Tree Physiology 23, 505–516
© 2003 Heron Publishing—Victoria, Canada
Above- and belowground biomass and net primary production in a
73-year-old Scots pine forest
CHUN-WANG XIAO,1,2 J. CURIEL YUSTE,1 I. A. JANSSENS,1 P. ROSKAMS,3
L. NACHTERGALE,4 A. CARRARA,1 B. Y. SANCHEZ1 and R. CEULEMANS1,5
1
Department of Biology, Research Group of Plant and Vegetation Ecology, University of Antwerpen (UIA), Universiteitsplein 1, B-2610 Wilrijk, Belgium
2
Present address: Laboratory of Quantitative Vegetation Ecology, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China
3
Institute for Forestry and Game Management (IBW), Ministry of the Flemish Community, Gaverstraat 4, B-9500 Geraardsbergen, Belgium
4
Laboratory for Forestry, University of Ghent (RUG), Geraardsbergsesteenweg 267, B-9090, Gontrode- Melle, Belgium
5
Author to whom correspondence should be addressed ([email protected])
Received August 13, 2002; accepted November 9, 2002; published online May 1, 2003
Summary We estimated above- and belowground biomass
and net primary production (NPP) of a 73-year-old Scots pine
(Pinus sylvestris L.) forest stand in the Belgian Campine region. Total biomass for the stand was 176 Mg ha –1, of which
74.4% was found in stems. The root system contained 12.6% of
total biomass, most of it in coarse roots (> 5 mm). Fine roots
(< 5 mm) comprised only about 1.7% of total biomass, and
more than 50% of fine root biomass was retrieved in the litter
layer and the upper 15 cm of the mineral soil. The ratio of
belowground biomass to aboveground biomass was 0.14,
which is lower than that of other Scots pine forests and other
coniferous forests. Between 1995 and 2001, mean annual NPP
was 11.2 Mg ha –1 year –1, of which 68.7% was allocated to
aboveground compartments. Stems, needles and cones made
relatively high contributions to total NPP compared with
branches. However, branch NPP was possibly underestimated
because litterfall of big branches was neglected. The proportion of total NPP in belowground components was 31.3%.
Coarse root NPP (2% of total) was low compared with its biomass. Fine root NPP was 3.3 Mg ha –1 year –1, representing
about 29.5% of total NPP; however, the estimate of fine root
NPP is much more uncertain than NPP of aboveground compartments. The ratio NPP/GPP (gross primary production) was
0.32, which was low compared with other coniferous forests.
Keywords: allometric relationships, biomass distribution, fine
roots, NPP/GPP ratio, Pinus sylvestris, root system.
Introduction
Global climate change has inspired an increasing interest in
global carbon storage and carbon balance (Landsberg et al.
1995). Evaluation of the role of terrestrial ecosystems in the
global carbon budget and their responses to climatic changes
requires a detailed understanding of the underlying ecosystem
processes and a methodology to integrate the interactions between these processes (Cao and Woodward 1998). Primary
production is the main force driving the functioning of ecosystems, providing resources for a diversity of consumers, as well
as participating in the regulation of the global climate through
the carbon and water cycles (Roy and Saugier 2001). The increasing interest in a better understanding and quantification
of the carbon cycle of forest ecosystems has resulted in several
recent reviews on net primary production (NPP) (Vogt et al.
1996, Cao and Woodward 1998, Cramer and Field 1999,
Gower et al. 2001, Nakane 2001, Roy et al. 2001).
Forests contain about 90% of the carbon stored in terrestrial
vegetation, and account for about 40% of carbon exchange
between the atmosphere and the terrestrial biosphere
(Schlesinger 1997). Scots pine (Pinus sylvestris L.) is the most
widely distributed of the pines and one of the most important
timber species in Eurasia (Stanners and Bourdeau 1995,
Oleksyn et al. 2002). Its natural range extends from Spain in
the west (5° W) to northern Manchuria and the Sea of Okhotsk
(130° E) in the east and from 70° N in northern Scandinavia to
38° N in Turkey (Oleksyn et al. 2002). Because Scots pine forests cover 24% of the total forested area (75 million km 2 ), they
are a key component of Europe’s carbon budget (Stanners and
Bourdeau 1995).
The study of biomass and net primary production in Scots
pine could lead to improved models of carbon budgets and
fluxes in forest ecosystems. Recent studies on Scots pine have
mainly focused on biomass distribution (Breymeyer et al.
1996, Vanninen et al. 1996, Regina et al. 1997, Janssens et al.
1999, Vanninen and Mäkelä 1999, Ilvesniemi and Liu 2001),
with only a few studies reporting both above- and belowground NPP (Malkönen 1974, Nilsson and Albrektson 1993,
Gower et al. 1994, Helmisaari et al. 2002, Wirth et al. 2002).
Fine root production is seldom reported, mainly because of
practical difficulties in recovering fine roots and the poor
reproducibility of the data. A complete inventory of both biomass distribution and NPP of stems, branches, needles, cones,
coarse roots and fine roots has rarely been undertaken for
Scots pine forests.
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XIAO ET AL.
Our primary objective was to determine the NPP and the
amount of above- and belowground biomass of a 73-year-old
Scots pine forest in northern Belgium. We also compared the
observed distribution patterns of biomass and NPP with those
of other pine forests. The second objective was to obtain basic
data and parameters of each biomass component and of NPP to
assess the carbon balance of the Scots pine forest.
Materials and methods
Study site description
The study was carried out in an even-aged, 2-ha Scots pine
stand, representing a portion of the 150-ha mixed coniferous–deciduous De Inslag forest. The forest is located in Brasschaat, in the Campine region of the province of Antwerpen,
Belgium (51°18′3″ N and 4°31′14″ E, altitude 16 m a.s.l, orientation NNE; de Pury and Ceulemans 1997). The stand is part
of the European CARBO-EUROFLUX network (http://www.
bgc.mpg.de/public/carboeur/) and is a level-II observation plot
of the European program for intensive monitoring of forest
ecosystems (EU/ICP Forests) managed by the Institute for
Forestry and Game Management, Flanders, Belgium.
The site is almost flat (slope 0.3%) and belongs to the plateau of the northern lower plain basin of the Scheldt River. The
climate at the site is moist subhumid, rainy and mesothermal.
Long-term (30-year average) mean annual and growing season temperatures at the site are 9.8 and 13.7 °C, respectively.
Mean temperatures of the coldest and warmest months are 3
and 18 °C, respectively. Mean annual and growing season precipitation are 767 and 433 mm, respectively. Mean annual and
growing season potential evapotranspiration values are 670
and 619 mm, respectively (Èermák et al. 1998). The site has a
moderately wet sandy soil with a distinct humus or iron B-horizon, or both (Baeyens et al. 1993), characterized as psammentic haplumbrept in the USDA classification, and umbric
regosol in the FAO classification. The upper soil layer is about
1.8 m thick and consists of aeolian northern Campine cover
sand (Dryas III). Beneath this sand layer, at a depth between
1.5 and 2 m, lies a shallow clay layer (Tiglian) and below this
is another sand layer (sand of Brasschaat, Pretiglian; Baeyens
et al. 1993). The soil is typically moist, but rarely saturated because of the high hydraulic conductivity of the upper sandy
layers. A detailed report of the physical and chemical properties of the topsoil is presented by Roskams et al. (1997) and
Janssens et al. (1999).
The original climax vegetation in the area was a Querceto–
Betuletum (Tack et al. 1993). The experimental Scots pine
stand was planted in 1929, and was 73 years old at the time of
the present study (i.e., 2001). The forest canopy is sparse, with
a projected leaf area index (LAI) in 1997 between 1.9 in late
spring (before bud burst) and 2.4 in early autumn before leaf
fall (Gond et al. 1999). Scots pine trees at the study site have
only two needle classes (current-year and 1-year-old needles;
Janssens et al. 1999). Needle concentrations of magnesium
and phosphorus were low (Van den Berge et al. 1992, Roskams
et al. 1997); however, needle nitrogen concentrations were
high (> 2% in current-year needles; Roskams and Neirynck
1999), probably because the site is located in an area with high
NOx and ammonia deposition (30–40 kg ha –1 year –1; Neirynck
et al. 1999, 2002).
Forest inventories and thinning
The spring 1995 forest inventory data were reported by
Èermák et al. (1998). Although they reported a standing stock
of 542 trees ha –1, a thorough revision of their data resulted in a
tree density in 1995 of 538 trees ha –1.
New detailed forest inventories were made in winter 2000–
2001 and winter 2001–2002, and included measurements of
stem diameter at base and at breast height (DBH, at 1.30 m
above ground), and tree height to the top and to the base of the
crown (i.e., the lowest green whorl). In total, 749 trees were
measured in the 2-ha stand and divided into five categories
(dominant, co-dominant, sub-dominant and suppressed trees)
based on tree height and number of dead trees.
The difference in standing stock between the inventories of
1995 and 2000–2001 was ascribed to the thinning in November 1999. In 1999, 162.5 trees ha –1 were harvested, the DBH of
the harvested trees was immediately measured on 140 trees
ha –1, and this mean DBH was extrapolated to the 22.5 unmeasured trees ha –1. The thinning was done because of poor site
management in the past, and it was mainly suppressed trees
that were removed. In July 2001, 1 tree ha –1 was removed because of dangerous inclination and its DBH was immediately
measured.
Aboveground biomass
Aboveground biomass was defined as the sum of dry mass of
stems, branches, needles and cones of all Scots pine trees in
the stand. In February 2002, nine trees (three dominant/codominant, three sub-dominant and three suppressed individuals) were selected for harvest to estimate stand biomass. The
trees were selected as follows. First, trees in each dominance
class were sorted by DBH. Then, the trees in each dominance
class were separated into three groups based on DBH, and the
mean DBH for each group was calculated. Finally, we selected
the individual tree whose DBH was closest to the mean of its
group. The selected trees were harvested and the crown separated from the main stem. For each sample tree, stem diameter
was measured from the base to the top at 1-m intervals, as well
as at breast height. Total tree height and depth of live crown
were also measured. Stem volume of the sample trees was calculated by summing the volume of the 1-m sections, which
were calculated from their upper and lower diameters assuming a truncated-cone shape. Stem biomass was calculated by
multiplying stem volume and stem density. Density of woody
samples was determined from the dry mass to fresh volume ratio. Stem density was determined in 1997 for three trees: one
dominant, one sub-dominant and one suppressed tree. From
each tree, samples were taken at one-fourth, one-third, half
and two-thirds of total height, at four different orientations
(north, east, south and west) at each height as well as in the
middle. These 20 density measurements per tree were aggre-
TREE PHYSIOLOGY VOLUME 23, 2003
BIOMASS AND NET PRIMARY PRODUCTION OF SCOTS PINE
gated using a weighted average (weighted according to the
volume taken in by each subsector). Overall mean stem density was estimated as the mean density of the three trees and
was 0.502 Mg m –3 (Janssens et al. 1999).
Branch and needle biomass of the sample trees was estimated as follows. First, total fresh mass of the entire tree
crown (including all branches and needles) was determined in
situ for each harvested tree. Then, for each tree, two to four
branches were selected randomly from upper, middle and bottom positions in the crown (8–10 branches per tree). Each
sample branch was labeled, weighed and then separately transferred to the laboratory in plastic bags. All needles were subsequently removed and separated into current-year needles and
1-year-old needles. Fresh mass of branches and both types of
needles was measured for each branch separately, and their
overall mean mass ratios were used to separate the in situ determined total fresh crown mass into branch, current-year
needles and 1-year-old needles. Dry biomass of each pool was
calculated by substracting the measured mass lost during drying (3 days at 75 °C) from the fresh mass. Tree characteristics
and biomass of the different compartments of nine trees are
given in Table 1.
Allometric relationships were established between stem,
branch and needle biomass (both age classes) and several tree
characteristics: DBH, tree height (H), crown length (CL),
DBH2 × height (DBH2H), and DBH2 × crown length
(DBH2CL) (Table 2). Allometric relationships of stem biomass with DBH, H and DBH2H, and the relationships of biomass of branches and needles with DBH, H, DBH2H and
DBH2CL showed a highly significant correlation (P < 0.001,
Table 2). The relationships were weaker for regressions with
CL (P < 0.01, Table 2). Because only the allometric relationships with DBH were consistently good (adjusted R 2 highest
or very close), and because DBH is easy to measure, we used
the biomass–DBH relationships to estimate biomass at the
stand level (Figure 1 and Table 2). Stem, branch and needle
biomass was scaled-up to the stand level by combining these
allometric relationships with the DBH inventory of the entire
stand.
Cone biomass was not measured. However, Helmisaari et al.
(2002) reported that cone biomass in Scots pine was similar to
507
cone NPP. We therefore assumed that cone biomass equalled
cone litterfall mass.
Belowground biomass
For coarse root (> 5 mm) biomass, we used the experimental
data obtained from four trees excavated in 1997 (Janssens et al.
1999) to establish a site-specific allometric relationship between DBH and coarse root (> 5 mm) biomass (Figure 1 and
Table 2). This allometric relationship was statistically significant (P < 0.05, Table 2), but because coarse root biomass was
not measured for the tallest trees, scaling with the allometric
relationship will be uncertain for the taller trees. Despite this
uncertainty, stand-level coarse root biomass was determined
based on this allometric relationship and the forest inventory
data.
Fine root (< 5 mm) biomass was determined in early March
2002 (when live root biomass was probably minimal) by core
sampling (Roberts 1976) to a depth of 90 cm. Soil samples
were taken at four to six distances from the nine harvested
trees (10, 50, 100, 200, 300 and 400 cm). A total of 39 sample
columns were excavated with a sharp-edged metal cylinder
(inner diameter of 15 cm) for litter columns and a soil corer
(inner diameter of 8 cm) for soil columns. Thus, only about
0.003% of the surface area was sampled for root biomass determination. Samples from different depths (surface litter,
0–5, 5–15, 15–30, 30–45, 45–60 and 60–90 cm) were labeled
and stored at –20 °C until processed. Fine roots were manually
removed from the soil sample, washed and sorted into three diameter classes (< 1, 1–2 and 2–5 mm). Live and dead root
fragments were subsequently separated by visual inspection as
described by Persson (1980) and Vogt and Persson (1991), i.e.,
the xylem of dead roots looks darker and deteriorated, the degree of cohesion between the cortex and the periderm decreases, and root tips become brittle and less resilient. Dry biomass was determined after oven-drying at 75 °C for 2–3 days.
Samples were taken at fixed distances from the nearest tree,
but because no relationship was observed between root biomass and the distance to the nearest tree, stand-level biomass
was estimated from the mean of all samples.
Table 1. Tree characteristics and biomass of different parts of nine 73-year-old Scots pine trees sampled in February 2002. Abbreviation: DBH =
diameter at breast height.
DBH
(cm)
Tree height
(m)
Crown length
(m)
Stem biomass
(kg)
Branch biomass
(kg)
Total
needle biomass
(kg)
Current-year
needle biomass
(kg)
One-year-old
needle biomass
(kg)
22.0
22.8
23.0
25.8
26.5
28.6
30.9
33.5
39.5
18.6
18.7
19.0
21.0
21.1
21.5
22.8
22.6
24.5
3.3
3.0
3.4
3.7
5.0
5.2
4.7
6.3
5.5
159.7
172.0
177.3
241.3
255.3
301.1
368.5
428.5
636.5
16.67
15.51
17.99
18.70
35.56
36.70
58.27
64.41
94.02
4.220
3.877
4.497
6.047
7.348
6.980
11.446
12.772
15.569
2.660
2.713
3.101
4.236
4.690
4.761
7.778
8.469
10.020
1.560
1.164
1.396
1.811
2.658
2.219
3.668
4.303
5.549
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Table 2. Regression coefficients of the allometric relationships between different parameters and biomass (kg tree –1) of the different compartments for the harvested Scots pine trees. The allometric relationship was adopted as a power-form equation, y = ax b with R 2adj = adjusted multiple
coefficient of determination. The symbols of parameters (x) are as follows: DBH = stem diameter at the breast height (cm); H = tree height (m);
and CL = crown length (m). Allometric relationships were based on nine sample trees (n = 9), except for the assessment of coarse roots (n = 4).
Significance level: ** = P < 0.01 and *** = P < 0.001.
Parameter (y)
Parameter (x)
Coefficients
a
b
R 2adj
Stem biomass
DBH
H
DBH2H
0.1227
2.11 × 10 –5
0.0253
2.3272
5.3743
0.9601
0.9988 ***
0.9607 ***
0.9999 ***
Branch biomass
DBH
H
CL
DBH2H
DBH2CL
0.0022
1.66 × 10 –8
1.6429
0.0003
0.0064
2.9123
7.0279
2.0958
1.2074
1.0542
0.9461 ***
0.9399 ***
0.5861 ***
0.9430 ***
0.9256 ***
Total needle biomass
DBH
H
CL
DBH2H
DBH2CL
0.0045
8.99 × 10 –7
0.6536
0.0010
0.0126
2.2372
5.2226
1.6639
0.9240
0.7848
0.9267 ***
0.9335 ***
0.6375 **
0.9240 ***
0.9165 ***
Current-year needle biomass
DBH
H
CL
DBH2H
DBH2CL
0.0039
1.1 × 10 –6
0.4735
0.0009
0.0109
2.1536
5.0268
1.6093
0.8896
0.7530
0.9142 ***
0.9311 ***
0.6332 **
0.9113 ***
0.9020 ***
One-year-old needle biomass
DBH
H
CL
DBH2H
DBH2CL
0.0008
8.56 × 10 –8
0.1848
0.0002
0.0024
2.4071
5.6284
1.7716
0.9943
0.8505
0.9304 ***
0.9191 ***
0.6295 **
0.9245 ***
0.9203 ***
Coarse root biomass
DBH
0.3399
1.4728
0.9040 ***
Net primary production
Net primary production (NPP) was calculated by combining
changes in standing biomass between spring 1995 and winter
2001–2002, biomass removed during the thinning in 1999
(plus one tree per hectare in 2001), and mean litterfall in the
periods 1996–1997 and 1999–2001. We determined the difference in standing biomass between 1995 and 2001 (seven
growing seasons) based on the allometric relationships described above and the forest inventory data from 1995 and
2001. Biomass removed during thinning was estimated by applying the same allometric relationships and the DBH data
from harvested trees in 1999 and 2001. Litterfall was measured in 1996, 1997, 1999, 2000 and 2001 with randomly
placed collectors with nylon-mesh netting. In 1996, 1997 and
2001, 10 collectors (surface area of 0.3 m 2) were used; in 1999
and 2000, 10 collectors each with a surface area of 0.2 m2 were
used. Thus the sampling area in proportion to the plot area for
litterfall is about 0.01–0.015%. All litter was dried and sorted
into branches, needles and reproductive organs. In the years
that we did not measure litterfall (1995 and 1998), branch and
cone litterfall were estimated as the mean of the other years before thinning. In 2001, litter was not separated into the differ-
ent fractions, and branch and cone litterfall were estimated
from total litterfall, assuming the same relative proportions as
observed in 2000.
Specifically, mean NPP of stems was calculated as:
SNPP1995 – 2001 = (B2001 − B1995 + BH1999 + BH 2001 ) / 7 (1)
SNPP2001 = (B2001 − B2000 + BH 2001 )
(2)
where SNPP1995–2001 is mean annual stem NPP from 1995 to
2001, SNPP2001 is annual stem NPP in 2001, B2001 and B2000 are
stem biomass at the end of 2001 and 2000, respectively, B1995 is
stem biomass in spring 1995, BH1999 is stem biomass harvested in 1999, and BH2001 is stem biomass harvested in 2001.
Litterfall of stem bark was ignored because it was very small.
The NPP of branches was calculated as the sum of the difference in standing branch biomass and branch biomass removed
at thinning (both estimated from allometric relationship and
forest inventories) plus branch litterfall. However, litterfall of
big branches (not collected by litter traps) was neglected.
The NPP of needles was estimated from the allometric relationship between current-year needles and DBH, and the stand
inventory data. Needle NPP before thinning was assumed
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BIOMASS AND NET PRIMARY PRODUCTION OF SCOTS PINE
509
Figure 1. Biomass of stems (upper
panel), branches, coarse roots (middle
panel) and needles (bottom panel) in
relation to diameter at breast height
(DBH) for nine harvested Scots pine
trees. Biomass of coarse roots was
measured on only four trees. Parameters of the different regression lines,
used for scaling-up to the stand level,
are listed in Table 2.
equal to that in 1995, and needle NPP after thinning was assumed equal to the estimate of 2001. The NPP of cones was assumed to equal mean cone litterfall and was calculated
similarly to needle NPP.
The NPP of coarse roots was estimated as the sum of
changes in standing coarse root biomass and estimated coarse
root biomass that died during the thinning in 1999 and 2001
(both based on allometric relationship and forest inventory).
We assumed no mortality of coarse roots.
The NPP of fine roots (< 5 mm) was estimated differently
from the NPP of coarse roots. Before the thinning, fine root
NPP was assumed equal to that measured in 1997 by a modified in-growth coring method (Janssens et al. 2002). After
thinning, fine root NPP was estimated by multiplying standing
fine root biomass with the fine root turnover rates measured
before thinning (Aber et al. 1985). Based on fine root biomass
and production data from Janssens et al. (1998, 2002), we calculated turnover rates of roots < 1, 1–2 and 2–5 mm to be 0.98,
0.37 and 0.25 year –1, respectively.
Aboveground net primary production (ANPP) was deter-
mined as the sum of stem, branch, needle and cone NPP.
Belowground net primary production (BNPP) was determined
as the sum of coarse root (> 5 mm) NPP and fine root (< 5 mm)
NPP.
Statistical analysis
A nonlinear least squares fitter (STATISTICA V.5, StatSoft,
Tulsa, OK) was used to determine allometric relationships between biomass of stems, branches, needles and coarse roots
and DBH, tree height and tree crown length. The paired t-test
was used to detect significant differences in biomass between
root diameter classes.
Results
Forest inventory
Changes in DBH frequency distributions (1995, 2000–2001,
2001–2002) are shown in Figure 2. The reduction in total
number of trees during thinning had the largest effect on the
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510
XIAO ET AL.
Figure 2. Frequency distribution of diameter at breast
height (DBH) classes of the
Scots pine forest at three different times.
smallest DBH classes, mainly because trees with smaller DBH
(< 30 cm) were removed. Frequency distributions were similar
between winter 2000–2001 and winter 2001–2002. Stocking
density in winter 2001–2002 was 374.5 trees ha –1, basal area
of the stand was 27.9 m2, mean DBH was 30 cm, median DBH
was 35.9 cm, and mean tree height was 21.4 m (Figures 2 and
3). The frequency distribution of tree diameter was skewed to
the right (Figure 2). Total basal area per DBH class was high-
Figure 3. Basal area (upper panel) and
mean stem and canopy height (bottom
panel) for diameter at breast height
(DBH) classes of the 73-year-old Scots
pine forest (winter 2001–2002 data).
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BIOMASS AND NET PRIMARY PRODUCTION OF SCOTS PINE
est for the DBH classes with a diameter around 26–32 cm
(Figure 3). The stand canopy was limited to a rather narrow
zone between 13 and 24 m, and green needles were not observed below 7 m. Overall, the mean depth of the canopy was
8.3 m. Larger trees had a deeper canopy than smaller trees
(Figure 3).
Aboveground and belowground biomass
In winter 2001–2002, total tree biomass was 176.4 Mg ha –1
(Table 3). Aboveground biomass totaled 154.1 Mg ha –1 and
contained 87.4% of total tree biomass (Tables 3 and 4). Stem
biomass and branch biomass were 131.2 and 17.8 Mg ha –1,
and contained 74.4% and 10.1% of total biomass, respectively.
Needle biomass was 3.5 Mg ha –1, comprising about 2% of total biomass. About two-thirds of total needle biomass was in
current-year needles and one-third in 1-year-old needles. Cone
biomass was estimated to be 1.6 Mg ha –1, comprising 0.9% of
total biomass.
Total belowground biomass was 22.3 Mg ha –1, and comprised about 12.6% of total biomass (Tables 3 and 4). Coarse
root (> 5 mm) biomass was 6 times larger than fine root (<
5 mm) biomass and amounted to 19.2 Mg ha –1, i.e., about
10.9% of total biomass. Total fine root (< 5 mm) biomass was
3.1 Mg ha –1, and represented 1.7% of total biomass (Tables 3
and 4). Slightly more than 50% of fine root biomass was found
in the litter and the upper 15 cm of the mineral soil. Few fine
roots occurred below 60 cm (Figure 4). The biomass of live
fine roots < 1 mm (1.5 Mg ha –1) was significantly higher than
that of the other two diameter classes of live fine roots, i.e.,
1–2 mm (0.7 Mg ha –1) and 2–5 mm (0.9 Mg ha –1; Table 3 and
Figure 5). Biomass of live roots was significantly higher than
that of dead roots, and the biomass of dead fine roots was similar in the three diameter classes (Figure 5).
511
Net primary production
Total NPP averaged over the 1995–2001 period was 11.2 Mg
ha –1 year –1 (Table 3). About 69% of total NPP was contributed
by aboveground components (7.7 Mg ha –1 year –1). Stems,
needles and cones had higher NPP (2.4, 2.5 and 1.7 Mg ha –1
year –1, respectively) than branches (1.1 Mg ha –1 year –1; Table 3). The proportions of total NPP to stem, branch and cone
NPP were 21.4, 9.8 and 15.2%, respectively (Table 4). Needle
NPP estimated with the allometric relationship (see Materials
and methods) was 2.5 Mg ha –1 year –1, and was similar to the
estimate obtained by summing the difference in standing needle biomass, needle biomass removed during thinning and
needle litterfall (2.6 Mg ha –1 year –1).
Total belowground NPP was 3.5 Mg ha –1 year –1, and comprised about 31.3% of total NPP (Tables 3 and 4). Coarse root
NPP was 0.2 Mg ha –1 year –1, and comprised a relatively low
proportion of total NPP (1.8%) compared with its higher proportion of total biomass (10.9%). Although fine roots represented a smaller proportion of total biomass than coarse roots,
they contributed more to total NPP (3.3 Mg ha –1 year –1, equaling 29.5% of total NPP). Fine root (< 1 mm) NPP was much
larger than that of the other two diameter classes of roots. The
NPP of fine roots in the < 1 mm, 1–2 mm and 2–5 mm classes
was 2.7, 0.3 and 0.3 Mg ha –1 year –1, respectively, and their relative proportions in total NPP were 24.1, 2.7 and 2.7%, respectively (Tables 3 and 4).
Because no forest inventory was made prior to thinning, we
could not estimate pre-thinning NPP directly. However, based
on the two inventories made after the thinning, post-thinning
NPP was estimated to be 8.5 Mg ha –1 year –1, which was 25%
lower than the mean NPP over the entire 7-year period (Table 3). From this, pre-thinning NPP was estimated to be
12.3 Mg ha –1 year –1. Furthermore, we observed a 25% de-
Table 3. Above- and belowground biomass, litterfall and net primary production (NPP) in the 73-year-old Scots pine forest.
Component
Standing biomass (Mg ha –1)
Biomass removed
Mean litterfall (Mg ha –1)
NPP (Mg ha –1 year –1)
1996–1997,
1999
2000–2001
1995–2001 2000–2001
0.8
0.4
2.7
1.7
5.2
2.0
1.6
4.0
at thinning
Stems
Branches
Current-year needles
One-year-old needles
Total needles
Cones
Aboveground total
Coarse roots (> 5 mm)
Fine roots
(2–5 mm)
(1–2 mm)
(< 1 mm)
Belowground total
Forest total
1
2
2001–2002
winter
2000–2001
winter
1995
spring
1999
2001
(Mg ha –1) (kg ha –1)
131.2
17.8
2.3
1.2
3.5
1.6
154.1
19.2
129.9
17.5
2.3
1.2
3.5
1.6
152.5
19.1
146.5
18.7
2.6
1.3
3.9
1.9
171.0
23.5
32.0
3.7
0.6
0.3
0.9
346.0
46.7
6.1
3.1
9.2
36.6
5.8
401.9
51.0
0.9
0.7
1.5
22.3
176.4
1.21
0.81
3.21
28.7
199.7
Data from Janssens et al. (1999) were collected in 1997.
Based on fine root turnover as estimated in 1997.
TREE PHYSIOLOGY ONLINE at http://heronpublishing.com
2.4
1.1
1.7
0.7
2.5
1.7
7.7
0.2
2.3
1.6
6.3
0.2
0.32
0.32
2.72
3.5
11.2
0.22
0.32
1.52
2.2
8.5
512
XIAO ET AL.
Table 4. Relative contributions of different tree compartments to total
standing biomass (2001) and net primary production (NPP) (mean of
1995–2001).
Component
Needles
Cones
Branches
Stems
Coarse roots
Fine roots
(2–5 mm)
(1–2 mm)
(< 1 mm)
Contribution to total (%)
Biomass
NPP
2.0
0.9
10.1
74.4
10.9
22.3
15.2
9.8
21.4
1.8
0.5
0.4
0.8
2.7
2.7
24.1
crease in needle litterfall after thinning compared with before
thinning (Table 3).
Discussion
Biomass distribution
Allometric relationships are commonly used to estimate tree
biomass in forest ecosystems, and involve destructive techniques in combination with the application of regression equations. The best fitting equation is often of the form y = ax b,
where y is biomass and x is tree DBH (Baskerville 1972,
Beauchamp 1973, Sprugel 1983). This method has been used
successfully by several authors (e.g., Canadell et al. 1988,
Rapp et al. 1992, Regina et al. 1997, Kitayama and Itow 1999,
Porté et al. 2002). In our study, all allometric relationships
used were statistically significant and thus provided a simple
but reliable method to estimate biomass of different components of the Scots pine trees.
Total biomass was 176 Mg ha –1 in 2001, which was less than
Figure 4. Vertical distribution of root mass density of live fine roots of
different root size classes in the Scots pine forest. Values represent
means and error bars represent ± SE of the means (n = 39; spring 2002
data).
Figure 5. Biomass of both live (open bars) and dead roots (shaded
bars) of different root size classes in the Scots pine forest. Boxes represent the means, and vertical bars represent ± SE of the means (n =
39; spring 2002 data).
that for the same forest in 1997 (199.7 Mg ha –1; Table 3). This
difference is mainly attributable to the thinning in 1999, which
removed 42.4 Mg ha –1 excluding the biomass of fine roots (Table 3). Aboveground biomass represented about 87.4% of total
biomass (84.5% in woody biomass), which was at the upper
end of the range reported for Scots pine stands (67.2–89.2%;
Gower et al. 1994, Vanninen et al. 1996) and for other pine
species (Knight et al. 1994). We found 74% of total biomass in
stems, which was just within the range reported for Scots pine
stands in Finland (32.3–76.3%; Vanninen et al. 1996). This
high proportion of total biomass in stems indicates that stems
are a large long-term carbon sink in this Scots pine stand.
The importance of roots, especially fine roots, for nutrient
uptake and soil development is well known (Berg 1984, Ruess
et al. 1996, Vanninen and Mäkelä 1999). However, in terms of
biomass, roots are of minor importance. In our study, standing
fine root biomass (< 5 mm) represented only a minor proportion of total biomass (1.7%), and fine root biomass in 2001
was less than in 1997 (Table 3), which was probably mainly a
result of the thinning in 1999. The decrease in standing biomass of fine roots < 1 mm, however, was disproportionally
large compared with the reductions in biomass of all other
compartments. We hypothesize that this large decrease in fine
root biomass is because our fine root data (2002) were
collected in early March before the onset of the growing season, whereas the data for 1997, which were obtained by
Janssens et al. (1999), are mean values estimated from minimum and maximum biomass. The large seasonality of fine
root biomass, as well as the interannual variability could thus
contribute to the disproportionally large decrease in fine root
biomass (Persson 1978, Santantonio and Hermann 1985,
Makkonen and Helmisaari 1998, Vanninen and Mäkelä 1999).
Furthermore, although 39 soil cores were assessed, only
0.003% of the total surface area was sampled for root biomass,
making the estimates for both 1997 and 2002 uncertain.
The root to foliage ratios for small fine roots (< 2 mm) and
fine roots (< 5 mm) were 0.63 and 0.89, respectively, which
TREE PHYSIOLOGY VOLUME 23, 2003
BIOMASS AND NET PRIMARY PRODUCTION OF SCOTS PINE
were similar to the values of 0.69 and 0.85, respectively, reported by Vanninen and Mäkelä (1999) for a 78-year-old Scots
pine forest in southern Finland. The ratio of below- to aboveground biomass of 0.14 was at the low end, but within the
range for Scots pine forests in Finland (0.14–0.47; Vanninen
et al. 1996), and lower than the values reported for a Scots pine
forest in Siberia (0.19–0.26; Pozdynakov et al. 1969) and for
coniferous forests in general (0.24–0.26; Cannell 1982,
Körner 1994, Cairns et al. 1997). One reason for the low below- to aboveground biomass ratio in our study could be underestimation of coarse root biomass owing to the small
sample size and associated uncertainty in the allometric relationship between coarse root biomass and DBH. Observations
of six other coarse root systems at this site (Èermák et al.
1998) also indicated relatively shallow root systems, and thus
probably low coarse root biomass. The shallow rooting system
at our site probably developed because there was no need for
the trees to invest in larger and deeper root systems: the clay
layer prevents the soil from drying out and gives structural
support, and the subsoil is poor in nutrients (Janssens et al.
1999).
Net primary production
Over the 1995–2002 period, mean NPP was 11.2 Mg ha –1
year –1, but NPP was much larger before thinning than directly
after thinning. This reduction in NPP was probably caused by
the removal of 30% of the trees (25.4% of total basal area)
from the stand. In general, thinning is applied to sustain tree
growth, but this study site was thinned to correct for mismanagement in the past. Before harvest, the projected canopy covered only 65% of the surface, and peak LAI was only 2.4 with
a high degree of clumping (Gond et al. 1999). Thus, light was
probably not limiting growth before the harvest, which could
explain why NPP after thinning was estimated to be 25%
lower than the mean NPP over the entire 7-year period (Table 3). However, post-thinning NPP was calculated from forest
inventories performed in two consecutive winters and is therefore representative only for 2001. Because of the large interannual variability in tree growth, it is unwise to extrapolate
NPP from one year to another. Nevertheless, we estimated
post-thinning NPP to be 30% lower than pre-thinning NPP
based on the assumption that NPP in 2000 was similar to that
in 2001.
The NPP/GPP ratio indicates the efficiency of conversion of
photosynthetically fixed carbon to plant tissues (Ryan et al.
1997, Law et al. 1999). Based on seasonal measurements of
photosynthesis and LAI, and the SECRETS model, GPP at
this site was estimated to be 39 and 38 Mg ha –1 year –1 in 1997
and 1998, respectively (Sampson et al. 2001). During this
pre-thinning period, NPP was estimated to be 12.3 Mg ha –1
year –1. The resulting NPP/GPP was therefore 0.32, which was
low, but within the range reported for other coniferous forests
(0.3–0.5; Hamilton et al. 2002) as well as temperate forests in
general (0.3–0.7; Ryan et al. 1997, Waring et al. 1998, Amthor
and Baldocchi 2001). Our low NPP/GPP ratio may be related
to the large standing biomass at our site compared with sites
included in the reviews cited. A large biomass requires more
513
maintenance respiration, and thus will have a lower NPP/GPP
ratio. However, we note that, because most of the biomass at
our site resides in non-respiring wood, the size effect probably
explains only part of the low NPP/GPP ratio. Another reason
for the low NPP/GPP ratio at our site could be that the NPP estimate did not include litterfall of large branches or mortality
of coarse roots. A slightly overestimated GPP would also result in a lower NPP/GPP ratio.
Some 70% of total NPP was allocated to aboveground compartments (7.7 Mg ha –1 year –1), which was much higher than
that reported for a 100-year-old Scots pine forest in eastern
Finland (31.6%; Helmisaari et al. 2002), but in the middle of
the range reported for Scots pine forests (66.1–85.2%; Gower
et al. 1994). Stems accounted for 21.4% of total NPP. Our estimate of 2.4 Mg ha –1 year –1 was similar to that reported for a
smaller section of this stand over the 1995–1999 period
(5.3 m3 ha –1 year –1 or 2.7 Mg ha –1 year –1; De Schrijver 2000),
but much lower than that reported for the same sub-section between 1988 and 1995 (8.1 m3 ha –1 year –1 or 4.1 Mg ha –1
year –1; Neirynck and De Keersmaeker 1996). This decrease is
probably a result of the thinning in 1993.
Needle NPP represented a slightly larger proportion of total
NPP than stems (22.3% or 2.5 Mg ha –1 year –1), and was well
within the range reported for Scots pine forests (19.3–39.3%;
Gower et al. 1994). Cone NPP also represented a rather large
proportion of total NPP (14% or 1.7 Mg ha –1 year –1), being
much higher than that reported for Finnish Scots pine stands
(1.4–2.8%; Helmisaari et al. 2002). Our cone NPP, which was
measured by litter traps, seems extraordinarily high. We note,
however, that the litter traps sampled only 0.01–0.015% of the
total plot area, and so the reliability of the data is uncertain.
Branch NPP, which represented a lower proportion of total
NPP (9.8%) than needle, stem and cone NPP, was probably underestimated because litterfall of big branches was not considered in the estimation of branch NPP.
Belowground production, especially fine root production, is
extremely difficult to estimate accurately (Nadelhoffer et al.
1985, Neill 1992, Helmisaari et al. 2002). Our results indicated that belowground NPP was 3.5 Mg ha –1 year –1, comprising about 31.3% of total NPP, which was within the range
reported for other pine forests (17–73%; Ewel and Gholz
1991). Coarse root (> 5 mm) NPP comprised only a small proportion of total NPP (1.8%), but may have been underestimated because we assumed no mortality and because of the
limited number of measurements on which the allometric relationship was constructed. Fine roots (< 5 mm) contributed
most to total NPP (29.5%), which was also well within the
range for temperate forests (7–76% of total NPP; Vogt 1991,
Gower et al. 1995). Among different fine root classes, fine root
(< 1 mm) NPP was most important, representing 24.1% of total NPP. Its turnover rate was 0.98, indicating that fine roots
(< 1 mm) are nearly completely replaced each year. The turnover rate of fine roots (< 2 mm) was 0.79, which was slightly
higher than that estimated for a 120-year-old Scots pine forest
(0.7; Person 1983). Turnover rates of close to 1 have been reported for fine roots in other coniferous forests (Ruess et al.
1996, Steele et al. 1997). We note that our fine root NPP data
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514
XIAO ET AL.
are uncertain because three assumptions were made in the calculations of fine root NPP. First, fine root NPP measured in
1997 was also used as an estimate for 1995, 1996, and 1998.
Second, after harvest, fine root turnover rates were assumed to
be similar to that measured in 1997. Third, post-harvest fine
root biomass was assumed to be similar to fine root biomass
measured in early 2002. Because of these assumptions, our estimates of fine root NPP, belowground NPP, and total NPP are
uncertain. However, until the large variability in all root- and
soil-related processes can be accommodated, and the difficulties involved in measuring root production can be overcome,
assumptions will have to be made when constructing a complete carbon budget for mature forests.
Acknowledgments
The authors thank B. Assissi for assistance with field measurements,
W. Hendrickx for help with root assessments and Dr. Li Zhengqin for
critical comments on the manuscript. We are also grateful to forest
ranger M. Schuermans and his crew for thinning the trees as well as to
the Division of Forests and Green Areas, Ministry of the Flemish
Community for logistic support and access to the forest. This research
was, in part, financially supported by the EC’s Fifth Framework
Programme through the CARBOEUROFLUX (EVKL-CT-199900032) and MEFYQUE (QLK5-CT-2001-00345) research contracts.
CWX acknowledges support from the research fund of the University
of Antwerpen (UIA). IAJ is indebted to the Fund for Scientific Research, Flanders (F.W.O.) for a post-doctoral fellowship.
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