Forest Ecology and Management 205 (2005) 227–240
www.elsevier.com/locate/foreco
Soil carbon dynamics in a Sitka spruce (Picea sitchensis
(Bong.) Carr.) chronosequence on a peaty gley
Argyro Zerva*, Tom Ball, Keith A. Smith, Maurizio Mencuccini
School of GeoSciences (IERM), Edinburgh University, Darwin Building, Mayfield Road, Edinburgh EH9 3JU, UK
Received 22 January 2004; received in revised form 5 October 2004; accepted 12 October 2004
Abstract
We investigated whether the establishment of forests on organic grassland soils leads to significant losses in soil carbon, due
to the site preparation for the planting of trees and other disturbances. We also investigated whether subsequent biomass
accumulation over two consecutive rotations separated by a clearfell leads to a recovery in the initial soil carbon losses.
Soil respiration, soil carbon stocks and annual litter fall were measured, while allometric equations were used for the
estimation of above- and belowground biomass, in a replicated forest chronosequence of Sitka spruce (Picea sitchensis) on peaty
gley soil, in Harwood Forest (NE England). The sites chosen were: 40-year-old first rotation stands, 12, 20 and a 30-year-old
second rotation stands, one 18-month-old clearfelled site and unplanted natural grassland sites. The soil carbon stock of the firstrotation 40-year-old stands was 140 15 t C ha1, far lower than in the surrounding unplanted grasslands (274 54 t C ha1),
while clearfelling caused a further decline (100 13 t C ha1). Soil carbon accumulated again as the forest grew during the
second rotation (147 8, 181 17 and 249 40 t C ha1 at the 12, 20 and 30-year-old stands, respectively). Soil respiration
was the highest at the grassland site (14.2 3.1 t C ha1 year1), possibly due to high respiration by the grasses. After forest
establishment, soil respiration was: 2.3 0.9, 2.2 0.7, 5.4 0.7 and 5.0 0.4 t C ha1 year1 at the age of 12, 20, 30 and 40
years, while in the clearfelled site soil respiration was 5.6 1.6 t C ha1 year1.
The inputs and outputs of carbon into the soil were combined to evaluate the long-term effects of forest management on soil
carbon dynamics. It was concluded that the establishment of coniferous forests on peaty gley grassland soils in the uplands can
lead to a net accumulation of soil carbon during the second rotation.
# 2004 Elsevier B.V. All rights reserved.
Keywords: Soil respiration; Soil carbon stocks; Litter fall; Sitka spruce; Forest management
1. Introduction
* Corresponding author. Tel.: +44 131 650 5437;
fax: +44 131 662 0478.
E-mail address: [email protected] (A. Zerva).
Globally, soils contain more than two-thirds of the
total C stored in vegetation (Post et al., 1982; Eswaran
et al., 1993) and almost twice the amount in the
atmosphere (Schimel, 1995). Dixon et al. (1994)
0378-1127/$ – see front matter # 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.foreco.2004.10.035
228
A. Zerva et al. / Forest Ecology and Management 205 (2005) 227–240
estimated that forest ecosystems contain 1146 1015 g C while forest soils (including peaty soils)
contain approximately 69% of the total forest C
pool.
The amount of C stored in the soil is the balance
between inputs of organic material from the biota,
which depends on the type of vegetation and its
productivity at a particular site, and losses, primarily
through soil respiration (Post et al., 1982). Forests
continuously recycle C through photosynthesis and
respiration; however, the net sequestration of C in
vegetation and especially in soil can range over time
periods from years to centuries, depending on the
species, site conditions, disturbance regime and
management practices (Dixon et al., 1994).
Currently, forest plantations globally occupy an
area of 187 106 ha; however, they account for less
than 5% of the global forest cover (FRA, 2000).
Recent trends towards harvesting younger stands raise
concerns about how such forest management will
impact on soil processes and global carbon sequestration, as well as on site productivity and forest
biodiversity (Harmon et al., 1990; Johnson, 1992).
Forest plantations are usually planted in areas that did
not have forest cover before (at least in temperate
regions), such as grasslands or abandoned agricultural
land. For forest establishment, site preparation often
involves disturbing the soil, e.g. by the creation of
drainage ditches or ploughing. These practices may
accelerate organic matter decomposition by disturbing
soil structure and breaking soil aggregates, thus
leading to a loss of soil C (Turner and Lambert,
2000; Guo and Gifford, 2002).
Substantial losses of C from vegetation and soils
can also be caused by harvesting (Houghton, 2003).
Soil carbon storage is likely to initially decline after
clearcutting, because C inputs from plant production
are too low to counteract losses by soil respiration.
Furthermore, intensive forest management may also
lead to long term decreases in soil organic matter
content (Harmon et al., 1990). On the other hand,
regenerating forests and plantations may represent
important carbon sinks as a result of carbon storage in
both plant biomass and soils (IPPC, 2000). For a given
site, forest management may thus result in net
accumulation or loss of soil C, depending on the
balance between net photosynthesis (of trees) and the
various processes resulting in C export (Johnson et al.,
1995). Carbon accumulation rates during afforestation
depend on tree species and the length of the rotation
(Thuille et al., 2000).
In Britain, about 315,000 ha of shallow peatlands
(mainly peaty gleys) have been planted with
coniferous forests, mostly Sitka spruce (Picea
sitchensis (Bong.) Carr) (Cannell et al., 1993).
Afforestation on peaty soils may cause an increase
in the rates of oxidation of the peat due to improved
aeration by the drainage and the lowered water table
under a maturing tree stand (King et al., 1986).
Growing trees can sequester carbon in the aboveground biomass as well as in the litter layer and soil;
however, whether or not afforestation will give a net
benefit of C sequestration depends on the rate of peat
oxidation.
Soil carbon storage is an important factor in longterm ecosystem stability but slow changes in a large
pool are difficult to detect, although even small
changes in the soil carbon pool can result in relatively
large changes in fluxes of CO2 to the atmosphere
(Keith et al., 1997). Because of the difficulty in
determining changes in large pools, the analysis of soil
CO2 fluxes may be more informative.
Soils contribute about 50–76.5 1015 g C year1
to the atmosphere through soil CO2 efflux (Raich and
Schelesinger, 1992; Raich and Potter, 1995). True soil
respiration under field conditions is unknown (Giardina and Ryan, 2002). Different methods have been
used to measure soil respiration, such as open dynamic
chambers (Rayment and Jarvis, 1997), closed dynamic
chambers (Rochette et al., 1991; Kim et al., 1992) and
closed static chambers (Grahammer et al., 1991). The
closed static chamber method has sometimes been
criticised for underestimating the soil respiration
fluxes, compared to the closed dynamic chamber
method which has been shown to be more accurate for
a wide range of flux rates (Healy et al., 1996; Jensen
et al., 1996; Janssens et al., 2000). However, Rochette
et al. (1997) found little difference in fluxes measured
by either the closed dynamic or the static chamber
method.
Soil respiration is a combination of biotic, chemical
and physical processes. The two main sources of soil
respiration are the heterotrophic (decomposition of
organic compounds by soil microorganisms) and the
autotrophic (respiration of plant roots and rhizomes),
from different soil depths (Buchmann, 2000). Soil
A. Zerva et al. / Forest Ecology and Management 205 (2005) 227–240
respiration is a sensitive indicator of essential
processes in ecosystems such as: metabolic activity
of roots, mycorrhizae and other soil organisms,
decomposition of plant residues in soil and conversion
of soil organic carbon to atmospheric CO2 (Ewel et al.,
1987; Rochette et al., 1997). Several factors can affect
soil respiration rate, the most important one being soil
temperature (Loyd and Taylor, 1994; Kätterer et al.,
1998).
Litterfall is the largest natural flow of C and
nutrients to the forest floor (Berg and Meentemeyer,
2001). On a global scale, soil respiration increases
systematically with litterfall in forest ecosystems
(Raich and Nadelhoffer, 1989).
Roots play an important role in soil C cycling;
stand age and disturbances due to forest management
can affect the number and mass of roots present in the
soil (Grier et al., 1981; Vogt et al., 1983) and thus can
have a great impact on the C balance in the soil. A
significant amount of C is allocated to fine roots
annually, even though they comprise only a small
fraction of the C content of forest trees (Gower et al.,
1996). Accurate measurements of turnover of fine
roots and mycorrhizae are essential for understanding
and quantifying belowground carbon allocation
(Nadelhoffer and Raich, 1992; Ryan et al., 1997;
McDowell et al., 2001). However, this is the most
difficult carbon flux to measure (Vogt et al., 1986).
Raich and Nadelhoffer (1989) used the conservation of mass approach in order to estimate the
belowground C allocation for forest ecosystems
globally. Total belowground carbon allocation
(TBCA) is the sum of mycorrhizae and root (fine
and coarse) production, respiration and exudates. All
carbon that enters the soil must either leave the soil or
increase soil carbon stocks. Raich and Nadelhoffer
(1989) assumed that if the forest is near steady state,
the change in soil carbon stock will be near zero and
thus the main regulators of TBCA can be estimated
from measurements of annual rates of soil respiration
and aboveground litterfall. Many have followed their
example (e.g. Ryan, 1991; Smith and Resh, 1999);
however, this simple approach cannot be applied to
aggrading or disturbed forests (Gower et al., 1996). A
few studies have examined the TBCA patterns with
age and the findings are not consistent. Ryan et al.
(1997) concluded that TBCA may increase with stand
age, while Smith and Resh (1999) estimated that
229
TBCA declined with stand age in an age sequence of
Lodgepole pine (Pinus contorta L.) stands and
Giardina and Ryan (2002) concluded the same for
Eucalyptus saligna stands. Although TBCA may be a
large fraction of GPP (more than 30%, Gower et al.,
1996) and it is the primary source of detrital C to the
soil (Giardina and Ryan, 2002), the mechanisms that
control the allocation of carbon belowground are still
poorly understood.
The vital role of soils as a sink or source for C at the
global scale and in offsetting atmospheric CO2
concentrations (Johnson and Curtis, 2001) makes it
important to evaluate accurately the effects of forest
management on soil C storage.
Here we describe work in which we measured soil
C stocks, aboveground litterfall and soil respiration,
and estimated fine and coarse root production and
TBCA along a Sitka spuce (P. sitchensis) chronosequence, from natural unplanted grassland to second
rotation growth stands, in order to determine how
stand age and management practices affect the soil C
balance.
2. Materials and methods
2.1. Site description
The study area is located in Harwood Forest,
Northumberland, NE England (558100 N, 2830 W),
30 km inland from the North Sea coast. The size of
the forest is approximately 4000 ha and its elevation
varies from 200 to 400 m a.s.l. The average annual
rainfall is about 950 mm. The establishment of the
forest started in the 1930s and now Sitka spruce stands
of several different ages dominate the area. The
previous land cover was grassland (most abundant
species: Calluna vulgaris, Festuca ovina, Eriophorum
vaginatum, Deschampsia flexuosa). The forest is
managed with rotations of about 40 years, the cycle
being determined by the age at which risk of
windthrow becomes unacceptably high (mean annual
increment peaks at about 60 years of age). At this age a
whole stand is clearfelled and replanting takes place
after 2–3 years. Thinning in Harwood is extremely
limited because of the risk of windthrow.
The dominant soil type is peaty gley, i.e., a
seasonally waterlogged soil with a black-coloured,
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A. Zerva et al. / Forest Ecology and Management 205 (2005) 227–240
organic O horizon, varying in depth between 15 and
40 cm. The experimental sites were identified from
stock and soil maps. There was no understorey
vegetation in the forest stands after canopy closure.
After clearfelling, grasses (Juncus sp., Deschampsia
sp., Molinia caerulea, Holcus mollis) invaded the
site.
2.2. The chronosequence approach
The research was undertaken in stands of different
ages, an area where a mature stand had been
clearfelled, and areas under natural grassland that
were representative of the land cover prior to any
forest establishment. All stands were on peaty gley
soil. The following stands were used in the study: three
40-year-old, three 30-year-old, three 20-year-old, and
four 12-year-old. Two unplanted (grassland) areas
were also used, together with a single clearfelled area,
for which no comparable replicate was available.
In addition to comparisons made between stands of
similar age, intra-stand variability in relation to soil
carbon stocks and rates of litterfall were also
investigated, by sampling in replicated plots for only
one stand in each age class. Soil respiration studies
made use of multiple replicate microsites, all falling
within a radius of 15 m, within each of the investigated
stands. Details of the sampling procedures are given in
the relevant sections below.
2.3. Aboveground litter fall
To measure litterfall four circular traps (0.2 m2)
were randomly placed within a 2 m radius north, east,
south and west, respectively, from the centre of five
random plots within each stand. Traps were constructed by using water-permeable, reusable acetate
lining bags within frames made from 25 l plastic
containers, and mounted on wooden pegs, so that the
height of the trap opening was ca. 80 cm aboveground
level. The traps were installed in the 12, 20, 30 and 40year-old stands during May and June 2000. Litter was
collected for the first time in October 2000, and then
every 2 months from January 2001 until the end of
September 2001. After collection, all litter was dried
at 80 8C for 48 h and weighed. Average annual litter
fall was then calculated. A C content of 50% was
assumed for the litter.
2.4. Soil C stocks
2.4.1. Soil sampling
Soil sampling took place during the summer of
2000 and 2001. In summer 2000, a nested factorial
design was used to investigate the within-stand
variability (Anderson and McLean, 1974). Five plots
were randomly selected in a single stand in each of
four different ages (12, 20, 30 and 40-year-old,
respectively), as well as in an unplanted control site
(UN). All the sites (except the unplanted ‘‘control’’)
were part of a chronosequence selected for eddy
covariance measurements (Kowalski et al., 2004). All
the sites were in their second rotation, except for the
40-year-old one, which was in its first rotation. In each
plot eight samples were taken from eight points at
randomly selected distances from the centre of the plot
in clockwise order and within a radius of 10 m from
the centre. The samples were taken with a 45 cm long
soil auger with a cross-section of about 2 cm diameter
and were visually separated into three horizons: litter,
organic and mineral. The samples were put in
polyethylene bags and were stored in a cold room
(4 8C) pending preparation and analysis.
During summer 2001, additional stands of each age
were sampled (single, randomly selected plots in each
stand). These were three additional 12-year-old
stands, two additional for the 20, 30 and 40-yearold stands and one additional unplanted grassland
area. Results were averaged with the corresponding
stand mean obtained in 2000, to obtain the mean
values for the age class. The new stands were chosen
to be as close to each other as possible, in order to
avoid topographic influences on soil C. A single
clearfell area (clearfelled 18 months prior to sampling,
referred to as CF from now on) was also sampled, but
no further comparable areas were available.
The samples were taken using a manually driven
soil corer (5.5 cm diameter) with a slide hammer
attachment (Giddings Machine Company, Inc., U.S.),
to a depth of about 50 cm. The samples were kept in
the corer liners and were transferred to the laboratory,
where the depth of the total core and each horizon
(litter, organic and mineral) were measured and the
layers separated. The samples were kept in polythene
bags in a freezer (4 8C) till further analysis when
they were oven dried at 105 8C for 24 h (Jackson,
1958; Allen, 1989). Coarse fragments were removed
A. Zerva et al. / Forest Ecology and Management 205 (2005) 227–240
by hand and the soil was ground to pass a 0.5 mm
mesh.
2.5. Determination of C concentration
Two hundred and thirty samples from all layers
were analysed both in a C/N analyser (Carlo-Erba, NA
2500) and by loss on ignition (LOI). Finely ground
sub-samples of about 4 mg for the litter and the
organic layer and 10 mg for the mineral layer were
combusted in the C/N analyser, and their C
concentration was determined. Total C was assumed
to equal organic C as the samples did not come from a
calcareous soil. Other sub-samples of approximately
1 g (Allen, 1989) were weighed and then ignited in a
furnace at 500 8C, for 5 h. After burning the samples
were weighed again and the percentage loss of mass
(L, %) was calculated.
The C (%) obtained from the C/N analyser and the
mass loss (L, %) obtained from the LOI were found to
be significantly related to each other. Also a significant
effect of soil layer was found (data not shown).
Therefore separate regression equations were calculated for each layer and were used to estimate the C
(%) for the remaining samples on the basis of the LOI
method only. The regression equations used were:
Cð%Þ ¼ 0:513L ð%Þ 0:092;
R2 ¼ 0:99 for the litter layer;
Cð%Þ ¼ 0:542L ð%Þ þ 0:184;
R2 ¼ 0:99 for the organic layer;
Cð%Þ ¼ 0:533L ð%Þ 0:700;
R2 ¼ 0:99 for the mineral layer:
(1)
(2)
(3)
2.6. Soil respiration measurements
Soil respiration was measured weekly or biweekly,
from July 2001 to October 2002, in the 40-year-old
stand, while in the CF, 20 and 30-year-old stands
measurements were taken biweekly or once a month.
In the 40-year-old stand and in a recently clearfelled
site soil respiration was measured using two methods.
With the first method, 10 collars (diameter = 10 cm,
height = 5 cm) were permanently inserted to a depth
of approximately 3 cm. A visual examination con-
231
firmed that no roots were cut. Soil respiration was
measured with a portable, dynamic closed chamber
system (EGM-3, SCR-1, PP-Systems, Hitchin, UK),
equipped with a portable infrared gas analyser (IRGA),
with a slightly modified chamber to obtain an effective
gas seal. A small, low-speed fan inside the chamber
ensured mixing of air during the measurements while a
mesh at the bottom of the chamber eliminated potential
Venturi effects. Fan speed tests showed very small
pressure differentials (0.1 Pa) at the mesh.
The second method employed was the static closed
chamber (CC) technique. Twelve chambers consisting
of PVC cylinders (inside diameter = 40 cm and height
20 = cm) open at the top and the bottom were inserted
into the soil to a depth of about 5 cm to create a gas
tight seal. An aluminium sheet with a foam rubber
sealing ring on the under side acted as a lid on the top
of the chamber during the period of the measurement.
The chambers were left permanently in the field in
order to minimise the effects of disturbance caused by
their insertion in the soil. After taking an initial sample
of ambient air, the chambers were kept closed for 1 h.
At the end of this period air samples from inside the
chambers were taken with 60 ml syringes. The
samples were transferred to the laboratory and gas
chromatographic analysis (Perkin Elmer gas chromatograph fitted with a thermal conductivity detector)
was used for determination of CO2 within 24 h of their
collection. The CO2 concentrations in the chambers
showed an almost linear increase over time.
Soil respiration at the other sites was measured with
the CC method on 8–16 chambers (of diameter 20–
40 cm). To allow a comparison between C stocks and
CO2 efflux measurements at all sites, we also
estimated the annual respiration flux at the 12-yearold stand from a relationship obtained between annual
litterfall and annual soil respiration (R2 = 0.93, n = 4).
Soil temperature was measured with a digital
temperature probe (Fisher Scientific) inserted adjacent
to each collar and chamber, to 5 cm depth, every time a
measurement of soil CO2 efflux was taken.
2.7. Root biomass
Fine root biomass, MFR (t ha1) was estimated
from the equation:
MFR ¼ 0:12 age þ 7:23;
(4)
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A. Zerva et al. / Forest Ecology and Management 205 (2005) 227–240
R2 = 0.94, from Dimitriadis (2000) who used a C
balance approach to estimate the amount of carbon
allocated to fine roots.
Coarse root biomass was estimated from empirical
allometric equations (Dimitriadis, 2000):
MCR ¼ 0:0149 d02:3302 ;
(5)
where MCR is the coarse root biomass:
d0 ¼ 2:4 þ 6:9 0:85DBH þ 1:4DBH
(6)
and DBH is the tree diameter at breast height (1.33 m).
Annual changes in fine and coarse root biomass
were estimated from the same allometric equations,
while the change in DBH was estimated from
measured annual mean growth data for each age
class (Van Der Eb, 2002). Root biomass (fine and
coarse) was assumed to be 50% C.
2.8. Total belowground carbon allocation (TBCA)
Total belowground allocation (TBCA) was estimated by using a conservation of mass approach as in
Giardina and Ryan (2002), where outputs from the
belowground system must equal inputs minus any
change in storage over a defined time period:
FS þ FE ¼ TBCA þ FA ðDCS þ DCR Þ=Dt;
(7)
where FS is the soil respiration, FE the export of C
(CH4 flux or erosion or leaching), TBCA the total of
root respiration, carbohydrates used for mycorrhizae
or exudates and production of fine roots), FA the
aboveground litterfall, DCS the change is soil C stock,
DCR the change in C stored in roots (fine and coarse)
and Dt = 1 year for this study. All the components are
expressed in t C ha1 year1.
Thereafter, TBCA can be expressed by difference
by measuring fluxes out of the soil (FS and FE), into
the soil (FA) and any change in the C storage
((DCS + DCR)/Dt):
the first rotation 40-year-old stand and the unplanted
grassland site, divided by the period length, while for
second rotation the DCS was estimated by the difference in C stocks between different age classes divided
by the period length, and with starting value the C
stock in the clearfelled site.
The variance in the TBCA was estimated from the
sum of the variances of the other components, with the
exception of DCR, since this term was estimated from
an allometric equation. However, compared to the
other fluxes, DCR is a very small component in the
TBCA equation therefore variance was assumed to be
negligible and was ignored.
2.9. Statistical analysis
Because of the lack of stand replication, the
significance of the differences in soil respiration or
litterfall among stands of different age could not be
tested. However, the means for the replicate plots
within each stand and the standard errors were
calculated. For the soil C stocks, means for each
stand were similarly calculated and in turn averaged to
give means for each age class. One-way ANOVA was
then used to test for significant differences among age
classes.
3. Results
3.1. Components of the TBCA budget
(8)
3.1.1. Litterfall
Mean annual litterfall mass ranged from 1.1 to
1.9 t C ha1 year1 (Table 1). The litterfall was almost
the same in the 12 and 20-year-old stands (1.1 0.2
and 1.1 0.3 t C ha1 year1, respectively) and it
increased as the stands grew older to 1.7 0.3 t C ha1 year1 in the 30-year-old and
1.9 0.2 t C ha1 year1 in the 40-year-old stand.
The fluxes of C in leaching, runoff and erosion were
ignored, but these are probably minor in most closed
canopy forests (Raich and Nadelhoffer, 1989). The
annual soil CH4 flux in the 40-year-old stand was
0.05 0.03 t C ha1 year1 (Zerva et al., 2003), and
because it was so low it was assumed to be zero in the
estimation of TBCA. For the first rotation, the DCS
was estimated by the difference in C stocks between
3.1.2. Soil C stocks
Soil C stocks across the chronosequence are shown
in Fig. 1. The planting of trees led to a decrease in soil
C stocks from 274 54 t C ha1 in the unplanted sites
(UN) to 140 15 t C ha1 (P < 0.001) in the first
rotation 40-year-old stands. Clearfelling at the end of
first rotation led to a further decrease in soil C to
TBCA ¼ FS þ FE FA þ ðDCS þ DCR Þ=Dt:
A. Zerva et al. / Forest Ecology and Management 205 (2005) 227–240
233
Table 1
Flux compounds of the total belowground carbon allocation
Stand age
(years)
FS
(t C ha1 year1)
FA
(t C ha1 year1)
MFR
(t C ha1)
MCR
(t C ha1)
DCR(F + C)
(t C ha1 year1)
DCS
(t C ha1 year1)
UN
40, first rotation
CF
12
20
30
14.2
5.0
5.6
2.3
2.2
5.4
–
1.9
–
1.1
1.1
1.7
–
2.4
–
5.8
4.8
3.6
–
56.3
–
11.1
24.0
27.1
–
1.2
–
0.5
0.9
0.8
–
3.4
–
3.9
4.3
6.8
(3.1)
(0.4)
(1.6)
(0.9)
(0.7)
(0.7)
(0.2)
(0.2)
(0.3)
(0.3)
(1.4)
(1.3)
(1.1)
(1.4)
FS is the soil respiration, FA the litterfall, MFR the fine root biomass, MCR the coarse root biomass, DCR(F + C) the change in root biomass (fine plus
coarse) over a year and DCS the change in soil C stocks over a year. The numbers in the brackets represent the standard error of the mean.
100 13 t C ha1. Soil started accumulating C again
during the second rotation, with soil C stocks of
147 8, 181 17, and 249 40 t C ha1 in the 12,
20 and 30-year-old stands, respectively. The soil C
stocks in the 30-year stands were similar to that in the
UN site (P > 0.05).
3.1.3. Soil respiration
For the two sites where respiration was measured
with both methods, the two series were linearly
correlated
(CO2(PP-Systems) = 1.77 CO2(CC),
R2 = 0.84, Fig. 2). Further comparisons of the two
methods by using a soil monolith in a controlled
environment indicated that the static closed chamber
method underestimated the soil respiration fluxes
(Zerva, 2004) and the above relationship was used to
adjust the CC soil respiration values to those given by
the dynamic closed chamber system (PP-Systems)
method. All values cited below are in terms of those
given by the dynamic closed chamber method.
Annual soil respiration ranged from 2.2 0.7 to
14.2 3.1 t C ha1 year1, with the lowest value in
the 20-year stand and the highest in the UN (Table 1).
The CF had similar soil respiration rates to the mature
(40-year-old) stand, 5.6 1.6 and 5.0 0.4 t C ha1
year1, respectively. Soil respiration was 2.3 0.9 t C ha1 year1 in the 12-year-old, and 2.2 0.7 t C ha1 year1 in the 20-year-old, but more than
doubled to 5.4 0.7 t C ha1 year1 in the 30-yearold and 5.0 0.9 t C ha1 year1 in the 40-year-old
stand. As mentioned before, annual soil respiration
was linearly related to annual litterfall (R2 = 0.93,
n = 4) for the four stands for which measurements
were available.
Soil respiration showed a strong seasonal trend at
all sites, with higher fluxes during the summer and low
fluxes during the winter (Fig. 3).
Fig. 1. Soil C stocks (t C ha1) along the Sitka spruce chronosequence. The vertical bars represent the standard error of the mean.
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A. Zerva et al. / Forest Ecology and Management 205 (2005) 227–240
Fig. 2. Linear relationship between soil respiration (g CO2 m2 day1) measured with the static closed chamber method and the dynamic closed
chamber method (PP-Systems) in the 40-year-old stand and a recently clearfelled site. The regression was forced through the origin.
Soil respiration data combined for all forest stands
and all seasons was strongly related to soil temperature, with an exponential relationship:
RS ¼ 0:50 e0:25T5
ðR2 ¼ 0:56; apparent Q10 ¼ 13:3Þ;
where RS is soil respiration (g CO2 m2 day1) and T5
is the soil temperature at 5 cm depth (8C). Most of the
variability around this relationship was accounted for
by the differences across stands and age classes
(Zerva, 2004).
3.1.4. Root biomass
Modelled fine-root biomass decreased from
5.8 t ha1 in the 12-year to 2.4 t ha1 in the 40-year
stand (Table 1). In contrast coarse root mass increased
from 11.1 t ha1 at the 12-year to 56.3 t ha1 in the
40-year (Table 1).
3.1.5. Total belowground carbon allocation (TBCA)
Fig. 4 gives all the values employed to calculate
TBCA for the four studied age classes. The values of
some additional parameters are listed in Table 1.
TBCA was found to range from 1.0 0.9 t C ha1
Fig. 3. Monthly soil respiration (t C ha1) in the chronosequence. Soil respiration follows the same seasonal trend at all sites. Values calculated
using the dynamic closed chamber method. The vertical bars represent the standard error of the mean.
A. Zerva et al. / Forest Ecology and Management 205 (2005) 227–240
235
Fig. 4. Total belowground C allocation and its components in the forest stands of first and second rotations. The vertical bars represent the
standard error of the mean.
year1, in the 40-year-old stand in first rotation to
11.3 1.2 t C ha1 year1, in the 30-year-old stand
second rotation.
Soil respiration was the largest flux contributing to
TBCA, for the 40-year-old stands, while DCS/Dt was
the largest flux for the second rotation stands, 12, 20
and 30-year-old and stands (Fig. 4).
4. Discussion
4.1. Litterfall
The aboveground litterfall values in this study (1.1–
1.9 t C ha1 year1) are within the range of 0.57–
3.48 t C ha1 year1 for temperate forests, referred to
by Gower et al. (1996). The values increased with age,
but this trend could not be tested statistically because
of the absence of stand replication. Litterfall values are
also similar to those measured by Pedersen and BilleHansen (1999) in 35 years old Sitka spruce and
Norway spruce on poor soil in Denmark during 6
years.
4.2. Soil C stocks
The unplanted grassland (UN) in the forest area
contained 274 54 t C ha1, which agrees with the
estimation by Cannell et al. (1993) of soil C in the
range of 200–240 t C ha1 in shallow peat (peaty
gleys and peaty ironpan soils) in Britain. However, soil
C stocks in the 40-year-old stands were only
140 15 t C ha1, suggesting a major decrease
following afforestation, possibly due to the accelerated decomposition of soil organic matter caused by
improved aeration, initially by drainage for the
planting of trees and then by a natural lowering of
the water table under the trees, as observed in the
nearby Kielder Forest by King et al. (1986). The loss
due to the conversion of grassland to forest
corresponds to a decrease of about 2.7 t C ha1
year1, which agrees with the estimate made by
Armentano and Menges (1986), of 2.81 t C ha1
year1 in the temperate region.
Soil C stocks in the CF site were considerably
lower than in the 40-year-old stand. Although the
difference in the soil C cannot be definitely related to
clearfelling, as only the one clearfell site was available
for sampling, there is evidence from other work that
increased decomposition and the cessation of litter
inputs after clearfelling may lead to such a decrease.
Ballard (2000) indicated that clearfelling changes the
soil temperature regime, which is likely to be
significant in contributing to increased biological
activity and increased rates of organic matter
decomposition. Smethurst and Nambiar (1990) found
that clear felling of a Pinus radiata plantation caused a
decrease in the soil C of about 14 t C ha1 during the
first 3 years after planting on sandy podzol soil in
south-eastern Australia, while Knoepp and Swank
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A. Zerva et al. / Forest Ecology and Management 205 (2005) 227–240
(1997) found that soil C declined slightly in the 0–
10 cm depth following clearfelling in a white pine
plantation in the southern Appalachians in the USA.
Although several other authors have indicated that
clearfelling may not cause large declines in soil C
stocks (Johnson and Curtis, 2001; Johnson, 1992;
Pennock and van Kessel, 1997), in Harwood clearfelling
is accompanied by additional soil disturbances which
may stimulate C loss, e.g., restoration of the ditches to reactivate drainage channels, and mounding, a technique
by which about 10–15% of the soil surface to about
30 cm depth is turned over in patches of about 0.5 m2
each to create elevated mounds, on which the new
transplants (1 + 1) are planted.
The increase of soil C stocks in the stands growing
in second rotation indicates that soil C stocks can
recover towards the end of this second cycle to values
approaching those prevailing before the initial
planting, some 75 years earlier. Wilde (1964) found
that soil organic matter concentration (%) at a depth of
15 cm increased linearly with stand age (13–48 years)
in red pine plantations in Wisconsin. He also found a
faster increase with age (12–30 years) in the soil
organic matter content in a jack pine plantation in the
same area. Black and Harden (1994) studied the soil
carbon storage in a mixed conifer chronosequence in
California and found an initial loss of about 15%
(30 t ha1) of organic C from the soil within 1–7 years
after harvesting. The loss continued until the forest
was 17 years old (another 15%). The carbon
accumulation rates exceeded rates of loss after 80
years of re-growth, but carbon storage had declined
and it was not likely to recover to pre-harvest levels.
On the other hand, Boone et al. (1988) estimated
that it took more than 100 years for the organic layer in
a Tsuga mertensiana (Bong.) Carriere forest to recover
to the pre-disturbance values in thickness and carbon
storage in Oregon, USA. Switzer et al. (1979) found a
steady state in the organic layer carbon pools after
about 70 years of old field succession to oak–hickory–
pine forests in eastern Mississippi, USA.
4.3. Soil respiration
The annual FS in the UN site was far higher
compared to the FS from forest stands or the CF site.
This is in agreement with Raich and Tufekgcioglu
(2000) who reported consistently greater soil respira-
tion rates in grasslands than in forests under similar
conditions, world-wide. This appears to be because
grasses, with virtually no allocation of C to wood
production, may have more photosynthate available to
allocate belowground than trees do (Raich and
Tufekgcioglu, 2000).
The annual FS fluxes in the forest stands were much
lower (about a third to one-half) than the mean rates
for temperate coniferous forests reported by Raich and
Schelesinger (1992) and those estimated by Law et al.
(1999), in mixed age stand of ponderosa pine in
Oregon. On the other hand, our measured fluxes are
similar to those reported by Wingate (2003) for a
similar Sitka spruce stand in Griffin (Scotland).
Rates of FS at the clearfell site were similar to those
in the 40-year-old (first rotation) stand. Londo et al.
(1999) reported higher soil respiration rates in a
clearfelled bottomland hardwood forest in Texas
between 6 and 22 months after clearfelling. They
also reported vigorous vegetation recovery in the first
growing season following harvesting from rapid
invasion of herbaceous species. However, Striegl
and Wickland (1998) found that clearfelling of a
boreal jack pine (Pinus banksiana Lamb.) forest in
Canada reduced soil respiration to about 40% of that in
an uncut stand of similar age (60–90-year-old), in the
first season following harvest. They attributed the
major part of this reduction to destruction of nearsurface soil autotrophic and heterotrophic respiration
and to tree-root die-off. At our site, colonisation by
grasses and shrubs is generally vigorous after about
one or two years since harvesting. The data reported
here are for the third year after clearfelling.
4.4. Roots
Our estimations of fine root biomass in the
chronosequence (except for the 40-year-old stand)
are within the range of 3.5–11 t ha1, as estimated by
Fogel (1985) for coniferous forests. The estimation of
fine root biomass with Eq. (4) gives results in
agreement with Deans (1981), who estimated fine
root biomass (<2 mm) of 5.2 t C ha1 for a 16-yearold Sitka spruce plantation. If this age is used in the
above equation we obtain 5.3 t C ha1. Fine root
biomass was estimated to decrease with stand age; this
was similar to the trend observed by John et al. (2001)
in Pinus kesiya stands in north east India. Vanninen
A. Zerva et al. / Forest Ecology and Management 205 (2005) 227–240
and Makela (1999) studied fine root biomass in Scots
pine (Pinus sylvestris) stands of different ages in poor
and fertile stands in Finland. They found that fine root
biomass increased with age at the poor site, while root
biomass decreased with stand age at the fertile sites.
Vogt et al. (1983) found that fine root biomass
decreased after canopy closure in a Douglas fir
(Pseudotsuga menziesii (Mirb) Franco) chronosequence in Washington.
Coarse root mass was estimated to increase with
stand age, as expected, since coarse roots primarily
serve a support function and need to increase with
stand size and age (Giardina et al., 2003). Such an
increase in coarse root biomass with age was also
shown by John et al. (2001) for Pinus kesiya.
4.5. Total belowground carbon allocation (TBCA)
The TBCA in this study for the stands growing in
second rotation is within the range of 2.33–
10.13 t C ha1 year1 for temperate forests referred
to by Gower et al. (1996), and the global range of 2.6–
11 t C ha1 year1 by Raich and Nadelhoffer (1989).
However, Raich and Nadelhoffer (1989) only estimated TBCA in near-steady-state forests; the chronosequence in this study cannot considered to be steady
state, since it is probably still affected by the land use
change which took place between 40 and 70 years ago.
TBCA increased with stand age in stands growing
in second rotation from 12 to 30 years old. However,
Giardina and Ryan (2002) found a linear decline with
age in TBCA in a Eucalyptus saligna stand over a
period of 4 years, from 0.224 t C ha1 year1 in year 1
to 0.161 t C ha1 year1 in year 4. Similarly Smith
and Resh (1999) found a decline of TBCA with age in
lodgepole pine (Pinus contorta) stands in Wyoming.
As a further check, we compared our estimated
rates of TBCA with values of GPP measured with eddy
covariance. This comparison showed that between 33
and 57% of GPP was allocated belowground in the 20
and 30-year stands at our sites (Clement et al., 2003;
Kowalski et al., 2004). Law et al. (1999) found that
about 61% of GPP was allocated belowground in a
ponderosa pine (Pinus ponderosa) forest in Oregon,
which consisted of old (250-year-old), young (45year-old) and mixed-aged stands, whereas Giardina et
al. (2003) estimated that TBCA was about 50% of GPP
in a Eucalyptus salinga plantation during 4 years of
237
measurements. Therefore, our comparison suggested
that the rates of carbon flowing belowground
estimated from eddy covariance estimates of productivity and the TBCA calculated using a carbon balance
approach agreed to a considerable extent.
Total belowground carbon allocation has been
reported to increase with increased litterfall (Raich
and Nadelhoffer, 1989). Although this report was for
closed canopy forests near steady state, the trend
matched that observed for our stands growing in a
second rotation, despite the fact that litterfall was not
the main factor contributing to TBCA.
Accurate estimations of TBCA depend on measuring
the annual fluxes of inputs, outputs and changes in soil C
stockandroot masswitha reasonableprecision.SinceFS
and DCS are the major fluxes controlling TBCA they
have the greatest potential contribution to the error in the
estimation of TBCA. Different methods for measuring
FS can give different values and a correction factor may
be needed (Norman et al., 1997). In this study, FS was
measured with static closed chambers for most of the
sites, and a correction factor using the dynamic closed
chamber method was required. Also theFS in the 12-year
stand had to be estimated, as no soil respiration
measurements were available at this site.
DCS can be negative during the first rotation due to
decomposition of the drying peat and positive during
second rotation when C starts accumulating again as
the trees produce more and more litter. Measurements
at smaller time intervals would be required in order to
determine changes in the storage of soil C more
accurately.
In summary, average estimates of TBCA suggest
fairly high rates of C storage belowground as a result
of the high productivity of plantations of Sitka spruce
in the British Isles. However, our estimates of soil
respiration appear lower than equivalent estimates for
temperate coniferous forests. The resulting substantial
rates of C accumulation in the soil of second rotation
forests found in this study are remarkable, but similar
to values found for Sitka spruce stands in Ireland (K.
Byrne, personal communication).
5. Conclusions
The establishment of Sitka spruce forests on
previous grassland on peaty gley soils may lead to
238
A. Zerva et al. / Forest Ecology and Management 205 (2005) 227–240
a decrease in soil C during the first rotation but also to
net accumulation of soil carbon during a second
rotation, bringing the soil C stock back to a similar
level to that prevailing in the grassland prior to
afforestation. When the standing tree biomass is also
taken into account, a mature second rotation forest
system with a restored level of soil C will have more
total C than the grassland and thus constitute a
substantial C sink.
Also, C accumulation in the soil occurring during
the second rotation was probably caused by fairly high
rates of C storage belowground, coupled to low rates
of soil respiration.
A more intensive investigation of C efflux and
storage in the chronosequence over a longer period is
required to better understand the soil C balance of
these forests.
Acknowledgements
We wish to acknowledge the help of Johanna Pulli
who carried out the litterfall measurements, and
Massimo Quinto, Henrike Gabler and Leonie FitzGerald who helped with collecting and analysing the
soil samples. We also acknowledge support for Argyro
Zerva from the Greek State Scholarship Foundation
(I.K.Y.), and for Tom Ball through NERC grant no.
NER/A/S/1999/00053. Additional resources were
provided through EU CARBO-AGE contract no.
EVK2-CT-1999-00045 and NERC grant no. GR9/
4806.
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