ORIGINAL PAPER

Soil compaction and forest floor removal reduced microbialbiomass and enzyme activities in a boreal aspen forest soil

Xiao Tan & Scott X. Chang & Richard Kabzems

Received: 3 November 2006 /Revised: 11 July 2007 /Accepted: 12 July 2007 / Published online: 1 August 2007# Springer-Verlag 2007

Abstract Soil enzymes are linked to microbial functionsand nutrient cycling in forest ecosystems and are consid-ered sensitive to soil disturbances. We investigated theeffects of severe soil compaction and whole-tree harvestingplus forest floor removal (referred to as FFR below,compared with stem-only harvesting) on available N,microbial biomass C (MBC), microbial biomass N(MBN), and microbial biomass P (MBP), and dehydroge-nase, protease, and phosphatase activities in the forest floorand 010 cm mineral soil in a boreal aspen (Populustremuloides Michx.) forest soil near Dawson Creek, BritishColumbia, Canada. In the forest floor, no soil compactioneffects were observed for any of the soil microbial orenzyme activity parameters measured. In the mineral soil,compaction reduced available N, MBP, and acid phospha-tase by 53, 47, and 48%, respectively, when forest floor wasintact, and protease and alkaline phosphatase activities by28 and 27%, respectively, regardless of FFR. Forest floorremoval reduced available P, MBC, MBN, and protease andalkaline phosphatase activities by 38, 46, 49, 25, and 45%,respectively, regardless of soil compaction, and available N,

MBP, and acid phosphatase activity by 52, 50, and 39%,respectively, in the noncompacted soil. Neither soil com-paction nor FFR affected dehydrogenase activities. Reduc-tions in microbial biomass and protease and phosphataseactivities after compaction and FFR likely led to thereduced N and P availabilities in the soil. Our resultsindicate that microbial biomass and enzyme activities weresensitive to soil compaction and FFR and that suchdisturbances had negative consequences for forest soil Nand P cycling and fertility.

Keywords Microbial biomass . Protease . Phosphatase .

Available N . Available P. Long-termsoil productivity (LTSP)

Introduction

Soil enzymes are known to be involved in nutrient cycling,and as such, their activities can be used as potentialindicators of nutrient cycling processes. In addition, soilenzymes are specific for the types of chemical reactions inwhich they participate. For example, dehydrogenase playsan important role in the initial oxidation of soil organicmatter and occurs only in viable cells; therefore, it isbelieved that dehydrogenase is an intracellular enzymeinvolved in microbial respiratory processes (Dick 1994). Incontrast, protease and phosphatase have extracellularcomponent. Protease activity is involved in breaking downproteins, resulting in the release of NH4 N (Ladd andButler 1972). Phosphatase activity plays a critical role inthe production of inorganic P, catalyzing the hydrolysis oforganic P esters to inorganic P (Speir and Ross 1978). Soilenzyme activities may be sensitive to both natural andhuman-induced disturbances, and measurements of the

Biol Fertil Soils (2008) 44:471479DOI 10.1007/s00374-007-0229-3

X. Tan : S. X. Chang (*)Department of Renewable Resources, University of Alberta,442 Earth Sciences Building,Edmonton, AB T6G 2E3, Canadae-mail: Scott.Chang@ualberta.ca

R. KabzemsMinistry of Forests and Range,Dawson Creek, BC V1G 4A4, Canada

Present address:X. TanAlbian Sands Energy Inc.,P.O. Box 5670, Hwy 63 North,Fort McMurray, AB T9H 4W1, Canada

activities of a range of enzymes may provide a validestimation of the metabolic response of soils to manage-ment practices and environmental stress (Dick et al. 1988;Nannipieri 1994).

Soil compaction and forest floor removal are two mostcommon disturbances caused by forest harvesting practicesand mechanical site preparation in boreal forests (Corns1988; McMinn and Hedin 1990). Many studies have foundthat soil physical and chemical properties such as soilporosity, aeration, water content, temperature, and substrateavailability are affected by soil compaction and forest floorremoval (Tew et al. 1986; Zabowski et al. 1994; Gomezet al. 2002; Tan et al. 2005). By changing the percentage ofmacro- and microporosity, soil compaction may causeoxygen deficiency by reducing oxygen diffusion rateswhich then affect the activities of enzymes such as catalaseand phosphatase (Glinski et al. 1986; Pagliai and De Nobili1993). Soil compaction has been found to reduce phospha-tase, amidase, and dehydrogenase activities (Dick et al.1988; Jordan et al. 2003); however, higher phosphataseactivity has been found in compacted soils, suggesting thatmicrobial communities may be tolerant and resilient to soilcompaction (Buck et al. 2000; Shestak and Busse 2005).Postharvest forest management practices have been foundto reduce extracellular enzyme activities (e.g., glucosidase,cellobiohydrolase, and phenol oxidase) involved in litterdecomposition (Waldrop et al. 2003; Hassett and Zak2005). Quilchano and Maran (2002) found that sitefactors (soil pH, available nutrients, and soil texture) andsampling season had greater influence on enzyme activitiesthan management factors (shrub-clearing and stand thin-ning). Changes in soil enzyme activities after soil compac-tion and forest floor removal can be complicated and maybedependant on enzyme type, site or soil types, and climaticconditions (Dick et al. 1988; Li et al. 2002).

In an earlier study, we found that soil compactionreduced microbial biomass N in the mineral soil and forestfloor removal tended to reduce microbial biomass C and Nin the surface mineral soil (Tan et al. 2005). We hypothesizethat soil compaction and forest floor removal will alsoreduce soil enzyme activities at this study site. The linkbetween enzyme activities and microbial biomass may helpprovide microbial community parameters that can berelated to potential rates of organic compound degradation.For example, enzyme activity to microbial biomass ratiogives a measure of the enzyme activity per unit biomass,which may be used as a better index to evaluate theresponse of soil enzyme activities to management practices(Landi et al. 2000). Because dehydrogenase, protease, andphosphatase play important roles in carbon, nitrogen, andphosphorus cycling, the objectives of this study were todetermine the effects of soil compaction and forest floorremoval on these enzyme activities and to relate enzyme

activities to soil physical and chemical properties andmicrobial biomass in a boreal aspen (Populus tremuloides-Michx.) forest long-term soil productivity (LTSP) site nearDawson Creek in British Columbia, Canada.

Materials and methods

Study site and experimental design

The study site is located near Dawson Creek (5558 N,12028 W), in north-eastern British Columbia. The site isrepresentative of mesic aspen ecosystems in the moist andwarm subzone of the Boreal White and Black Sprucebiogeoclimatic zone (BWBSmw) (DeLong et al. 1991).Elevation is approximately 720 m, and the average slope is4%, with a south aspect. The area has a mean annualtemperature of 1.6C and mean annual precipitation of482 mm, with approximately half of which fall as snow,and about 70% of rainfall occurs in the growing seasonbetween May and August (Environment Canada 2006).Soils on the study site were developed on a silt loamveneer, 20 to 30 cm thick, laid over a clay loam. The soil isclassified as Orthic Luvic Gleysols (Soil ClassificationWorking Group 1998). Details of soil properties beforeharvesting or posttreatment can be found in Tan et al.(2005).

The LTSP study uses a 33 completely randomizedfactorial experimental design with three replications imple-mented over a 4-year period. Treatment plots measuring4070 m were delineated before logging and wererandomly assigned to one of nine combinations of soilcompaction and organic matter removal treatments. Plotswere harvested on frozen ground to ensure that minimal soildisturbance occurred during the harvesting phase. In thisstudy, we investigated the extreme treatment levels withineach factor to form a factorial combination of twocompaction (C0: no soil compaction, the undisturbed plotsdid not receive any postharvest compaction and C2: severesoil compaction, the mineral soil was depressed by 4 to5 cm using a vibrating pad mounted on an excavator) andtwo organic matter removal levels (OM1: stem-onlyharvesting, the trees were delimbed on-site, with tree tops,limbs and all non-merchantable woody materials left on theforest floor; and OM3: whole-tree harvesting plus forestfloor removal (referred to as FFR hereafter). In the OM3treatment, all the woody and nonwoody material wasremoved from the plot, and the forest floor was strippedto expose the mineral soil using an excavator. As wasindicated in Tan et al. (2005), all 12 studied plots were notestablished in the same year. In the statistical analysisdescribed below, we treated the year since plot estab-lishment as a covariable to remove the effect of year

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since plot establishment on the measured soil biologicalparameters.

Soil sampling

Forest floor and 010 cm mineral soil samples werecollected on June 20 and August 20 of 2005. Three soilcores (6.3 cm in diameter) were collected in each plot fromrandomly selected locations and bulked to form a compos-ite sample for each layer. Forest floor and mineral soilsamples were immediately placed on ice and shipped to thelaboratory in a cooler. Fresh samples were homogenized,then sieved (4 mm) and stored at 4C until further analysis.Half of each sample was used for enzyme activities andmicrobial biomass. The other half was promptly air-dried,ground, and sieved (

tricloracetic acid. After centrifugation, 2 ml of the super-natant was mixed with 3 ml 1.4 mol l1 Na2CO3 and 1 mlFolin reagent. Absorbance was measured at 700 nm (bluecolor) compared to the similarly treated tyrosine standards.Tyrosine reacts with Folin to produce an unstable productthat becomes reduced to molybdenum/tungsten blue. Con-trols either without soil or without substrate were used.

Phosphomonoesterases (acid and alkaline phosphatase)activities were measured based on the colorimetricestimation of the p-nitrophenol release from p-nitrophenylphosphate (PNP) (Tabatabai 1994). One gram of freshmineral soil (0.1 g for forest floor) was placed in a 50-mlErlenmeyer flask, and then 0.2 ml toluene, 4 ml tris-hydroxymethyl aminomethane (THAM, with maleic,citric, and boric acids) buffer (pH 6.5 for acid phosphataseassay or pH 11 for alkaline phosphatase assay), 1 mlp-nitrophenyl phosphate solution made in the same bufferwas added, and then the flask was swirled for a fewseconds to mix the content. After stoppering the flask, theflask was placed in an incubator at 37C for 1 h. Afterremoving the stopper, 1 ml 0.5 mol l1 CaCl2 and 4 ml0.5 mol l1 NaOH was added, the mixture was swirled fora few seconds, and then the soil suspension was filteredthrough Whatman No. 2 filter papers. The yellow colorintensity was measured with a spectrophotometer at420 nm. Control measurements were made with eachenzyme assay to account for the color not derived fromproduct released by the enzyme substrate. To obtain thecontrol samples, we followed the procedures describedabove for the assay of the enzyme activities but made the

addition of the substrate immediately after the addition ofthe solutions to stop the enzyme reaction.

Statistical analysis

The SAS package was used to perform all statisticalanalyses (SAS Institute Inc. 1999). Assumptions of nor-mally distributed errors and homogeneity of variances weretested. A GLM procedure for the mixed model was used totest the effects of soil compaction and FFR on soil moisturecontent, soil chemical properties, microbial biomass, andenzyme activities for each depth. Because treatment plotswere established in different years, year since installationwas used as a covariable to test if it affected the dependentvariables. No significance of the year since installation wasfound for any of the dependent variables tested. Correlationanalysis was used to evaluate the relationship between soilphysical and chemical properties, microbial biomass, andenzyme activities. Statistical significance was accepted at=0.05 for all analyses.

Results

In the forest floor, soil moisture content, soil pH, total C, N,and P concentrations, and available N and P concentrationswere not affected by soil compaction or sampling date, withthe exception of available N being significantly higher inAugust than in June (Table 1). In the mineral soil, soilcompaction did not affect any soil properties other than

Table 1 Effects of soil compaction and forest floor removal on soil physical and chemical properties in June and August 2005

Treatmenta Moisture content(g kg1)

Soil pH(in H2O)

Total C(g kg1)

Total N(g kg1)

Total P(g kg1)

Available N(mg N kg1)

Available P(mg P kg1)

Jun. Aug. Jun. Aug. Jun. Aug. Jun. Aug. Jun. Aug. Jun. Aug. Jun. Aug.

Forest floorOM1C0 1,950 2,310 5.3 5.40 372 367 14.6 17.7 1.5 1.5 49.5 73.6 219.4 228.5

(140) (320) (0.1) (0.0) (11) (8) (1.2) (0.4) (0.1) (0.1) (4.3) (15.9) (15.9) (14.3)OM1C2 2,430 2,750 5.4 5.30 399 398 17.5 18.1 1.7 1.8 37.8 67.7 208.4 203.9

(310) (230) (0.2) (0.1) (8) (1) (0.4) (0.8) (0.1) (0.1) (3.2) (19.0) (28.5) (20.2)Mineral soilOM1C0 290 330 6.1 6.1 15 14 0.9 0.9 0.6 0.6 1.8 2.0 11.0 15.2

(13) (20) (0.1) (0.1) (1) (2) (0.1) (0.1) (0.01) (0.1) (0.4) (0.4) (1.7) (1.6)OM1C2 280 310 6.0 6.1 14 12 1.0 0.8 0.6 0.5 0.7 1.0 10.0 14.5

(14) (24) (0.1) (0.1) (2) (2) (0.1) (0.1) (0.1) (0.1) (0.1) (0.5) (1.8) (1.2)OM3C0 270 280 6.3 6.1 9 9 0.7 0.6 0.5 0.5 0.7 1.0 5.5 10.8

(34) (17) (0.1) (0.1) (1) (0) (0.1) (0.1) (0.1) (0.1) (0.1) (0.4) (1.4) (1.5)OM3C2 210 260 6.1 6.1 10 9 0.7 0.7 0.5 0.5 0.7 0.9 5.7 10.2

(28) (12) (0.1) (0.1) (2) (2) (0.1) (0.1) (0.1) (0.1) (0.1) (0.1) (1.7) (0.7)

Values are means with standard errors given in parentheses (n=3).a Treatment codes: OM1C0 Stem-only harvest with no compaction, OM1C2 stem-only harvest with severe compaction, OM3C0 forest floorremoval with no compaction, OM3C2 forest floor removal with severe compaction.

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reducing available N by 53% when the forest floor wasintact (Table 1). Forest floor removal did not affect soil pHor total P, but significantly reduced soil moisture content,total C, total N, and available P by 16, 34, 25, and 38%,respectively. Available N was reduced by 52% by FFR inthe noncompacted soil, but was not affected by FFR in thecompacted soil. Only available P in the mineral soilincreased from June to August (Table 1).

In the forest floor, MBC, MBN, and MBP were notaffected by soil compaction or sampling date (Tables 2 and

4). In the mineral soil, soil compaction reduced MBP by47% when the forest floor was intact but did not affectMBC or MBN regardless of FFR (Tables 2 and 4). Forestfloor removal reduced MBC and MBN in the mineral soilby 46 and 49%, respectively, regardless of soil compaction,and MBP by 50% in the noncompacted soil, but did notaffect MBP in the compacted soil. Soil MBC, MBN, andMBP were not different between the two sampling dates.

In the forest floor, soil compaction did not affectdehydrogenase, protease, or acid and alkaline phosphatase

Table 2 Effects of soil compaction and forest floor removal on microbial biomass C (MBC), microbial biomass N (MBN), and microbial biomassP (MBP), and microbial C:N and C:P ratios in June and August 2005

Treatmenta MBC (mg C kg1) MBN (mg N kg1) Microbial C:N ratio MBP (mg P kg1) Microbial C:P ratio

Jun. Aug. Jun. Aug. Jun. Aug. Jun. Aug. Jun. Aug.

Forest floorOM1C0 14,000 13,000 1,950 1,750 6 7 630 640 22 18

(1,100) (1,160) (310) (140) (0) (0) (20) (80) (4) (1)OM1C2 13,100 12,540 1,940 1,780 7 7 600 700 22 18

(340) (730) (140) (80) (1) (3) (60) (40) (4) (0)Mineral soilOM1C0 530 550 70 70 8 7 40 30 13 16

(170) (120) (4) (20) (0) (0) (3) (5) (1) (1)OM1C2 410 480 50 50 9 9 20 20 22 22

(10) (40) (1) (6) (0) (0) (1) (2) (1) (2)OM3C0 390 250 40 30 8 8 20 20 14 15

(10) (20) (2) (1) (1) (1) (1) (1) (1) (0)OM3C2 240 200 30 20 7 7 20 20 14 11

(10) (10) (4) (3) (1) (0) (3) (1) (1.4) (1)

Values are means with standard errors given in parenthesis (n=3).a Treatment codes are described in the footnote of Table 1.

Table 3 Effects of soil compaction and forest floor removal on dehydrogenase, protease, and phosphatase activities in June and August 2005

Treatmenta Dehydrogenase (mg TPFkg1 soil d1)

Protease (mg NH2Nkg1 soil d1)

Acid phosphatase(mg p-nitrophenolkg1 soil d1)

Alkaline phosphatase(mg p-nitrophenolkg1 soil d1)

Total phosphatase(mg p-nitrophenolkg1 soil d1)

Jun. Aug. Jun. Aug. Jun. Aug. Jun. Aug. Jun. Aug.

Forest floorOM1C0 21,500 32,900 32,100 53,100 5,600 6,300 3,400 2,300 9,000 8,600

(1,900) (6,200) (4,400) (3,900) (620) (550) (110) (230) (730) (610)OM1C2 18,100 28,600 23,300 51,400 5,400 6,100 3,500 2,800 8,900 8,900

(6,200) (4,600) (690) (4,300) (380) (630) (120) (470) (500) (250)Mineral soilOM1C0 440 830 490 810 250 310 100 120 350 420

(140) (120) (60) (120) (30) (50) (20) (20) (40) (60)OM1C2 420 860 440 510 100 180 50 80 160 270

(130) (240) (150) (50) (30) (30) (10) (20) (40) (40)OM3C0 330 750 420 570 150 180 80 50 230 230

(140) (100) (100) (30) (10) (20) (20) (10) (20) (20)OM3C2 310 440 280 420 120 170 80 40 200 210

(110) (120) (70) (50) (10) (20) (20) (20) (20) (20)

Values are means with standard errors given in parentheses (n=3).a Treatment codes are described in the footnote of Table 1.

Biol Fertil Soils (2008) 44:471479 475

activities (Tables 3 and 4). Dehydrogenase and Proteaseactivities were greater in August than in June. In themineral soil, soil compaction did not affect dehydrogenaseactivities (Tables 3 and 4), but reduced protease andalkaline phosphatase activities by 28 and 27%, respectively,regardless of FFR, and acid phosphatase activity by 48%when forest floor was intact, but did not affect acidphosphatase activity when forest floor was removed(Tables 3 and 4). Forest floor removal did not affectdehydrogenase activity, but reduced protease activity by25% regardless of soil compaction, and acid phosphataseactivity by 39% in the noncompacted soil but did not affectacid phosphatase activity in the compacted soil (Tables 3and 4). The interaction between FFR and sampling date on

alkaline phosphatase activity was significant, showing thatalkaline phosphatase activities were reduced by FFR by45% in August but not affected by FFR in June (Tables 3and 4). In the forest floor, dehydrogenase:MBC, protease:MBN, and phosphatase:MBP ratios were not affected bysoil compaction (data not shown). In the mineral soil, soilcompaction did not affect the dehydrogenase:MBC, prote-ase:MBN, and phosphatase:MBP ratios, while forest floorremoval increased dehydrogenase:MBC ratio by 66% inAugust and protease:MBN ratio by 45 and 76% in June andAugust, respectively (data not shown).

Many positive correlations were observed among soilphysical, chemical, and microbial biomass and enzymeactivities (Table 5). For example, soil moisture content had

Table 4 Analysis of variance (P values) of the effects of soil compaction, forest floor removal, and sampling date on microbial biomass C,microbial biomass N, and microbial biomass P, and activities of dehydrogenase, protease, acid and alkaline phosphatase measured in June andAugust 2005

Source of variance df Microbialbiomass C

Microbialbiomass N

Microbialbiomass P

Dehydrogenase Protease Acidphosphatase

Alkalinephosphatase

Forest floorCompaction (C) 1 0.552 0.789 0.664 0.434 0.418 0.776 0.423Time (T) 1 0.346 0.645 0.758 0.023 0.037 0.996 0.779CT 1 0.653 0.699 0.818 0.365 0.423 0.878 0.652Mineral soilC 1 0.535 0.185 0.037 0.072 0.022 0.002 0.055Forest floorremoval (OM)

1 0.048 0.003 0.017 0.060 0.039 0.008 0.025

COM 1 0.835 0.477 0.048 0.502 0.812 0.016 0.125T 1 0.283 0.624 0.067 0.305 0.117 0.113 0.326CT 1 0.698 0.710 0.089 0.398 0.420 0.160 0.213OMT 1 0.296 0.696 0.196 0.242 0.108 0.253 0.047COMT 1 0.885 0.988 0.326 0.941 0.654 0.394 0.874

The P values less than 0.05 are in italics.

Table 5 Correlation coefficient (r value) among soil moisture content, pH, total C (TC), total N (TN), total P (TP), available N (AN), available P(AP), microbial biomass C (MBC), microbial biomass N (MBN), and microbial biomass P (MBP), and activities of dehydrogenase (DHG),protease (PRT), acid phosphatase (ACP) and alkaline phosphatases (AKP) in the mineral soil

Variable* Moisture content pH TC TN TP AN AP MBC MBN MBP DHG PRT ACP

pH 0.34TC 0.84 0.02TN 0.75 0.17 0.94TP 0.43 0.39 0.69 0.84AN 0.53 0.38 0.47 0.47 0.46AP 0.49 0.17 0.60 0.47 0.63 0.50MBC 0.72 0.19 0.70 0.53 0.27 0.62 0.81MBN 0.69 0.14 0.74 0.57 0.30 0.69 0.82 0.98MBP 0.67 0.04 0.75 0.61 0.25 0.65 0.71 0.76 0.82DHG 0.35 0.09 0.33 0.27 0.43 0.68 0.44 0.60 0.58 0.26PRT 0.54 0.05 0.66 0.54 0.43 0.83 0.67 0.73 0.82 0.84 0.60ACP 0.36 0.01 0.42 0.31 0.14 0.59 0.58 0.69 0.75 0.70 0.48 0.67ALP 0.56 0.16 0.73 0.59 0.61 0.47 0.78 0.83 0.82 0.76 0.35 0.72 0.61

Correlation coefficients significant at =0.05 are in italics (n=12).

Table 4 Analysis of variance (P values) of the effects of soilcompaction, forest floor removal, and sampling date on microbialbiomass C, microbial biomass N, and microbial biomass P, and

activities of dehydrogenase, protease, acid and alkaline phosphatasemeasured in June and August 2005

Table 5 Correlation coefficient (r value) among soil moisture content,pH, total C (TC), total N (TN), total P (TP), available N (AN),available P (AP), microbial biomass C (MBC), microbial biomass N

(MBN), and microbial biomass P (MBP), and activities of dehydro-genase (DHG), protease (PRT), acid phosphatase (ACP) and alkalinephosphatases (AKP) in the mineral soil

476 Biol Fertil Soils (2008) 44:471479

significant positive correlations with total C and N, andMBC, MBN, and MBP. Both available N and P werepositively correlated with microbial biomass and mostenzyme activities. Strong correlations were observedbetween microbial biomass and all enzyme activities.

Discussion

The lack of soil compaction effects on microbial biomassand enzyme activities was consistent with an earlier fieldstudy on the same site where soil compaction did not affectmicrobial biomass, microbial respiration, and N availability(Mariani et al. 2006). Statistically significant alterations inbulk density and other chemical properties of the forestfloor caused by soil compaction have been reported (Demiret al. 2007; Choi et al. 2005). The bulk density of the forestfloor in the LTSP experiment was found to be the same asthat in the mature forest, suggesting that physical andbiological properties of the forest floor may be recoveredfrom compaction a few years after the treatment wasapplied (Kabzems and Haeussler 2005; Mariani et al.2006; Corns 1988). We cannot, however, rule out thepossibility that the compaction treatment may never hadcaused negative effects on soil microbiological propertiesand enzyme activities in the forest floor.

Soil compaction reduced protease and phosphataseactivities in the mineral soil, most likely due to reducedaeration porosity (Tan et al. 2005). Soil enzyme activitieshave been found to be positively correlated with the volumeof soil occupied by pores ranging in size from 30 to200 m, which are considered the most important poresresponsible for soil aeration (Pagliai and De Nobili 1993).Lower MBC and enzyme activities (dehydrogenase, phos-phatase, arysulfatase, and amidase) in compacted mineralsoil have been attributed to changes in soil physicalproperties (e.g., decreased total porosity, water infiltrationrate and aeration porosity) and reduced root growth (Dicket al. 1988). This was supported by Li et al. (2002), whoreported that increased bulk density (from 1.3 to 1.6 gcm3) reduced protease activity, and tended to reduce acidand alkaline phosphatase activities in a sandy loam soil in apot experiment planted to maize (Zea mays L.).

Contrary to the findings above, in a laboratory experi-ment, Buck et al. (2000) found higher acid phosphataseactivity in a compaction treatment, possibly due tofavorable conditions for colonization by the decomposermicroflora on the basis of closer contact between themineral soil and organic mulch material. Acid phosphataseactivity may be more sensitive to soil compaction thanalkaline phosphatase activity in forest soils that aregenerally acidic; for example, Jordan et al. (2003) in agreenhouse study also found that severe soil compaction

(bulk density at 1.8 g cm3) reduced acid phosphataseactivity, but did not affect alkaline phosphatase activity in aloamy soil with soil pH of 5.7. It is well recognized thatacid phosphatase activities prevail over alkaline phospha-tase activities in acid soils, and the opposite is true inalkaline soils (Renella et al. 2006; Eivazi and Tabatabai1977). In our study, reduced microbial biomass, andprotease and phosphatase activities (those involved in Nand P transformations) most likely led to reductions innutrient availabilities in the soil. Reduced trembling aspenand white spruce [Picea glauca (Moench) Voss] growthcaused by soil compaction, as previously reported (Tanet al. 2006) may be directly related to reductions inmicrobial biomass and enzyme activities that may reflectchanges in soil fertility (Nannipieri et al. 2002). Furtherresearch is needed to quantify the relationship betweenenzyme activities associated with nutrient cycling and long-term soil productivity in aspen-dominated boreal forestecosystems.

Forest floor removal reduced microbial biomass, andprotease and phosphatase activities in the mineral soil inthis study. Reductions in enzyme activities and microbialbiomass caused by FFR may have limited the decomposi-tion of organic residues, thereby, reducing available N andP concentrations in the mineral soil (Table 1). Our resultsare consistent with the literature; for example, Hassett andZak (2005) reported 1030% reductions in extracellularenzyme activities caused by intensive aspen harvesting(merchantable bole harvest, whole tree harvest, and wholetree harvest plus forest floor removal) compared with noharvesting, and they attributed those effects to reduced litterinput and changes in soil climate after clear-cut harvest. Inanother similar study, Waldrop et al. (2003) found thatphosphatase, peroxidase, and a-glucosidase activities inforest floor were reduced by postharvest management(slashing, mechanical chipping and piling, and broadcastburning), as a result of changes in water potential and litterquality. In our study, lower microbial biomass and enzymeactivities after FFR were related to reduced soil moisturecontent (Table 5) or nutrient loss (Tan et al. 2005), aschanges in environmental conditions and nutrient availabil-ity may affect soil microbial populations and enzymeactivities. In contrast, Jordan et al. (2003) found thatplacing forest litter (tree leaves) on the mineral soil surfacereduced alkaline phosphatase activity in the mineral soil ina greenhouse study. The mechanism for such an effect wasnot clear. No differences in arylsulfatase and phosphataseactivities between whole tree harvesting and whole treeharvesting plus scarification treatments were found in a jackpine (Pinus banksiana Lamb.) ecosystem (Staddon et al.1998). Forest soil type, regional climate, composition ofmicroorganisms, and specificity of enzymes to catalyzecertain reactions (Nannipieri et al. 2002) make the

Biol Fertil Soils (2008) 44:471479 477

predictions on the response of enzyme activities to FFRdifficult.

Soil enzyme activities may integrate information aboutmicrobial population size and activities and soil physicaland chemical properties and may be used as a usefulindicator of soil fertility (Sinsabaugh et al. 1993; Nannipieriet al. 2002). We found positive correlations between mostsoil enzyme activities and microbial biomass, similar toother studies that have been reported in the literature (Dicket al. 1988; Li et al. 2002; Waldrop et al. 2003; Hassett andZak 2005). It is necessary to note that enzyme activities areassociated with not only soil biotic (the activity associatedwith living cells) but also abiotic components (whichincludes extracellular enzymes) and may not reflect theoverall soil microbial activity (Nannipieri et al. 2002).Enzyme activity per unit microbial biomass may provide abetter understanding of the link between enzyme activityand microbial biomass (Landi et al. 2000). The higher ratiosof dehydrogenase:MBC and protease:MBN after forestfloor removal may indicate the increasing enzyme produc-tion and enzyme release by microorganisms. In otherwords, although forest floor removal reduced microbialbiomass and enzyme activities, enzyme activities as aproportion of microbial population size were not reduced.In this study, reduction in available N was related todecreases in MBN and protease activities after soilcompaction and FFR, suggesting that MBN and proteaseactivities may play important roles in N cycling bygenerating NH4 N, making N available for plant uptake.Similarly, soil available P was positively correlated withMBP and phosphatase activities in this study, indicating asimilar role of MBP and phosphatase in P cycling and thus,P availability. In our study, higher available soil N and Pconcentrations did not depress the protease and phosphataseactivities in soils with forest floor intact, although it is wellestablished that enzymes such as phosphatase are repress-ible enzymes (Nannipieri 1994; Zahir et al. 2001).However, we know that relationships between microbialbiomass, enzyme activities, and soil nutrients are often sitespecific (Nannipieri et al. 2002).

This study suggests that microbial biomass and certainenzyme activities were sensitive to and negatively affectedby soil compaction and FFR in the studied boreal forestsoil. Reductions in microbial biomass and enzyme activitieslikely led to reduced rates of N and P transformations,thereby, decreasing N and P availabilities. Our findingsindicate that if microbial populations and enzyme activitiesdo not recover after stands establish, reductions in N and Pavailability could potentially limit the long-term produc-tivity in boreal forest ecosystems. Our enzyme assaysmeasured the potential enzyme activities under artificialconditions rather than under natural conditions of substratesupply; therefore, caution needs to be exercised when

applying the findings of potential enzyme activities to therealistic in situ conditions in the field.

Acknowledgements We thank the Faculty of Graduate Studies andResearch and the Department of Renewable Resources at theUniversity of Alberta for financial support in the form of a graduatescholarship to the senior author. Natural Sciences and EngineeringResearch Council of Canada (NSERC) and the Canadian Foundationfor Innovation (CFI, through an equipment grant) also providedfunding for this project. The Long-term Soil Productivity Studyexperiment in Dawson Creek Forest District, British Columbia, wasalso supported by funding from the Forest Investment Account and theResearch Branch, British Columbia Ministry of Forests. We thank ananonymous reviewer and the Editor-in-Chief for helpful commentsthat improved an earlier version of the manuscript.

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Soil compaction and forest floor removal reduced microbial biomass and enzyme activities in a boreal aspen forest soilAbstractIntroductionMaterials and methodsStudy site and experimental designSoil samplingPhysical and chemical analysesMicrobial biomass measurementsEnzyme assaysStatistical analysis

ResultsDiscussionReferences

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