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1 23
European Journal of Forest Research
ISSN 1612-4669
Eur J Forest Res
DOI 10.1007/s10342-013-0706-1
Long-term study of above- and below-
ground biomass production in relation
to nitrogen and carbon accumulation
dynamics in a grey alder (Alnus incana (L.)
Moench) plantation on former agricultural
land
Jürgen Aosaar, Mats Varik, Krista
Lõhmus, Ivika Ostonen, Hardo Becker &
Veiko Uri
1 23
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ORIGINAL PAPER
Long-term study of above- and below-ground biomass production
in relation to nitrogen and carbon accumulation dynamics
in a grey alder (Alnus incana (L.) Moench) plantation
on former agricultural land
Ju
¨rgen Aosaar •Mats Varik •Krista Lo
˜hmus •
Ivika Ostonen •Hardo Becker •Veiko Uri
Received: 5 September 2012 / Revised: 30 April 2013 / Accepted: 11 June 2013
ÓSpringer-Verlag Berlin Heidelberg 2013
Abstract In the Northern and Baltic countries, grey alder
is a prospective tree species for short-rotation forestry.
Hence, knowledge about the functioning of such forest
ecosystems is critical in order to manage them in a sus-
tainable and environmentally sound way. The 17-year-long
continuous time series study is conducted in a grey alder
plantation growing on abandoned agricultural land. The
results of above- and below-ground biomass and produc-
tion of the 17-year-old stand are compared to the earlier
published respective data from the same stand at the ages
of 5 and 10 years. The objectives of the current study were
to assess (1) above-ground biomass (AGB) and production;
(2) below-ground biomass: coarse root biomass (CRB), fine
root biomass (FRB) and fine root production (FRP); (3)
carbon (C) and nitrogen (N) accumulation dynamics in
grey alder stand growing on former arable land. The main
results of the 17-year-old stand were as follows: AGB
120.8 t ha
-1
; current annual increment of the stem mass
5.7 t ha year
-1
; calculated CRB 22.3 t ha
-1
; FRB 81 ±
10 g m
-2
; nodule biomass 31 ±19 g m
-2
; fine root nec-
romass 11 ±2gm
-2
; FRP 53 g DM m
-2
year
-1
; fine
root turnover rate 0.54 year
-1
; and fine root longevity
1.9 years. FRB was strongly correlated with the stand basal
area and stem mass. Fine root efficiency was the highest at
the age of 10 years; at the age of 17 years, it had slightly
reduced. Grey alder stand significantly increased N and
C
org
content in topsoil. The role of fine roots for the
sequestration of C is quite modest compared to leaf litter C
flux.
Keywords Grey alder Alnus incana Fine roots
Biomass production Nitrogen Carbon
Introduction
Utilizing fast-growing tree species, e.g., woody biomass,
may be possible substitute to fossil fuels for producing
energy in order to decelerate the trend of increasing CO
2
level in the atmosphere. The EU 20-20-20 strategy
(Directive 2009/28/EC) foresees an increase in the share of
renewable energy to 20 % by 2020. One possible means to
reach the goal is to utilize woody biomass from short-
rotation forestry (SRF) plantations more extensively. SRF
is a silvicultural practice employing high-density planta-
tions of fast-growing tree species on fertile land (Weih
2004). Woody biomass from SRF plantations may have
great potential as a CO
2
neutral replacement for fossil fuels
(Hall and House 1994; Tuskan and Walsh 2001).
Grey alder (Alnus incana (L.) Moench) is one of the
most prospective fast-growing tree species in Scandinavia
and the Baltic countries for SRF. Several studies dem-
onstrate that grey alder is a suitable tree species for SRF
in Estonia (Uri et al. 2002,2003,2009). This species is
highly productive both on mineral and organic soils
(Granhall and Verwijst 1994; Saarsalmi 1995; Rytter
1996; Telenius 1999; Hyto
¨nen and Saarsalmi 2009). It is
estimated that there are 385–472 million ha abandoned
arable land suitable for SRF plantations in the world
Communicated by C. Ammer.
J. Aosaar (&)M. Varik H. Becker V. Uri
Department of Silviculture, Institute of Forestry and Rural
Engineering, Estonian University of Life Sciences,
Kreutzwaldi 5, 51014 Tartu, Estonia
e-mail: jaosaar@emu.ee
K. Lo
˜hmus I. Ostonen
Department of Botany Institute of Ecology and Earth Sciences,
University of Tartu, Lai 40, 51005 Tartu, Estonia
123
Eur J Forest Res
DOI 10.1007/s10342-013-0706-1
Author's personal copy
(Campbell et al. 2008). In Eastern Europe, the increase in
such areas after the collapse of the USSR has been sig-
nificant (Mander and Palang 1994; Astover et al. 2006;
FAO 2008; Henebry 2009). Furthermore, grey alder as an
actinorhizal N
2
-fixing tree species can be used effectively
for the biological fertilization of soil with nitrogen
(N) (Granhall 1994).
To understand the functioning of grey alder stands, it is
crucial to study all forest ecosystem components, including
the below-ground part. Since the beginning of the current
century, different aspects of the functioning of grey alder
ecosystems have been studied in Estonia (Uri et al. 2002,
2003,2009,2011; Vares et al. 2003;Lo
˜hmus et al. 2006;
Aosaar and Uri 2008; Mander et al. 2008; Aosaar et al.
2011). Special attention should be paid to fine roots
(d\2 mm) due to their importance in water and mineral
nutrient uptake and the synthesis of certain growth hor-
mones (Makita et al. 2011). Although the fine roots of
forest trees make up \2 % of tree biomass (Brunner and
Godbold 2007), they may account for up to 75 % of the
annual net primary production (NPP) in mature forests
(Vogt et al. 1996; Gill and Jackson 2000; Helmisaari et al.
2002). Thus, fine roots contribute significantly to the
functioning of forest ecosystems and the below-ground
accumulation of carbon (C). More adequate data on below-
ground biomass and fine root turnover of different tree
species are important in order to estimate soil carbon
storage and fluxes, to specify the role of fine roots in the
carbon cycle of forests (Gill and Jackson 2000) and to
compile carbon budget models.
The variability of below-ground biomass estimates is
higher than that of above-ground biomass estimates due to
the methodological difficulties related to studying root
system components (Akkermans and van Dijk 1976;
Sharma and Ambasht 1986; Rytter 1989; Tateno et al.
2004; Hendricks et al. 2006; Coleman 2007; Helmisaari
et al. 2007; Sakai et al. 2007). Thus, variation in root
productivity data among different stands could either
reflect methodological differences or real differences in
productivity (Hertel and Leuschner 2002; Finer et al.
2011a). The most common approaches for estimating the
fine root biomass (FRB) and fine root production (FRP) in
the field have been the sequential coring method (Ahlstro
¨m
et al. 1998; Vogt and Persson 1991; Helmisaari et al.
2002), the in-growth core method (Persson 1983; Makko-
nen and Helmisaari 1999) and the minirhizotron method
(Majdi and Nylund 1996; King et al. 2002). In recent years,
the new prospective root mesh method (Hirano et al. 2009;
Lukac and Godbold 2010) has been introduced.
Species of actinorhizal Alnus that fix atmospheric
nitrogen (N
2
) through the metabolic activity of the fila-
mentous bacterial symbiont Frankia play an important role
in the nitrogen cycle of temperate forest ecosystems
(Tjepkema et al. 1986; Baker and Schwintzer 1990; Huss-
Danell 1997; Dawson 2008). Measuring nodule biomass is
essential for estimating the amount of N
2
fixation (Tobita
et al. 2010).
New knowledge of FRB and nodule biomass (NB)
dynamics and FRP and fine root efficiency (FRE) is needed
for the better understanding of a highly productive alder
forest ecosystem development and functioning. So far, only a
few scientific studies have been published reporting the fine
root data of grey alder (Rytter 1989; Elowson and Rytter
1993; Uri et al. 2002,2009). The current study presents the
results of FRB, NB, FRP and FRE dynamics throughout the
development of the grey alder stand (age 5–17 years).
The chronosequence approach is commonly used to
study and model stand development dynamics. However,
the variability of abiotic and biotic factors (soil properties,
water regime, stand density, stand management, etc.) in the
chronosequence of study sites cannot be avoided com-
pletely. Hence, the apparent advantage of the current paper
is that the 17-year period of fine root and nodule growth
dynamics along with thorough background data about soil
properties and stand characteristics is presented as a con-
tinuous time series. Furthermore, the new knowledge pre-
sented is a prerequisite for compiling carbon accumulation
and nutrient budgets in similar stands.
The hypotheses of the study were as follows: (1) grey
alder is a highly productive species suitable for SRF; (2)
fine roots (FR) play an important role in C and N budgets;
(3) there is a strong relationship between the above- and
below-ground parts of the stand.
In order to verify the hypothesis, the objectives of the
study were (1) to estimate the above-ground biomass
(AGB) production capability of grey alder plantation; (2) to
estimate the dynamics of the grey alder coarse root biomass
(CRB), FRB, NB and FRP in a short-rotation plantation
growing on former arable land; (3) to estimate the role of
tree roots in the N and C sequestration in soil; (4) to study
the relationships between the above- and below-ground
parts of the trees in the stand at different ages.
Materials and methods
Study area and stand characteristics
The research area is located in the south-eastern part of
Estonia (58°30N; 27°120E). According to the data from the
meteorological station (Vo
˜ru) closest to the experimental
area, the mean annual temperature is 6 °C, the mean pre-
cipitation is 653 mm and the mean length of the vegetation
period is 191 days. The plantation was established on
abandoned agricultural land in spring 1995. The soil is
classified as Eutric Podzoluvisol (according to the FAO
Eur J Forest Res
123
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classification) (Table 1). The area of the plantation is
0.08 ha and altogether 1,260 one-year-old transplants of
natural origin were planted; hence, the initial density of the
plantation was 15,750 trees per hectare. The survival and
growth of the planting stock of different origins has been
described previously (Uri et al. 2002,2003,2009). Before
the establishment of the plantation, the area had been out of
use for 2 years. No soil preparation, weed control, fertil-
ization or other treatment were performed before or after
planting.
The data of above- and below-ground (Tables 2,3)
characteristics of the stand at the age of 5 and 10 years
have been published earlier (Uri et al. 2009); the respective
data of the 17-year-old stand are original.
Estimating above-ground biomass and production
All the stand characteristics and AGB were always deter-
mined at the end of August, when the dimensions of the
trees and the biomass had reached their annual maximum
(Table 2). All the presented values reporting mass units
throughout the article are given in dry mass (DM).
The AGB of the stand was estimated by using dimension
analyses (Bormann and Gordon 1984) and has been descri-
bed in detail in earlier studies (Uri et al. 2002,2009). The
stem breast height diameter (D
1.3
) was measured in case of
all trees. The trees were divided into five classes on the basis
of D
1.3
, and a model tree was selected randomly from each
class. A total of seven model trees were felled in order to
determine the above-ground biomass of the stand—one tree
from each diameter class and one additional model tree from
two diameter classes which presented a larger number of
trees growing in the stand. The model trees were divided into
sections and in every section, the mass and share of stem
wood, stem bark, branches and leaves was found.
To estimate the biomass of the above-ground part of the
plantation (y) for the following years, an allometric Eq. (1)
was used:
y¼axb:ð1Þ
To avoid the edge effect, model trees were selected from
the middle of the study area.
The annual production of the stem wood, bark and
branches was calculated as difference between the masses
of the current and the previous year (Uri et al. 2002,2009).
Estimating coarse root biomass and production
The coarse root biomass (CRB) (d[2 mm) of grey alder
trees was calculated on the basis of earlier studies by
Lo
˜hmus et al. (1996) and Uri et al. (2009), in which the
CRB of a grey alder stand at the ages of 5, 10 and 40 years
was estimated by excavating the root systems of model
trees. In the studies referred to above, the share of coarse
roots of the above-ground leafless biomass was found to be
approximately 19 %. Based on the earlier results, it is
assumed here that AGB and CRB develop proportionally.
Hence, CRB and the share of CRB production in the cur-
rent year of total CRB were calculated as follows (2and 3,
respectively):
CRB t ha1
¼AGBleafless
ðÞ0:19;ð2Þ
CRBprod %ðÞ¼AGBprodAGB:ð3Þ
Estimating the biomass and production of fine roots
and nodules
Soil core method
In this paper, only the FRB and FRP of trees are estimated;
the respective values of understory vegetation are not
included. In this study, fine roots are defined as roots with a
diameter of \2 mm.
The soil coring method (Vogt and Persson 1991) was
used to estimate the biomass and necromass of fine roots
and nodules of grey alder. The coring was always carried
out in October. The number of samples is: 20 in 1998
(stand age 5 years), 25 in 2003 (10) and 20 in 2010 (17).
The results of the years 1998 and 2003 are presented in Uri
et al. 2002 and 2009, respectively.
Soil cores were taken randomly from the whole area of
the plantation with a cylindrical soil auger (diameter of the
cutting edge 48 mm). Soil cores were divided into four
equal 10 cm layers to a depth of 40 cm, placed in poly-
ethylene bags and kept frozen until further processing.
Alder roots and nodules were washed out of the soil cores
very carefully during 1 week after sampling. For washing
the roots and nodules, fine-meshed sieves were used in
order not to lose any root fragments. Further, the fractions
of living and dead fine roots and nodules were separated
under a binocular microscope and cleaned from soil par-
ticles. The samples were dried at the temperature of up to
70 °C and weighed with the accuracy of 0.001 g. Soil core
data were used to calculate the biomass of fine roots and
nodules per hectare, summing up the average values for
Table 1 Soil characteristics of the studied stand in the upper 10 cm
soil layer
Age
(year)
N (%) C (%) Texture pH
KCl
Organic
matter (%)
5 0.108
a
1.59
a
Loamy sand 5.37
a
2.74
a
10 0.136
b
1.80
b
Loamy sand 5.07
b
3.10
b
17 0.134
b
1.86
b
Loamy sand 4.77
c
3.23
b
Presented the average significant differences (indicated by different
letters) according to the Tukey HSD test (P\0.05)
Eur J Forest Res
123
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successive soil layers from the soil cores. The share of fine
roots and nodules of the root systems was calculated.
In-growth cores
Altogether, 150 in-growth cores (d=40 mm, mesh size
6 mm) were inserted into the soil to estimate fine root growth
dynamics and FRP. The cores were inserted in five random
transect groups all over the stand, into the topsoil to a depth of
30 cm in October 1999 (stand age 6 years). The meshes were
filled with sieved root-free soil according to the genetic
horizons of the soil. A total of 105 in-growth cores were
extracted during 2000–2003: 7 samplings and 15 meshes per
sampling. Samplings were carried out in November 2000;
June, August 2001; June, August, November 2002 and June
2003. In November 2001, sampling was skipped due to the
fact that the soil was frozen. All the subsamples obtained
were transported to the laboratory and stored frozen
(-18 °C) until processing. In the laboratory, soil cores were
divided into depth layers of 0–10, 10–20 and 20–30 cm.
Roots and nodules were carefully washed out of the soil,
using fine-meshed sieves. The fractions of fine roots and
nodules were separated and cleaned from soil particles under
a binocular microscope. Dead roots and nodules were
separated as well. The samples were dried at a temperature of
up to 70 °C and weighed with the accuracy of 0.001 g.
Total FRP was calculated on the basis of in-growth core
data and by balancing the biomass compartments of living
and dead roots according to the decision matrix of Fairley
and Alexander (1985). The FRP was calculated on the basis
of FRB data from June 2002–2003. It included four sam-
plings: June, August and November 2002, and June 2003.
Root turnover rate (year
-1
) was calculated from in-growth
cores as annual root production (g m
-2
year
-1
) divided by
the mean FRB (g m
-2
). To avoid large fluctuations during
the vegetation period, mean FRB was used to calculate the
fine root turnover rate (Ostonen et al. 2005).
The FRP values for the 5- and 17-year-old stand were
calculated using the same fine root turnover rate (FRT)
(0.54 year
-1
) as was used in case of the 9-year-old stand.
As the estimation of FRB and FRP is very labour-intensive,
it was assumed that FRT is a stable and stand-specific
parameter. The assumption is based on Finer et al. (2011a),
who state that the variation of the FRT of trees can be
explained neither with environmental nor with stand-rela-
ted factors and that the FRT is species-specific.
Fine root efficiency (FRE) (t t
-1
year
-1
) was calculated
by dividing the CAI with the FRB.
Table 2 Grey alder stand characteristics and above-ground biomass data: leaf area index (LAI), mean annual increment (MAI), current annual
increment (CAI)
Age (year) Mean
height (m)
Mean
D
1.3
(cm)
Basal area
(m
2
ha
-1
)
Density,
trees (ha
-1
)
LAI
(m
2
m
-2
)
Stand characteristics
5 4.6 2.6 6.7 12,660 2.2
10 9.5 5.7 18.9 7,400 4.0
16 13.9 8.7 31.9 5,360 4.2
17 14.3 9.3 34.6 5,100 3.8
Age (year) Stems
(t ha
-1
)
Leaves
(t ha
-1
)
Branches
(t ha
-1
)
Total
(t ha
-1
)
MAI
(t ha
-1
year
-1
)
CAI
(t ha
-1
year
-1
)
Above-ground biomass
5 8.1 2.0 2.2 12.3 1.6 3.3
10 41.0 3.0 5.4 49.4 4.1 6.4
16 99.7 3.2 13.9 116.8 6.2 14.2
17 105.4 3.3 12.1 120.8 6.2 5.7
Table 3 Coarse root biomass
and N and C concentrations
(mean ±standard error) in the
17-year-old grey alder stand on
abandoned agricultural land
a
Data from Uri et al. (2011)
Fraction Percentage Biomass (t ha
-1
) N (g kg
-1
)
a
C (%)
Stump 40.4 9.0 0.4 ±0.3 51.46 ±0.13
Coarse roots d[10 mm 35.1 7.8 7.9 ±0.7 49.89 ±0.03
Coarse roots 5 \dB10 mm 10.7 2.4 9.1 ±0.5 49.73 ±0.04
Coarse roots 2 \dB5 mm 13.8 3.1 10.0 ±0.2 49.73 ±0.03
Total 100 22.3
Eur J Forest Res
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N and C storages
The N and C pools in the below-ground biomass of the
stand were calculated by multiplying the biomass of root
fractions with the respective N or C concentrations in the
fractions. The weighted average was used in order to cal-
culate average N and C concentrations in CRB; the fraction
percentage was multiplied by the respective concentration.
The ash content, which was \10 % in all cases, was
determined to check the possible soil contamination of
roots.
N and C storage in soil was calculated on the basis of
soil bulk density and the mean concentration of N or C in
soil. Soil bulk density was determined in 2002 from 10 soil
pits reaching to a depth of 50 cm. The density samples
were taken with a stainless steel cylinder (d=40 mm;
volume 50.24 cm
3
) from different soil layers (0–10 cm,
10–20 cm, etc.), three samples from each layer. After
drying at the temperature of 105 °C, soil samples were
weighed.
Soil N and C concentrations were studied annually
during the period October 1995–2010 (stand age
2–17 years) when plant growth had ceased. Samples from
soil layers were taken in 10 random points at the depths
0–10, 10–20, 20–30, 30–40 and 40–50 cm and three
composite samples were formed from each depth layer.
N and C input into soil via leaf and fine root litter was
included in the study.
The N and C input flux into soil was calculated on the
basis of foliage biomass and NC concentrations of col-
lected leaf litter from an earlier study period (10-year-old
stand). The litter was collected twice a month from 10 litter
traps with the area of 0.25 m
2
each located randomly all
over the plantation (Uri et al. 2011).
Root litter was considered as the dead fine root mass
estimated in case of in-growth cores.
Chemical analyses
Nitrogen (N) and carbon (C) were determined from root
and nodule samples. Tecator ASN 3313 was employed to
test total N (Kjeldahl) in soil samples. Plant samples were
analysed for total N by the Kjeldahl method using a Kjeltec
Auto 1030 analyser. The dry combustion method was used
with a varioMAX CNS elemental analyser (ELEMEN-
TAR, Germany) to test the C content in oven-dried plant
material samples. Soil pH in 1 M KCl suspensions was
measured with the ratio of 10 g/25 ml. Total C content in
soil was determined by the dry combustion method using a
varioMAX CNS elemental analyser (ELEMENTAR, Ger-
many). The analyses were carried out at the Biochemistry
Laboratory of the Estonian University of Life Sciences.
On the basis of average concentrations, the total N and C
accumulation in fine root and nodule biomass, and the C
and N input via leaves and fine roots into the soil were
calculated.
Statistical methods
The normality of the variables was checked with Lilliefors
and Shapiro–Wilk tests. The data of model trees were
analysed by means of regression analysis. So as to find
allometric relationships (1), D
1.3
served as the independent
variable in all cases. The statistical significance of differ-
ences in biomass on different years between respective
layers was checked with the ttest (two-sample assuming
unequal variances). There was no autocorrelation of the
FRB data (d=2.2), which was checked with the Durbin–
Watson test. The software STATISTICA 7.1 was used and
the significance level a
9=0.05 was accepted in all cases.
Results
Above-ground biomass and production
The increase in AGB has been vigorous, exceeding
100 t ha
-1
in the 17-year-old stand. The CAI of the
16-year-old stand was 14.2 t ha
-1
, which is an impressive
value considering the conditions in Estonia. However, in
the next growing season, it underwent a drastic decline
(Table 2). The average mass of a single stem in the 16- and
17-year-old stand was 18.6 and 20.7 kg, respectively. The
leaf mass as well as the leaf area index stabilized after the
5-year growth of the stand. The leaf mass has been fluc-
tuating around 3 t ha
-1
ever since (Table 2).
Coarse root biomass and production
The largest share of CRB formed from stump and the
fraction d[10 mm, being 9 and 7.8 t ha
-1
, respectively,
in the 17-year-old grey alder stand (Table 3). To estimate
the N and C accumulation in below-ground biomass, N and
C concentration values from the 10-year-old stand were
used (Table 3). The calculated CRB for the 16- and
17-year-old stand exceeded 20 t ha
-1
(Table 4). The cal-
culated coarse root production values were 3.2 and
0.7 t ha
-1
for the 16- and 17-year-old stand, respectively
(Table 4).
Fine root standing biomass and necromass on the basis
of soil cores
The total standing FRB in the 17-year-old grey alder stand
was estimated to be 81 ±10 g m
-2
. It has increased 32 %
Eur J Forest Res
123
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compared to the 5-year-old stand; compared to the 10-year-
old stand, FRB was virtually the same (Table 4); the slight
decrease in FRB was statistically insignificant (ttest;
P=0.14). The difference between FRB in the 5- and
10-year-old stand in the upper 0–10 cm soil layer was
statistically significant (P\0.05).
Fine root biomass (FRB) in deeper soil layers has not
changed significantly throughout the studied years (Fig. 1).
The principal share of FRB was always located in the upper
0–10 cm soil layer, remaining in the range of 47–57 % of
the total fine root biomass. FRB in the upper 20 cm soil
layer has increased gradually from 74 to 84 % of total FRB
with the increase in stand age.
The necromass of fine roots in the 10- and 17-year-old
stand has remained quite stable, fluctuating between 10 and
20 g m
-2
(Table 4). However, the relative share of nec-
romass of FRB has decreased with increasing stand age,
being 22 and 14 % in 2003 and 2010, respectively.
Fine root standing biomass in in-growth cores
Fine root biomass (FRB) in in-growth cores was low during
the first two growing seasons (the vegetation periods of
2000 and 2001) (Fig. 2). After the first growing season, in
November 2000, the FRB was 15 g m
-2
in 0–30 cm soil
layer. FRB was always highest in the upper 10 cm soil
layer, forming 50 % of the total biomass. The highest
standing FRB for the 0–30 cm soil layer was 123 g m
-2
in
June 2002 (the third growing season after the installation of
the cores). The mean biomass in cores in the period June
2002–2003 was 98 g m
-2
. The FRB value of June 2002 is
not comparable to the autumn values due to the annual
growth dynamics of fine roots (Fig. 2). Since the in-growth
core data reflected FRB data in soil layers with the depth of
up to 30 cm, but the soil cores were up to 40 cm deep, we
used the extrapolation of data. As the share of standing
biomass in soil cores in 2003 of the 30–40 cm soil layer
was 7 %, the calculated respective values of standing
biomass in June and November 2002 in in-growth cores
(0–40 cm) would be 132 and 66 g m
-2
.
Net primary production of fine roots
Fine root production (FRP) in the in-growth cores after the
first growing year (October 1999–November 2000) was
15 g m
-2
year
-1
, being the most vigorous in the upper
10 cm soil layer (48 % of the total). The calculation was
made on the basis of the FRB in in-growth cores. Estimated
FRP in the 9-year-old stand was 53 g m
-2
year
-1
and the
calculated FRP values for the 5- and 17-year-old stand
were 30 and 44 g m
-2
year
-1
, respectively.
In the 9-year-old stand, the turnover rate of fine roots
was 0.54 year
-1
and longevity 1.9 years.
Nodule biomass
The living nodule biomass (NB) in the 17-year-old stand
has doubled compared to respective values in the younger
stand, reaching up to 31 ±19 g m
-2
(Table 4). The NB
has accumulated in the upper 20 cm soil layer and half of it
in the 10 cm topsoil. The depth distribution of the nodules
has changed in the 17-year-old stand compared to earlier
stages (Fig. 3); in both the 5- and 10-year-old stand,
approximately 80 % of all nodules were located in the
upper 10 cm soil layer. In the 17-year-old stand, the nodule
depth distribution in the 0–10 and the 10–20 cm soil layer
Table 4 Coarse root, fine root and nodule biomass and necromass (mean ±standard error) dynamics in grey alder stand growing on abandoned
agricultural land
Stand age
(year)
Coarse root
biomass (t ha
-1
)
Coarse root
production
(%
a
/t ha
-1
)
a
Fine
root biomass
(g m
-2
)
Fine root
necromass
(g m
-2
)
Nodule
biomass
(g m
-2
)
Nodule
necromass
(g m
-2
)
5 2.0 37.9/0.76 55 ±11 – 17 ±8–
10 8.7 16.4/1.43 87 ±14 19 ±416±62±1
17 22.3* 3.3/0.33 81 ±10 11 ±231±19 1 ±1
a
Calculated
Fig. 1 Vertical distribution of fine root biomass in grey alder stand in
1998, 2003 and 2010. The box indicates mean ±standard error; the
whiskers indicate 95 % confidence intervals
Eur J Forest Res
123
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was equal. Almost no nodules have been found in deeper
soil layers throughout the study period.
The average NB per tree increased with increasing stand
age. In the 5-year-old stand, the average NB per tree was
13.4 g; in the 10- and 17-year-old stand 21.6 and 60.8 g,
respectively.
Relationships between fine roots and above-ground
stand characteristics
A very strong relationship (R=0.96) was found between
stand age and average FRB per tree. As stand stem mass
and stand basal area are strongly correlated characteristics,
similar correlations exist between FRB and stand stem
mass and FRB and stand basal area.
Fine root efficiency (FRE) was the highest at the stand
age of 10 years (7.3 t t
-1
year
-1
). The respective values
have been lower in the 5- and 17-year-old stand as well,
being 5.9 and 7.0 t t
-1
year
-1
, respectively.
Carbon and nitrogen accumulation in the below-ground
part of the stand
With the increasing age of stand, CRB has also increased
(Table 4). Hence, the N and C storage in CRB increased
during the stand development, reaching almost 70 kg ha
-1
and 5 t ha
-1
in the 17-year-old stand, respectively
(Table 5).
The average nitrogen concentration of fine roots and
nodules in the 17-year-old stand was 1.246 ±0.02 and
1.923 ±0.02 %, respectively. The average C concentra-
tion in fine roots was 51.46 ±0.13 %.
Carbon accumulation in fine root biomass peaked at the
age of 10; the N and C accumulation in fine roots in the
17-year-old stand was also lower than the respective values
in the 10-year-old stand (Table 5).
Discussion
Above-ground part of the stand
The estimated AGB of the stand is very high for the con-
ditions in Estonia as well as other Baltic and Scandinavian
countries. Stem volume in the stand, calculated from the
stem wood density of 396 kg m
-3
(Aosaar et al. 2011), was
266 m
3
ha
-1
in the 17-year-old grey alder stand. The result
exceeds the highest values of the grey alder yield tables in
Aosaar et al. (2012), in which the highest stand volumes at
the ages of 15 and 20 years are 170 m
3
ha
-1
(Latvia) and
225 m
3
ha
-1
(Latvia, Norway), respectively. High stem
volume results of single stands are reported from Central
Sweden, where the stem volumes of 15-year-old stands
growing on fine sand were 390 and 368 m
3
ha
-1
(Johans-
son 2000), calculated from the stem wood density of
359 kg m
3
(Johansson 2005). These numbers reflect the
high biomass production potential of the grey alder.
The CAI in the 16-year-old stand was also extremely
high—18.8 t ha
-1
year
-1
(stem mass 14.1 t ha
-1
year
-1
).
The result is comparable to the production numbers
reported by Tullus et al. (1998)—12.1 t ha
-1
year
-1
(6-
year-old stand) and Granhall and Verwijst (1994)—
17.0 t ha
-1
year
-1
(5-year-old stand).
However, in the present study, CAI decreases drastically
at the age of 17 years. As grey alder bioproduction is very
sensitive to the water deficit in the vegetation period,
drought conditions in summer 2010 may have had a con-
siderable impact on the growth of the stand. Further, the
onset of bulk maturity is expected to occur at the stand age
of 15–20 years, as pointed out by many authors (Lo
˜hmus
et al. 1996; Rytter 1995; Rytter et al. 2000; Daugavietis
0 20 40 60 80 100 120 140
June 2003
Nov 2002
Aug 2002
June 2002
Aug 2001
June 2001
Nov 2000
FRB DM g m-2
Sampling time
0…10 cm
10…20 cm
20…30 cm
Total
0 20 40 60 80 100 120 140
June 2003
Nov 2002
Aug 2002
June 2002
Aug 2001
June 2001
Nov 2000
FRB DM g m-2
Sampling time
0…10 cm
10…20 cm
20…30 cm
Total
Fig. 2 Fine root standing biomass dynamics in in-growth cores.
Experiment installed in October 1999
Fig. 3 Dynamics of the relative
vertical distribution of fine roots
(d\2 mm) and nodules in the
5-, 10- and 17-year-old grey
alder stand on abandoned
agricultural land. The data of
the years 1998 and 2003 have
been published earlier in Uri
et al. (2009)
Eur J Forest Res
123
Author's personal copy
et al. 2009; Uri et al. 2009) and it is in good accordance
with several yield tables reported in Aosaar et al. (2012),
which leads to the decrease in CAI. Hence, the decrease in
CAI was probably caused by the concurrence of the
inherent growth-reducing period and unfavourable weather
conditions.
The question of initial stand density and stand density in
mature age is of crucial importance in respect of SRF
stands. In the studied stand, the initial density was high
(15,750 ha
-1
), which is the characteristic of natural grey
alder stands. In case of a plantation, such initial density can
be considered irrational due to the high costs. In the liter-
ature, there is almost no data about the thinning of grey
alder stands. However, according to an experiment by
Rytter (1995), thinning is not essential to achieve the
higher bioproductivity of the alder stand, since an equal
amount of obtainable biomass was produced both in thin-
ned and unthinned stands. The density of the studied stand
at the age of 17 years was 5,100 ha
-1
; neither thinnings
nor other silvicultural treatments were implemented
throughout the growth of the stand. However, the density
of 5,100 ha
-1
can be considered optimum since it is in
good accordance with the stand density values of most
productive yield tables reported in Aosaar et al. (2012), in
which, at the age of 15, density ranged from 2,700 to
6,500 ha
-1
. Hence, it may be assumed that similar stand
volumes would have been produced in case of the lower
initial density of the plantation.
Below-ground part of the stand
In the 5-year-old stand, fine root biomass (FRB) was
55 ±11 g m
-2
(Uri et al. 2002) and FRB per tree was
43.3 g. Compared to the younger stand, FRB increased and
remained stable in the 10- and 17-year-old stand. Although
the FRB of stand stabilized, FRB per tree increased due to
the natural self-thinning of the stand and following an
increase in the dimensions of trees in order to meet their
rising need for nutrients and water. However, the foliage
mass stabilized after canopy closure in the level of
3–4 t ha
-1
and the stem mass increment is gradually
decreasing in older stands. Hence, the infinite enlargement
of the fine root system is unnecessary for trees. However,
on the basis of available data, it is impossible to predict the
period of time needed for the stabilization of FRB per tree.
Fine root biomass (FRB) in the grey alder plantation has
remained at \1tha
-1
. It seems to be an optimum FR
supply for the grey alder stand growing on fertile soil, as
there were no increases in the FRB value in the 17-year-old
stand compared to the 10-year-old stand. The FRB value
can be considered modest, as the mean FRB in boreal and
temperate forests is 526 ±321 and 775 ±474 g m
-2
,
respectively (Finer et al. 2011b). According to Bloom et al.
(1985), trees growing on poor sites should allocate a
greater proportion of their resources into FRB than those
growing on fertile sites. In a study by Kalliokoski et al.
(2010), the FRB of Picea abies and Pinus sylvestris
increased with decreasing soil fertility, while the FRB of
Betula pendula remained the same. According to the lit-
erature, nitrogen limitation in soil increased the FRB of
different tree species (Finer et al. 2007; Helmisaari et al.
2007; Graefe et al. 2010). In the studied plantation, the N
content in topsoil was high; the respective value has
increased significantly in the 10- and 17-year-old stand,
compared to the initial situation (Uri et al. 2011).
In November 2000, the FRB in in-growth cores was
0.15 t ha
-1
, which can be also handled as fine root pro-
duction (FRP) of the first growing year. In August 2001,
the FRB in in-growth cores was at the same level as it was
in November 2000 (Fig. 2). These values indicate very low
FRP values during the first and second growing year. This
is in good accordance with the literature (Vogt et al. 1998;
Makkonen and Helmisaari 1999; Ostonen et al. 2005), in
which it is indicated that in absolute values, fine root
biomass may still be lower during the second and third year
in the in-growth cores. The FRB estimated from in-growth
cores after the first or second year is significantly lower
than the FRB in soil cores, i.e., the actual FRB in soil. FRB
in in-growth cores fluctuates seasonally, reaching its peak
in June and decreasing due to root mortality until the
beginning of the next growing season (Fig. 2). Quite a
good accordance between the autumnal FRB values
Table 5 Accumulation of nitrogen (N) and carbon (C) in below-ground biomass and the annual production and NC pool in the upper soil layer
Stand age (year) Accumulation in biomass (kg ha
-1
) Accumulation in annual production (kg ha
-1
) Pool in 0–10 cm soil layer (t ha
-1
)
Fine roots Nodules Coarse roots Fine roots Coarse roots
NC N NC N C N C N C
5 6.9 282.6 3.3 13.6 988 3.7 154.1 5.2 374 1.38 20.5
10 10.8 447.0 3.1 59.4 4,299 6.7 277.5 9.7 705 1.74 23.5
17 10.1 416.2 5.9 68.9 11,000 5.5 226.1 2.3 165 1.72 24.3
Both N and C pools in soil have increased significantly during the development of the stand (Table 5). In the 17-year-old stand, the N and C flux
into soil via leaf litter was 112 and 1,635 kg ha
-1
, respectively. The respective numbers of fine roots were 5.4 and 225 kg ha
-1
Eur J Forest Res
123
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estimated by different methods was found: the FRB on the
basis of in-growth core data was 66 g m
-2
in 9-year-old
stand and on the basis of soil cores 87 g m
-2
in 10-year-
old stand.
Although the installing of in-growth meshes strongly
modifies the disturbed environment of surrounding roots, it
allows us to calculate FRP directly. Therefore, it is suit-
able for comparing FRP between sites or treatments
(Messier and Puttonen 1993). Since the period of stabil-
ization for in-growth cores is required (Ostonen et al.
2005) and roots are still expanding into the meshes in the
third growing year (Makkonen and Helmisaari 1999), then
the production, turnover rate and longevity of fine roots
were calculated on the basis of samples taken in 2002 and
2003. FRP in our grey alder plantation was low
(54 g m
-2
), which may have been caused by the droughty
summer (Nikolova et al. 2009). According to the literature,
the in-growth core method may give some underestimation
of FRP (Finer et al. 2011a). For the estimation of FRP,
several direct methods are used by the researches,
sequential soil coring, in-growth cores and minirhizotron
methods, which all have their advantages and disadvan-
tages (Vogt et al. 1998; Majdi et al. 2005; Strand et al.
2008), and selecting the appropriate method for the esti-
mation of FRP is always a complicated issue. Estimation
of FRP is more complicated than the estimation of FRB,
and factors affecting fine roots dynamics are still poorly
understood (Finer et al. 2011b). Hendricks et al. (2006)
found that in-growth method gave lower estimates for FRP
than the minirhizotron method, whereas Vogt et al. (1998)
did not find any significant differences between the
methods. Thus, the FRP estimation is always related to
high variability of results and absolutely accurate method
does not exist. Even if we assume that actual FRP in
studied grey alder stand is significantly higher and our
results are underestimated, the FRP formed quite a modest
share from the total stands annual biomass production.
However, in some cases, the proportion of below-ground
production may form significant share and attain up to
75 % of the total annual production of the stand (Jackson
et al. 1997).
The longevity of fine roots in in-growth cores was cal-
culated to be approximately 2 years, and hence, fine roots
necromass (FRN) during the first two growing periods in
cores was close to zero. The maximum FRB in in-growth
cores was estimated in June 2002 (123 g m
-2
); by
November 2002, it had halved, so the mass of dead roots
should have been relatively high. However, the mass of
dead roots in in-growth cores in November 2002 was
\1kgha
-1
, i.e., the process of the decomposition of dead
fine roots in the fertile sites of the grey alder plantation
should be extremely rapid and nutrients and C captured in
fine roots should reach the soil quickly.
The decomposition of organic matter, including fine
roots, depends on environmental conditions and the nutri-
ent composition of organic matter. The decreased C/N ratio
stimulates the decomposition of organic matter (Scott and
Binkley 1997; Vervaet et al. 2002). Due to the high content
of N in fine roots (1.25 %) and the favourable C/N ratio,
the decomposition of dead fine roots was promoted and
therefore very intense. Hence, the storage of dead fine roots
in soil remains low.
As grey alder is a N
2
-fixing species, it is essential to
estimate the biomass of nodules. The nodule biomass of
Alnus species varies, depending on the tree size and stand
density (Bormann and Gordon 1984), but also on the age of
the stand (Sharma and Ambasht 1986; Son et al. 2007).
Nodules can be several years old and grow to a large size
(Akkermans and van Dijk 1976). Nodule biomass in the 5-
and 10-year-old plantation was similar. However, both
estimations are smaller than in the 4-year-old grey alder
coppiced stand in Finland (25–29 g m
-2
) (Saarsalmi et al.
1985). Bormann and Gordon (1984) found that the average
mass of the nodules in a 5-year-old Alnus rubra stand was
15 g m
-2
. In the 17-year-old stand, the NB value had
doubled compared to the 10-year-old stand. However, the
number of nodules was very low. NB in the 17-year-old
stand was greatly affected by one single nodule (0.65 g)
found in the 10–20 cm soil depth layer; only 2 nodules in
total were found in the 10–20 cm soil layer. However,
since the NB was estimated using the soil coring method, it
was probably underestimated. It differs from the younger
stand (10 y), in which several nodules were found. With
increasing stand age, the mean weight of nodules increases
as the number of nodules decreases. This is in good
accordance with Tobita et al. (2010), in which the size of
nodules shifted from smaller to larger size classes with the
increasing breast height diameter of trees. A very low
number of nodules in deeper soil layers is reported in the
literature: In a study carried out in Estonia by Lo
˜hmus et al.
(1996), no nodules were found deeper than 10 cm; a sim-
ilar tendency is described by Johnsrud (1978) in Norway;
Elowson and Rytter (1993) reported the following nodule
allocation—98 % were found in the upper 20 cm of the
soil profile; according to Rytter (1989), more than 90 % of
the total mass of the nodules on intensively managed
organic soil were contained in the upper 0–6 cm soil layer.
Furthermore, the increasing N content in soil increases
nodule weight (Bond et al. 1954); the soil N content in the
plantation has increased significantly over the years
(Table 1). Hence, with increasing age and soil fertility,
alders grow fewer nodules, which are larger, leading to
greater variations in nodule biomass, as shown in Table 4.
Fine root efficiency (FRE) in the studied stand was the
highest at the age of 9–10 years (in 2002–2003); at the age
of 17 years, FRE had slightly decreased. The low FRB and
Eur J Forest Res
123
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FRP indicate the high activity of fine roots, which is
described as intensive fine root strategy (Lo
˜hmus et al.
2006; Ostonen et al. 2011). Trees using the extensive
strategy increase the mass, surface area and length of fine
roots. In the case of the intensive strategy, trees increase
the efficiency of fine roots and rhizosphere processes
(Leuchner et al. 2004;Lo
˜hmus et al. 2006; Ostonen et al.
2011). In the studied stand, the difference between the soil–
root interface and bulk soil microbial activity and diversity
was markedly higher than in grey alder stands growing on
forest land; the specific root area (SRA; m
2
kg
-1
) was also
significantly bigger (Lo
˜hmus et al. 2006) than in natural
alder stands. Hence, the low fine root biomass and turnover
rate both indicate the significantly greater role of the
intensive fine root strategy in the studied grey alder stand.
Furthermore, intensive competition between trees
occurred at the age of 9–10, as stand density was still rather
high. Hence, probably, it was more effective for a tree to
enlarge its above-ground part and operate its fine roots very
efficiently in order to survive in a dense stand. At the age of
17 years, stand density, the increment of stem mass and
FRE had declined compared to the 10-year-old stand. As
suggested in many studies (Bjo
¨rklund and Ferm 1982;
Rytter 1995,2000;Lo
˜hmus et al. 1996; Miez
ˇite and
Dreimanis 2006; Uri et al. 2009; etc.), the bulk maturity
and optimal rotation length of grey alder fall between the
ages 15–20. Hence, as the intense and rapid increase in the
above-ground part of the stand had dwindled, the FRE of
the grey alder fine roots had also declined.
Nitrogen-fixing species, owing to their N
2
-fixing ability
through microbial symbiosis, can increase soil N and C
content. N
2
-fixing trees significantly affect the soil C pool by
increasing detritus input or humus formation, or by
decreasing the rate of decomposition (Binkley 2005). Such
species have been widely used as pioneer plants in the
recovery of degraded areas (Fisher 1995; Johnson and Curtis
2001). Both the N and C content in the upper soil layer has
increased significantly during the growing period of the grey
alder stand (Table 1). However, the contribution of fine roots
and nodules to the soil N and C increase has been modest due
to the constantly low FRB and NB values (Table 4). As N
and C concentrations in fine roots and nodules have been at a
constant level throughout the study period, the main factors
affecting N and C accumulation in soil are FRB and NB.
However, the fine roots contribution for the N and C flux to
soil could have been larger, supposing that the in-growth
core method may have given systematically lower FRP
estimation (Finer et al. 2011a).
In our stand, fine root litter formed merely 14 % of the
total annual tree litter input into soil; the main input of the N
and C in grey alder stand comes from leaf litter instead. The
total C stock in the soil of the studied stand has significantly
increased, which is in good accordance with other studies
carried out in short-rotation stands (Liski et al. 2001). The
effect of alders on the N and C content of soil is significant and
fast: the N storage in the upper 10 cm soil layer had increased
from 1.40 to 1.72 t ha
-1
, while the respective increase in C
was from 18.2 to 24.3 t ha
-1
. The average C accumulation in
soil during the period 1998–2010 was 0.32 t C ha
-1
year
-1
and average N accumulation 28.3 kg ha
-1
year
-1
. However,
only 0.6 % of the total C input of the tree biomass of the
17-year-old grey alder stand is accumulated in fine roots.
Thus, C sequestration into soil via fine roots in studied alder
forest ecosystem is much smaller than via the above-ground
litter flux.
Conclusions
Bioproduction of grey alder stand growing on abandoned
agricultural land was very high at a young age; the species
can be considered suitable for SRF. The CAI of grey alder
fluctuates greatly, probably depending on weather condi-
tions in different years and the age of the stand. The FRB
dynamic in grey alder stand stabilized already at the stand
age of 10 years, and in the 17-year-old stand, it had not
increased. However, the FRB per tree had increased con-
tinuously throughout the stand development due to the
natural self-harvesting process and the decreasing number
of trees. A strong positive correlation was established
between FRB and stands basal area and stem mass. The NB
increased during stand development but at the same time,
the number of nodules decreased. However, the NB was
probably underestimated due to used methods. Grey alder
stand affects the N and C status of soil to a great extent;
however, it is mainly affected by the above-ground litter
flux. The contribution of fine roots to the sequestration of N
or C into soil is modest owing to their small biomass and
annual production. Due to favourable conditions, the
decomposition of fine roots was rapid and fine root nec-
romass in soil remains low.
Acknowledgments This study was supported by the Estonian Sci-
ence Foundation grant No. 9342 and by the Environmental Investment
Centre projects No. 11-10-8/196 and No. 3406. We would like thank
Ms. Ragne Rambi for revising the English text of the manuscript.
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