Soil Biology & Biochemistry 82 (2015) 74e80

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Soil Biology & Biochemistry

journal homepage: www.elsevier.com/locate/soilbio

Logging residue harvest may decrease enzymatic activity of boreal

forest soils
Bartosz Adamczyk*, Sylwia Adamczyk, Mikko Kukkola, Pekka Tamminen, Aino Smolander
Finnish Forest Research Institute, Vantaa Unit, P.O. Box 18, FIN-01301 Vantaa, Finland

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 30 August 2014
Received in revised form
4 December 2014
Accepted 25 December 2014
Available online 8 January 2015

Nowadays conventional stem-only harvest where logging residues are left on the site is often displaced
by whole-tree harvest, in which logging residues are harvested for use as bioenergy. Logging residues
consist of tree branches and tops of stems with needles. The aim of this study was to evaluate the effect
of logging residue harvest on soil enzyme activities involved in C, N and P cycling, namely b-glucosidase,
b-glucosaminidase, protease and acid phosphatase in relation to other soil characteristics (i.e. soil
respiration, net N mineralization, microbial biomass C and N). Soil samples were taken from the humus
layer of ve study sites, differing in fertility, dominating tree species and time elapsed after treatment.
The study sites were Norway spruce (Picea abies, (L.) Karst) and Scots pine (Pinus sylvestris L.) stands in
different parts of Finland. Four of the study sites were single-tree experiments, where thinning was
performed 4e5 years before this study and 3e4 different doses of logging residues (from 0 up to
37.5 Mg ha
1) were distributed on a circle around a single tree in 3 replicates. The last eld experiment
had been thinned twice, 23 and 13 years ago; the treatments in 3 replicates were whole-tree harvest and
stem-only harvest. In the whole-tree harvest vs. stem-only harvest experiment, activities of b-glucosidase, b-glucosaminidase, acid phosphatase were similar in both treatments. In general, in the single-tree
experiment with pine, enzymes raised the activity in response to increasing amount of logging residue.
The pattern was less clear for the spruce single-tree experiment, but acid phosphatase and protease
activities increased with the increase in amount of logging residue. In general, other soil characteristics
were less affected than enzyme activities by logging residue removal; however, in some sites logging
residues seemed to increase net C and N mineralization with increasing logging residue amount. Our
results suggest that retaining logging residues on the site can increase soil enzyme activities and C and N
mineralization.
2015 Elsevier Ltd. All rights reserved.

Keywords:
Boreal forest soil
C and N transformations
Enzyme activities
Logging residue harvest
Picea abies
Pinus sylvestris

1. Introduction
According to Kyoto Agreement, nations must maintain emission
of CO2 on the same level as in the year 1990 (Hakkila, 2006). This
aim can be partly achieved by the use of renewable bioenergy, such
as bioenergy from the forest logging residues (Nurmi, 2007). It is
assumed that burning of logging residues does not increase CO2
emissions like fossil fuels in long-term (Schlamadinger et al., 1995).
However, logging residue harvest may potentially affect forest
productivity.
In traditional forest management only tree stems are removed
(stem-only harvest, SOH). In whole-tree-harvest (WTH), most of

* Corresponding author: Tel.: 358 10 211 2595; fax: 358 10 211 2206.
E-mail address: Bartosz.Adamczyk@metla. (B. Adamczyk).
http://dx.doi.org/10.1016/j.soilbio.2014.12.017
0038-0717/ 2015 Elsevier Ltd. All rights reserved.

the aboveground tree parts are removed, namely stems, branches

and stem tops with needles. Logging residues are harvested in both
clear-cutting and thinning stands (Rolff and gren, 1999). In thinning stands, whole-tree harvest has been shown to decrease forest
productivity (Helmisaari et al., 2011; Kaarakka et al., 2014). Wholetree harvest resulted in a long-term decrease in tree growth in both
Norway spruce stands and Scots pine stands, the decrease was
larger in spruce (5 and 13% during the rst and second 10-year
periods, respectively) than in pine stands (4 and 8%) (Jacobson
et al., 2000; Helmisaari et al., 2011). Reduction of growth may be
caused by a decrease in nutrient supply. Leaving logging residues
on the site after thinning exposes these materials to the mineralization process, and the mineralized nutrients can be utilized by the
nen et al., 2000).
remaining trees (Hyvo
Logging residues with needles provide rich input of nutrients to
the forest ecosystem, but also provide compounds that affect soil

B. Adamczyk et al. / Soil Biology & Biochemistry 82 (2015) 74e80

properties and decomposition processes, including enzyme activities. Whole-tree harvest in Norway spruce and Scots pine stands
decreased the rates of net N and C mineralization (Piatek and Allen
1999; Smolander et al., 2008, 2010, 2013) and the total C and N
pools in the combined organic mineral soil layer compared to the
SOH treatment were decreased in a Norway spruce stand (Kaarakka
et al., 2014). However, some sites showed little response to the
logging residue harvest (e.g. Brais et al., 2002; Johnson et al., 2002;
Smolander et al., 2013).
Changes in site productivity and soil decomposition processes
after logging residue harvest may originate from changes in the
enzyme machinery in the soil, as enzymes are the keys to making
nutrients available to plants. Enzyme activities in different forest
soils were widely studied before (reviewed by Caldwell, 2005 Burns
et al., 2013; Baldrian, 2014). It was shown that thinning decreased
the enzyme activities in comparison with undisturbed forest (Geng
et al., 2012) and that wildre mitigation strategies modify soil
enzyme activity (Boerner et al., 2006). Ponder and Eivazi (2008)
showed that excluding weeds from the growing forest site of oakhickory (Quercus- L. e Carya Nutt.) reduced soil enzyme activity.
However, it is not known how different amounts of logging residues affect the soil enzymatic activity. In this study we determined
the inuence of logging residue harvest on enzyme activities and
other soil characteristics in the soil organic layer of thinned stands
in a boreal forest. We hypothesize that harvest of logging residue
decrease the enzyme activities and C and N mineralization. Mechanically, the decrease in enzyme activities may be caused by
diminished amount of substrates due to logging residue harvest.
We report the activities of: a) b-glucosidase, degrading cellulose to
glucose, b) b-glucosaminidase degrading chitin to amino sugars; bglucosaminidase (chitinase) is one of the enzymes that play a major
role in N mineralization (Ekenler and Tabatabai, 2002), c) protease
releasing amino acids from peptides/proteins (Nduwimana et al.,
1995) and d) acid phosphatase which produces plant available
phosphates (Acosta-Martinez et al., 2007). Soil samples were taken
from ve study sites, that differed in fertility, dominating tree
species and time elapsed after treatment. In four of the experiments, different amounts of fresh logging residue were distributed
on a circle around a single tree. In one experiment the treatments
were whole-tree harvest and stem-only harvest. Our results for

75

enzyme activities has never been presented earlier, however results

for other soil characteristics from 2 sites (Kannonkoski and Ruokolahti) were already presented (Smolander et al., 2010, 2013).
2. Materials and methods
2.1. Study sites, experimental design and sampling
The experiments were long-term eld experiments established
by The Finnish Forest Research Institute. They differed in characteristics and in experimental design (Table 1). In the Ruokolahti
experiment (735) logging residue was either harvested (WTH) or
evenly distributed on the site (SOH) in thinnings done 23 and 13
years ago. For both treatments, there were three study plots, each
30 m  30 m. Other experiments were single-tree experiments at
spruce and pine sites, in which in thinning different amounts of
fresh logging residues (from 0 to 37.5 Mg ha
1 of dry matter; see
Table 1) were distributed evenly on a circle around individual trees
(diameter 5 m). Nevertheless spruce produces more logging residues than pine in our studies for comparison purposes, we used
similar amounts of logging residue for both species. Treatments
were replicated three times. For a more detailed description of the
Ruokolahti experiment (735) see Smolander et al. (2010) and for
the Kannonkoski experiment (746) see Smolander et al. (2013);
msa
experiment (416) before harvesting are
characteristics of the Ja
given by Saarsalmi et al. (2010).
One composite sample, consisting of 20 subsamples, was
collected systematically with a steel cylinder (d 58 mm) from the
humus layer (Ofh) of the circle surrounding each tree in the singletree experiments and from each study plot in other experiment
(Ruokolahti). Sampling from Ruokolahti and Kannonkoski was
done in September and October 2009, and from the other experiments in September 2011. The fresh soil samples were sieved
(4 mm mesh) after the plant material and roots had been removed.
Soil samples were kept in plastic bags at 4  C in cold room. The
enzyme analyses were performed within a few days after sample
collection. Dry weight (105  C, 16 h) was determined, and organic
matter content was measured as loss on ignition (550  C, 4 h). Soil
pH was measured in a soil-water suspension consisting of 15 ml soil
in 25 ml ultrapure water.

Table 1
Logging residue harvest experiments.

Latitude
Longitude
Elevation (m)a
Annual mean temp. ( C)a
Effective temp. sum ( C)a
Annual mean precipit. (mm)a
Tree species
Soil texture
Humus type
Soil type
Organic layer, mm
Organic matter content, %
pH
Site typeb
Stand age during sampling, years
Time since thinning, growing seasons
Logging residue, Mg ha
1 dry matter

Salla, 406

Kiikala,
409

msa
, 416
Ja

Ruokolahti, 735

Kannonkoski, 746

67 180 N
29 140 E
260

1.0
695
551
Scots pine
Fine sand
Mor
Podzol
24
85
3.8
EMT
92
4
0, 12.5, 25

60 280 N
23 400 E
120
4.8
1343
631
Scots pine
Fine sand, coarse sand
Mor
Podzol
40
70
3.7
CT
58
5
0, 12.5, 25, 37.5

61 550 N
25 020 E
106
3.9
1308
575
N. spruce
Fine sand
Mor
Podzol
36
75
4.0
MT
63
4
0, 15, 30

61 160 N
28 490 E
68
3.9
1318
562
N. spruce
Fine sand
Mor
Podzol
38
45
3.9
OMT
72
23 and 13
n.d.c

62 580 N
25 150 E
122
3.2
1194
520
Scots pine
Loamy sand
Mor
Podzol
20
63
3.9
VTeMT
39
5
0, 10, 20, 30

msa
(416) from Saarsalmi et al. (2010);
Data about Ruokolahti (735) taken from Smolander et al. (2010); data for Kannonkoski (746) from Smolander et al. (2013); data for Ja
data for Kiikala (409) and Salla (406) via personal communication from Anna Saarsalmi (2014).
a
inen et al., 2011).
Data calculated for a 30-year period before taking samples based on the dataset of the Finnish Meteorological Institute (Ven
ala
b
Site types according to Cajander (1949): EMT e Empetrum nigrum e Vaccinium myrtillus, CT e Calluna vulgaris, MT e Vaccinium myrtillus; OMT e Oxalis acetosellaVaccinium myrtillus; VTeMT e Vaccinium vitis-ideae e Vaccinium myrtillus. Fertility order of site types: CT < EMT < VTeMT < MT < OMT.
c
n.d. not determined, but an estimated mean value was 16 Mg ha
1 dry matter of logging residue left on a site in stem-only-harvest.

76

B. Adamczyk et al. / Soil Biology & Biochemistry 82 (2015) 74e80

2.2. Determination of soil enzyme activities

Activities of b-glucosidase, b-glucosaminidase, protease and
acid phosphatase were measured as described previously
(Adamczyk et al., 2014). The acetate buffers used have had the same
pH value as the studied soils (from 3.7 to 4.0).
Briey, for measurements of protease activity, 0.2 g of soil was
mixed with buffer and substrate, hemoglobin (modied from Ladd
and Butler, 1972). After 1 h of incubation, trichloroacetic acid was
added to stop the reaction. After centrifugation, the supernatant
was mixed with the Folin reagent and the absorbance was read at
750 nm spectrophotometrically. Results are expressed as mmol of
tyrosine equivalents released h
1 g
1 of soil organic matter.
To study acid phosphatase activity, 0.2 g of soil was mixed with
acetate buffer and with substrate, p-nitrophenyl phosphate
(modied from Garzillo et al., 1996). After 5 min of incubation,
CaCl2 and TRIS-NaOH were added. After centrifugation, the absorbance of the supernatant was measured at 405 nm. Results are
expressed as mmol of para-nitrophenyl released min
1 g
1 of soil
organic matter.
To study b-glucosidase activity, 0.2 g of soil was mixed with
acetate buffer and with substrate, p-nitrophenyl b-D-glucopyranoside (Eivazi and Tabatabai, 1988). After 30 min of incubation, CaCl2
and TRIS-NaOH were added. After centrifugation the absorbance of
supernatant was measured at 405 nm. Results are expressed as
mmol of para-nitrophenyl released h
1 g
1 of soil organic matter.
To study b-glucoaminidase activity, 0.2 g of soil was mixed with
acetate buffer and with substrate, p-nitrophenyl N-acetyl-b-D-glucosamidine (Parham and Deng, 2000). After 30 min of incubation,
CaCl2 and TRIS-NaOH were added. After centrifugation the absorbance of the supernatant was measured at 405 nm. Results are
expressed as mmol of para-nitrophenyl released h
1 g
1 of soil
organic matter.
2.3. Determination of other soil characteristics
Soil characteristics, described below, were now determined for
msa
416). With
three experiments (Kiikala, 409; Salla, 406; and Ja
regard to Kannonkoski (746) and Ruokolahti (735) this information
was presented earlier for samples taken 1 year before (Smolander
et al., 2013) and 2 years before (Smolander et al., 2010),
respectively.
Total C and N in the soil were measured as described by Priha
and Smolander (1999). Amount of C and N in microbial biomass
were measured with fumigation-extraction method (Smolander
et al., 1994). Net N and C mineralization were measured in a 6week incubation experiment at constant moisture (WHC 60%) and
temperature (14  C). Rates of net N mineralization were determined
after KCl extraction as described by Smolander et al. (1995). Net
mineralization of N was estimated as the accumulation of NH4eN
and (NO2 NO3)eN during incubation. Ammonium N and nitrite
and nitrate N were measured with a ow injection analyzer (FIA
Star 5020, Tecator). The CO2 production was measured by sampling
the headspace and analyzing the amount of CO2eC on a gas chromatograph (Hewlett Packard HP 6890) as described by Smolander
et al. (1994). Glucose-induced respiration was measured to determine whether soils were limited by availability of C (Smolander
et al., 2013).
2.4. Statistical analysis
For the single-tree experiments having 3e4 levels of logging
residues Pearson's correlation coefcient was determined to reveal
any linear relationships between the amount of logging residues
and enzyme activity or other soil characteristic. In cases where

there was no linear correlation differences in variables between

treatments were tested using ANOVA followed by Tukey test. For
the Ruokolahti experiment having WTH and SOH treatments, differences between treatments were tested using one-way ANOVA.
Pearson's correlation coefcient was determined to reveal linear
relationships between enzyme activities and soil characteristics.
P < 0.05 was considered as signicant. For all statistical analyses we
used SPSS.
3. Results
3.1. Enzyme activities
In the Ruokolahti spruce experiment, activities of b-glucosidase,
b-glucosaminidase, acid phosphatase were similar in both SOH and
WTH. However, proteolytic activity had a higher value in the SOH
treatment (Fig. 1).
ms
In the single-tree spruce experiment in Ja
a, acid phosphatase
and protease activities increased signicantly with increasing
amount of logging residue, whereas b-glucosaminidase and bglucosidase were not dependent on amount of logging residue
(Fig. 2).
In all pine single-tree experiments sites, in general, enzyme
activities tended to increase with increasing amount of logging
residue (Fig. 3). The increase in enzyme activity was the most
visible for the Kannonkoski study site. To study the relationship
between enzyme activities and the amount of residues for the
whole dataset, deviation from the mean was calculated for each site
to standardize the results. For all of studied enzymes the change in
activity correlated positively with the logging residue amount
(protease r 0.777; p < 0.001; b-glucosidase r 0.681, p < 0.001;
acid phosphatase r 0.576, p < 0.001, b-glucosaminidase r 0.681,
p < 0.001).
3.2. Other soil characteristics
For Kannonkoski experiment, linear correlation between the
amount of logging residues and organic matter content, C mineralization and glucose-induced respiration has been already
described (Smolander et al., 2013). In Ruokolahti experiment (735)
removal of logging residue tended to decrease microbial biomass C
and N and also net N and C mineralization; these results has been
already described (Smolander et al., 2010).
For the new single-tree experiments, the relationship between
the amount of logging residues and soil characteristics appeared
not to be linear (no signicant linear correlations; results not
shown). ANOVA revealed some signicant differences between the
treatments (Table 2). In Salla site (406), the highest total C was
observed for the highest logging residue amount, however in Kiikala, the highest values for C mineralization and SIR were observed
for 12.5 Mg ha
1 of logging residues.
3.3. Correlations between enzyme activities and soil characteristics
msa
were used to nd relaResults from Salla, Kiikala and Ja
tionship between enzyme activities and other soil characteristics as
sampling from these sites was done in the same time for both
enzyme activities and other soil characteristics. Enzyme activities,
except proteases, showed some correlations with soil characteristics. Carbon and N mineralization and microbial biomass N were
positively correlated with acid phosphatase and glucosaminidase
activities (Table 3). Moreover, glucose-induced respiration was
positively correlated with glucosidase and glucosaminidase
activities.

B. Adamczyk et al. / Soil Biology & Biochemistry 82 (2015) 74e80

77

Fig. 1. Enzyme activities in the humus layer from the Ruokolahti spruce site. Values are means of three replicate plots. Error bars indicate standard deviation. Signicant differences
(P < 0.05) between treatments are indicated by different letters. SOH e stem-only harvest, WTH e whole-tree harvest, SOM e soil organic matter.

4. Discussion
Since logging residue is commonly used as a bioenergy source,
we need to estimate all the ecological costs of whole-tree harvest.

msa
spruce site. Values are
Fig. 2. Enzyme activities in the humus layer from the Ja
means of three replicate trees. Error bars indicate standard deviation. SOM e soil
organic matter.

Earlier papers (Smolander et al., 2008, 2010, 2013) showed that

logging residues may have an effect on microbial biomass or net C
and N mineralization. Here we studied the inuence of logging
residue harvest on the activity of enzymes involved in N, C and P
cycling. The importance of enzyme studies originates from the fact
that the enzyme machinery plays a crucial role in the biochemical
functioning of soil, including degradation processes and nutrient
cycling (Acosta-Martinez et al., 2007). In general, the enzymes
studied, namely protease, b-glucosaminidase, b-glucosidase and
acid phosphatase, showed a tendency to increase their activity with
increasing amount of the logging residue left on a site. However,
there were site specic differences.
In the Ruokolahti experiment, with thinnings done 13 and 23
years before b-glucosidase, b-glucosaminidase, acid phosphatase
activities did not differ between stem-only harvest and whole-tree
harvest; however, proteases showed higher activity in SOH. Studies
done earlier on the same site and some other sites with a similar
history showed that harvesting of logging residue decreased the
rates of net N mineralization and the amount of C and N in the
microbial biomass; C mineralization also tended to decrease
(Smolander et al., 2008, 2010). There were also changes in the
composition of organic matter due to logging residues. Enzyme
activity is driven by numerous factors but has a tendency to follow
the amount of microbial biomass C and N (Acosta-Martinez et al.,
2007). This was seen in the Ruokolahti experiment for proteases.
It is possible that other soil enzyme activities measured from the
WTH treatment managed to recover to an activity similar to SOH, as
13 years had elapsed since the last harvest. Logging residues after
such a long time, especially needles and branches, were degraded
in substantial amounts. Degradation of needles and small twigs
may take 5e10 years, but thicker woody residues require up to 30
nen et al., 2000;
years to degrade (Fahey et al., 1991; Hyvo
Smolander et al., 2008, 2013). Moreover, the amount of logging
residue left in the SOH plots may not have been large enough to
make differences between SOH vs WTH visible; the amount of
logging residue was not determined, but the average amount for
spruce thinning stands is about 16 Mg ha
1 (Tamminen et al., 2012).
The other experiments were more short-term studies; 4e5
years had elapsed since their establishment. Therefore most of the
changes in the humus layer may have been caused by decomposing
needles and perhaps by leachates or volatiles from the thicker
wood material (Smolander et al., 2013). Moreover, treatments were
organized in a different way than in the SOH vs WTH experiment.
Logging residue was spread around a tree in different amounts,
from 0 Mg ha
1 to 37.5 Mg ha
1 in order to underline the inuence
of these materials on the soil processes. In the Kannonkoski pine
experiment all the enzyme activities studied increased with
increasing amount of logging residue. Studies conducted on the
same site also showed the stimulative effect of the logging residue
on C mineralization, glucose-induced respiration, net N mineralization (Smolander et al., 2013), increase in aboveground tree
biomass production, increase in abundance of 0e2 mm length

78

B. Adamczyk et al. / Soil Biology & Biochemistry 82 (2015) 74e80

Fig. 3. Enzyme activities in the humus layer from pine sites. Values are means of three replicate trees. Error bars indicate standard deviation. SOM e soil organic matter.

enchytraeids, increase in specic root length (length per unit mass)

and ectomycorrhizal root tip abundance (Dighton et al., 2012).
In other experiments the increase in enzyme activities was
not as clear, but similar trends were observed, i.e. the overall
results showed strong relationship between the amount of logging residue left on a site and activity of b-glucosidase, protease
and acid phosphatase on the pine sites (Salla, Kiikala), and for
msa
). For bacid phosphatase and protease on spruce site (Ja
glucosaminidase activity there was no clear relationship, but still
the positive trend was observed. One reason could be that logging residue does not directly provide more substrate for that
enzyme, chitin. Moreover, as stated by Ponder and Eivazi (2008),
individual enzymes may respond differently to the same soil
factors.
We compared changes in enzyme activities to other soil characteristics of humus layer, as it is proposed that enzyme activities
correlate well with other soil properties, like soil respiration (Leiros

et al., 2000). Comparison of enzymatic activity with soil characmsa

)
teristics studied from the same samples (sites Salla, Kiikala, Ja
showed that activities of some enzymes correlated well with net N
and C mineralization and SIR, supporting the conclusion that
removal of logging residue has negative impact on decomposition
process in soil.
We observed site specic differences in response to logging
residue removal. These differences in the response to the logging
residue harvest of both enzymatic activity and other soil characteristics may origin from various factors: site fertility, age of the tree
stand, climate conditions, time elapsed after logging residue harvest, distribution of the logging residue on the site, quantity and
chemical composition of compounds in the logging residue.
Inconsistent effect of different stress/disturbance (freeze-thaw
events, wetedry cycles, Cu addition, and changing pH) on
biochemical properties of soils was observed earlier by Chaer et al.
(2009).

B. Adamczyk et al. / Soil Biology & Biochemistry 82 (2015) 74e80

79

Table 2
Effect of the amount of logging residue on humus layer characteristics in three single-tree experiments, mean (standard deviation). Signicant differences between treatments
are indicated by different letters. WTH e whole tree harvest; SOH e stem only harvest; min-net mineralization, SIR e substrate induced respiration, mic. e microbial biomass.
Logging residue,
Mg ha
1

Total C g kg
1

Total N g kg
1

C min. CO2eC
mg kg
1 d
1

SIR CO2eC
mg kg
1 h
1

N min. N mg kg
1 d
1

Mic. C g kg
1

Mic. N g kg
1

Salla (406)

0
12.5
25

501 (6.1)a
508 (5.8)ab
521 (6.4)b

13.3 (0.64)
12.7 (0.82)
13.1 (0.56)

369 (85)
375 (19)
377 (108)

161 (16)
158 (9.5)
168 (29)

0.2 (0.13)
0.3 (0.21)
0.2 (0.09)

9.1 (0.98)
9.3 (0.08)
9.2 (1.22)

1.0 (0.12)
1.0 (0.04)
1.0 (0.08)

Kiikala (409)

0
12.5
25
37.5

551
513
518
504

17.7
16.7
17.2
16.6

158
226
179
153

0.5
0.9
0.4
0.3

7.1
8.3
7.4
6.4

0.7
0.9
0.8
0.7

J
ams
a (416)

0
15
30

505 (11.9)
496 (13.7)
508 (11.9)

(37.3)
(45.6)
(12.0)
(11.9)

(0.66)
(0.94)
(0.75)
(0.21)

17.7 (0.70)
17.4 (1.05)
17.8 (1.27)

(1.7)a
(26)b
(8.7)a
(17)a

449 (123)
467 (92)
447 (56)

82
101
98
82

(5.7)a
(7.9)b
(1.0)ab
(9.7)a

135 (28)
132 (18)
130 (18)

(0.19)
(0.76)
(0.06)
(0.07)

4.5 (2.51)
5.2 (1.24)
5.6 (2.93)

(1.35)
(1.01)
(1.09)
(1.15)

8.0 (1.53)
8.0 (0.81)
7.3 (0.88)

(0.05)
(0.08)
(0.02)
(0.05)

1.1 (0.14)
1.1 (0.21)
1.0 (0.09)

Variables are presented per unit of organic matter.

Table 3
Pearson's correlation coefcients between enzyme activities and humus layer characteristics in the combined data from the pine stands Salla (406) and Kiikala (409) and the
msa
(416). min-net mineralization; SIR e substrate induced respiration; mic. e microbial biomass; tot. e total. Statistically signicant results are bolded.
spruce stand Ja

b-glucosidase

C tot.
N tot.
C min.
SIR
N min.
C mic.
N mic.

b-glucosaminidase

Protease

Acid phosphatase

0.122
0.097
0.150
0.487
0.203
0.312
0.170

0.520
0.204
0.430
0.007
0.111
0.093
0.368

0.327
0.214
0.858
0.669
0.577
0.367
0.675

0.078
0.225
0.001
0.001
0.001
0.046
0.001

0.002

0.091
0.139

0.105

0.135

0.014

0.107

0.991
0.632
0.434
0.582
0.475
0.943
0.573

0.196
0.507
0.593
0.107
0.652
0.090
0.466

0.300
0.005
0.001
0.575
0.001
0.133
0.009

5. Conclusions
In conclusion, logging residue removal affects soil processes,
including the enzyme machinery which is standing behind all the
biochemical processes in the soil. In general, enzymes involved in
N, C and P transformations, namely protease, b-glucosaminidase, bglucosidase and acid phosphatase, increased their activities in
relation to the amount of logging residue left on a site. Moreover,
some of enzyme activities correlated well with net N and C
mineralization and substrate-induced respiration. An increase in
enzymatic activity after leaving logging residues on a site indicates
that these materials are an important factor in supporting the
sustainable productivity of the forest ecosystem. The ecological
effects of logging residue harvest needs more study. Increased
understanding of the relationship between enzymatic activity and
harvesting practices will allow us to determine the effects of logging residue harvest on nutrient availability for subsequent tree
growth as enzymes are the key to making nutrients available to
trees.
Acknowledgment
We are grateful to Dr Joann von Weissenberg for checking the
English language of this paper. In addition, we thank Anneli Rautiainen for helping with laboratory work. This study was funded by
Metla, the Academy of Finland (grant no. 126667) and Emil Aaltonen Foundation.
References
Acosta-Martinez, V., Cruz, L., Sotomayor-Ramirez, D., Perez-Alegria, L., 2007.
Enzyme activities as affected by soil properties and land use in a tropical
watershed. Applied Soil Ecology 35, 35e45.

inen, P., Kitunen, V., Smolander, A., 2014. Potential activities of

Adamczyk, B., Kilpela
enzymes involved in N, C, P and S cycling in boreal forest soil under different
tree species. Pedobiologia 57, 97e102.
Baldrian, P., 2014. Distribution of extracellular enzymes in soils: spatial heterogeneity and determining factors at various scales. Soil Science Society of America
Journal 78, 11e18.
Brais, S., Pare, D., Camire, C., Rochon, P., Vasseur, C., 2002. Nitrogen net mineralization and dynamics following whole-tree harvesting and winter windrowing
on clay sites in northern Quebec. Forest Ecology and Management 157, 119e130.
Boerner, R.E.J., Waldrop, T.A., Shelbourne, V.B., 2006. Wildre mitigation strategies
affect soil enzyme activity and soil organic carbon in loblolly pine (Pinus taeda)
forests. Canadian Journal of Forest Research 36, 3148e3154.
Burns, R.G., DeForest, J.L., Marxsen, J., Sinsabaugh, R.L., Stromberger, M.E.,
Wallenstein, M.D., Weintraub, M.N., Zoppini, A., 2013. Soil enzymes in a
changing environment: current knowledge and future directions. Soil Biology
and Biochemistry 58, 216e234.
Cajander, A.K., 1949. Forest types and their signicance. Acta Forestalia Fennica 556
(5), 71.
Caldwell, B.K., 2005. Enzyme activities as a component of soil biodiversity: a review.
Pedobiologia 49, 637e644.
Chaer, G.M., Myrold, D.D., Bottomley, P.J., 2009. A soil quality index based on the
equilibrium between soil organic matter and biochemical properties of undisturbed coniferous forest soils of the Pacic Northwest. Soil Biology and
Biochemistry 41, 822e830.
Dighton, J., Helmisaari, H.-S., Maghirang, M., Smith, S., Malcolm, K., Johnson, W.,
Quast, L., Lallier, B., Gray, D., Set
al
a, H., Starr, M., Luiro, J., Kukkola, M., 2012.
Impacts of forest post thinning on soil chemistry, fauna and roots: implications
of residue removal in Finland. Applied Soil Ecology 60, 16e22.
Eivazi, F., Tabatabai, M.A., 1988. Glucosidases and galactosidases in soils. Soil Biology
and Biochemistry 20, 601e606.
Ekenler, M., Tabatabai, M.A., 2002. Effects of trace elements on betaglucosaminidase activity in soils. Soil Biology and Biochemistry 32, 1829e1832.
Fahey, T.J., Stevens, P.A., Hornung, M., Rowland, P., 1991. Decomposition and nutrient
release from logging residue following conventional harvest of sitka spruce in
North Wales. Forestry 64, 289e301.
Garzillo, A.M.V., Badalucco, L., De Cesare, F., Grego, S., Buonocore, V., 1996. Synthesis
and characterization of an acid phosphatase - polyresorcinol complex. Soil
Biology and Biochemistry 28, 1155e1161.
Geng, Y., Dighton, J., Gray, D., 2012. The effects of thinning and soil disturbances on
enzyme activities under pitch pine soil in New Jersey Pinelands. Applied Soil
Ecology 62, 1e7.
Hakkila, P., 2006. Factors driving the development of forest energy in Finland.
Biomass Bioenergy 30, 281e288.

80

B. Adamczyk et al. / Soil Biology & Biochemistry 82 (2015) 74e80

Helmisaari, H.-S., Hanssen, K.H., Jacobson, S., Kukkola, M., Luiro, J., Saarsalmi, A.,
Tamminen, P., Tveite, B., 2011. Logging residue harvest after thinning in Nordic
boreal forests: long-term impact on tree growth. Forest Ecology and Management 261, 1919e1927.
nen, R.B., Olsson, H., Lungkvist, H., Staaf, H., 2000. Decomposition and nutrient
Hyvo
release from Picea abies (L.) Karst. and Pinus sylvestris L. logging residues. Forest
Ecology and Management 126, 97e112.
Jacobson, S., Kukkola, M., M
alkonen, E., Tveite, B., 2000. Impact of whole-tree
harvesting and compensatory fertilization on growth of coniferous thinning
stands. Forest Ecology and Management 129, 41e51.
Johnson, D.W., Knoepp, J.D., Swank, W.T., Shan, J., Morris, L.A., Van Lear, D.H.,
Kapeluck, P.R., 2002. Effects of forest management on soil carbon: results
of some long-term resampling studies. Environmental Pollution 116,
201e208.
Kaarakka, L., Tamminen, P., Saarsalmi, A., Kukkola, M., Helmisaari, H.-S., Burton, A.J.,
2014. Effects of repeated whole-tree harvesting on soil properties and tree
growth in a Norway spruce (Picea abies (L.) Karst.) stand. Forest Ecology and
Management 313, 180e187.
Ladd, J.N., Butler, J.H.A., 1972. Short-term assays of soil proteolytic enzyme activities
using proteins and dipeptide derivatives as substrates. Soil Biology and
Biochemistry 4, 19e30.
Leiros, M.C., Trasar-Cepeda, C., Seoane, S., Gil-Sotres, F., 2000. Biochemical properties of acid soils under climax vegetation (Atlantic oakwood) in an area of the
European temperate-humid zone (Galicia, NW Spain): general parameters. Soil
Biology and Biochemistry 32, 733e745.
Nduwimana, J., Guenet, L., Dorval, I., Blayau, M., Le Gall, J.Y., Le Treut, A., 1995.
Proteases. Annales de Biologie Clinique 53, 251e264.
Nurmi, J., 2007. Recovery of logging residues for energy from spruce (Picea abies)
dominated stands. Biomass Bioenergy 31, 375e380.
Parham, J.A., Deng, S.P., 2000. Detection, quantication and characterization of bglucosaminidase activity in soil. Soil Biology and Biochemistry 32, 1183e1190.
Piatek, K.B., Lee Allen, H., 1999. Nitrogen mineralization in a pine plantation fteen
years after harvesting and site preparation. Soil Science Society of America
Journal 63, 990e998.

Ponder Jr., F., Eivazi, F., 2008. Activities of ve enzymes following soil disturbance
and weed control in a Missouri forest. Journal of Environmental Monitoring and
Restoration 5, 68e76.
Priha, O., Smolander, A., 1999. Nitrogen transformations in soil under Pinus sylvestris, Picea abies and Betula pendula at originally similar forest sites. Soil
Biology and Biochemistry 31, 965e977.
Rolff, C., gren, G.I., 1999. Predicting effects of different harvesting intensities with a
model of nitrogen limited forest growth. Ecological Modelling 118, 193e211.
Saarsalmi, A., Smolander, A., Kukkola, M., Arola, M., 2010. Effect of wood ash and
nitrogen fertilization on soil chemical properties, soil microbial processes, and
stand growth in two coniferous stands in Finland. Plant and Soil 331, 329e340.
Schlamadinger, B.J., Spitzer, G.H., Kohlmaier, G.H., Ludeke, M., 1995. Carbon balance
of bioenergy from logging residues. Biomass Bioenergy 8, 221e234.
Smolander, A., Kitunen, V., Kukkola, M., Tamminen, P., 2013. Response of soil
organic layer characteristics to logging residues in three Scots pine thinning
stands. Soil Biology and Biochemistry 66, 51e59.
lko
nen, E., 1994. Microbial biomass C and N
Smolander, A., Kurka, A., Kitunen, V., Ma
and respiratory activity in soil of repeatedly limed and N- and P-fertilized
Norway spruce stands. Soil Biology and Biochemistry 26, 957e962.
Smolander, A., Kitunen, V., Tamminen, P., Kukkola, M., 2010. Harvest of logging
residue in Norway spruce thinning stands: long-term changes in organic layer
properties. Soil Biology and Biochemistry 42, 1222e1228.
nen, E, 1995. Nitrogen transformations in
Smolander, A., Kitunen, V., Priha, O., M
alko
limed and nitrogen fertilized soil in Norway spruce stands. Plant Soil 172,107e115.
Smolander, A., Levula, T., Kitunen, V., 2008. Response of litter decomposition and
soil C and N transformations in a Norway spruce thinning stand to harvest of
logging residue. Forest Ecology and Management 256, 1080e1086.
Tamminen, P., Saarsalmi, A., Smolander, A., Kukkola, M., Helmisaari, H.-S., 2012.
Effects of logging residue harvest in thinnings on amounts of soil carbon and
nutrients in Scots pine and Norway spruce stands. Forest Ecology and Management 263, 31e38.
Ven
al
ainen, A., Tuomenvirta, H., Pirinen, P., Drebs, A., 2011. A basic Finnish climate
data set 1961-2000 descriptions and illustrations. Finnish Meteorological
Institute. ISSN: 0782-6079 5. Reports No. 2005.