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Published online 31 August 2007
Published in J Environ Qual 36:1470-1478 (2007)
DOI: 10.2134/jeq2006.0530
© 2007 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
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TECHNICAL REPORTS

Nitrogen Mineralization and Microbial Activity in Oil Sands Reclaimed Boreal Forest Soils

R. McMillan, S. A. Quideau*, M. D. MacKenzie and O. Biryukova

Dep. of Renewable Resources, Univ. of Alberta, Edmonton, AB Canada T6G 2E3

* Corresponding author (sylvie.quideau{at}ualberta.ca).

Received for publication December 9, 2006.

   ABSTRACT
TOP
 NOTES
 ABSTRACT
INTRODUCTION
 Materials and Methods
 Results
 Discussion
 Conclusion
 REFERENCES
 
Organic materials including a peat-mineral mix (PM), a forest floor-mineral mix (L/S), and a combination of the two (L/PM) were used to cap mineral soil materials at surface mine reclamation sites in the Athabasca oil sands region of northeastern Alberta, Canada. The objective of this study was to test whether LFH provided an advantage over peat by stimulating microbial activity and providing more available nitrogen for plant growth. Net nitrification, ammonification, and N mineralization rates were estimated from field incubations using buried bags. In situ gross nitrification and ammonification rates were determined using the 15N isotope pool dilution technique, and microbial biomass C (MBC) and N (MBN) were measured by the chloroform fumigation-extraction method. All reclaimed sites had lower MBC and MBN, and lower net ammonification and net mineralization rates than a natural forest site (NLFH) used as a control, but the reclamation treatment using LFH material by itself had higher gross and net nitrification rates. A positive correlation between in situ moisture content, dissolved organic N, MBC, and MBN was observed, which led us to conduct a moisture manipulation experiment in the laboratory. With the exception of the MBN for the L/S treatment, none of the reclamation treatments ever reached the levels of the natural site during this experiment. However, materials from reclamation treatments that incorporated LFH showed higher respiration rates, MBC, and MBN than the PM treatment, indicating that the addition of LFH as an organic amendment may stimulate microbial activity as compared to the use of peat alone.

Abbreviations: RNI, relative nitrification index • MBC, microbial biomass carbon • MBN, microbial biomass nitrogen • DOC, dissolved organic carbon • DON, dissolved organic nitrogen • TDN, total dissolved nitrogen • L/S, forest floor-mineral mix over secondary • L/PM, forest floor-mineral mix over peat-mineral mix • PM, peat-mineral mix • NLFH, natural (undisturbed) forest floor layer


   INTRODUCTION
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
Materials and Methods
 Results
 Discussion
 Conclusion
 REFERENCES
 
THE Athabasca oil sands, located near Fort McMurray in northeastern Alberta, Canada, is the largest single oil deposit in the world, with an estimated reserve of one trillion barrels bitumen (AEP, 1998; Alberta Government, 2005). Current bitumen extraction is focused on shallow oil sands deposits where surface mining is feasible. Surface mining disturbs whole ecosystems for long periods of time by removing aboveground biomass and the geologic substrate, which is stockpiled for later use. Currently, the impacted area is approximately 150 km2, but it is predicted that by the year 2023, the disturbance may be as much as 10 times the area currently affected (AEP, 1998; Alberta Government, 2005). The magnitude of this industrial practice raises concerns about our ability to reconstruct ecosystem function and productivity at such large scales.

Two important parameters of ecosystem function and productivity are microbial community dynamics and nitrogen (N) cycling, as they relate to above and below ground productivity and carbon (C) sequestration. There is currently a lack of information on how these parameters will be affected by the disturbance and reclamation practices of oil sands surface mining. Practices such as stockpiling soil before reclamation, combining topsoil and subsoil, and reclaiming large areas with heavy equipment have been shown to alter soil properties such as bulk density, organic matter content, and microbial biomass (Grigal, 2000; Mummey et al., 2002). Nitrogen fluxes may also be affected by reclamation practices, but to date mine reclamation studies are generally limited to coal mining, which uses different materials and equipment than oil sands mine reclamation (Coyne et al., 1998; Frouz and Novakova, 2005).

Following oil sands mining, land reclamation entails the re-establishment of functioning ecosystems through the creation of soil-like profiles using salvaged mineral soil materials, tailings sand, and surface organic materials. A peat-mineral mix is typically used as a surface treatment, due to high peat availability in large portions of the mining footprint (Fung and Macyk, 2000). More recently, salvage operations have used forest floor (LFH) stripped from pre-mining areas as an alternate source of organic matter for soil reclamation. In addition to LFH acting as an excellent source of seeds and propagules for native plant species (Granström, 1981; Qi and Scarratt, 1998), mineralization of the large organic matter pools in the forest floor provides a source of energy and nutrients for microbial activity (Fyles and McGill, 1986; Van Cleve et al., 1993). The chemical, physical, and biological properties of peat-mineral mixes have been characterized by Li et al. (2003) and Lanoue (2003), but there are no studies to date that have investigated combinations of LFH amendments with peat-mineral mixes, or LFH by itself. The main objectives of this study, therefore, were to compare the properties of soils reclaimed with LFH to those reclaimed with the traditional peat-mineral mix, a combination of the two, and an undisturbed forest ecosystem. More specifically, we were interested in testing whether the use of LFH during reclamation provided a benefit when compared to peat in terms of microbial activity and nitrogen mineralization.


   Materials and Methods
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and Methods
Results
 Discussion
 Conclusion
 REFERENCES
 
Site Characteristics and History
The study area, located 40 km north of Fort McMurray, northeastern AB (56°39' N, 111°13' W), is characterized by a continental boreal climate where winters are typically long and cold, with short and cool summers. Mean daily temperatures range from –18.8°C in January to 16.8°C in July (Environment Canada, 2002). Annual precipitation is 455 mm, which falls predominantly as rain (342 mm) during the summer months. Vegetation of the Fort McMurray area, which lies within the Boreal forest region, includes white spruce (Picea glauca (Moench) Voss), black spruce (Picea mariana (Mill.) BSP), trembling aspen (Populus tremuloides Michx.), balsam poplar (Populus balsamifera L.), white birch (Betula papyfrifera Marsh.), and jack pine (Pinus banksiana Lamb.) as the main tree species (Fung and Macyk, 2000). The majority of soils have developed on glacial and post-glacial deposits. Gray Luvisols are associated with till and lacustrine deposits, while Dystric Brunisols developed in coarser parent material such as glaciofluvial outwash and eolian sands (Turchenek and Lindsay, 1982; Lanoue, 2003).

Syncrude Canada Ltd., one of the major oil sand operators in the Athabasca region, is the largest producer of crude oil, from oil sands, in the world (Syncrude Canada Ltd., 2001). In areas where the oil sand deposit is less than 45 m below the surface, Syncrude uses surface mining to access the oil-impregnated sands (Fung and Macyk, 2000). Surface soils and near surface geological materials (to a depth of 3 m) are salvaged before mining, and placed as a soil cover on the newly reconstructed landforms during site reclamation. Salvaged mineral substrates include Pleistocene deposits with relatively high clay content (called secondary materials when used for reclamation), as well as Cretaceous overburden, a non-sodic/non-saline material salvaged from directly above the oil sands (Lanoue, 2003). Tailings sand, the material remaining after the oil has been extracted, also makes up a substantial proportion of the reclaimed soil profile on reclaimed landforms (Fung and Macyk, 2000).

Reclamation Treatments
Reclaimed sites included in this study were established from August 1998 to January 1999 on tailings sand slopes located at the Syncrude Canada Ltd. Mildred Lake Mine site. Organic materials used for site reclamation included mesic peat extracted from a nearby peatland, and forest floor material salvaged from an upland aspen-dominated forest that had been harvested in 1996, as part of conventional pre-mining activities. Mineral soil (25 to 50% by volume) was incorporated into the reclamation materials, as the organic layers are typically over-stripped during salvage operations, hence creating a peat-mineral mix and a forest floor-mineral mix. No attempt was made to remove vegetative propagules, roots, or seeds present in the reclamation materials.

Three different reclamation treatments were implemented to cap the tailings sands present at the sites: (i) forest floor-mineral mix (18 cm) over 23 cm of secondary material (L/S), (ii) forest floor-mineral mix (11 cm) over peat-mineral mix (18 cm) over 23 cm of secondary material (L/PM), and (iii) peat-mineral mix (15 cm) over 35 cm of secondary material (PM). It should be noted that reported thicknesses constitute average values, and that a large degree of variability exists given that these treatments were established at an operational scale. Materials for reclamation were hauled using large, 777 and 789 Caterpillar trucks, and D5 dozers were used to spread the materials into 50 x 50 m blocks. In 1999, the peat-mineral mix treatment (PM) received a one-time 500 kg/ha application of 10-30-15-4 (N-P-K-S) fertilizer, and was planted to barley. The two LFH treatments (L/S and L/PM) did not receive any fertilizer and were left to revegetate naturally. Vegetation was well established at all reclaimed sites at the time this study was initiated, and was dominated by herbaceous species including common yarrow (Achillea millefolium L.), fireweed (Epilobium augustifolium L.), graceful cinquefoil (Potentilla gracilis Dougl. Ex Hook var. gracilis), peavine sp. (Lathyrus sp.), sweet clover sp. (Melilotus sp.), and wild strawberry (Fragaria virginiana Mill.). Total plant cover as measured in summer 2003 ranged from 170 to 220% of ground surface (Clara Qualizza, Syncrude Canada Ltd., personal communication, 2006). Finally, an undisturbed upland aspen dominated forest 4 km south of the site, adjacent to where the forest floor material had been extracted, was included as an undisturbed control site (NLFH) for comparison to the reclaimed treatments. The soil at the natural site was classified as an Orthic Gray Luvisol, with an average forest floor depth of 5.1 cm (Soil Classification Working Group, 1998).

Experimental Design
At each treatment, including the control (NLFH) site, three 10 x 10 m plots were established randomly, and sample collection was completed on the following three dates: 1 June 2003, 1 July 2003, and 1 May 2004. At four different randomly selected locations per plot, and for each date, a pair of aluminum cores (7 cm diameter, 7 cm long) was driven into the ground with a 2-cm distance between cores. The soil from one core was taken to the laboratory for initial analysis while the soil from the other core was placed in a polyethylene bag and buried just below the soil surface at the L/PM site for a 30-d field incubation (Eno, 1960). In June 2004, gross ammonification and nitrification rates were measured using the isotope pool dilution method (Hart et al., 1994). At four different randomly selected locations per plot, two pairs of soil cores were sampled within a 2-cm distance, and one pair was injected with 6 mL of 30 mg/L 15NH4Cl. The other pair was injected with 6 mL of 30 mg/L K15NO3. The soil from one core of each pair was taken to the laboratory for initial analysis, while the soil from the other core was buried in situ for 48 h. Four samples per plot were also collected in July 2003 for determining bulk density using an aluminum core (7 cm diameter, 4 cm long).

Laboratory Analysis
All samples were sieved to 4 mm before analysis, except for bulk density and moisture measurements, where samples were directly dried for 48 h at 70°C and then weighed. Soil pH was measured with a glass electrode in a 1:4 soil/0.01 mol/L CaCl2 solution (Kalra and Maynard, 1991). Soil texture was determined using the hydrometer method with a pre-treatment of 30% H2O2 to remove organic matter (Kalra and Maynard, 1991).

Soil total C and N concentrations were measured by dry combustion using a CNS elemental analyzer (NA 1500, Carlo-Erba, Italy) on air-dried samples that were homogenized with a ball grinder to pass a 100-µm mesh. Ammonium and nitrate were extracted from field fresh soil samples using a 0.5 mol/L K2SO4 solution (1:10 soil/solution) as described by Mulvaney (1993). Ammonium and nitrate concentrations in the extracts were determined using a Technicon Auto Analyzer II (Technicon Industrial Systems, Tarrytown, New York). For each pair of cores mentioned in the experimental design, net ammonification rate (mg N kg–1 mo–1) was calculated to be the concentration of ammonium in the field-incubated soil minus the concentration in the initial sample. Net nitrification rate (mg N kg–1 mo–1) was determined the same way based on nitrate concentrations, and net mineralization rate (mg N kg–1 mo–1) was calculated as the difference between the sum of ammonium and nitrate concentrations before and after incubation. The relative nitrification index (RNI) was further computed as the net nitrification/net mineralization ratio (Lapointe et al., 2005).

Isotope Pool Dilution for N Mineralization
To estimate gross ammonification and nitrification rates, the 15N enrichment in ammonium and nitrate was compared between the field-incubated and the initial soil sample, i.e.; across each pair of cores mentioned in the experimental design. Specifically, ammonium and nitrate were extracted from 15N-labeled soil samples using 75 mL of a 2 mol/L KCl solution, and concentrations analyzed on a Technicon Auto Analyzer II (Technicon Industrial Systems, Tarrytown, New York). The extracts were prepared for isotopic analysis using the diffusion method of Brooks et al. (1989). Briefly, 40 mL of the filtrates from the 15NH4 labeled soils were placed in 120 mL capped sample vials, to which 0.2 g of MgO was added, and an acidified filter disk was suspended from the lid to trap the 15NH3 evolved. Disks were encapsulated for analysis and the atom percentage 15N enrichment was measured using an isotope ratio mass spectrometer (V.G. Isogas LTD, Aston Way, Middlewich Cheshire, CW10 OHT, United Kingdom) with a direct combustion preparation system (Carlo Erba NA 1500 Strumentazione, Strada Rivoltana, 20090 Rodano Milan, Italy). The 15N enrichment in nitrate was determined in a similar fashion, however after the initial addition of 0.2 g of MgO, subsamples were left open to the air for 6 d to allow NH3 to volatilize. After this initial incubation, 0.6 g of Devarda's alloy was added to the samples to reduce NO3– to NH3, acidified filter disks were added, the lids closed, and the samples were allowed to incubate for six additional days. Again, disks were encapsulated and analyzed for 15N by the method described above.

Microbial Biomass by Fumigation-Extraction
Microbial biomass C and N were determined by the chloroform fumigation-extraction method (Jenkinson et al., 1982). Two field-fresh soil samples were weighed to 10 g (dry weight equivalent), one was extracted directly using 0.5 mol/L K2SO4 and the other was fumigated with chloroform for 24 h and then extracted (Horwath and Paul, 1994). Dissolved organic carbon (DOC) was analyzed on these samples using a soluble carbon analyzer (Astro 2001 II, Texas, USA). Dissolved organic N (DON) was determined using the persulfate oxidation method (Cabrera and Beare, 1993) where the organic nitrogen and NH4+ in a sample are oxidized to NO3– and compared to an initial, non-oxidized sample. Inorganic N (NO3– + NH4+) concentrations were measured using a Technicon Auto Analyzer II (Technicon Industrial systems, Tarrytown, New York). Microbial biomass C (MBC) and N (MBN) were further calculated using MBC = DOCfumigated – DOCunfumigated and MBN = DONfumigated – DONunfumigated (Jenkinson et al., 1982).

Moisture Manipulation Experiment
In August 2004, six soil cores (0–7 cm) were randomly sampled at each of the three experimental plots established at each site, thoroughly homogenized into one composite sample per plot, and sieved to 4 mm. Composite samples obtained from the reclaimed sites were then divided into a control sample, where the original moisture content was not changed, as well as into three additional samples where moisture contents were adjusted to 30, 45, and 60% by weight. Sixty percent was chosen as the highest moisture content as it was the average moisture content of the natural forest site at the time of sampling, while the reclamation treatments had an average moisture content of 20%. Composite samples obtained from the undisturbed natural forest site (NLFH) were not manipulated but instead incubated at their original moisture content as control samples. All of these samples were further split into two laboratory replicates as to allow measurement of soil microbial C and N in addition to respiration rates. Each laboratory replicate consisted of twenty grams of soil placed in a 1 L Mason jar with a septum on top and was incubated at 20°C. Respiration rates (mg C g–1 d–1) were estimated from weekly measurements of CO2 concentrations (mg C g–1) from headspace sampling using a gas chromatograph (5890 series II Hewlett-Packard, Wilmington, Delaware). To avoid development of an anoxic environment, the Mason lids were removed for aeration for 2 h after CO2 concentration measurements were taken. At the same time, soils were weighed to ensure that the correct moisture content was maintained and water was added as needed. Wetting soil typically yields a short-term increase in respiration and mineralization rates (Fierer and Schimel, 2002). Measurements of respiration rates indicated that samples had stabilized after 2 wk of incubation, at which time one set of laboratory replicates was extracted for microbial C and N determination (McMillan, 2005). Respiration measurements continued for an additional 4 wk, and respiration rates (mg C g–1 d–1) as reported in this paper are average values from week 3 to week 6 of the laboratory incubation.

Statistical Analysis
Because treatments were not replicated at the landscape scale, each experimental plot may be considered a pseudo-replicate of that treatment. However, given that the reclamation treatments are operational in size, and furthermore that the three replicate plots are located at distances that exceed the spatial dependence of many soil variables including nitrogen availability (Gross et al., 1995), we chose to consider each plot as a true replicate of reclamation treatments found in the Fort McMurray area. Measurements from each plot within a site were averaged to calculate bulk density, total C and N, DOC and DON concentrations, gross and net N mineralization, ammonification and nitrification rates, MBC and MBN, pH, and moisture content. One-way analysis of variance (ANOVA) was used to determine if significant differences existed among treatments (n = 3). Interactions between sampling date and treatments were examined by a two-way ANOVA and are indicated when present. All data conformed to the assumptions of normality, including non-autocorrelation, constant variance and error independence, or were transformed to do so. We chose a conservative multiple comparison test (Tukey LSD) to examine differences among treatments, and only accepted p-values with {alpha} ≤ 0.05. Correlation analysis was used to indicate the strength of the relationship between field measurements listed above. All tests were performed using SAS version 8.01 (SAS Institute, 1999.


   Results
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
Discussion
 Conclusion
 REFERENCES
 
Soil and Vegetation Characteristics
The reclaimed treatments had a significantly (p ≤ 0.05) higher bulk density, pH, lower total C, lower total N and a higher C/N ratio than the natural forest site (Table 1). There were only a few significant differences in physical and chemical properties among reclaimed treatments, including a lower pH and higher total C and total N in the peat-mineral mix as compared to the LFH treatments. All reclaimed sites had a silty loam texture in the top 7 cm of soil, and had an average temperature for May 2004 that was approximately 5°C higher than in the natural forest. The reclaimed materials also exhibited significantly lower DOC and DON compared to the natural forest. The reclaimed sites had significantly lower moisture contents than the natural forest site for each sampling month, but there was no significant difference among treatments in any month (Table 2).


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  		Table 1. Selected properties for the topsoil layer (0–7 cm) at the natural (NFLH) and reclaimed sites (L/S: forest floor-mineral mix over secondary; L/PM: forest floor-mineral mix over peat-mineral mix; PM: peat-mineral mix). Sampling time was June 2003 except for soil temperature, which was measured in May 2004.

 

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  		Table 2. Moisture content for the topsoil layer (0–7 cm) at the natural (NFLH) and reclaimed sites (L/S: forest floor-mineral mix over secondary; L/PM: forest floor-mineral mix over peat-mineral mix; PM: peat-mineral mix).

 
Microbial Biomass C and N
Reclamation treatments had a significant effect on MBC and MBN, which were always significantly lower when compared to the NLFH site (Table 3). There were also significant differences in MBN among the types of reclamation treatment applied, with the PM treatment having significantly lower values than both LFH treatments. Although differences were not statistically significant, microbial C/N ratios differed among reclamation treatments, with the PM treatment exhibiting a higher ratio than both LFH treatments and the NLFH site. When MBC and MBN were compared among treatments as a proportion of total soil C and N contents, there were no significant differences for MBC, although the PM treatment showed the lowest value (Table 3). Microbial biomass N as a proportion of total soil N again was lowest for the PM treatment and significantly different from the L/S treatment. The L/PM treatment and the natural site (NLFH) showed intermediate values that were not significantly different from either the L/S and PM treatments.


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  		Table 3. Microbial biomass C and N for the topsoil layer (0–7 cm) as determined in June 2003 at the natural (NFLH) and reclaimed sites (L/S: forest floor-mineral mix over secondary; L/PM: forest floor-mineral mix over peat-mineral mix; PM: peat-mineral mix).

 
A positive correlation was observed between moisture content, MBC (p < 0.001, r = 0.69), and MBN (p < 0.001, r = 0.53). A correlation was also found between DON, MBC (p = < 0.001, r = 0.63) and MBN (p = < 0.001, r = 0.56). However, MBC and MBN did not correlate with any other property measured (DOC, extractable ammonium and nitrate, temperature, and pH).

Nitrogen Fluxes
Reclamation treatments did not affect gross ammonification rates as compared to the NLFH site, and there were no differences among reclamation treatments (Fig. 1a ). However, gross nitrification rates were significantly higher (p = 0.008) for the L/S treatment as compared to the NLFH (Fig. 1b), but again, there were no significant differences among the reclamation treatments.


Figure 1
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  		Fig. 1. Gross nitrogen (N) ammonification (a) and nitrification (b) rates (mg N kg–1 d–1) as determined in June 2004 for oil sand reclamation treatments (L/S: forest floor-mineral mix over secondary; L/PM: forest floor-mineral mix over peat-mineral mix; PM: peat-mineral mix) compared to forest floor (NLFH) from an undisturbed natural forest site. Errors bars represent one standard error from the means (n = 3), and different letters signify significant differences among materials at {alpha} = 0.05.

 
Reclamation treatments showed a significant effect on net ammonification, nitrification, and mineralization rates when compared to the natural site, but only in the first sampling period of June 2003 (Fig. 2 ). The natural forest site (NLFH) exhibited the highest net ammonification rate in June 2003, while the reclamation treatments did not differ among each other, and there were no significant differences among treatments during the other two incubation months (Fig. 2a). Net nitrification rates showed the opposite response when compared to net ammonification rates, with the highest net nitrification rate occurring in June 2003 on the L/S reclamation treatment (Fig. 2b), which was significantly higher than the natural NLFH site. Again, there were no significant differences among treatments during the other 2 mo (July 2003 and May 2004). A correlation between moisture content and net ammonification was found for each month (June 2003 p = 0.0008, r = 0.83; July 2003 p = 0.0194, r = 0.66; May 2004 p = 0.0077, r = 0.72), but there was no correlation detected between moisture content (Table 2) and net nitrification rates in any month (McMillan, 2005).


Figure 2
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  		Fig. 2. Net nitrogen (N) ammonification (a), nitrification (b) and mineralization (c) rates (mg N kg–1 mo–1) for oil sand reclamation treatments (L/S: forest floor-mineral mix over secondary; L/PM: forest floor-mineral mix over peat-mineral mix; PM: peat-mineral mix) compared to forest floor (NLFH) from an undisturbed natural forest site. Errors bars represent one standard error from the means (n = 3), and different letters signify significant differences among materials at {alpha} = 0.05.

 
Net N mineralization rates exhibited significant differences among treatments in June 2003 (Fig. 2c), that reflected observed differences for net ammonification and nitrification rates (Fig. 2a, 2b). The natural site (NLFH), with a significantly higher net ammonification rate, also showed the highest net N mineralization rate. The L/S site, with a significantly higher net nitrification rate, had the second highest value, although this was not significantly different from any of the other sites (Fig. 2c). The relative nitrification index (RNI), which is an indicator of the prevalence of nitrification over ammonification during mineralization processes, further showed significant differences among reclamation treatments as well as between the reclamation treatments and the NLFH site (Fig. 3 ). In June 2003, the L/PM treatment had the statistically highest RNI while the L/S and PM treatments had the next highest, and the NLFH had the lowest. The trend was slightly different in May 2004, where all reclamation treatments showed a statistically higher RNI compared to the NLFH site. In all cases, it is interesting to note that the natural site exhibited the lowest RNI at all dates, which is indicative of the high net ammonification, but considerably lower net nitrification rate at this site.


Figure 3
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  		Fig. 3. Relative nitrification index (RNI) for oil sand reclamation treatments (L/S: forest floor-mineral mix over secondary; L/PM: forest floor-mineral mix over peat-mineral mix; PM: peat-mineral mix) compared to forest floor (NLFH) from an undisturbed natural forest site. Errors bars represent one standard error from the means (n = 3), and different letters signify significant differences among materials at {alpha} = 0.05.

 
Moisture Manipulation
Cumulative respiration rates remained statistically higher in the natural forest (NLFH) than in the reclamation treatments at all moisture contents; however, the difference between the NLFH site and the reclamation treatments decreased with increasing moisture (Fig. 4a ). A regression analysis indicated that respiration rates significantly increased with increasing moisture content (p < 0.0001 for all reclamation treatments). Within the reclamation treatments, the L/S material had the highest respiration rate at all moisture content levels, and was significantly higher than the respiration rate found in the PM material over the entire moisture gradient. The L/PM material also showed higher respiration than the PM material, although differences were not statistically significant at the higher (45 and 60%) moisture contents.


Figure 4
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  		Fig. 4. (a) Respiration rate (mg C g–1 d–1), (b) microbial biomass C (mg C kg–1), and (c) microbial biomass N (mg N kg–1) for a moisture manipulation experiment performed with oil sand reclamation treatments (L/S: forest floor-mineral mix over secondary; L/PM: forest floor-mineral mix over peat-mineral mix; PM: peat-mineral mix) compared to un-manipulated forest floor (NLFH) from an undisturbed natural forest site. Errors bars represent one standard error from the means (n = 3), and different letters signify significant differences among materials at {alpha} = 0.05.

 
Microbial biomass C and MBN values exhibited differences among treatments similar to those observed during the respiration rate measurements, and decreased in the following order: NLFH > L/S > L/PM > PM (Fig. 4b, 4c). In particular, MBC values were significantly higher for L/S than P/M at all moisture contents (Fig. 4b), while MBN became significantly higher for L/S than PM when the moisture content was increased to 45 and 60% (Fig. 4c). The L/PM samples showed an intermediate response between the L/S and PM treatments in all cases (Fig. 4b, 4c). However, it is interesting to note that MBC and MBN responded differently to the increase in moisture content. While MBC did not increase with increasing moisture content, MBN showed a positive correlation to moisture in all reclamation treatments (p < 0.05).


   Discussion
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
Conclusion
 REFERENCES
 
Soil Characteristics at the Reclaimed Sites
The differences found between reclaimed and natural sites for soil properties including bulk density, pH, total C, and total N have been reported in other studies (Schwenke et al., 1999; Stolt et al., 2001) and result from the extraction and stockpiling of soil materials and their re-placement on the landscape as a form of land reclamation treatment. Bulk density is often higher on reclaimed sites, as shown here (Table 1), due to surface compaction caused by the use of large equipment during reclamation (Bradshaw, 1983; Grigal, 2000). The salvaged mineral materials of the Athabasca oil sand region are typically associated with a high pH (Fung and Macyk, 2000), and mixing this alkaline material with surface organic material during over-stripping and finally, re-placement at reclamation sites may produce a more alkaline reclaimed material compared to the natural forest floor. Higher pH of reclaimed material has been observed in other mine reclamation studies (Mummey et al., 2002). In our study, while pH values were statistically higher for the reclaimed sites when compared to the natural site (Table 1), actual differences were small (≤0.5) and all values remained below 6. Finally, higher soil moisture content and lower soil temperature at the natural site may be attributed to the forest canopy cover, which insulates the soil, slowing evaporation and providing shade that decreases soil temperature.

Microbial Dynamics in Disturbed Soils
Soil microbial biomass typically decreases following disturbance (Visser et al., 1983; Breland and Hansen, 1996). Mummey et al. (2002) found that MBC was still 56% lower in reclaimed surface mined sites than in adjacent undisturbed soils, 20 yr after land reclamation. They cite soil stockpiling as being extremely detrimental to fungi, in particular mycorrhizal fungi, and state that reclaimed soils may not be able to provide any inoculant for regenerating plants. This is potentially a large problem in the boreal forest, where most tree species rely on mycorrhizal associations to secure nutrients from the system of extremely tight nutrient cycling that develops (Jonsson et al., 1999). In our study, lower MBC and MBN at the reclaimed sites compared to the natural forest site may be the result of lower moisture content and/or differences in organic matter composition (Tables 1–3GoGo). Composition of the organic matter present at the reclaimed sites further results from the combined influence of: (i) the original composition of the organic amendments applied at the sites, (ii) potential changes in composition of these amendments by decomposition processes that occurred during the 4 yr between placement and the time this study was initiated, and (iii) addition of fresh organic substrates from the vegetation currently growing at the reclaimed sites, including aboveground and root litter as well as root exudates. While our study does not allow us to differentiate among the specific processes mentioned above, it is interesting to note that both LFH treatments had higher MBN than the reclamation treatment relying on peat only (Table 3). Hence, it may be hypothesized that the use of forest floor material may have acted as a better inoculant for microorganisms, including mycorrhizae, than peat, although this hypothesis remains to be tested.

In our study, in situ MBC and MBN were positively correlated to moisture content and DON concentrations. Other field studies have reported a positive relationship between these factors (Bohlen et al., 2001; Chen et al., 2003; Hannam and Prescott, 2003); however, it has been difficult to tease apart the causal mechanisms of the differences. For example, Hannam and Prescott (2003) used a buried bag incubation to examine changes in microbial N, soluble organic N, and soluble inorganic N, but found no simple relationship to explain why changes in one N pool were not reflected by opposite changes in the other pools. We chose to perform a moisture manipulation experiment under controlled laboratory conditions to test for the influence of moisture on microbial dynamics, including respiration rates, MBC, and MBN (Fig. 4). The general trend was for an increase in respiration rates and MBN with increasing moisture content, while MBC stayed relatively constant. In other words, the MBC/MBN ratios decreased while the metabolic quotients qCO2 (respiration/MBC ratios) increased with increasing moisture. These results may indicate a shift from fungal-dominated microbial activity to a greater proportion of bacterial activity with increasing moisture, since bacteria typically have lower MBC/MBN and are less efficient at utilizing carbon substrates, hence have proportionally higher respiration rates than fungi (Sylvia et al., 2005).

With the exception of the MBN for the L/S treatment, none of the reclamation treatments ever reached the levels of the natural site during our moisture manipulation experiment (Fig. 4). These results indicate that lower microbial activity in the reclaimed treatments as compared to the natural site was not solely limited by moisture, but also by differences in composition of the organic matter substrate. More specifically, the L/S treatment showed significantly higher respiration rates, MBC, and MBN than the PM treatment when moisture was increased to 45% or above, indicating that this treatment had the most active microbial community after the natural site. Furthermore, field measurements indicated that both LFH treatments had a significantly higher MBN than the peat-mineral mix alone, even though the reclaimed LFH sites had significantly less total C and N (Tables 1 and 3). Taken together, our results show that the addition of LFH as an organic amendment stimulated microbial activity as compared to the use of peat alone. This is essentially the opposite of what happens when fresh forest floor is removed by harvesting, where removal results in decreased microbial N (Hannam and Prescott, 2003).

Nitrogen Fluxes at the Reclaimed Sites
The net N mineralization rates found in this study were within the range reported during May to July field incubations in other boreal forest soils, which ranged from 5.3 to 25 mg N m–2 d–1 (Carmosini et al., 2003). A positive correlation between moisture content and net N mineralization rates has been reported in the literature (Kowalenko and Cameron, 1976; Carmosini et al., 2003; Zaman and Chang, 2004), with optimum net N mineralization rates recorded at 10 to 35% moisture content by weight (Stanford and Epstein, 1974). Our results agree with the literature in terms of the relationship between moisture and net ammonification, but not for net nitrification as shown by correlation analysis.

By using the isotope pool dilution technique with 15N, it is possible to get an idea of how the different reclamation treatments affect gross inorganic N release rates before microbial immobilization has occurred (Davidson et al., 1992). It appears that the reclamation practices established in this study did not affect gross ammonification rates as compared to the undisturbed forest site (Fig. 1), indicating that the heterotrophic microbial communities had the same potential to mineralize organic N at each site. This is contrary to what might be expected given that the natural site had significantly more DON, total N, MBC, and MBN than the reclaimed sites (Tables 1 and 3). It may be that the concentration of recalcitrant organic N (e.g., heterocyclic N) was higher at the natural site, or that DOC, which was also significantly higher for this site, contained compounds that inhibited microbial growth (Wardle et al., 1998).

Net ammonification was significantly higher at the natural site as compared to the reclaimed sites (Fig. 2a). As gross ammonification rates were not different among sites (Fig. 1), this result indicates either a more strongly immobilizing environment or faster nitrification at the reclaimed sites. Annual net nitrification rates in mature mixed-wood boreal forests are generally low (Walley et al., 1996) and comparable to the results found in our study. Measured gross as well as net nitrification rates were lower at the natural site than at the reclaimed treatments, showing that these lower net nitrification rates in the natural forest came from lower nitrate production, rather than from higher microbial immobilization. The importance of net nitrification at the reclaimed sites was further evidenced by higher RNI values than those found at the natural site, in particular for the two reclamation treatments that used LFH as an organic amendment (Fig. 3). Low nitrification rates in boreal soils have been linked to low pH (Ste-Marie and Paré, 1999), anaerobic conditions, low substrate (ammonium) availability, low nitrifying bacterial populations (Davidson et al., 1992), and chemical inhibition (Wardle et al., 1998). In our study, it seems that there was sufficient substrate for nitrification. However, the pH was lower on the natural site compared to the reclaimed sites (Table 1), which may partially account for the lower nitrification occurring in the natural forest. The activity of both ammonium oxidizing bacteria (AOB) and nitrite oxidizing bacteria (NOB) is suppressed when pH is below 5.5 (Hunik et al., 1992), resulting in inhibition of nitrification (Painter, 1986). Without any direct evidence for chemical inhibition, we are not able to comment further on this form of microbial suppression, but recommend that it be examined in future studies.


   Conclusion
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 Conclusion
REFERENCES
 
Reclamation treatments that used organic amendments in the form of LFH material had higher microbial activity compared to the reclamation treatment that used peat material alone. However, in many cases the reclamation treatments were significantly different from the natural LFH site, indicating that the goal of re-establishing natural ecosystem functionality is not complete. This goal may only be realized after some period of time has allowed natural processes to become re-established, such as the development of soil structure and the establishment of biocycling feedbacks between soil and the re-growing vegetation. In the meantime, more research is needed to examine how management practices can help develop landscapes that require a minimum of time to rehabilitate, including a better understanding of microbial communities and mycorrhizal fungi in reclaimed soils in relation to the re-establishment of vegetation, and specific quantification of the influence of re-growing vegetation on microbial activity, as well as of its contribution to organic matter composition at the reclaimed sites through aboveground litter and root turnover. Finally, in view of the relatively high nitrification rates observed at the reclaimed sites, nitrate leaching losses should be measured to test whether these represent a significant N loss from these soils.


   ACKNOWLEDGMENTS
 
The authors wish to thank the many individuals who contributed time and effort into making this work possible, including Steve Clark, Cherie Frantik, Jeff MacLean, Jennifer Lloyd, and Greg Slemp. A special thanks is extended to Jennifer Pichach and Clara Qualizza. This work was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC)-Collaborative Research and Development (CRD) grant to SAQ and industrial partnerships with Syncrude Canada Ltd., Suncor Energy Inc., and Albian Sands Energy Inc.; a NSERC Industrial Postgraduate Scholarship (IPS) to RM sponsored by Syncrude Canada Ltd.; and Northern Scientific Training Program (NSTP) and Circumpolar/Boreal Alberta Research (C/BAR) grants to RM.


   NOTES
TOP
 NOTES
ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 Conclusion
 REFERENCES
 
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   REFERENCES
TOP
 NOTES
 ABSTRACT
 INTRODUCTION
 Materials and Methods
 Results
 Discussion
 Conclusion
 REFERENCES
 




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