Directory UMM :Data Elmu:jurnal:S:Soil Biology And Chemistry:Vol32.Issue8-9.Aug2000:
Soil Biology & Biochemistry 32 (2000) 1091±1100
www.elsevier.com/locate/soilbio
Soil microbial activity and biomass in the primary succession of
a dry heath forest
Sami Aikio a,*, Henry VaÈre b, 1, Rauni StroÈmmer a, 2
a
Department of Biology, P.O. Box 3000, 90014, University of Oulu, Oulu, Finland
b
Botanical Museum, P.O. Box 3000, 90014, University of Oulu, Oulu, Finland
Accepted 2 February 2000
Abstract
Changes in vegetation, soil organic matter content, soil nutrient concentration, microbial activity and microbial biomass were
studied in Scots pine (Pinus sylvestris ) forests on the post-glacial land uplift island of Hailuoto in Finland, along altitudinal
transects representing about 1000 years of primary succession. The characteristics of microbial communities in the humus layer
were compared both within altitude classes and within TWINSPAN (two-way indicator species analysis) clusters of ®eld layer
vegetation. Non-metric multidimensional scaling (NMDS) was employed to reveal gradients in the data. During succession, the
vegetation changed from dominance by bryophytes and deciduous dwarf shrubs to evergreen dwarf shrubs and lichens. The
thickness of the humus layer and the amount of organic matter in the soil decreased along the succession, which in turn reduced
microbial biomass, microbial activity and soil nutrients when calculated on an areal basis. The nutrient concentration of the soil
OM (organic matter) showed no successional trend on a concentration basis but the C-to-N ratio of organic matter increased
with increasing soil age and lichen coverage. Thus, the nutrient availability decreased during succession but this could not be
demonstrated by calculating results against unit weight of organic matter. Soil basal respiration and microbial biomass increased
during the succession when calculated per unit weight of organic matter. The successional decrease in site productivity appeared
to be due to leaching of nutrients from the sandy mineral soil and thinning of the humus layer. Plants and soil microbes became
increasingly N limited during the course of the succession, suggesting the increased importance of mycorrhizal symbiosis for
plant performance and increased energy costs among soil microbes in nutrient uptake. 7 2000 Elsevier Science Ltd. All rights
reserved.
Keywords: Primary succession; Soil respiration; Scots pine; Nutrient leaching
1. Introduction
Age is a useful explanatory variable for many vegetation patterns, and a lot of research has been carried
out in constructing a mechanistic view of the processes
* Corresponding author. Tel.: +358-8-553-1530; fax:+358-8-5531061.
E-mail address: sami.aikio@oulu.® (S. Aikio).
1
Present address: Botanical Museum, P.O. Box. 7, 00014 University of Helsinki, Helsinki, Finland.
2
Present address: Department of Ecological and Environmental
Sciences, University of Helsinki, Niemenkatu 73, 15140 Lahti, Finland.
behind successional pathways (Connell and Slatyer,
1977; Tilman, 1982, 1985, 1988; Glenn-Lewin and van
der Maarel, 1992). However, there has been little
research into the changes in soil microbial activity and
biomass during the primary succession (Insam and
Haselwandter, 1989; Wardle and Ghani, 1995; Ohtonen et al, 1999), and few theoretical principles have
therefore been developed in this area. Soil fungi and
bacteria are the major organisms responsible for nutrient cycling and for controlling the amounts of nutrients available to plants. Plants in turn add energy to
the soil subsystem in the form of litter and root exudates, and act as symbiotic partners for mycorrhizal
fungi. Therefore, microbial succession should be stu-
0038-0717/00/$ - see front matter 7 2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 3 8 - 0 7 1 7 ( 0 0 ) 0 0 0 1 9 - 5
1092
S. Aikio et al. / Soil Biology & Biochemistry 32 (2000) 1091±1100
died in the context of the vegetation succession and
not merely as a function of soil age.
Plants exploit nutrients from their area of occupation and therefore nutrient availability and other
soil properties should be measured on volume or area
basis, in order to be relevant for explaining vegetation
patterns. Soil microbes are mostly decomposers and
are therefore dependent on the nutrient concentrations
of soil organic matter (OM). Microbial processes
should therefore be explained in terms of soil nutrient
concentrations relative to the unit mass of OM present
(VaÈre et al., 1996b; Ohtonen et al., 1997, 1999). However, when soil properties are discussed in the context
of ecosystem development, interpretations on areal
basis are most appropriate.
Net primary production increases in the early stages
of the primary succession, but often starts to decrease
in the middle or later stages when the ratio of photosynthetic to heterotrophic phytomass decreases and the
leaching of soil nutrients causes increased nutrient
limitation (Odum, 1969; Tilman, 1988; Peet, 1992).
The detritus of later successional coniferous forests
resists decomposition due to its high concentration of
recalcitrant compounds and low concentration of N.
Our hypotheses are that soil microbial activity and
biomass, when expressed on areal basis, are directly
proportional to measures of system productivity,
whereas the microbial properties per unit mass of OM
are directly proportional to measures of the decomposability of OM. The productivity of the system is
assumed to be proportional to the concentration of
nutrients per unit area of habitat. The decomposability
of soil OM is measured as the nutrient concentration
and the C-to-N ratio of OM.
We have tested these hypotheses by using data on
vegetation, soil microbial activity, microbial biomass
and soil nutrient concentrations during primary succession of Scots pine forests in a land uplift area. The importance of organic matter decomposition, nutrient
leaching and mycorrhizal symbiosis are discussed in
terms of ecosystem development.
2. Materials and methods
Soil samples and vegetation data were collected
from the island of Hailuoto (65802 'N, 24835 'E,
about 230 km2 in area) in the Gulf of Bothnia
between Finland and Sweden which belongs geobotanically to the intermediate part of the oceanic-continental sector of the middle-boreal vegetation zone
(Ahti et al., 1968; Tuhkanen, 1984).The annual mean
temperature is 1.98C and precipitation is 465 mm/year
(Institute of Meteorology, 1991). Hailuoto began to
emerge from the sea 1700±1800 years ago as a consequence of post-glacial land uplift and this uplift con-
tinues at the annual rate of 8.6±9.0 mm in this area
(Alestalo, 1979). This makes the age of a site proportional to its altitude above sea level. On sandy
shores, ¯uvial and aeolian processes have formed belts
of dunes running parallel to the shoreline. These dunes
have been dated dendrochronologically from trees buried in the sand, indicating that the 5 and 10 m contours correspond to where the shoreline was present
about 400 and 1000 years ago, respectively (Alestalo,
1971, 1979). The island becomes dominated by Scots
pine (Pinus sylvestris L.) on soils of age about 300
years, and the oldest soils on Hailuoto have been
forested for about 1000 years.
Three transects (labelled A, B and C) perpendicular to the shore line were established in Scots pine
forests, one of them situated in the south-western
part of the island and the other two in the northern part. The altitudes 2.5, 4, 5, 10 and 15 m a.s.l.
(labelled 1±5) on each transect were located in the
®eld according to a map of scale 1:20,000 and chosen as sites for closer examination. Five 100 m2
quadrats (labelled a±e) on the tops of dunes and
located 5 m apart were established perpendicular to
the transect at each site, giving 75 quadrats in all.
Each 100 m2 quadrat was given a code in which the
®rst capital letter indicates the transect, the following
numeral the altitude and the last small case letter the
quadrat, e.g. B4c is the quadrat c in the 10 m altitude
class on transect B. The vegetation cover was estimated on a percentage scale as an average of 10 systematically selected 1 m2 squares in each quadrat. The
nomenclature and identi®cation of species follows
HaÈmet-Ahti et al. (1998) for vascular plants, Koponen
(1994) for bryophytes and Vitikainen et al. (1997) for
lichens.
Soil samples were taken twice, in August 1995 and
August 1997. The 1995 samples, for microbial analysis,
were taken from the humus layer with a soil corer of 3
cm in diameter to a depth of 3 cm at 20 cm intervals
along the diagonal of each quadrat. The soil samples
were pooled for each quadrat and sieved through a 5
mm mesh over an ice bath and stored frozen before
analysis. Soil water and organic matter (OM) were
determined gravimetrically after drying two subsamples at 1058C for 12 h and after combustion at
4758C for 4 h, respectively. For the microbial analyses,
the soils were moistened immediately before analysis
to a 250% water content of OM, which is reported to
be the optimal amount for microbial respiration in forest soils (Nordgren et al., 1988). Samples C1d±e and
C5a±d had water content higher than 250% of OM
(max. 312%), and were not moistened. The 1997
samples, intended for nutrient analyses, were taken
with soil corer of 6 cm diameter through the entire
humus layer and the top 10 cm of the mineral soil.
The material was homogenized by hand but not sieved.
S. Aikio et al. / Soil Biology & Biochemistry 32 (2000) 1091±1100
Soil water and OM content were determined as above,
but the soils were not moistened.
Microbial analyses were performed on the 1995
samples in two replicates per quadrat using the Respicond II respirometer apparatus of Nordgren (1988)
with a soil quantity corresponding to 1 g OM (d.w.
bases). Basal respiration (Bas) was analysed for 40 h
of stable respiration rate after an initial respiration
pulse following the melting of the samples. A substrate
of 200 mg glucose, 103.7 mg (NH4)2SO4 and 10.1 mg
KH2PO4 was mixed into the samples in order to
obtain substrate-induced respiration (SIR; Anderson
and Domsch, 1978, as modi®ed by Nordgren et al.,
1988). SIR was transformed to microbial biomass carbon (Cmic) by the equation: Cmic (mg C g soilÿ1) =
22.24 SIR (m g CO2±C g soilÿ1 hÿ1) + 0.0037 (modi®ed from Anderson and Domsch, 1978).
The total N concentrations of the soil samples were
determined with micro-Kjeldahl method with three
replicates per quadrat (Kubin, 1978). Soluble P was
determined colorimetrically from CaCl2-solution (25
ml soil, 50 ml 10 mM CaCl2) according to the method
by John (1970). The same CaCl2-solution was also
used for pH-measurements. Electrical conductivity was
measured from a 1:2 soil:water extraction. The NH+
4
concentrations in the soil samples were determined by
the indophenol blue method of Page et al. (1982) with
three replicates. Exchangeable cations (Fe, K, Ca, Mg)
were determined in three replicates from the ammonium acetate extraction (25 ml soil, 125 ml 1 -M
NH4OAc, pH 4.65) with an atomic absorption spectrophotometer (AAS), according to Halonen et al. (1983).
The vegetation data were classi®ed by means of a
two-way indicator species analysis (TWINSPAN, Hill,
1979) to detect the convergence between vegetational
and altitudinal change. This analysis forms clusters of
vegetationally similar quadrats and detects one or
more species that are particularly good diagnostic dividers between clusters. The resulting clusters were compared with the altitudinal change. TWINSPAN
classi®cation was performed with the following pseudospecies cut-o levels:
www.elsevier.com/locate/soilbio
Soil microbial activity and biomass in the primary succession of
a dry heath forest
Sami Aikio a,*, Henry VaÈre b, 1, Rauni StroÈmmer a, 2
a
Department of Biology, P.O. Box 3000, 90014, University of Oulu, Oulu, Finland
b
Botanical Museum, P.O. Box 3000, 90014, University of Oulu, Oulu, Finland
Accepted 2 February 2000
Abstract
Changes in vegetation, soil organic matter content, soil nutrient concentration, microbial activity and microbial biomass were
studied in Scots pine (Pinus sylvestris ) forests on the post-glacial land uplift island of Hailuoto in Finland, along altitudinal
transects representing about 1000 years of primary succession. The characteristics of microbial communities in the humus layer
were compared both within altitude classes and within TWINSPAN (two-way indicator species analysis) clusters of ®eld layer
vegetation. Non-metric multidimensional scaling (NMDS) was employed to reveal gradients in the data. During succession, the
vegetation changed from dominance by bryophytes and deciduous dwarf shrubs to evergreen dwarf shrubs and lichens. The
thickness of the humus layer and the amount of organic matter in the soil decreased along the succession, which in turn reduced
microbial biomass, microbial activity and soil nutrients when calculated on an areal basis. The nutrient concentration of the soil
OM (organic matter) showed no successional trend on a concentration basis but the C-to-N ratio of organic matter increased
with increasing soil age and lichen coverage. Thus, the nutrient availability decreased during succession but this could not be
demonstrated by calculating results against unit weight of organic matter. Soil basal respiration and microbial biomass increased
during the succession when calculated per unit weight of organic matter. The successional decrease in site productivity appeared
to be due to leaching of nutrients from the sandy mineral soil and thinning of the humus layer. Plants and soil microbes became
increasingly N limited during the course of the succession, suggesting the increased importance of mycorrhizal symbiosis for
plant performance and increased energy costs among soil microbes in nutrient uptake. 7 2000 Elsevier Science Ltd. All rights
reserved.
Keywords: Primary succession; Soil respiration; Scots pine; Nutrient leaching
1. Introduction
Age is a useful explanatory variable for many vegetation patterns, and a lot of research has been carried
out in constructing a mechanistic view of the processes
* Corresponding author. Tel.: +358-8-553-1530; fax:+358-8-5531061.
E-mail address: sami.aikio@oulu.® (S. Aikio).
1
Present address: Botanical Museum, P.O. Box. 7, 00014 University of Helsinki, Helsinki, Finland.
2
Present address: Department of Ecological and Environmental
Sciences, University of Helsinki, Niemenkatu 73, 15140 Lahti, Finland.
behind successional pathways (Connell and Slatyer,
1977; Tilman, 1982, 1985, 1988; Glenn-Lewin and van
der Maarel, 1992). However, there has been little
research into the changes in soil microbial activity and
biomass during the primary succession (Insam and
Haselwandter, 1989; Wardle and Ghani, 1995; Ohtonen et al, 1999), and few theoretical principles have
therefore been developed in this area. Soil fungi and
bacteria are the major organisms responsible for nutrient cycling and for controlling the amounts of nutrients available to plants. Plants in turn add energy to
the soil subsystem in the form of litter and root exudates, and act as symbiotic partners for mycorrhizal
fungi. Therefore, microbial succession should be stu-
0038-0717/00/$ - see front matter 7 2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 3 8 - 0 7 1 7 ( 0 0 ) 0 0 0 1 9 - 5
1092
S. Aikio et al. / Soil Biology & Biochemistry 32 (2000) 1091±1100
died in the context of the vegetation succession and
not merely as a function of soil age.
Plants exploit nutrients from their area of occupation and therefore nutrient availability and other
soil properties should be measured on volume or area
basis, in order to be relevant for explaining vegetation
patterns. Soil microbes are mostly decomposers and
are therefore dependent on the nutrient concentrations
of soil organic matter (OM). Microbial processes
should therefore be explained in terms of soil nutrient
concentrations relative to the unit mass of OM present
(VaÈre et al., 1996b; Ohtonen et al., 1997, 1999). However, when soil properties are discussed in the context
of ecosystem development, interpretations on areal
basis are most appropriate.
Net primary production increases in the early stages
of the primary succession, but often starts to decrease
in the middle or later stages when the ratio of photosynthetic to heterotrophic phytomass decreases and the
leaching of soil nutrients causes increased nutrient
limitation (Odum, 1969; Tilman, 1988; Peet, 1992).
The detritus of later successional coniferous forests
resists decomposition due to its high concentration of
recalcitrant compounds and low concentration of N.
Our hypotheses are that soil microbial activity and
biomass, when expressed on areal basis, are directly
proportional to measures of system productivity,
whereas the microbial properties per unit mass of OM
are directly proportional to measures of the decomposability of OM. The productivity of the system is
assumed to be proportional to the concentration of
nutrients per unit area of habitat. The decomposability
of soil OM is measured as the nutrient concentration
and the C-to-N ratio of OM.
We have tested these hypotheses by using data on
vegetation, soil microbial activity, microbial biomass
and soil nutrient concentrations during primary succession of Scots pine forests in a land uplift area. The importance of organic matter decomposition, nutrient
leaching and mycorrhizal symbiosis are discussed in
terms of ecosystem development.
2. Materials and methods
Soil samples and vegetation data were collected
from the island of Hailuoto (65802 'N, 24835 'E,
about 230 km2 in area) in the Gulf of Bothnia
between Finland and Sweden which belongs geobotanically to the intermediate part of the oceanic-continental sector of the middle-boreal vegetation zone
(Ahti et al., 1968; Tuhkanen, 1984).The annual mean
temperature is 1.98C and precipitation is 465 mm/year
(Institute of Meteorology, 1991). Hailuoto began to
emerge from the sea 1700±1800 years ago as a consequence of post-glacial land uplift and this uplift con-
tinues at the annual rate of 8.6±9.0 mm in this area
(Alestalo, 1979). This makes the age of a site proportional to its altitude above sea level. On sandy
shores, ¯uvial and aeolian processes have formed belts
of dunes running parallel to the shoreline. These dunes
have been dated dendrochronologically from trees buried in the sand, indicating that the 5 and 10 m contours correspond to where the shoreline was present
about 400 and 1000 years ago, respectively (Alestalo,
1971, 1979). The island becomes dominated by Scots
pine (Pinus sylvestris L.) on soils of age about 300
years, and the oldest soils on Hailuoto have been
forested for about 1000 years.
Three transects (labelled A, B and C) perpendicular to the shore line were established in Scots pine
forests, one of them situated in the south-western
part of the island and the other two in the northern part. The altitudes 2.5, 4, 5, 10 and 15 m a.s.l.
(labelled 1±5) on each transect were located in the
®eld according to a map of scale 1:20,000 and chosen as sites for closer examination. Five 100 m2
quadrats (labelled a±e) on the tops of dunes and
located 5 m apart were established perpendicular to
the transect at each site, giving 75 quadrats in all.
Each 100 m2 quadrat was given a code in which the
®rst capital letter indicates the transect, the following
numeral the altitude and the last small case letter the
quadrat, e.g. B4c is the quadrat c in the 10 m altitude
class on transect B. The vegetation cover was estimated on a percentage scale as an average of 10 systematically selected 1 m2 squares in each quadrat. The
nomenclature and identi®cation of species follows
HaÈmet-Ahti et al. (1998) for vascular plants, Koponen
(1994) for bryophytes and Vitikainen et al. (1997) for
lichens.
Soil samples were taken twice, in August 1995 and
August 1997. The 1995 samples, for microbial analysis,
were taken from the humus layer with a soil corer of 3
cm in diameter to a depth of 3 cm at 20 cm intervals
along the diagonal of each quadrat. The soil samples
were pooled for each quadrat and sieved through a 5
mm mesh over an ice bath and stored frozen before
analysis. Soil water and organic matter (OM) were
determined gravimetrically after drying two subsamples at 1058C for 12 h and after combustion at
4758C for 4 h, respectively. For the microbial analyses,
the soils were moistened immediately before analysis
to a 250% water content of OM, which is reported to
be the optimal amount for microbial respiration in forest soils (Nordgren et al., 1988). Samples C1d±e and
C5a±d had water content higher than 250% of OM
(max. 312%), and were not moistened. The 1997
samples, intended for nutrient analyses, were taken
with soil corer of 6 cm diameter through the entire
humus layer and the top 10 cm of the mineral soil.
The material was homogenized by hand but not sieved.
S. Aikio et al. / Soil Biology & Biochemistry 32 (2000) 1091±1100
Soil water and OM content were determined as above,
but the soils were not moistened.
Microbial analyses were performed on the 1995
samples in two replicates per quadrat using the Respicond II respirometer apparatus of Nordgren (1988)
with a soil quantity corresponding to 1 g OM (d.w.
bases). Basal respiration (Bas) was analysed for 40 h
of stable respiration rate after an initial respiration
pulse following the melting of the samples. A substrate
of 200 mg glucose, 103.7 mg (NH4)2SO4 and 10.1 mg
KH2PO4 was mixed into the samples in order to
obtain substrate-induced respiration (SIR; Anderson
and Domsch, 1978, as modi®ed by Nordgren et al.,
1988). SIR was transformed to microbial biomass carbon (Cmic) by the equation: Cmic (mg C g soilÿ1) =
22.24 SIR (m g CO2±C g soilÿ1 hÿ1) + 0.0037 (modi®ed from Anderson and Domsch, 1978).
The total N concentrations of the soil samples were
determined with micro-Kjeldahl method with three
replicates per quadrat (Kubin, 1978). Soluble P was
determined colorimetrically from CaCl2-solution (25
ml soil, 50 ml 10 mM CaCl2) according to the method
by John (1970). The same CaCl2-solution was also
used for pH-measurements. Electrical conductivity was
measured from a 1:2 soil:water extraction. The NH+
4
concentrations in the soil samples were determined by
the indophenol blue method of Page et al. (1982) with
three replicates. Exchangeable cations (Fe, K, Ca, Mg)
were determined in three replicates from the ammonium acetate extraction (25 ml soil, 125 ml 1 -M
NH4OAc, pH 4.65) with an atomic absorption spectrophotometer (AAS), according to Halonen et al. (1983).
The vegetation data were classi®ed by means of a
two-way indicator species analysis (TWINSPAN, Hill,
1979) to detect the convergence between vegetational
and altitudinal change. This analysis forms clusters of
vegetationally similar quadrats and detects one or
more species that are particularly good diagnostic dividers between clusters. The resulting clusters were compared with the altitudinal change. TWINSPAN
classi®cation was performed with the following pseudospecies cut-o levels: