Changes in microbial and soil properties following compost treatment of
degraded temperate forest soils
W. Borken*, A. Muhs, F. Beese
Institute of Soil Science and Forest Nutrition, University of GoÈttingen, BuÈsgenweg 2, 37077 GoÈttingen, Germany Received 13 March 2001; received in revised form 3 September 2001; accepted 25 September 2001
Abstract
The long-term effect of compost treatment on soil microbial respiration, microbial biomass carbon (Cmic) and biomass nitrogen (Nmic), soil
organic carbon (SOC), and soil total nitrogen (STN) was studied in six degraded forests, Lower Saxony, Germany. The study was conducted in mature beech (Fagus sylvaticaL.), pine (Pinus sylvestrisL.) and spruce (Picea abiesKarst.) forests on silty soils at Solling and on sandy soils at UnterluÈû. Mature compost from separately collected organic household waste was applied for soil amelioration at an amount of 6.3 kg m22on the soil surface. After 2 years, soil samples were taken from the control and compost plots and were separated into.2 and ,2 mm fractions of the O-horizon and into mineral soil intervals from 0±5, 5±10, and 10±20 cm depths. The original compost had a pH of 7.5, high inorganic salt content, low organic C content, narrow C-to-N ratio, and low microbial activity and biomass. Compost signi®cantly reduced the microbial respiration per mass unit in the O-horizons.2 mm by 17% and in the O-horizons,2 mm by 25%. Cmicand Nmic
decreased signi®cantly by 22 and 23% in the O-horizons,2 mm and by 35 and 28% in the O-horizons.2 mm, respectively. Our estimates suggest that the reduction in microbial respiration and biomass in the horizons resulted partly from the mixture of compost and the O-horizons. The average loss of 1.2 kg m22
organic matter may have also contributed to the reduction in microbial biomass and respiration in the O-horizons of the compost plots. However, it is not clear whether the decomposition of the original organic matter in the O-horizons was increased by the compost application. In the mineral soils, the compost treatment caused signi®cant increases in microbial respiration, Cmic
and Nmicby 14±21% at 0±5 cm and by 14±23% at 10±20 cm depth. Although not signi®cant, a similar trend was found for the 5±10 cm
depth. Increased release of nutrients and dissolved organic matter (DOM) could have promoted microbial growth and activity in the mineral soils. The signi®cant increase in STN and the narrowing C-to-N ratio indicate that the investigated forest soils were not N-saturated. This ®eld study suggests that super®cial application of compost from separately collected organic household waste increase microbial activity and biomass in the mineral soil by release of nutrients from the O-horizon to the mineral soil.q2002 Elsevier Science Ltd. All rights reserved.
Keywords: Amelioration; Compost; Microbial biomass; Microbial respiration; Temperate forests
1. Introduction
Excessive removal of biomass in past centuries and high atmospheric proton and N loads in recent decades caused a strong degradation and nutrient imbalance in many forest soils in Central Europe (Ulrich, 1994). During this long-term degradation, the incorporation of organic matter by soil burrowing organisms has been reduced in the upper mineral soil. Moreover, acid precipitation decreased the microbial biomass and C mineralization in the O-horizon of beech forests (Wolters, 1991), pine forests (Baath et al., 1980) and spruce forests (Zelles et al., 1987; von LuÈtzow et
al., 1992). Thus, soil acidi®cation has probably contributed to the accumulation of organic matter and nutrients in the forest ¯oor.
To counteract soil acidi®cation and nutrient imbalances various treatments such as liming, wood ash application, phosphorus and potassium fertilization have been per-formed in many degraded forests of Central Europe. Liming and wood ash application to the soil surface raise the soil pH of the forest ¯oor, improve base saturation, and decrease the
amount of Al31 in soil solution. Besides the chemical
improvements, these practices generally increase the micro-bial biomass and activity in the O-horizon of degraded forest soils (Zelles et al., 1990; Baath and Arnebrant, 1994; Smolander et al., 1994).
Little is known about the effect of organic fertilizers, such as compost, on microbial biomass and activity in degraded forest soils. In recent years, the separation of
0038-0717/02/$ - see front matterq2002 Elsevier Science Ltd. All rights reserved. PII: S 0 0 3 8 - 0 7 1 7 ( 0 1 ) 0 0 2 0 1 - 2
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* Corresponding author. Address: The Woods Hole Research Center, P.O. Box 296, Woods Hole, MA 02543, USA. Tel.:1 1-508-540-9375-152; fax:11-508-548-5633.
organic household waste and the use of new composting technologies have improved the compost quality (Ammar, 1996) and increased the amount of compost in some European countries. Therefore compost may be used not only in agriculture, horticulture, landscape conservation and reclamation of mining areas but also for amelioration of degraded forest soils (Borken and Beese, 2000). Guerrero et al. (2000) found increased bacteria and fungal popula-tions and improved stability of soil aggregates when municipal solid waste compost was applied to burnt forest soils. The authors pointed out that compost addition is a suitable technique for accelerating the natural recovery process of burnt soils. However, the release of nutrients and the effect on the autochthon microbial community of forest soils may vary with the maturity, chemical composi-tion and amount of compost. Certainly, the microbial community of compost and forest soils is different and, therefore, the competition between species may affect the decomposition of organic matter.
To study the application of mature compost from organic household waste in degraded forest soils, a long-term experiment was set up at six forest sites. We chose beech, pine and spruce stands on silty soils at Solling and on sandy soils at UnterluÈû. In the present study we focus on the inves-tigation of microbial respiration, Cmic and Nmic in the
O-horizons and in the upper mineral soil 2 years after compost was applied to the soil surface. Additionally, changes in soil organic carbon (SOC) and soil total nitrogen (STN) were related to microbial properties. We hypothesized that the application of compost would increase the microbial respiration, Cmic and Nmic in the upper mineral soil due to
increase of pH in soil solution and the release of nutrients and dissolved organic carbon from the compost in the long term. Limited nutrients such as phosphorus may stimulate the growth and activity of microorganisms.
2. Materials and methods
2.1. Sites
The experiment was carried out in beech (Fagus
sylva-tica), spruce (Picea abies) and pine stands (Pinus sylvestris) at Solling and at UnterluÈû in Lower Saxony, Germany (Table 1). All sites are characterized by strong soil acidi®-cation with a base saturation of less than 10% in the soil pro®le from 5 cm down to 100 cm depth. Aluminum is the dominating exchangeable cation of the soil matrix. Recently lime applications were used to alter the pH in the O-horizon, and increased the base saturation of the mineral soil at 0± 5 cm depth. Further chemical properties of the O-horizons and the mineral soils are given in Tables 2 and 3, respectively. The 150-year beech stand (SB) and the 115-year spruce stand (SS) at the Solling plateau above 500 m elevation have
a mean annual air temperature of 7.28C and an annual
precipitation of 1038 mm, evenly distributed throughout
the year. The 103-year pine stand at Solling (SP) was located at an elevation of 270 m and has a mean annual
temperature of 7.58C and an annual precipitation of
900 mm. The soils of these sites developed on 30±80 cm thick soli¯uction deposits, overlaying weathered Triassic Sandstone. Texture of the soils at 0±20 cm depth was dominated by the silt fraction (46±58%) with varying clay and sand contents. According to the FAO classi®cation (FAO, 1998), the soils of the stands were classi®ed as well-drained (SP) to poorly-drained (SS) dystric Cambisols with a moder-type O-horizon. Considerable amounts of
organic matter in the range of 9.0±12.4 kg m22are stored in the 5±8 cm thick O-horizon in the stands at Solling (Table 1).
The 131-year beech (UB), the 90-year spruce (US) and the 54-year pine stand (UP) at UnterluÈû were located close to each other at an elevation above 110 m (Table 1). The long-term average of mean annual air temperature is 8.48C and the mean annual precipitation is 837 mm. The soils are developed from ¯uvio-glacial sand and gravel deposited beyond a terminal moraine during the Warthe-stadium of the Saale/Riss ice age. The soils contain about 74±81%
W. Borken et al. / Soil Biology & Biochemistry 34 (2002) 403±412 Table 2
Properties of the amended compost and the O-horizon layers from the control plots in 1997
Horizon Site pH (KCl) Organic C (mg g21) N (mg g21) P (mg g21) S (mg g21) Na (mg g21) K (mg g21) M (mg g21) Ca (mg g21)
Compost 7.5 217 22.8 4.0 2.9 3.6 10.7 4.8 27.6
L SB ± 507 14.6 0.8 1.2 0.1 1.1 1.0 10.0
SS ± 503 15.2 0.8 1.2 0.1 1.7 0.6 3.9
SP ± 470 14.3 0.6 1.5 0.1 1.1 2.3 12.4
UB ± 461 12.1 0.7 1.1 0.1 1.1 1.5 12.0
US ± 497 13.0 0.6 1.1 0.1 0.9 0.5 4.7
UP ± 510 17.5 1.2 1.2 0.1 3.2 0.9 3.7
F SB ± 417 16.1 0.8 1.7 0.1 1.3 16.2 34.0
SS ± 387 15.2 0.8 2.1 0.2 1.3 29.6 55.3
SP ± 363 14.5 0.8 2.1 0.2 1.6 5.6 13.9
UB ± 447 15.1 0.8 1.5 0.1 1.0 2.2 11.9
US ± 446 16.7 0.8 2.0 0.1 0.9 2.2 8.5
UP ± 458 18.4 0.7 2.2 0.1 0.8 1.2 3.9
H SB 4.5 226 10.3 0.7 1.7 0.2 2.5 32.0 56.0
SS 3.6 341 13.3 0.8 1.9 0.2 3.6 8.7 16.2
SP ± ± ± ± ± ± ± ± ±
UB 3.3 344 14.3 0.6 1.8 0.1 0.8 1.9 4.1
US 2.9 358 12.2 0.5 1.5 0.1 0.9 1.1 4.0
UP 2.6 324 12.3 0.5 1.6 0.1 0.6 0.4 1.9
Table 3
Physical and chemical properties of the mineral soils from the control plots in 1997
Depth (cm) Site Bulk density (g cm23) pH (CaCl
2) CEC (mmol kg21)
0±5 SB 1.16 3.75 104
SS 1.00 3.34 180
SP 1.17 3.27 86
UB 1.32 3.20 49
US 1.42 3.05 57
UP 1.19 2.79 60
5±10 SB 1.30 3.81 76
SS 1.17 3.25 140
SP 1.40 3.68 52
UB 1.35 3.61 48
US 1.59 3.44 33
UP 1.32 2.91 44
10±20 SB 1.31 4.01 58
SS 1.20 3.70 101
SP 1.24 4.05 34
UB 1.41 4.03 34
US 1.60 4.15 18
sand, 16±23% silt and 3±8% clay at 0±20 cm depth. The soils have been classi®ed as well-drained dystric Cambisol (FAO, 1998) with moder-type O-horizons. The beech stand
(UB) had no ground vegetation and stored 12.7 kg m22
organic matter in the 6±9 cm thick O-horizon (Table 1). The spruce stand (US) and the pine stand (UP) stored 8.6 and 7.5 kg m22 organic matter in the O-horizon, respec-tively. The pine stand had a dense cover of grass and
Vacciniumspecies.
2.2. Experimental design and sampling
At all study sites, three control and treatment plots, each of 27 m2, were established within a fenced area of 500 m2.
At each compost plot 6.3 kg m22 of sieved (,10 mm)
mature compost (Fertigkompost, Umweltschutz Nord, Ganderkesee, Germany) was applied to the soil surface in the summer of 1997. The compost was produced from separately collected organic household waste consisting mainly of plant residues, wood shavings and to a lesser extent of leftovers. The compost had a bulk density of 0.42 g cm3, with 83% being,2 mm. The thickness of the compost layer applied to the soil surface was 1.5 cm. Because of the maturation during the composting process the compost had a low C content of 217 g kg21(Table 2) and a narrow C-to-N ratio of 9.5. The compost provided higher N, P, S, Na, K, Mg and Ca contents than the O-horizons of the study sites. At the time of application, the compost contained a large inorganic salt fraction of
13 g kg21. After 2 years the compost was partly mixed
with the O-horizon due to soil organisms such as epigeic earthworms. In May 1999, two soil cores of 10 cm in diameter were taken from each control and compost plot to a depth of 30 cm and were separated into the O-horizon, 0±5, 5±10, and 10±20 cm soil depth, for analysis of chemi-cal and microbial properties.
2.3. Chemical and microbial analysis
The O-horizons from the control and compost plots were separated into two fractions of.2 and,2 mm by
handpick-ing and sievhandpick-ing. The fraction,2 mm amounted to 54±92%
(control plots) and 68±96% (compost plots) of the total O-horizon. Both fractions from the compost plots included compost particles but the portion is unknown and may have varied within and among the plots. The mineral soil cores were passed through a 2 mm sieve. Subsamples were dried and homogenized for analysis of organic C and total N which were measured after combustion with an Carlo Erba C/N analyzer. For microbial analysis, the soil samples were
adjusted to 50^5% of water-holding capacity and were
stored for over 4 weeks at 48C. Water-holding capacity
ranged from 150 to 450% in the O-horizon material and from 20 to 90% in the mineral soils. All samples were incubated for 24 h at 228C before microbiological measure-ments. Microbial respiration of soil samples was determined as CO2production at 228C using air-tight jars, which were
connected to an automated gaschromatograph equipped with an electron capture detector (Loft®eld et al., 1997). CO2concentration was measured after closure of jars and
after 6 h of incubation.
Cmic and Nmic were measured by fumigation±extraction
(Brookes et al., 1985; Vance et al., 1987). One part of soil samples, i.e. 5 g of O-horizon material and 25 g of mineral soil, were extracted with 60 ml 0.5 M K2SO4 for 30 min
on an oscillating shaker at 250 rev min21 and ®ltered
(Schleicher & Schuell 595 1/2, Dassel, Germany). The
other part was fumigated with methanol-free CHCl3
(Merck, Darmstadt, Germany) for 24 h at 258C. The fumi-gant was removed and the soil then extracted as described before. Organic carbon was measured after ultraviolet-persulphate oxidation to CO2by infrared detection using a
Dohrman DC 80 automated system (Wu et al., 1990). Cmic
was estimated from the relationship EC/kEC, where EC is
[(organic C extracted from fumigated soil) minus (organic C extracted from non-fumigated soil)] andkEC 0:45 (Wu
et al., 1990; Joergensen, 1996). The N contents of the extracts were determined by a digesting process with UV radiation in a continuous ¯ow system (Skalar, Erkelenz). Nmicwas estimated from the relationshipEN/kEN, whereEN
is [(organic N extracted from fumigated soil) minus (organic
N extracted from non-fumigated soil)] and kEN 0:54
(Brookes et al., 1985; Joergensen and Mueller, 1996). Initial microbial respiration and microbial biomass C of original compost samples n6were measured in August 1997 by the same the methods as described before.
2.4. Statistics
Data were analyzed using SAS statistical software (SAS Institute, 1996). A 2-way ANOVA was performed to test the signi®cance of effects (sites and compost treatment) on microbial respiration, Cmic, Nmic, SOC, STN, and
C-to-N-ratio using means of three replications from each site. Linear and non-linear regressions were used to test for correlation between microbial properties, SOC and STN contents of soil samples. Students-t-tests were performed to compare linear regression equations from the control and compost plots. Values of microbial properties from the O-horizons were log-transformed for testing statisti-cal differences of exponential regression equations. The numbers presented in the tables are arithmetic means and are given on an oven dry basis (1058C, 24 h).
3. Results
3.1. Microbial properties
The 2-way ANOVA results revealed highly signi®cant effects p,0:0001of forest sites on microbial respiration,
Cmic and Nmic of the O-horizon .2 and ,2 mm and all
mineral soil depths (Table 4). With a few exceptions, the beech stands at Solling and UnterluÈû showed higher values
W.
Borken
et
al.
/
Soil
Biology
&
Biochemistry
34
(2002)
403
±
412
407
Amount of soil organic matter (SOM), contents of soil organic carbon (SOC) and soil total nitrogen (STN), C-to-N ratio, microbial respiration, contents of Cmicand Nmicin the fractionated O-horizons and the
mineral soils from the control (2) and the compost plots (1). CV stands for coef®cient of variation of all samples per depth n36
Fraction Site SOM (kg m22) SOC (mg g21) STN (mg g21) C-to-N ratio (g g21) Respiration (mg C g21h21) C
mic(mg g21) Nmic(mg g21)
2 1 2 1 2 1 2 1 2 1 2 1 2 1
O-horizon,.2 mm SB 1.8 1.8 462 400 17 17 27 24 40.4 28.6 7.25 6.51 1015 701
SS 2.4 3.3 481 323 17 18 29 18 25.7 22.5 4.82 3.63 423 326
SP 2.2 2.4 432 365 15 14 28 25 38.0 34.8 6.90 3.67 589 427
UB 1.0 0.6 429 296 17 14 25 21 41.4 33.8 15.68 11.81 1844 1332
US 3.7 1.7 439 394 15 17 30 23 29.1 28.8 7.58 6.58 668 820
UP 4.3 4.6 435 328 15 16 29 21 23.4 16.6 6.98 4.23 644 402
CV% 46 58 10 20 13 15 6 11 39 34 48 53 58 57
O-horizon,,2 mm SB 7.9 11.1 285 198 15 14 19 14 8.8 6.1 2.91 1.97 349 250
SS 7.9 12.6 402 248 17 15 24 17 10.1 5.7 3.52 1.68 346 122
SP 8.0 13.8 361 214 16 12 23 17 9.7 5.7 3.05 1.81 254 185
UB 11.3 15.2 268 262 12 13 23 20 10.0 9.6 2.70 1.89 334 263
US 4.8 13.7 316 242 12 13 25 18 11.3 10.7 2.58 2.17 174 233
UP 5.0 10.0 334 263 11 12 29 22 8.8 4.9 2.23 1.51 180 127
CV% 32 15 22 26 23 15 14 15 17 38 19 21 31 36
Soil depth (cm) Site SOC (mg C g21) STN (mg N g21) C-to-N ratio (g g21) Respiration (mg C g21h21) Cmic(mg C g21) Nmic(mg N g21)
2 1 2 1 2 1 2 1 2 1 2 1
0±5 SB 51.9 50.7 2.7 2.7 20 19 0.40 0.42 0.49 0.43 38.1 33.2
SS 45.8 49.7 2.3 2.8 20 18 0.46 0.47 0.29 0.35 23.3 25.2
SP 34.9 44.5 1.3 1.8 28 24 0.37 0.46 0.25 0.29 20.2 28.4
UB 26.8 31.0 0.8 1.2 32 26 0.37 0.37 0.22 0.26 24.8 28.2
US 24.2 22.6 0.7 0.9 34 25 0.24 0.28 0.15 0.23 16.6 25.3
UP 39.5 45.3 1.1 1.6 34 28 0.23 0.36 0.19 0.35 15.2 26.5
CV% 34 3156 43 23 17 37 25 88 26 79 22
5±10 SB 33.8 30.6 1.7 1.6 20 19 0.19 0.22 0.28 0.29 24.2 22.9
SS 27.2 24.4 1.4 1.7 19 15 0.22 0.20 0.19 0.18 15.6 14.5
SP 20.3 17.4 0.8 0.8 25 22 0.14 0.17 0.06 0.07 6.6 10.2
UB 18.1 18.9 0.6 0.7 31 28 0.21 0.19 0.13 0.13 13.6 12.8
US 10.3 9.2 0.4 0.4 27 23 0.11 0.14 0.07 0.07 6.6 6.8
UP 26.5 29.5 0.8 1.0 33 30 0.12 0.15 0.10 0.14 10.1 9.7
CV% 37 38 50 49 22 24 34 25 58 56 52 45
10±20 SB 28.6 25.0 1.4 1.5 20 17 0.16 0.17 0.24 0.25 19.0 18.5
SS 20.8 15.3 1.3 1.2 17 13 0.10 0.12 0.09 0.10 6.1 7.9
SP 11.6 10.7 0.6 0.6 20 19 0.11 0.16 0.02 0.05 2.5 5.8
UB 12.9 14.4 0.5 0.6 28 26 0.17 0.16 0.07 0.08 7.0 7.1
US 6.6 7.5 0.2 0.3 27 23 0.07 0.09 0.04 0.06 3.4 4.5
UP 19.7 26.6 0.7 0.9 30 30 0.12 0.14 0.07 0.11 6.3 6.9
for microbial properties than the respective spruce and pine stands of these study areas. However, there was no clear distinction for these properties between the spruce and pine stands in the O-horizon and mineral soil. Microbial properties at all sites followed a sharp gradient from both fractionated O-horizons down to the mineral soil at 10± 20 cm depth.
The compost treatment had a signi®cant effect on all
microbial properties in the .2 mm p,0:02 and
,2 mm fraction of the O-horizons p,0:0001; in the
mineral soils at 0±5 cm depth p,0:01and at 10±20 cm
depth p,0:04 (Table 4). However, the in¯uence of
compost treatment was different for the O-horizons and the mineral soils. Cmic decreased in the O-horizons by 22
(.2 mm) and by 35% (,2 mm). Also, Nmicdecreased by 23
and 28% in the O-horizons .2 and ,2 mm. Microbial
respiration was reduced by 17% in the O-horizons.2 mm
and by 25% in the O-horizons,2 mm. In contrast to the O-horizons, microbial respiration, Cmic and Nmicincreased by
14±21% in the mineral soil at 0±5 cm depth and by 14± 23% at 10±20 cm depth. Although the compost treatment was not signi®cant at 5±10 cm depth, the microbial respira-tion and microbial biomass tended also to increase.
Total Cmicand Nmicof the O-horizons generally decreased
by 6±30% (Fig. 1) although the total amount of organic matter increased by 28±82% due to the compost addition (Table 4). The only exceptions were the pine stand at
Solling with an increase of 8% in Nmic and the spruce
stand at UnterluÈû with increases of 17% in Cmic and 40%
in Nmic(Fig. 1). Compared to the other compost plots, there
was no or only little loss in total amount of organic matter at SP and US. On average, total Cmic and Nmicwere,
respec-tively, 10 and 4% lower in the compost plots. Total micro-bial respiration showed a distinct pattern: it increased at SP, SS, UB, and US by 1±29% and decreased at UP by 13% and at SB by 15%, but on average, there was no difference between compost and control plots.
Initial microbial respiration and microbial biomass C of compost were 6.0mg C g21h21 and 1.1 mg g21 (not shown). Based on these values, the compost addition of 6.3 kg m22 increased the total microbial respiration and Cmicof the O-horizons by 38 mg m22h21and 6.9 g m22in
the summer of 1997. Taking initial values into account, total microbial respiration and Cmic decreased on average by 23
and 27% in the compost plots during 2 years.
Cmicand Nmicwere linearly correlated for the O-horizon in
the control (R20:81; p,0:001) and compost plots
(R20:85;p,0:001). The C-to-N ratio of the microbial
biomass was 9.5 for the control plots and 9.4 for the com-post plots. Linear regressions for Cmic and Nmic of the
mineral soils resulted in R20:82 p,0:001 for the
control and R20:74 p,0:001 for the compost plots.
The average Cmic-to-Nmicratios were 11.3 and 12.0 for the
control and compost plots, respectively.
3.2. SOC and STN content
The results of the ANOVA indicate that the site effects on SOC and STN were not signi®cant for the fractionated O-horizons. There was only a site effect on STN p,0:007in
the O-horizon.2 mm. By contrast, a very large part of the variance in SOC p,0:0001;STN p,0:0001and
C-to-N ratio p,0:0001 were explained by site effects in all
mineral soil depths. The highest SOC and STN contents
W. Borken et al. / Soil Biology & Biochemistry 34 (2002) 403±412 408
occurred in the mineral soil of the beech and spruce stand at Solling (Table 4). These soils also had high silt contents (Table 1). Although variation in soil texture at UnterluÈû was negligible, the pine stand showed relatively high SOC and STN contents compared to the beech and spruce stands. The C-to-N ratios decreased down the mineral soil pro®le in all sites but were narrower in the silty soils from Solling than in the sandy soils from UnterluÈû.
Compost treatment had highly signi®cant effects on SOC
content and C-to-N-ratio in the O-horizons .2 mm p,
0:0001 and ,2 mm p,0:0001: SOC contents were
reduced by 21% in the.2 mm and by 27% in the,2 mm
fraction (Table 4). In contrast, STN content was not signi®-cantly affected by compost treatment. However, STN
content in the O-horizons,2 mm increased by 10% in the
sandy soils from UnterluÈû and decreased by 13% in the silty soils from Solling. No signi®cant differences were detected for the SOC contents in the mineral soils between the control and compost plots. STN contents were signi®cantly altered in the mineral soils by 24, 8.4 and 7.6% at 0±5 p, 0:001;5±10 p,0:06and 10±20 cm depths p,0:02;
respectively. The C-to-N ratios were signi®cantly reduced p,0:0001 by compost treatment in all mineral soil
depths.
3.3. Relationships between microbial and soil properties
All relationships between microbial and soil properties were highly signi®cant p,0:001 for the O-horizons
and mineral soils. However, the ®tted slopes from the control and compost plots were not signi®cantly different (Table 5). Thus, the compost treatment had no effect on the relationship between microbial and soil properties. For the O-horizons, microbial respiration and Cmicincreased
expo-nentially with increasing SOC. The SOC content explained 48 (control plots) and 65% (compost plots) of variance in microbial respiration, 39 (control plots) and 46% (compost plots) of the variance in Cmic. The increase of microbial
respiration per unit SOC was stronger than the increase of Cmicas indicated by the steeper slopes. An exponential trend
was also found for the relationship of Nmicand STN but the
relationships were weak for both the control plots R2 0:22and the compost plots R
20
:22:
For the relationships between microbial and soil proper-ties of the mineral soils, best results were obtained by performing linear regressions. SOC explained 60 and 53% of variance in microbial respiration, 56 and 64% of variance
in Cmic in samples from the control and compost plots,
respectively. STN content and Nmicof the mineral soil had
a higher correlation for the control R20:45and compost
plots R20:58than in the O-horizons.
4. Discussion
Microbial respiration (0.07±0.46mg C g21h21), Cmic
(0.02±0.49 mg C g21soil) and Nmiccontents (3±38mg N g2 1
soil) in the mineral soils from our study sites were low compared to undisturbed or less degraded temperate forest soils (e.g. Ross and Tate, 1993; Joergensen et al., 1995; Joergensen and Scheu, 1999). According to Raubuch and Beese (1995), soil microbial properties may re¯ect differ-ences in environmental conditions such as base saturation of mineral soils. For instance, the silty soils from Solling generally showed higher base saturation (Table 3), micro-bial biomass and respiration than the sandy soils at UnterluÈû (Table 4). Additionally, tree species and litter quality affect C and nutrient availability and thus control soil microbial properties. The higher microbial biomass and respiration in the mineral soil of the beech stands indicate higher C avail-ability than the respective spruce and pine stands at Solling and UnterluÈû. The overall low microbial biomass of our forest soils has been subjected to energy (C) and nutrient limitations (Scheu and Schaefer, 1998) but also to soil acidi-®cation (Wolters, 1991; von LuÈtzow et al., 1992). However, environmental stress may increase microbial respiration due to higher energy requirements for maintenance of active soil microorganisms as indicated by altered metabolic quotients (Anderson and Domsch, 1993).
The super®cial addition of large amounts of mature compost resulted in a signi®cant decrease in microbial
biomass and respiration in the O-horizons.2 and,2 mm
of our study sites. Accordingly, SOC contents of the
W. Borken et al. / Soil Biology & Biochemistry 34 (2002) 403±412 Table 5
Correlation matrix of microbial respiration, Cmicand Nmicwith soil organic carbon (SOC) and soil total nitrogen (STN) of the O-horizons n72and mineral soils n108from the control and compost plots
Fraction Parameter Control plots Compost plots
Regression ®t R2 Regression ®t R2
O-horizons Microbial respiration by SOC y2:1 5 e 0:0054x
0.48 y1:54 e 0:0072x
0.65
Cmicby SOC y0:82 e
0:0044x
0.39 y0:68 e 0:005x
0.46
Nmicby STN y0:08 e
0:11x
0.22 y0:05 e 0:13x
0.22
Mineral soils Microbial respiration by SOC y0:007x10:02 0.60 y0:006x10:06 0.53
Cmicby SOC y0:007x10:02 0.56 y0:007x10:010.64
O-horizons were signi®cantly reduced by the compost treat-ment while STN content was not affected. The amount of added compost was in the same range as the amount of organic matter in the O-horizons.
It is likely that microbial respiration and biomass of the O-horizons were partly reduced due to mixing with the compost. The initial microbial respiration rate and Cmic of
the applied compost were only 6.0mg C g21h21 and
1.1 mg C g21, respectively. These values are considerably lower than those of the O-horizons from the control and compost plots. Moreover, from a laboratory study it may be deduced that the original microbial respiration rate of the compost decreased during 2 years after addition to the O-horizon. Chodak et al. (2001) found a decrease of more than
50% in CO2 evolution for similar mature compost at a
temperature range from 5±258C during a 120-day incubation. From the microbial properties, based on dry weight, it is not clear whether the decrease in microbial respiration and biomass resulted only from the mixture of the O-horizons with compost or by additional processes. Therefore, we calculated proportional deviations in microbial properties of total O-horizons per unit area. Surprisingly, average total Cmic (210%) and Nmic (24%) decreased while the
total microbial respiration in the compost plots was not different from the control plots (Fig. 1). In fact, total micro-bial respiration and micromicro-bial biomass of the O-horizons initially increased by 38 mg m22h21and 6.9 g m22 when the compost was added. The reduction in microbial biomass may be partly explained by the strong loss of 1.2 kg m22 organic matter in the O-horizon from the compost plots during 2 years. Although the sample size (78.5 cm2) and the number of replications n6include a large error, it is likely that the amount of compost was reduced by decom-position (Chodak et al., 2001) and leaching of salts and dissolved organic matter (DOM).
Additionally, our results suggest that the original micro-bial community in the O-horizons was reduced by the compost treatment in two ways. On the one hand, the micro-bial community of the compost was probably different from the O-horizon. Guerrero et al. (2000) found high fungi popu-lation in municipal solid waste compost and pointed out that compost fungi are more tolerant to sodium chloride and sulfates than soil fungi. Competition between microorgan-isms and changes in microbial populations could have also affected the activity and biomass of key organisms such as lignin decomposing fungi. Scheu and Parkinson (1994) pointed out that fungi generally dominate the microbial biomass in the O-horizon. A reduction in the lignin break-down following compost application could affect growth of other microorganisms by decreasing contents of cellulose and hemicellulose protected by lignin structure. However, the constant C-to-N ratio of the microbial biomass indicates that there was no shift from fungal to bacterial population in the compost plots. Generally, bacteria have a low biomass C-to-N ratio in the range of 3±5 while that of fungi can vary between 4 and 15 (Paul and Clark, 1996).
On the other hand, elevated concentrations of mineral N could suppress the production of lignin-degrading enzymes by fungi (Fog, 1988; Tien and Myer, 1990). Changes in the species composition of micro-fungi have been found in forest soils treated with ammonium nitrate-fertilizer (Arnebrant et al., 1990). The amended mature compost contained considerable amounts of inorganic salts, particu-larly rich in nitrate, and thus may have diminished the auto-chthonous microbial community of the O-horizon in the long term. Our ®eld measurements of soil matric potential and seepage water at 10 cm depth (data not shown) reveal that inorganic salts from the compost remained for approxi-mately 3 months in the O-horizon. Several authors reported suppression of soil microbial biomass and respiration when high doses of inorganic salts were added (Martikainen et al., 1989; Smolander et al., 1994; Thirukkumaran and Parkinson, 2000).
According to previous ®ndings (SoÈderstroÈm et al., 1983), dissolved salts may have become toxic for some soil micro-organism due to increased osmotic potential in the O-horizons. Moreover, some soil microorganisms or microbial processes may be suppressed or diminished at critical concentrations of speci®c ions in soil solution. For instance, an inhibition of nitri®cation was observed when ammonium sulfate or ammonium chloride was applied in high dose (Lang et al., 1993). Our results suggest that the initial salt content of the compost could have contributed to the decline in the original microbial biomass of the O-horizons.
In contrast to the O-horizons, signi®cant increases in Cmic,
Nmic and microbial respiration were found in the mineral
soils at 0±5 and 10±20 cm depth. A trend towards higher Cmic, Nmicand microbial respiration rate was also measured
in the 5±10 cm depth. These changes could be related to the improved supply of nutrients in soil solution. We observed increased concentrations of dissolved organic carbon (DOC), nitrate, phosphate and potassium in the soil solution over the long term (data not shown). Super®cial application of lime and wood ash increase microbial biomass and respiration in the O-horizon (Zelles et al., 1990; Baath and Arnebrant, 1994; Smolander et al., 1994) but generally did not affect the mineral soil of forests.
During the ®rst 30±60 days, the population of bacteria and fungi decreased when a burnt forest soil was amended with municipal solid waste compost (Guerrero et al., 2000). However, the microbial population of the burnt soil increased only after the high salt content of compost was reduced by intense rainfall. It is obvious that reported effects of fertilizer treatments on microorganisms strongly related to salt concentration in soil solution and on type of fertilizer. As a result of improved phosphorous supply, SOM in the mineral soils may have become more available to micro-organisms. Phosphorous is known as a limiting nutrient in many German forests. Gallardo and Schlesinger (1994) found increased microbial biomass in the mineral soil of a warm temperate forest following phosphorous fertilization. By contrast, no phosphorous fertilization effect on microbial
biomass and activity was observed in the O-horizon of a Norway spruce stand (Smolander et al., 1994).
The release of DOC from the compost may have also promoted the growth of autochthonous microorganisms in the mineral soils. In a laboratory study, the release of DOC from mature compost decreased with increasing
tempera-ture and exceeded the CO2release at temperatures below
118C (Chodak et al., 2001). The rather high DOC release described by Chodak et al. (2001) may indicate that DOC from mature compost was an important C source for soil microorganisms in our forest sites. However, DOC is generally a small carbon resource for microorganisms in forest soils. Borken et al. (1999) found a net release of 60±
83 kg DOC-C ha21yr21 from the O-horizon and upper
10 cm of the mineral soil in an adjacent Norway spruce stand at Solling.
Zech et al. (1994) stated that the absorption of DOC by sesquioxides contributes to the storage of organic matter in mineral soils. The SOC contents in the mineral soils of our sites were not affected by the compost treatment. However, the observed increase in STN indicates transport of N from the compost to the mineral soil and retention in the mineral soil, perhaps by adsorption of DOM with a relatively low C-to-N ratio. Microorganisms could have modi®ed DOM by using it as a C source, thereby reducing the C-to-N ratio. An adsorption of DOM with a lower C-to-N ratio than SOM would have increased the STN content more than the SOC content. Transformation of inorganic N into organic N by microbial decomposition of plant residues (Barber, 1995) could also have increased the STN content. In accordance to our results, repeated additions of inorganic N fertilizers led to long-term retention of N in soils of pine and hardwood forests (Aber et al., 1998). Although the forest sites in the study of Aber et al. received moderately increased amounts of N by atmospheric deposition, 85±99% of additional N was accumulated in soils.
The Cmic-to-Nmicratios of 11.3 for the control plots and of
12.0 for the compost plots are wider than the mean of 7.7 reported for a large number of beech forest soils but within the wide range of 5.4±17.3 (Joergensen et al., 1995). According to Paul and Clark (1996) fungi would be expected to dominate the decomposition of SOM in the mineral soil of both plots. Moreover, the Cmic-to-Nmicratios
indicate that the increased STN content and altered supply of nitrate did not affect the fungi±bacteria ratio in the compost plots.
The Cmic-to-Nmicratio of forest soils is not related to C and
N availability, however, microbial N incorporation is affected by C and N availability (Joergensen et al., 1995). Our results suggest limited C availability in the control and compost plots. Availability of N to soil microorganisms is probably not limited due to high atmospheric N deposition in our forests. Furthermore, the increased N availability by the application of compost did not narrow the Cmic-to-Nmic
ratios. The weaker relationships between Nmic and STN
content compared to relationships between Cmic and SOC
content for the control and compost plots may also indicate suf®cient N is available for microorganisms.
In conclusion, the results of our study suggest that the addition of mature compost to the soil surface increase the microbial biomass and respiration of degraded mineral forest soils by altering the release of nutrients and DOM from the organic horizon in the long term. High inorganic salt contents and/or the microbial community of compost can reduce speci®c microbial transformations by diminish-ing the original biomass of O-horizons. Consequently, application of compost with low salt content is desired for better soil amelioration. The increase in STN content and the narrowing of the C-to-N ratio indicate that the forest soils were not N-saturated and have the capacity to accu-mulate additional amounts of N.
Acknowledgements
We thank E. Davidson and K. Savage for their comments on the manuscript. This study was ®nanced by Deutsche Bundesstiftung Umwelt. We wish to thank Umweltschutz Nord, Ganderkesee, Germany for delivering compost for the ®eld experiment. W. Borken acknowledges the ®nancial support received by the Deutsche Forschungsgemeinschaft.
References
Aber, J., McDowell, W., Nadelhoffer, K., Magill, A., Berntson, G., Kamakea, M., McNultry, S., Currie, W., Rustad, L., Fernandez, I., 1998. Nitrogen saturation in temperate forests ecosystemsÐhypotheses revisited. Bioscience 48, 921±934.
Ammar, S.B., 1996. Impacts of separation on compost quality. In: De Bertoldi, M., Sequi, P., Lemmes, B., Papi, T. (Eds.). The Science of Composting. Chapman & Hall, London, pp. 1071±1073.
Anderson, T.H., Domsch, K.H., 1993. The metabolic quotient for CO2 (qCO2) as a speci®c activity parameter to assess the effects of environ-mental conditions, such as pH, on the microbial biomass of forest soils. Soil Biology and Biochemistry 25, 393±395.
Arnebrant, K., Baath, E., SoÈderstroÈm, B., 1990. Changes in microfungal community structure after fertilization of Scots pine forests with ammo-nium nitrate or urea. Soil Biology and Biochemistry 22, 309±312. Baath, E., Arnebrant, K., 1994. Growth rate and response of bacterial
communities to pH in limed and ash treated forest soils. Soil Biology and Biochemistry 26, 995±1001.
Baath, E., Berg, B., Lohm, U., Lundgren, B., Lundkvist, H., Rosswall, T., SoÈderstroÈm, B., Wiren, A., 1980. Effects of experimental acidi®cation and liming on soil organisms and decomposition in a Scots pine forest. Pedobiologia 20, 85±100.
Barber, S.A., 1995. Soil Nutrient Bioavailability: A Mechanistic Approach. Wiley, New York 414 pp.
Borken, W., Beese, F., 2000. Chancen und risiken der kompostausbringung. Allgemeine Forstzeitschrift 6, 318±321.
Borken, W., Xu, Y.J., Brumme, R., Lamersdorf, N., 1999. A climate change scenario for carbon dioxide and dissolved organic carbon ¯uxes from a temperate forest soil: drought and rewetting effects. Soil Science Society of America Journal 63, 1848±1855.
Brookes, P.C., Landman, A., Pruden, G., Jenkinson, D.S., 1985. Chloro-form fumigation and the release of soil nitrogen: a rapid direct extraction method for measuring microbial biomass nitrogen in soil. Soil Biology and Biochemistry 17, 837±842.
Chodak, M., Borken, W., Ludwig, B., Beese, F., 2001. Effect of tempera-ture on the mineralisation of C and N of fresh and matempera-ture compost in sandy material. Journal of Plant Nutrition and Soil Science 164, 289± 294.
FAO, 1998. World reference base for soil resources. World Soil Resources Reports, 84, FAO, ISRIC and ISSS, Rome, Italy.
Fog, K., 1988. The effect of added nitrogen on the rate of decomposition of organic matter. Biological Reviews 63, 433±462.
Gallardo, A., Schlesinger, W.H., 1994. Factors limiting microbial biomass in the mineral soil and forest ¯oor of a warm-temperate forest. Soil Biology and Biochemistry 26, 1409±1415.
Guerrero, C., Gomez, I., Mataix Solera, J., Moral, J., Mataix Beneyto, J., Hernandez, M.T., 2000. Effect of solid waste compost on microbio-logical and physical properties of a burnt forest soil in ®eld experi-ments. Biology and Fertility of Soils 32, 410±414.
Joergensen, R.G., 1996. The fumigation extraction method to estimate soil microbial biomass: calibration of the kEC-factor. Soil Biology and Biochemistry 28, 25±31.
Joergensen, R.G., Mueller, T., 1996. The fumigation extraction method to estimate soil microbial biomass: calibration of thekEN-factor. Soil Biology and Biochemistry 28, 33±37.
Joergensen, R.G., Scheu, S., 1999. Response of soil microorganisms to the addition of carbon, nitrogen and phosphorous in a forest Rendzina. Soil Biology and Biochemistry 31, 859±866.
Joergensen, R.G., Anderson, T.H., Wolters, V., 1995. Carbon and nitrogen relationship in the microbial biomass of soils in beech (Fagus sylvatica L.) forests. Biology and Fertility of Soils 19, 141±147.
Lang, E., Beese, F., Jagnow, G., 1993. In¯uence of water content and salts on the nitri®cation in samples of a Dystric Cambisol. Journal of Plant Nutrition and Soil Science 156, 83±87.
Loft®eld, N., Flessa, H., Augustin, J., Beese, F., 1997. Automated gas chromatographic system for rapid analysis of the atmospheric trace gases methane, carbon dioxide, and nitrous oxide. Journal of Environ-mental Quality 26, 560±564.
von LuÈtzow, M., Zelles, L., Scheunert, I., Ottow, J.C.G., 1992. Seasonal effects of liming, irrigation, and acid precipitation on microbial biomass N in a spruce (Picea abiesL.) forest soil. Biology and Fertility of Soils 13, 130±134.
Martikainen, P.J., Aaarnio, T., Taavitsainen, V., Paivinen, L., Salonen, K., 1989. Mineralisation of carbon and nitrogen in soil samples taken from three fertilized pine stands: long term effects. Plant and Soil 114, 99± 106.
Paul, E.A., Clark, F.E., 1996. Soil Microbiology and Biochemistry. Second ed. Academic Press, San Diego.
Raubuch, M., Beese, F., 1995. Pattern of microbial indicators in forests along an European transect. Biology and Fertility of Soils 19, 362±368. Ross, D.J., Tate, K.R., 1993. Microbial C and N, and respiratory activity, in
litter and soil of a southern beech (Nothofagus) forest: distribution and properties. Soil Biology and Biochemistry 25, 477±483.
SAS Institute, 1996. SAS User's Guide: Statistics. SAS Institute, Cary, NC. Scheu, S., Parkinson, D., 1994. Changes in the bacterial and fungal biomass C, bacterial and fungal biovolume and ergosterol content after drying, remoistening and incubation of different layers of cool temperate forest soils. Soil Biology and Biochemistry 26, 1515±1525.
Scheu, S., Schaefer, M., 1998. Bottom-up control of the soil macro-fauna community in a beechwood on limestone: manipulation of food resources. Ecology 79, 1573±1585.
Smolander, A., Kurka, A., Kitunen, V., MaÈlkoÈnen, E., 1994. Microbial biomass C and N, respiratory activity in soil of repeatedly limed, and N- an P-fertilized Norway spruce stands. Soil Biology and Biochemistry 26, 957±962.
SoÈderstroÈm, B., Baath, E., Lundgren, B., 1983. Decrease in soil microbial activity and biomasses owing to nitrogen amendments. Canandian Journal of Microbiology 29, 1500±1506.
Thirukkumaran, C.M., Parkinson, D., 2000. Microbial respiration, biomass, metabolic quotient and litter decomposition in a lodgepole pine forest ¯oor amended with nitrogen and phosphorous fertilizers. Soil Biology and Biochemistry 32, 59±66.
Tien, M., Myer, S.B., 1990. Selection and characterization of mutants of Phanerochaete chrysosporum exhibiting ligninolytic activity under nutrient rich conditions. Applied and Environmental Microbiology 56, 2540±2544.
Ulrich, B., 1994. Nutrient and acid±base budget of central European forest ecosystems. In: Godbold, D.L., HuÈttermann, A. (Eds.). Effects of Acid Rain on Forest Processes. Wiley, New York, pp. 1±50.
Vance, E.D., Brookes, P.C., Jenkinson, D.S., 1987. An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry 19, 703±707.
Wolters, V., 1991. Biological processes in two beech forest soils treated with simulated acid rainÐa laboratory experiment withIsotoma tigrina (Insecta, Collembola). Soil Biology and Biochemistry 23, 381±390. Wu, J., Joergensen, R.G., Pommerening, B., Chaussod, R., Brookes, P.C.,
1990. Measurement of soil microbial biomass C by fumigation extrac-tion: an automated procedure. Soil Biology and Biochemistry 22, 1167±1169.
Zech, W., Guggenberger, G., Schulten, H.R., 1994. Budgets and chemistry of dissolved organic carbon in forest soils: effects of anthropogenic soil acidi®cation. Science of Total Environment 152, 49±62.
Zelles, L., Scheunert, I., Kreutzer, K., 1987. Effect of arti®cial irrigation, acid precipitation and liming on the microbial activity in soil of a spruce forest. Biology and Fertility of Soils 4, 137±143.
Zelles, L., Stepper, K., Zsolnay, A., 1990. The effect of lime on microbial activity in spruce (Picea abiesL.) forests. Biology and Fertility of Soils 9, 78±82.
