variability in productivity and in functional
and structural determinants has already been widely docu-
mented for the Populus genus [10]. Leaf characteristics and
their links with biomass production are also well documented
in poplar. High variations in morphological and physiological
leaf traits among clones, parentages and species, as well as
close links between foliage characteristics and productivity,
have been extensively reported for the genus [11–14]. How-
ever, the poplar root system remains the most poorly studied
and understood portion of the plant [15]. Indeed, only a very
limited number of studies have investigated the (fine) rooting
system of poplar trees. These few studies have shown that
the morphology and physiology of poplar roots vary among
species and among clones [16]. For example, Nguyen et al. [17]
and Pregitzer et al. [18] reported that two poplar clones
differed in fine root development, root carbohydrate content
and nitrogen dynamics. Most roots were found in the top
50 cm layer of soil when trees were excavated in an experi-
mental plantation of 2-year-old hybrid clones [19]. Poplar
clones seem to differ primarily in number and size of roots,
and in the depth and orientation of root growth. Significant
differences among families and among both male and female
parentages have been observed in the amount of vertical
rooting [20].
The objectives of the current study were to document the
variability among several Populus parentages in terms of roots
by comparing the fine root systems of five poplar clones
growing in a short-rotation plantation for which the above-
ground characteristics have already been extensively de-
scribed during the last decade [11,12,21–26]. More precisely,
we aimed:
105
(1)107
Plcuj.b
COto explore the variability in fine root biomass among five
poplar clones belonging to different parentages as a
function of soil depth and
(2)
109111
UNto relate below-ground root characteristics to above-ground biomass production and leaf area index (LAI).
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2. Materials and methods
2.1. Site and stand description
In April 1996, 17 poplar (Populus) clones were planted on an
experimental field site of 0.56 ha in an industrial zone at
Boom, province of Antwerp (Belgium, 511050N, 41220E, 5 m
ease cite this article as: Al Afas N, Marron N, Zavalloni C, Ceullture of poplar—IV: Fine root characteristics of fiveiombioe.2007.11.007
ED PROOF
elevation above sea level). The plantation was situated on a
capped landfill site, covered with a 2 m thick layer of sand,
clay and mixed rubble. As this was a rather old landfill site
(over 40 years), no gas leakage was detected any more. The
soil was characterised by a bulk density between 1.22 and
1.62 g cm�3 (heavy clay-loam soil), and a pH between 7.3 and
8.1. The upper soil horizon contained between 0.8% and 1.8%
organic matter. The nutrient and mineral reserves were high
in comparison with forest soils, but moderate in comparison
with agricultural soils [24]. As the time of plantation was only
few years after the capping of the landfill site, a clear soil
profile was not yet fully developed. Soil characteristics are
listed in Table 1.
Hardwood cuttings (25 cm long) were planted in a double-
row design with alternating inter-row distances of 0.75 and
1.5 m, and a spacing of 0.9 m within rows accommodating an
overall density of 10,000 trees ha�1. A randomised block
design with 17 clones�3 plot replications was adopted
according to the protocol prescribed by the UK Forestry
Commission [27]. Each monoclonal plot (n ¼ 100 trees) had a
double border row, leaving 36 assessment trees in the centre
of each plot [28]. The plantation was irrigated shortly after
planting and mechanical weed control was applied to
promote optimal establishment.
2.2. Plant material and management regime
The cuttings that did not establish in 1996 were replaced in
the spring of 1997 with new hardwood cuttings. At the end of
the establishment year in December 1996, as well as after the
first rotation cycle of 4 years, all shoots were cut back to a
height of 5 cm to create a multi-shoot coppice system. No
fertilisation or irrigation was applied after the establishment
of the experiment. Chemical weed control was applied during
the course of the plantation only when mechanical weeding
became insufficient. On three occasions (in June 1996, June
1997 and May 2001), herbicides—a mixture of glyphosate at
3.2 kg ha�1 and oxadiazon at 9.0 kg ha�1—were applied using a
spraying device with a hood-covered nozzle to reduce the
impact on trees. In January 2001 and February 2004, the
plantation was coppiced again to a height of 5 cm above soil
level, achieving three rotations of the coppice culture. Further
details on the plantation including site management, history
and plant materials can be found in [21,25].
emans R. Growth and production of a short-rotation coppicepoplar.... Biomass and Bioenergy (2007), doi:10.1016/
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B I O M A S S A N D B I O E N E R G Y ] ( ] ] ] ] ) ] ] ] – ] ] ] 3
UNCORRECT
All 17 poplar clones in the plantation had been selected for
superior biomass production and disease resistance. The five
clones selected for the current study belong to various
parentages and hybrid groups: clones Balsam Spire (BS,
Populus trichocarpa�Populus balsamifera, T�B), Columbia
River (CR, P. trichocarpa, T), Hazendans (HD, P. trichocar-
pa�Populus deltoides, T�D), Primo (PR, P. deltoides�Populus
nigra, D�N) and Wolterson (WO, P. nigra, N).
2.3. Fine root sampling
Fine roots (0–5 mm in diameter) were sampled by collecting
soil cores using a metal auger with a length of 25 cm and an
inner diameter of 4.8 cm (split-tube sampler, Eijkelkamp, The
Netherlands) in August 2005 (i.e., the second growing season
of the third rotation of the plantation). Twelve random
samples per clone (four samples per plot) were collected
mid-way between two rows of trees. Samples from four
different soil layers (at depths of 0–5, 5–10, 10–15 and
15–30 cm) were put in plastic bags and stored separately at
�20 1C until processed. Fine roots were manually separated
from the soil, and living roots were separated from dead roots
based on their lighter colour and greater resilience. Living
roots were also stiffer and showed a better cohesion between
the cortex and the periderm [29]. Roots were washed by tap
water in pots and put in Petri dishes with water.
2.4. Fine root morphology, biomass, carbon and nitrogen
Roots in Petri dishes were scanned on a flatbed scanner (AGFA
SnapScan, 1212). Pictures were filtered and pre-processed
with the GIMP 2.0 program (GNU Image Manipulation
Program, http://www.gimp.org). Root length, area and volume
were measured by processing the pictures on a DT-scan
program. Three classes of root diameter were identified:
diameter class 1 (0–1 mm), diameter class 2 (1–2 mm) and
diameter class 3 (2–5 mm). Relative root length (%) for each
diameter class was measured as (total root length of one
specific class�100)/P
total root length of all classes in one
soil layer. After scanning, fine roots were dried for 2 days at
75 1C; dry root mass was determined and expressed as mg of
root per cm3 of soil. The dry samples of the different soil
layers were ground; nitrogen (N) and carbon (C) concentra-
tions were determined with an NC element analyser
(NC-2100, Carlo Erba Instruments, Italy) and the C to N ratio
(C:N) was subsequently calculated.
Fine root (0–2 mm diameter) area index (RAI) was calculated
as:P
root area of all samples of diameter classes 1 and 2 per
replicate plot/core area, and expressed as m2 m�2 (dimen-
sionless). Fine root area density (RAD) was calculated asP
root area of all samples (of diameter classes 1 and 2 only)
per replicate/core volume, and expressed in cm2 cm�3.
2.5. Leaf area index
In August 2005, 10 shoots per replicate plot (of the 36 central
assessment trees) were harvested at 5 cm above soil level for
each of the five clones. All leaves of each shoot were removed
and brought to the laboratory for analysis. Individual leaf area
was measured for all leaves using a leaf area meter (CID Inc.
Please cite this article as: Al Afas N, Marron N, Zavalloni C, Ceulculture of poplar—IV: Fine root characteristics of fivej.biombioe.2007.11.007
ROOF
type CI-203, USA). The LAI was calculated from the total leaf
area of the 10 shoots and scaled-up to all assessment shoots
of each replicate plot per unit ground area (36 m2) of the plot.
2.6. Above-ground standing biomass
At the end of the second growing season of the third rotation
(2005), the diameter of all shoots was measured at 22 cm
above soil level with a digital calipers (Mitutoyo, type CD-
15DC, UK). Standing above-ground biomass was estimated
per clone using allometric power relationships between shoot
diameter and total shoot dry mass: M ¼ aDb, with a and b as
regression coefficients, D as shoot diameter and M as shoot
dry mass. These allometric relationships were established
and validated in 2002 during the second growing season of
the second rotation [25].
2.7. Statistical analyses
Data analyses were performed with the Statistical Package
SPSS (SPSS, Chicago, IL). Means were calculated with their
standard error (7SE) and compared using two-way ANOVA.
Clone and soil layer were considered as the main factors.
Interclonal comparisons were followed by a Scheffe test. All
differences were considered significant at Pp0.05. Linear
correlations between parameters were tested for significance
using Pearson’s correlation coefficient.
D P3. Results
3.1. Fine root biomass
Biomass of fine roots of diameter classes 1 and 2 from the
0–30 cm soil layers differed significantly among clones
belonging to the different parentages. The mean fine root
biomass ranged between 2.5 mg cm�3 for clone Hazendans
and 4.4 mg cm�3 for clone Primo. The highest biomass of fine
roots over the examined profile occurred in the upper 5 cm
layer of the soil, whereas the lowest was measured at a soil
depth of 15–30 cm for all clones (Fig. 1). Fine root biomass in
the deepest soil layer (15–30 cm) varied only slightly among
clones.
3.2. Fine root morphology and root area index
Total root length of diameter class 1 differed significantly
among clones and among soil layers (Fig. 2). At a soil depth of
0–5 cm, clones Primo and Wolterson had the highest root
length, while clones Hazendans and Columbia River had the
lowest values in the same soil layer. Similar variation in root
length among clones was observed at the other soil depths
examined. Clone Balsam Spire always showed intermediate
values (Fig. 2, top panel). In contrast, relative fine root lengths
of diameter classes 2 and 3 (1–2 and 2–5 mm in diameter,
respectively) were high for clones Hazendans and Columbia
River, and low for clones Primo and Wolterson for most soil
layers (Fig. 2, bottom panels). Relative root length of diameter
class 1 was high in all soil layers for clones Primo and
Wolterson. Total root length (sum of all root diameter classes)
emans R. Growth and production of a short-rotation coppicepoplar.... Biomass and Bioenergy (2007), doi:10.1016/
CORRECTED PROOF
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-30
-25
-20
-15
-10
-5
00
Balsam Spire
Columbia River
Hazendans
Primo
Wolterson
So
il d
ep
th (
cm
)
Fine root biomass (mg cm-3)
1 2 3
Fig. 1 – Fine root biomass density of five poplar clones as a function of soil depth for clone Balsam Spire (P. trichocarpa�P.
balsamifera), clone Columbia River (P. trichocarpa), clone Primo (P. deltoides�P. nigra), clone Hazendans (P. trichocarpa�P.
deltoides) and clone Wolterson (P. nigra). Mean values (7SE) of three replicates per clone.
0-5cm
5-10cm
10-15cm
15-30cm
Wolterson
80 85 90 95 100
Primo
0 2 4 6 8 0 2 4 6 8 0 2 4 6 8 0 2 4 6 8 0 2 4 6 8
HazendansColumbia RiverBalsam Spire
Relative root length (%)
Absolute root length (m)
So
il d
ep
th (
cm
)
0 80 85 90 95 1000 80 85 90 95 1000 80 85 90 95 1000 80 85 90 95 1000
0-5cm
5-10cm
10-15cm
15-30cm
Fig. 2 – Absolute (top panels; m) and relative root length (bottom panels; %) of three diameter classes of fine and small roots of
five poplar clones as a function of soil depth. Clone Balsam Spire (P. trichocarpa�P. balsamifera), clone Columbia River (P.
trichocarpa), clone Primo (P. deltoides�P. nigra), clone Hazendans (P. trichocarpa�P. deltoides) and clone Wolterson (P. nigra) are
shown. Root length class 1 (white bars) ¼ root diameter 0–1 mm; root length class 2 (black bars) ¼ root diameter 1–2 mm; and
root length class 3 (hatched bars) ¼ root diameter 2–5 mm. Mean values (7SE) of three replicates per clone.
B I O M A S S A N D B I O E N E R G Y ] ( ] ] ] ] ) ] ] ] – ] ] ]4
UNshowed a high clonal variation, especially in the 0–5 cm soil
layer (Fig. 3).
Fine RAI of diameter classes 1 and 2 varied among clones.
RAI ranged between 1.77 for clone Hazendans and 3.56 for
clone Wolterson (Table 2), and decreased with increasing soil
depth (data not shown). Fine RAD was high for clones
Wolterson and Primo, while it was low for clone Hazendans
(Table 2). RAD varied significantly among soil layers (data not
shown). The topsoil layer (0–5 cm) had higher RAD than the
other soil layers for all clones (data not shown).
Please cite this article as: Al Afas N, Marron N, Zavalloni C, Ceulculture of poplar—IV: Fine root characteristics of fivej.biombioe.2007.11.007
3.3. Fine root nitrogen and carbon
Fine root N concentration did not differ significantly among
clones, but differences in N concentration were detected
among the different soil layers. For instance, fine root N
concentration of clone Wolterson was significantly higher in
the 0–5 cm topsoil layer (1.18%70.07) than in the deepest
15–30 cm soil layer of the profile (0.81%70.03). Fine root C
concentration differed significantly among clones and ranged
between 36.2% for clone Primo and 44.3% for clone Balsam
emans R. Growth and production of a short-rotation coppicepoplar.... Biomass and Bioenergy (2007), doi:10.1016/
RECTE
OF
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Soil depth (cm)
0
2
4
6
8
10
Balsam Spire
Columbia River
Hazendans
Primo
WoltersonTo
tal ro
ot
len
gth
(m
)
0-5 cm 10-15 cm5-10 cm 15-30 cm
Fig. 3 – Total root length (sum of diameter classes 1, 2 and 3) of fine and small roots of five poplar clones in the second growing
season of the third coppice rotation. Mean values (7SE) of three replicates per clone.
Table 2 – General mean7standard error of fine root areaindex and fine root area density for the five poplar clones(three replicates per clone; root diameter classes 1 and 2)
Clone Parentage Rootarea
index
Root areadensity
(cm2 cm�3)
Balsam
Spire
T�B 3.2970.38 0.1670.02
Columbia
River
T 2.2270.14 0.1170.01
Hazendans T�D 1.7770.15 0.0970.01
Primo D�N 3.5370.29 0.1870.01
Wolterson N 3.5670.29 0.1970.01
B: P. balsamifera, D: P. deltoides, N: P. nigra; and T: P. trichocarpa.
B I O M A S S A N D B I O E N E R G Y ] ( ] ] ] ] ) ] ] ] – ] ] ] 5
RSpire. C concentration was not significantly different for fine
roots sampled from different soil layers.
O 105107
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UNC3.4. Leaf area index and above-ground standing biomass
LAI varied significantly among clones, and ranged between
2.1 for clone Hazendans and 6.0 for clone Wolterson. Clone
Primo (5.4) also had a high LAI, while clones Columbia River
and Balsam Spire had intermediate values (4.1 and 4.7,
respectively). Mean cumulated above-ground biomass (after
2 years) differed significantly among clones and ranged from
14.6 tonne ha�1 for clone Hazendans to 25.8 tonne ha�1 for
clone Wolterson. Clone Primo was also very productive,
showing values very similar to the ones of clone Wolterson
(above-ground biomass of 22.0 tonne ha�1 after 2 years). Clone
Columbia River showed a relatively high standing biomass
Please cite this article as: Al Afas N, Marron N, Zavalloni C, Ceulculture of poplar—IV: Fine root characteristics of fivej.biombioe.2007.11.007
D PRO(18.1 tonne ha�1), while clone Balsam Spire had an intermedi-
ate value of 15.9 tonne ha�1.
3.5. Correlations among traits
To avoid redundancy of the analogous results on root length,
area and volume, root length was primarily used in the
following analysis. Fine root biomass was significantly and
positively correlated with root length for all three diameter
classes (Table 3 and Fig. 4). Fine root biomass was also
positively correlated with N concentration and negatively
with the C:N ratio (Table 3). Furthermore, significant correla-
tions were found among fine root lengths of diameter classes
1, 2 and 3, as well as between fine root length of classes 1 and
2 and root N concentration. In general, root parameters were
not significantly correlated with above-ground standing
biomass (Table 3). However, a significant positive correlation
between LAI and RAI was found (Fig. 5).
4. Discussion
Three aspects of fine root growth deserve particular attention.
First, rapid rates of root length extension are known to be
usually well correlated with above-ground growth, at least in
young trees [4,30]. However, in mature and older trees, above-
and below-ground growth can become independent, which
could be the case in our study. Older trees rely not only on
current photosynthates but also on stored reserves in
permanent organs such as coarse roots and trunks. A second
important aspect of root growth is the fact that C allocation to
root growth appears to be under strong genetic control. There
are several reports of genotypic and species-level differences
in root growth [18,20]. The third aspect of root growth needing
particular attention is the understanding of root plasticity in
response to different environmental conditions. For instance,
emans R. Growth and production of a short-rotation coppicepoplar.... Biomass and Bioenergy (2007), doi:10.1016/
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Table 3 – Linear correlations (Pearson’s coefficients) between fine root parameters (biomass, root length of diameter class 1(0–1 mm), class 2 (1–2 mm), class 3 (2–5 mm), nitrogen (N), carbon (C) concentration and C:N ratio) with above-groundbiomass and root area index
Root traits
Biomass Length Nitrogen Carbon C:N ratio Root area index
Diameter class
1 2 3
Root traits
Length
Diameter class
1 0.80***
2 0.85*** 0.92***
3 0.70*** 0.77*** 0.86***
Nitrogen 0.30* 0.33* 0.31* ns
Carbon ns ns ns ns ns
C:N ratio �0.33* ns �0.36 ns �0.85*** 0.42**
Root area index 0.81*** 0.98*** 0.95*** 0.82*** 0.32* ns �0.26*
Above-ground biomass ns ns ns ns ns ns ns ns
Levels of significance are indicated by asterisks; ns ¼ non significant; *Pp0.05; **Pp0.01; ***Pp0.001.
r =0.70
0
1
2
3
4
0 0.1 0.2 0.3
Class 3 (diameter 2-5 mm)
r = 0.85
0 0.4 0.8 1.2 1.6 2
r = 0.80
0
1
2
3
4
0 4 6 8 10
Class 1 (diameter 0-1 mm)
Root length
Fin
e r
oo
t b
iom
ass (
mg
cm
-3)
Fin
e r
oo
t b
iom
ass (
mg
cm
-3)
Class 2 (diameter 1-2 mm)
2
A B C
Fig. 4 – Relationships between fine root biomass and root length of class 1 (A), class 2 (B) and class 3 (C). Mean values of three
replicates per clone are presented. Linear correlations (Pearson’s coefficients) and their level of significance are indicated in
Table 3.
r = 0.91
0
2
4
6
8
0
Le
af
are
a in
de
x
Root area index
Balsam Spire
Columbia River
Hazendans
Primo
Wolterson
X
1 2 3 4 5
Fig. 5 – Relationship between root area index and leaf area
index. Mean values (7SE) of three replicates per clone are
shown. Both indices are dimensionless (m2 m�2).
B I O M A S S A N D B I O E N E R G Y ] ( ] ] ] ] ) ] ] ] – ] ] ]6
Please cite this article as: Al Afas N, Marron N, Zavalloni C, Ceulculture of poplar—IV: Fine root characteristics of fivej.biombioe.2007.11.007
elevated atmospheric CO2 and soil N availability have been
shown to increase root production and mortality of the hybrid
poplar clone Eugenei (P. deltoides�P. nigra) [4].
4.1. Clonal variability
In this study, significant variation in fine root biomass was
found among different poplar clones. This confirms what has
been reported in few studies on the clonal variability in fine
root growth of poplar [31,32]. The variability in fine root
biomass is related to the large genotypic variations in above-
ground leaf and stem characteristics, and to the genetic
variation between parents and their hybrids [11–14,25,33]. For
instance, Nguyen et al. [17] and Pregitzer et al. [18] observed
for two hybrid poplar clones in a short-rotation culture (SRC)
that the clones differed significantly in fine root production.
Clone Tristis (Populus tristis�P. balsamifera) produced more
and longer fine roots in the 0–30 cm soil layer than did clone
Eugenei (P. deltoides�P. nigra), even though Tristis trees were
emans R. Growth and production of a short-rotation coppicepoplar.... Biomass and Bioenergy (2007), doi:10.1016/
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much smaller. Similarly, the vigorous P. trichocarpa root
growth differed from the poor root growth of P. deltoides [34],
while the hybrids between P. trichocarpa and P. deltoides
showed intermediate root growth characteristics. The hy-
brids’ fine root production ranged between 1.0 and
5.0 tonne ha�1 year�1 [35]. Thus, interclonal differences in fine
root production occur in the genus Populus. Compared with
other tree species, fine roots of poplar are long, relatively
unbranched and very thin. In addition, species within the
genus Populus have very similar fine root morphology and
anatomy [36]. Genotypic variation could be related to the
plasticity of the response to environmental conditions such
as drought, frost or pathogens. Dickmann et al. [31] reported
that clone Eugenei was quite plastic in its above-ground
response to environmental changes, while no below-ground
response was observed. Clone Tristis was just the opposite,
showing only minor above-ground responses, but with major
morphological below-ground responses. This phenomenon
may be related to the competition among clones growing in a
SRC, because this kind of management reduces the fine root
production and induces an immediate increase in mortality
of fine roots, especially after coppicing [31].
4.2. Root profiles
In our study, all clones showed higher values of fine root
biomass in the topsoil layer (0–5 cm). This has also been
shown in other studies on poplar [31,32] and on other genera
[37–40], whereby fine root biomass production was largest in
the upper 15 cm of the soil layer. The differences in fine root
biomass in soil layers could be related to the C inputs via
coarse roots, which could vary with soil depth, nutrient
availability (especially N), microbial activity and soil char-
acteristics such as temperature and moisture [35]. These
latter factors are more dynamic in the topsoil layer and
consequently stimulate the fine root turnover more inten-
sively in the upper soil layers than in the deeper ones [40].
Fine root production is very dynamic in poplar, reaching its
highest rate in summer, which coincided with our sampling
period [15].
Fine RAI and RAD were high in the topsoil layer (0–5 cm). A
number of forest ecosystem studies have reported that fine
roots were most abundant in the uppermost soil layer while
their density steadily decreased with increasing depth [41–43].
On the contrary, the study of Lopez et al. [44] showed that root
distribution of Holm oak growing in a Mediterranean forest
was higher at the 10–20 cm soil depth than at the topsoil
horizon of 0–10 cm.
4.3. Relationships among traits
Fine root length of diameter class 1 was highest in all clones
and at all soil layers, followed by the length of root diameter
class 2. Clones with high root biomass had higher root length
in the different diameter classes, because of the positive
correlation between fine root biomass and fine root length.
Many studies conducted on fine roots have arbitrarily defined
roots with o2 mm as fine roots assuming that all roots within
this diameter category act in a similar manner. In reality,
poplar roots o2 mm in diameter can include new roots,
Please cite this article as: Al Afas N, Marron N, Zavalloni C, Ceulculture of poplar—IV: Fine root characteristics of fivej.biombioe.2007.11.007
D PROOF
suberised roots and woody roots [15]. Fine root production
and mortality are highly dynamic and often simultaneous
[35,45,46]. The positive correlation between fine root length
and N concentration can be explained by the general
importance of N for growth.
RAI is comparable to LAI in terrestrial ecosystems, and is in
most systems substantially larger [47]. In this study, fine RAI
correlated positively with LAI. Thus, clones with high LAI had
high RAI. Moreover, fine RAI in the present study was in the
range reported by Larcher [48], but it was higher than the RAI
values of 0.01–0.4 (for roots o5 mm in diameter) reported by
Addington et al. [49] for pine trees growing in xeric and mesic
habitats. Along the same line, RAI values estimated for
Belgian beech and spruce forests were 6.8 and 5.4 m2 m�2
for fine roots o5 mm in diameter, with fine roots o1 mm in
diameter comprising 85–90% of total RAI [50].
In SRC the root system is of major importance for regrowth
and production of the culture after each rotation cycle. It is
evident that the coarse roots play a dominant role in this
regrowth after coppice. However, to maximise growth and
production of the culture, e.g. for bio-energy purposes, an
optimal nutrient and water supply to the leaves and the
above-ground plant organs are crucial. This nutrient and
water supply depends on the root exploration by fine and
small roots. An improved knowledge of the characteristics of
fine roots as provided by this study is therefore necessary.
Furthermore, the C consumption by the short-living fine roots
is a very important aspect of the C balance of an SRC
plantation.
In conclusion, our study confirmed that clonal as well as
profile variations of fine root traits exist in an SRC plantation.
All root traits exhibited highest values in the topsoil layer
(0–5 cm). Positive correlations were found among fine root
biomass, N concentration and root length. Moreover, the
above-ground biomass could not be considered as a relevant
indicator of fine root biomass, possibly because of the smaller
dependence of above-ground from below-ground character-
istics due to the age of the plantation (stump age of 10 years).
Two strategies were recognised among the five poplar clones:
clones with high root density and high LAI (clones Primo and
Wolterson), and clones with low fine root density and low LAI
(clone Hazendans). LAI was a reliable indicator of fine RAI.
Further root studies are necessary to extrapolate these
conclusions to more poplar clones and over different rota-
tions of SRC.
Acknowledgements
This study was supported by a research contract of the
Province of Antwerp. The project was carried out in close
cooperation with Eta-com B., who supplied the grounds and
part of the infrastructure, and with the logistic support of the
city council of Boom. All plant materials were kindly provided
by the Research Institute for Nature and Forestry (INBO,
Geraardsbergen) and by Forest Research of the Forestry
Commission (UK). We are grateful to Zakareya Hleibie and
Ine Pauwels for help with field data collection, to Fred
Kockelbergh for image analysis, to Nadine Calluy for nitrogen
and carbon analysis, and to Ivan Janssens and Jan Cermak for
emans R. Growth and production of a short-rotation coppicepoplar.... Biomass and Bioenergy (2007), doi:10.1016/
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critical comments on an earlier version of the manuscript.
The first author was supported by a fellowship from the
Syrian University (Al Baath).
R E F E R E N C E S
[1] Amthor JS. Evolution and applicability of a whole plantrespiration model. Journal of Theoretical Biology1986;122:473–90.
[2] Lambers H, Chapin III FS, Pons TL. Plant physiologicalecology. 1st ed. New York: Springer; 2000. p. 540.
[3] Chen X, Eamus D, Hutley LB. Seasonal patterns of fine rootproductivity and turnover in a tropical savanna of northernAustralia. Journal of Tropical Ecology 2004;20:221–4.
[4] Pregitzer KS, Zak DR, Curtis PS, Kubiske ME, Teeri JA, VogelCS. Atmospheric CO2, soil nitrogen and turnover of fine roots.New Phytologist 1995;129:579–85.
[5] Kozlowski TT, Pallardy SG. Physiology of woody plants. 2nded. San Diego: Academic Press; 1997. p. 411.
[6] Persson H. Methods of studying root dynamics in relation tonutrient cycling. In: Harrison AF, Ineson P, Heal OW, editors.Nutrient cycling in terresterial ecosystems. Field methods,application and interpretation. London, New York: ElsevierApplied Science; 1990. p. 198–217.
[7] Kramer PJ, Kozlowski TT. Physiology of woody plants. NewYork: Academic Press; 1979. p. 811.
[8] Hendricks JJ, Nadelhoffer KJ, Aber JD. Assessing the role offine roots in carbon and nutrient cycling. Tree 1993;8:174–8.
[9] Zsuffa L, Giordano E, Pryor LD, Stettler RF. Trends in poplarculture: some global and regional perspective. In: Stettler RF,Bradshaw HD, Heilman PE, Hinckley TM, editors. Biology ofPopulus and its implications for management and conserva-tion. Ottawa: NRC Research Press, National Research Councilof Canada; 1996. p. 515–39.
[10] Ceulemans R. Genetic variation in functional and structuralproductivity determinants in poplar. Amsterdam, The Neth-erlands: Thesis Publishers; 1990. p. 100.
[11] Al Afas N, Pellis A, Niinemets U, Ceulemans R. Growth andproduction of a short rotation coppice culture of poplar. II.Clonal and year-to-year differences in leaf and petiolecharacteristics and stand leaf area index. Biomass andBioenergy 2005;28:536–47.
[12] Al Afas N, Marron N, Ceulemans R. Clonal variation instomatal characteristics related to biomass production undershort rotation coppice culture. Environmental and Experi-mental Botany 2006;58:279–86.
[13] Monclus R, Dreyer E, Delmotte FM, Villar M, Delay D,Boudouresque E, et al. Productivity, leaf traits and carbonisotope discrimination in 29 Populus deltoides� P. nigra clones.New Phytologist 2005;167:53–62.
[14] Marron N, Ceulemans R. Genetic variation of leaf traitsrelated to productivity in a Populus deltoides� Populus nigrafamily. Canadian Journal of Forest Research 2006;36:390–400.
[15] Pregitzer KS, Friend AL. The structure and function of Populusroot systems. In: Stettler RF, Bradshaw HD, Heilman PE,Hinckley TM, editors. Biology of Populus and its implicationsfor management and conservation. Ottawa: NRC ResearchPress, National Research Council of Canada; 1996. p. 331–54.
[16] Friend AL, Scarascia-Mugnozza G, Isebrands JG, Heilman PE.Quantification of two-year-old hybrid poplar root systems:morphology, biomass, and 14C distribution. Tree Physiology1991;8:109–19.
[17] Nguyen PV, Dickmann DI, Pregitzer KS, Hendrick R. Late-season changes in allocation of starch and sugar to shoots,coarse roots, and fine roots in two hybrid poplar clones. TreePhysiology 1990;7:95–105.
Please cite this article as: Al Afas N, Marron N, Zavalloni C, Ceulculture of poplar—IV: Fine root characteristics of fivej.biombioe.2007.11.007
ED PROOF
[18] Pregitzer KS, Dickmann DI, Hendrick R, Nguyen PV. Whole-tree carbon and nitrogen partitioning in young hybridpoplars. Tree Physiology 1990;7:79–93.
[19] Hinckley TM, Ceulemans R, Dunlap JM, Figliola A, HeilmanPE, Isebrands JG, et al. Physiological, morphological andanatomical components of hybrids vigour in Populus. In:Kreeb KH, Richter H, Hinckley TM, editors. Structural andfunctional responses to environmental stresses. The Hague,The Netherlands: SPB Academic Publishing; 1989. p. 199–217.
[20] Heilman PE, Ekuan G, Fogle D. Above- and belowgroundbiomass and fine roots of 4-years-old hybrids of Populustrichocarpa� Populus deltoides and parental species in a short-rotation culture. Canadian Journal of Forest Research1994;24:1186–92.
[21] Deraedt W, Ceulemans R. Clonal variability in biomassproduction and conversion efficiency of poplar during theestablishment year of a short rotation coppice culture.Biomass and Bioenergy 1998;15:391–8.
[22] Deraedt W, Ceulemans R. Production physiology and growthpotential of poplars under short-rotation forestry culture.Forest Ecology and Management 1999;121:9–23.
[23] Laureysens I, Deraedt W, Indeherberge T, Ceulemans R.Population dynamics in a six-year old coppice culture ofpoplar. I. Clonal differences in stool mortality, shootdynamics and shoot diameter distribution in relation tobiomass production. Biomass and Bioenergy 2003;24:81–95.
[24] Laureysens I, Bogaert J, Blust R, Ceulemans R. Biomassproduction of 17 poplar clones in a short rotation coppiceculture on a waste disposal site and its relation to soilcharacteristics. Forest Ecology and Management2004;187:295–309.
[25] Laureysens I, Pellis A, Willems J, Ceulemans R. Growth andproduction of a short rotation coppice culture of poplar. III.Second rotation results. Biomass and Bioenergy2005;29:10–21.
[26] Al Afas N, Marron N, Ceulemans R. Variability in Populus leafanatomy and morphology in relation to canopy position,biomass production, and varietal taxon. Annals of ForestScience 2007;64:521–32.
[27] Armstrong A. United Kingdom network of experiments onsite/yield relationships for short rotation coppice. Edinburgh,UK: Forestry Commission Research Information, ForestryCommission; 1997 Note 294.
[28] Zavitkovski J. Structure and seasonal distribution of litterfallin young plantations of Populus ‘Tristis-1’. Plant and Soil1981;60:409–22.
[29] Vogt KA, Persson H. Measuring growth and development ofroots. In: Lassoie JP, Hinckley TM, editors. Techniques andapproaches in forest ecophysiology. Boca Raton, FL: CRCPress; 1991. p. 477–501.
[30] Pallardy S, Kozlowski TT. Early root and shoot growth ofPopulus clones. Silvae Genetica 1979;28:153–6.
[31] Dickmann DI, Nguyen PV, Pregitzer KS. Effects of irrigationand coppicing on above-ground growth, physiology, and fineroot dynamics of two field-grown hybrid poplar clones.Forest Ecology and Management 1996;80:163–74.
[32] Lukac M, Calfapietra C, Godbold DL. Production, turnover andmycorrhizal colonization of root systems of three Populusspecies grown under elevated CO2 (POPFACE). Global ChangeBiology 2003;9:838–48.
[33] Pellis A, Laureysens I, Ceulemans R. Genetic variation of thebud and leaf phenology of seventeen poplar clones in a shortrotation coppice culture. Plant Biology 2004;6:38–46.
[34] Dickmann DI, Stuart KW. The culture of poplars in easternNorth America. East Lansing, MI: Michigan State UniversityPublications; 1983. 168p.
emans R. Growth and production of a short-rotation coppicepoplar.... Biomass and Bioenergy (2007), doi:10.1016/
1
3
5
7
9
11
13
15
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21
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25
27
29
31
33
35
37
39
41
43
45
47
49
ARTICLE IN PRESSJBB : 1470
B I O M A S S A N D B I O E N E R G Y ] ( ] ] ] ] ) ] ] ] – ] ] ] 9
[35] Block RMA, Van Rees KCJ, Knight JD. A review of fine rootdynamics in Populus plantations. Agroforestry System2006;67:73–84.
[36] Brundrett M, Murase G, Kendrick B. Comparative anatomy ofroots and mycorrhizae of common Ontario trees. CanadianJournal of Botany 1990;68:551–78.
[37] Friend AL, Jifon JL, Berrang PC, Seiler JR, Mobley JA. Elevatedatmospheric CO2 and species mixture alter N acquisition oftrees in stand microcosms. Canadian Journal of ForestResearch 2000;30:827–36.
[38] Janssens IA, Sampson DA, Curiel-Yuste J, Carrara A, Ceule-mans R. The carbon cost of fine root turnover in a Scots pineforest. Forest Ecology and Management 2002;168:231–40.
[39] Konopka B, Curiel-Yuste J, Janssens IA, Ceulemans R.Comparsion of fine root dynamics in Scots pine andpedunculate oak in sandy soil. Plant and Soil 2005;276:33–45.
[40] Konopka B, Noguchi K, Sakata T, Takahashi M, Konopkova Z.Fine root dynamics in a Japanese cedar (Cryptomeria japonica)plantation throughout the growing season. Forest Ecologyand Management 2006;225:278–86.
[41] Joslin JD, Henderson GS. Organic matter and nutrientsassociated with fine root turnover in a white oak stand.Forest Science 1987;33:330–46.
[42] Hendrick RL, Pregitzer KS. Temporal and depth-relatedpatterns of fine root dynamics in northern hardwoodforests. Journal of Ecology 1996;84:167–76.
[43] Steele SJ, Gower ST, Vogel JG, Norman JM. Root mass, netprimary production and turnover in aspen, jack pine and
UNCORRECTE
Please cite this article as: Al Afas N, Marron N, Zavalloni C, Ceulculture of poplar—IV: Fine root characteristics of fivej.biombioe.2007.11.007
OF
black spruce forests in Saskatchewan and Manitoba, Canada.Tree Physiology 1997;17:577–8.
[44] Lopez B, Sabate S, Gracia CA. Vertical distribution of fine rootdensity, length density, area index and mean diameter in aQuercus ilex forest. Tree Physiology 2001;21:555–60.
[45] Finer L, Messier C, De Grandpre L. Fine root dynamics inmixed boreal conifer–broad forest stands at different suc-cessional stages after fire. Canadian Journal of ForestResearch 1997;27:304–14.
[46] Cote B, Hendershot WH, Fyles JW, Roy AG, Bradley R, BironPM, et al. The phenology of fine root growth in a maple-dominated ecosystem: relationships with some soil proper-ties. Plant and Soil 1998;201:59–69.
[47] Jackson RB, Mooney HA, Schulze E-D. A global budget for fineroot biomass, surface area, and nutrient contents. Proceed-ings of the National Academy of Sciences of the UnitedStates of America 1997;94:7362–6.
[48] Larcher W. Physiological plant ecology. 4th ed. Berlin–Hei-delberg–New York: Springer; 2003. 513p.
[49] Addington RN, Donovan LA, Mitchell RJ, Vose JM, Pecot SD,Jack SB, et al. Adjustments in hydraulic architecture of Pinuspalustris maintain similar stomatal conductance in xeric andmesic habitats. Plant, Cell and Environment 2005;29:535–45.
[50] Van Praag HJ, Sougnez-Remy S, Weissen F, Carletti G. Rootturnover in a beech and a spruce stand of the BelgianArdennes. Plant and Soil 1988;105:87–104.
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