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Published online 5 July 2005
Published in J Environ Qual 34:1319-1327 (2005)
DOI: 10.2134/jeq2005.0436
© 2005 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

Plant and Environment Interactions

White Spruce Response to Co-Composted Hydrocarbon-Contaminated Drilling Waste

Effects of Compost Age and Nitrogen Fertilization

Woo-Jung Choia, Scott X. Changb,* and Xiying Haoc

a Department of Biosystems & Agricultural Engineering and Institute of Agricultural Science & Technology, Chonnam National University, Gwangju 500-757, Korea
b Department of Renewable Resources, 442 Earth Sciences Building, University of Alberta, Edmonton, AB, Canada T6G 2E3
c Agriculture and Agri-Food Canada, Lethbridge Research Centre, P.O. Box 3000, Lethbridge, AB, Canada T1J 4B1

* Corresponding author (scott.chang{at}ualberta.ca)

Received for publication November 15, 2004.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
There are growing interests to use co-composted drilling wastes contaminated with hydrocarbons as growth media for planting in land reclamation. However, such use of the compost may have potential problems such as inherent toxicity of residual hydrocarbon and microbial N immobilization due to high compost C to N ratios. We investigated the growth, biomass production, N uptake, and foliar {delta}13C of white spruce (Picea glauca [Moench] Voss) seedlings in a pot experiment using 1-, 2-, 3-, and 4-yr-old composts (with different hydrocarbon concentrations and C to N ratios) and a local noncontaminated soil with (200 kg N ha–1) or without N fertilization. Growth and N content of seedlings (particularly N content in roots) were lower when grown in the compost media as compared with those grown in the soil. Within the compost treatments seedling growth was affected by compost age, but the magnitude of growth reduction was not linearly proportional to hydrocarbon concentrations. Plant N uptake increased with compost age, which corresponds with an increase in indigenous mineral N concentration. Effects of N fertilization on N uptake were curtailed by the presence of indigenous mineral N (e.g., in the 4-yr-old compost) and by fertilization-induced stimulation of microbial activities (e.g., in the 1-yr-old compost). The differences in foliar {delta}13C values between seedlings grown in compost and soil (P < 0.05) suggest that limitations on water uptake caused by the residual hydrocarbon might have been the predominant factor limiting seedling growth in the compost media. This study suggests that water stress caused by residual hydrocarbons may be a critical factor for the successful use of co-composted drilling wastes as a growth medium.

Abbreviations: Ci/Ca, the ratio of intercellular to ambient CO2 partial pressure • HC, hydrocarbon • NDFF, nitrogen derived from fertilizer • TPH, total petroleum hydrocarbon • WHC, water holding capacity • {Delta}, carbon isotope discrimination • {delta}13C, carbon isotope abundance


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
ONE OF THE MAJOR ENVIRONMENTAL CONCERNS in the oil and gas industry is the disposal of hydrocarbon (HC)-contaminated wastes generated by drilling activities. Drilling wastes are very heterogeneous mixtures of water, drilling mud, borehole cuttings, and various additives including diesel oil added as lubricants during the drilling process (Monenco Consultants Ltd., 1990). Composting has been extensively tested to treat the wastes and is now being accepted as an alternative to incineration, landfarming, and landfilling, because of its low cost, high treatment efficiency, and environmental soundness over other methods (Monenco Consultants Ltd., 1990; Semple et al., 2001). Through the composting process, hydrocarbon contents are reduced to minimize the negative effects of hydrocarbons on phytotoxicity and environmental pollution, in addition to altering soil physical and chemical properties (Graham, 2005).

In composting of oil-contaminated wastes, organic amendments such as livestock manure (Kirchmann and Ewnetu, 1998), sewage sludge (Namkoong et al., 2002), wood chips (Jørgensen et al., 2000), or a mixture of vegetable, garden waste, and paper (Gestel et al., 2003) are often added with inorganic nutrients to provide carbon substrate, nutrients, and aeration (Chang and Weaver, 1998; Semple et al., 2001). The removal efficiency of HC during composting ranges from 70 to 90%, depending on the HC type and treatment process (Song et al., 1990; Kirchmann and Ewnetu, 1998; Jørgensen et al., 2000). Composting does not completely remove HC and the residual fraction is likely recalcitrant (Heusemann, 1997). Further biodegradation of the aged residual HC fraction in the compost can be achieved by land application. Plant roots may expose sequestered HC fraction to microbial decomposition by breaking up coarse fragments and root exudates stimulate microbial activity (Cunningham et al., 1996; Davis et al., 2002). Through land application, the compost can be used as a soil amendment for remediation purposes, such as reclamation of disturbed well sites, because of the high organic carbon and nutrient contents in the compost (Semple et al., 2001). However, in the land application stage, two major concerns are raised: (i) residual HC can inhibit plant growth (Baker, 1970; Xu and Johnson, 1997; Adam and Duncan, 1999); and (ii) composts with high C to N ratios can reduce nutrient availability due to competition by microorganisms for available N (Amadi et al., 1993; Xu and Johnson, 1997; Chaîneau et al., 2000). However, because composting of HC-contaminated materials is still an emerging technology, few have examined plant growth response to HC-contaminated compost treatments.

The relative abundances of 13C to 12C (expressed as {delta}13C) in plant tissues can serve to measure the effects of HC-contaminated compost on plant growth because carbon isotope discrimination caused by a faster diffusion and reaction rate of 12CO2 than 13CO2 during photosynthesis is affected by environmental conditions such as water and nutrient status (O'Leary, 1981). The carbon isotope discrimination ({Delta}) against 13C of C3 plants is described as follows (Farquhar et al., 1989):

[1]
where Ci/Ca is the ratio of intercellular to atmospheric CO2 concentrations; and a and b are discriminations against 13C during CO2 diffusion through stomata (normally approximately 4.4{per thousand}) and during CO2 fixation (normally approximately 27{per thousand}), respectively. Although discrimination during CO2 dissolution, diffusion in the liquid phase, and (photo-) respiration may also affect {Delta}, this simple equation is widely used to represent the relationship between {Delta} and Ci/Ca. Increases in {Delta} result in more negative {delta}13C values and vice versa. Several studies observed decreases in {Delta} in pine species under poor-watered conditions and increases in {Delta} under N-deficient conditions relative to the control because of their respective effects on CO2 diffusion rates and carboxylation efficiencies, which control the Ci/Ca ratio (Korol et al., 1999; Livingston et al., 1999; Warren et al., 2001).

We hypothesized that (i) plant growth response might vary depending on compost age or residual HC concentration; (ii) the adverse impact of organic amendments with high C to N ratios on growth may be ameliorated by adding inorganic N fertilizer; and (iii) growth conditions in the HC-contaminated media might result in more positive or negative foliar {delta}13C values than those grown in a noncontaminated soil. To test the hypotheses, we investigated the growth, N uptake, and foliar {delta}13C of white spruce seedlings grown in differently aged composts containing HC-contaminated drilling waste with or without the addition of an inorganic N fertilizer and in a noncontaminated forest soil. We used a 15N-labeled N fertilizer to trace the fate of the applied N in the growth media–plant systems. White spruce is widely distributed in the boreal region and has been extensively used in land reclamation in the boreal (Watson et al., 1980).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Co-Composted Drilling Waste
Co-composted drilling waste (or compost) with different composting age (1, 2, 3, and 4 yr; codes are 1Y, 2Y, 3Y, and 4Y, respectively) used in this study was provided by Newpark Environmental Services, Calgary, AB, Canada. The compost samples were collected in August 2003 from the Wildcat Hills area (51°13' N, 114°39' W) about 100 km northwest of Calgary. The compost was made through the following process. To construct composting piles, gas drilling waste contaminated with lubricating oil (mainly diesel oil) was mixed with wood chips at a 1:3 ratio (volume/volume of the drilling waste to wood chips). Wood chips were obtained from local forest industries or from wood harvested at the well site. A fertilizer blend was amended to balance C to N to P ratio to 500:10:1. The constructed piles were monitored for HC concentration, temperature, chemical (C to N ratio, available N and P contents, pH, electrical conductivity), and physical (bulk density and moisture content) properties every four months (Newpark Environmental Services, 2003). All the analyses were performed using standard methods documented in Carter (1993). If necessary, the piles were turned, and water and nutrients were applied during the turning to maintain the C to N to P ratio and compost temperature to about 40°C (Danielson, 1998). The compost samples collected for this greenhouse study were homogenized with a cement mixer.

Soil
To compare seedling growth and the fate of applied N in the compost-based growth media with those in a noncontaminated field soil, a surface (0–20 cm) soil sample was collected in July 2003 from a recently clearcut site near Whitecourt (54°8' N, 115°47' W), Alberta. The soil is a Luvisolic Brunisol (Soil Classification Working Group, 1998). The soil sample was sieved through a 4-mm screen.

Pot Experiment
A pot experiment planted with white spruce seedlings was conducted in a controlled environmental chamber in the Department of Biological Sciences, University of Alberta. White spruce is a native tree species and widely used in reclamation in Alberta. The compost was mixed with washed sand in a 3:1 v/v ratio (which is the equivalent of 1.2 kg of compost and 1.0 kg of sand on oven-dry basis for each pot) to improve aeration. For the soil, 2.5 kg of soil was mixed with 1.0 kg of sand to achieve a 3:1 v/v ratio.

For each pot, the growth medium was hand-mixed with 0.79 g of Ca(H2PO4)2 (equivalent to 50 kg P ha–1 and 33 kg Ca ha–1) and 0.79 g of K2SO4 (equivalent to 100 kg K ha–1 and 41 kg S ha–1). The mixtures were placed into pots (15-cm bottom diameter x 20-cm top diameter x 16-cm height, volume is approximately 3873 cm3) to 13 cm in height (volume is around 3310 cm3), resulting in a bulk density of 0.66 Mg m–3 for compost and 1.06 Mg m–3 for soil.

The bottom of the pots was lined with nylon nets to minimize loss of growth media from the pots. Aluminum pans were placed under each pot, and the leachates collected were rinsed back to the pots. The pots were laid out in a completely randomized design. For the compost-based growth media, a total of 32 pots (with four replications) were set up for eight treatment combinations that include four different ages (1Y, 2Y, 3Y, and 4Y) of compost without N addition (treatment codes are 1YN0, 2YN0, 3YN0, and 4YN0, respectively) or with N addition (1YN1, 2YN1, 3YN1, and 4YN1, respectively). For the soil medium, only four pots (N addition treatment with four replications) were prepared, because comparison between with and without N addition in the soil media was not an objective of this study.

The white spruce seedlings (containerized stock type 412A, produced from plugs with 4-cm diameter and 12-cm depth) were provided by the PRT Nursery in Beaverlodge, Alberta, with the seedlings produced from a seedlot (ww 54-24-5-79) collected from the Hinton area in Alberta. One seedling was transplanted into each pot on 21 Oct. 2003. The water contents of the pots were maintained at 65% water holding capacity (WHC) during the experiment by adding tap water. The initial pot weight was recorded, and tap water was added as necessary to restore their initial weights every other day. Twenty days after the planting of the seedlings (10 Nov. 2003), a 50-mL solution containing 2.96 g of (NH4)2SO4 labeled with 15N (5.0 15N atom %) was applied to each pot (equivalent to 200 kg N ha–1) of N addition treatments. To minimize N loss through ammonia volatilization, the top 3 cm of the growth media was taken out before the application of the solution, and was placed back after addition of the solution. The seedlings were grown in a growth chamber under artificial lighting (300 E s–1 m–2). Daylight was maintained at 18 h, and temperature was set at 24°C (day) and 15°C (night). Throughout the experiment, pot locations were periodically rotated to minimize edge effects.

Seedling Growth Measurements and Sampling
Seedling shoot height and root-collar diameter were measured on 20 October immediately after the seedlings were planted and at harvest on 23 Feb. 2004. Seedling diameter was measured in two directions perpendicular to each other at the ground level using a caliper and then averaged. Seedling height was measured using a meter stick. On 20 October, the diameter and height of the seedlings ranged from 1.8 to 3.8 mm and from 18.0 to 29.0 cm, respectively. Although the initial size of the individual seedling was quite variable, the mean height (20.5 ± 2.1 to 25.1 ± 3.7 cm) and diameter (2.4 ± 0.6 to 3.1 ± 0.5 mm) at a treatment level (n = 4) were not significantly different among treatments. Growth increment was calculated as the difference between the final and initial seedling sizes.

Eighteen weeks after planting, seedlings were cut at the ground level and separated into leaf and stem plus branch components. The growth medium containing roots in each pot was placed in a plastic tub, and all visible roots were collected after crushing the medium. The above- and belowground components were washed with distilled water, dried at 60°C, and weighed to determine dry weight. After harvest, the growth medium was mixed thoroughly, and a subsample was collected and used for analyses.

To estimate the initial dry weight and nitrogen content of the seedlings planted, we developed a correlation equation between seedling size (height x diameter2) and dry weight or nitrogen content of each tree component (leaf, stem plus branch, and root) using data from 10 randomly selected seedlings (from the same batch as those used in the pot experiment). The R2 values of the correlation between seedling size and dry weight or nitrogen content were 0.42 and 0.39 for leaf (P < 0.05 for both), 0.92 and 0.88 for stem plus branch (P < 0.001 for both), 0.57 and 0.56 for root (P < 0.01 for both), and 0.66 and 0.58 for whole components (P < 0.01 for both), respectively. The initial dry weight and nitrogen content of the whole components of the planted seedlings calculated using the equation ranged from 2.1 to 5.4 g plant–1 (1.0 to 2.1 for foliage, 0.5 to 1.6 for stem plus branch, and 0.6 to 1.7 g plant–1 for root) and from 50.1 to 121.7 mg N plant–1 (8.1 to 24.8 for foliage, 12.2 to 37.1 for stem plus branch, and 50.1 to 121.7 mg N plant–1 for root), respectively. At a treatment level, the average estimated whole dry weight and nitrogen content ranged from 3.0 ± 0.4 to 4.0 ± 0.8 g plant–1 and 67.7 ± 34.2 to 91.4 ± 18.5 mg N plant–1, respectively. Increments of dry weight and N content were calculated by subtracting the initial values (at planting) from the final values (at harvest).

Chemical Analyses
Before the initiation of the pot experiment, subsamples of the collected compost were determined for chemical and physical properties as follows: water content by oven drying, WHC with the gravimetric method using a funnel (Fierer and Schimel, 2002), pH (a compost-to-water ratio of 1 to 2.5) using a pH meter, total N and C concentrations using a combustion method on an elemental analyzer (NA 1500; Carlo Erba, Milan, Italy), and mineral N using a steam distillation system (Vapodest 20; C. Gerhardt GmbH & Co. KG, Königswinter, Germany) with 0.5 mol L–1 KCl extract at a 1:3 ratio of compost-to-solution (Keeney and Nelson, 1982). The concentration of petroleum hydrocarbon (carbon number from C11 to C40) was measured with a gas chromatograph (CP-3800; Varian, Palo Alto, CA) after extraction using methylene chloride and hexane following the Alberta Environmental Centre method (Alberta Environmental Centre, 1992), and referred to as total petroleum hydrocarbon (TPH). The physical and chemical properties of the soil were measured using the same method as described above for the compost. Soil texture was determined using the pipette method (Gee and Bauder, 1986).

At the end of the pot experiment, all plant and growth media samples were ground to fine powder in a ball mill (MM 200; Retsch GmbH & Co. KG, Hann, Germany) and analyzed for concentration and 15N atom % excess of total N. Foliage samples were also analyzed for {delta}13C. All C and N analyses were conducted on a continuous-flow stable isotope ratio mass spectrometer (Optima-EA; Micromass, Crewe, UK) linked to a CN analyzer (NA Series 2; CE Instruments, Italy) at Lethbridge Research Centre of Agriculture and Agri-Food Canada. Pure N2 (atom % 15N = 0.3655 ± 0.0001) and CO2 ({delta}13CVPDB = –39.7 ± 0.1{per thousand}) gases served as reference gases for N and C, respectively. A corn (Zea mays L.) stover sample ({delta}13C, –12.5 ± 0.1{per thousand}; 15N atom % excess, 0.0054 ± 0.0001) for plant samples and a soil sample (15N atom % excess, 0.0053 ± 0.001) for growth medium samples, calibrated against international isotope standards (IAEA-N2 and NIST SRM 8542), were used as internal standard materials. The accuracy and reproducibility of the measurements checked with the standard materials were better than 0.2 and 0.1{per thousand} for C isotope and 0.0003 and 0.0002 15N atom % for N isotope compositions, respectively.

Microbial Respiration
To characterize microbial activity of the composts, microbial respiration was determined in a laboratory incubation experiment (Stotzky, 1965). To homogenize the compost material before the incubation, coarse wood chips in the compost samples were crushed to pass a 4-mm sieve and thoroughly mixed. A 100-mL beaker containing 20 g (dry basis) of the fresh sample with or without N addition at the same rate as the pot experiment and a 50-mL beaker containing 20 mL of 0.5 mol L–1 NaOH were placed into a 1-L Mason jar, and sealed with an air-tight screw-top lid. The treatments were replicated three times. The water contents of the samples were adjusted to 65% WHC. The jars were incubated at room temperature in the dark. During 115 d of incubation, the beakers were removed periodically, and 10 mL of 1 mol L–1 BaCl2 was added into the NaOH solution, and the CO2 trapped in the alkali was determined by titration with 1 mol L–1 HCl. After each measurement, the jars were aerated with fresh air, water content of the samples was adjusted by adding distilled water to restore the initial weight, and a new beaker with fresh NaOH solution was placed into the jar.

Calculation and Statistical Analysis
The total amount of nitrogen derived from fertilizer (NDFF) was calculated for each N pool including seedling components and the growth media by the following isotope method (Hauck and Bremner, 1976):

[2]
where T is total N content (N concentration x dry weight) in each N pool, AS is atom % excess 15N of N in each N pool, and AF is atom % excess 15N (4.6337) of N fertilizer applied. The recovery of applied 15N was calculated as a percentage of applied fertilizer N (628.4 mg N pot–1).

Carbon isotope compositions were calculated as follows:

{joenq-1319-eqn3}

where R is the ratio of 13C/12C, and the standards are the Pee Dee Belemnite (PDB) standard.

For statistical analysis, data were tested first for homogeneity of variance and normality of distribution with the descriptive statistics function of the SPSS 11.5 package (SPSS, 2002). Transformation of data was not needed as no heterogeneity was detected in the data set and distribution was normal. Analysis of variance (ANOVA) was performed on all experimental variables using the general linear models (GLM) procedure of SPSS to assess the significance of the effects of compost age, N addition, and their interactions. When significant in the ANOVA, differences in treatment means were explored by Duncan's multiple range test at {alpha} = 0.05. Factorial analysis of N fertilization and compost age was done excluding the soil treatment. The level of significance was set at {alpha} = 0.05. Pearson correlation analysis was performed to examine relationships between parameters (e.g., foliar {delta}13C vs. foliar N concentration) also using the SPSS 11.5 package.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
Properties of the Composts
The properties of the composts at the initiation of the pot experiment are presented in Table 1. Although there were some exceptions, total N concentration increased, but total C concentration, C to N ratio, and TPH concentrations decreased with compost age. The lower mineral N concentrations in the 1Y and 2Y composts than in the 3Y and 4Y composts probably suggest that mineral N in the compost tends to be immobilized by microbial activity in the younger composts that have higher C to N ratios, but in the older composts the immobilized N is likely to be remineralized as available C decreases (Hadas and Portnoy, 1994).


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  		Table 1. Physical and chemical properties of the soil and co-composted drilling wastes with different ages. Values in the parentheses are standard errors of the means (n = 3).

 
In the first 5 d of incubation, the amount of CO2 released from the composts was not different among the treatments and was around 0.9 mg C g–1 (Fig. 1) . Over a period of 115 d, however, microbial respiration was significantly affected by compost age (P < 0.05), decreasing in the order of 3Y > 2Y > 1Y > 4Y composts. An inconsistent pattern of microbial respiration with compost age (Fig. 1) might be due to the combination of adverse (e.g., inherent toxicity; Brohon et al., 2001) and beneficial (e.g., available C source; Dominguez-Rosado and Pichtel, 2004) effects of HC on microbial respiration. Nitrogen addition increased (P < 0.05) the cumulative amount of CO2 in composts 1Y (from 13.4 to 16.1 mg C g–1) and 2Y (from 14.3 to 16.0 mg C g–1), but had no effect on composts 3Y (18.6 to 18.8 mg C g–1) and 4Y (7.7 to 7.6 mg C g–1). Increased microbial respiration caused by N addition in the 1Y and 2Y composts with a relatively low mineral N and high C concentrations is consistent with the general finding that N addition to N-starved and C-enriched soil stimulates microbial activity (Chantigny et al., 1999; Han et al., 2004). On the other hand, lack of response of microbial respiration to N addition for the 3Y and 4Y composts suggests that organic C rather than mineral N is more limiting for microbial activity in these composts compared with the 1Y and 2Y composts (Han et al., 2004).



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  		Fig. 1. Cumulative CO2 production in co-composted drilling wastes in a pot experiment using 1-, 2-, 3-, and 4-yr-old composts. Error bars are standard errors of the means (n = 3). At the end of incubation, cumulative CO2 production was significantly (P < 0.05) affected by compost age and N fertilization.

 
Seedling Growth
Seedlings grown in the composts showed significantly (P < 0.05) lower height (38–84%), diameter (33–67%), and total dry weight (34–55%) increments than those grown in the soil growth media (Table 2). This most likely reflects the adverse impacts of HC remaining in the composts (Tables 1 and 2). Adverse effects of HC compounds on plant growth have been shown for a variety of plant species including trees (Nicoletti and Egli, 1998), grasses (Hutchinson et al., 2003), and crop species (Dominguez-Rosado and Pichtel, 2004), although the susceptibility of plant species to HC varies and is affected by the type of HC contained in the contaminated soil (Baker, 1970). Apparently, totally different properties of the compost media from that of the soil medium (such as pH, C to N ratio, carbon concentration, and other physical properties including aeration) might also contribute to the difference in seedling growth.


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  		Table 2. Increments of height, diameter, and dry weight of seedlings grown for 18 wk in soil or co-composted drilling wastes. Values in the parentheses are standard errors of the means (n = 4). Probability values from the analysis of variance are listed in the bottom half of the table.

 
Within the compost treatments, seedling growth was not affected by N fertilization. Height, foliar biomass, and stem plus branch biomass were significantly (P < 0.05) affected by compost age, but the patterns were not linearly proportional to compost age (e.g., height increment was greatest for the 3Y compost and diameter increment and total dry weight were greatest for the 2Y compost). Meanwhile, seedlings grown in the 1Y compost showed consistently lower growth response than those grown in other composts except for diameter increment (Table 2). This suggests that not only hydrocarbon but also other physicochemical factors (such as nutrient availability, C to N ratio, and microbial activity) also affected seedling growth. In a greenhouse experiment with bean (Phaseolus vulgaris L.), wheat (Tritium aestivum L.), and maize exposed to different contamination levels of fuel oil (from 0 to 12 g kg–1), Chaîneau et al. (1997) also found that the inhibition of plant growth was not linearly related to the contamination level.

Very little data on the effect of HC contamination on root growth is available, because most such studies focused on aboveground rather than belowground parts of plants (White et al., 2003). In an experiment with 39 species native, exotic, or naturalized in western Canada, Robson et al. (2003) found that addition of crude oil at 0.5 to 5 g kg–1 significantly decreased both total plant and root biomass by at least 22% as compared with the control. In our study, compared with other plant components, root dry weight showed the greatest difference between the compost (range: 0.6 to 1.6 g plant–1) and soil (5.7 g plant–1) treatments, resulting in high shoot to root ratios that range from 1.6 for 1YN0 to 8.6 for 3YN0, as compared with 1.1 for the soil treatment. This suggests that impairment of root growth might be the primary cause of growth inhibition in the HC-contaminated growth media. This is consistent with the observation that plant roots tend to avoid the HC-contaminated zone (Adam and Duncan, 1999). It has been also hypothesized that HC reduces plant growth by coating plant roots (Baker, 1970; Xu and Johnson, 1997), and thus reducing plant water and nutrient uptake. Therefore, plants grown in HC-contaminated growth media often exhibit chlorosis or necrosis because of inherent toxicity of HC, water deficiency, and nutrient imbalance (Udo and Fayemi, 1975). Amadi et al. (1993) reported that maize grown in soil contaminated with HC (3% v/w) and treated with sawdust experienced die-back and necrosis of leaves, and Chaîneau et al. (1997) found that bean and wheat grown in soils contaminated with fuel oil (up to 12 g kg–1) showed symptoms of chlorosis. In our study, chlorosis of needles was also observed in the 1Y compost treatment 13 wk after planting, regardless of N fertilization.

Nitrogen Uptake and Nitrogen-15 Recovery
Analysis of variance showed that both compost age and N fertilization significantly (P < 0.05) affected increment of N content except in the root component (Table 3). For example, N content of the whole plant increased with compost age from 24.4 to 121.7 mg N plant–1 without N addition and from 26.9 to 124.7 mg N plant–1 with N addition. Among plant components, root N increment (range: 7.3 to 16.7 mg N plant–1) was much smaller in the compost treatments as compared with that in the soil treatment (104.4 mg N plant–1). Such a tremendous difference resulted in lower total N increments in the compost as compared with that in the soil treatments. This finding is consistent with Xu and Johnson (1997), who reported that shoot and root N concentrations of barley (Hordeum vulgare L.) and field pea (Pisum sativum L.) grown in soils contaminated with HC (55 g TPH kg–1) for 80 d were much lower (up to 10-fold) than those grown in the uncontaminated soil. In our study, the greater N uptake by seedlings in the 3Y and 4Y composts than those in the 1Y and 2Y composts (Table 3) could be primarily attributed to higher mineral N concentration in the older composts (Table 1). On the other hand, when indigenous mineral N is sufficient for plant uptake (such as in the 3Y and 4Y composts), seedling N uptake was lower in the 3Y compost (86.8 mg N plant–1) with higher microbial activities than in the 4Y compost (121.7 mg N plant–1) with lower microbial activities, probably due to microbial competition with plant roots for mineral N (Fig. 1). However, such differences disappeared when external N was added (Table 3). This result suggests that both indigenous mineral N concentration and microbial activities might affect plant N uptake in the HC-contaminated compost media concurrently.


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  		Table 3. Increments of N content of seedlings grown for 18 wk in soil or co-composted drilling wastes. Values in the parentheses are standard errors of the means (n = 4). Probability values from the analysis of variance are listed in the bottom half of the table.

 
Nitrogen fertilization increased N content from 19.7 to 50.5 mg N plant–1 for 2Y and from 86.8 to 126.9 for 3Y composts, but had no effect for 1Y and 4Y composts. For the 1Y compost, microbial immobilization of applied N could be responsible for the lower plant uptake of applied N (Table 4), because N fertilization significantly stimulated microbial activity (Fig. 1). Microbial immobilization of fertilizer N to reduce tree uptake is well established (Choi et al., 2001; Xu and Johnson, 1997; Chang et al., 1997). On the other hand, for the 4Y compost, which has a relatively higher indigenous mineral N concentration (Table 1) and lower microbial activity (Fig. 1) than the others, the indigenous mineral N concentration might be sufficient to meet the N requirement of both plant and microbes, and thus leading to the lack of response to N application (Han et al., 2004). Hence, this result suggests that different N management is necessary between younger and older composts for the better use of the composts as a growth medium.


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  		Table 4. Nitrogen derived from fertilizer (NDFF) in seedlings grown for 18 weeks in soil or co-composted drilling wastes. Values in the parentheses are standard errors of the means (n = 4). Probability values from the analysis of variance are listed in the bottom half of the table.

 
Consistent with the seedling growth and total N uptake data, seedlings grown in the soil absorbed more fertilizer N than those in the compost media (Table 4). The total nitrogen derived from fertilizer (NDFF) in the soil treatment was 130.4 mg N plant–1 and those in the compost treatments ranged between 19.2 and 47.3 mg N plant–1. Compost age significantly (P < 0.05) affected NDFF in the foliage and stem plus branch components, but not in the root or at the whole plant level. Recovery of applied 15N in the soil treatment (20.7% in plant and 55.9% in soil) was significantly (P < 0.05) higher than those in the compost treatments (Fig. 2) . For the compost treatments, recoveries of 15N in plant and compost were significantly (P < 0.05) affected by compost age (but not in a linear fashion), and it ranged from 3.1 (1YN1) to 7.5% (3YN1) in the plant and 34.3 (4YN1) to 52.0% (3YN1) in the growth medium. Consequently, total 15N recoveries were in the order of soil (76.6%) > 3YN1 (59.5%) > 1YN1 (52.2%) > 2YN1 (48.0%) > 4YN1 (41.7%). While statistically insignificant, 15N recovery in the growth media increased linearly with increasing cumulative microbial respiration over 115 d of incubation (R2 = 0.82, P = 0.096), with the highest 15N recovery in the 3Y and the lowest in the 4Y composts. This indicates that microbial immobilization increases the potential of composts to store N, which minimizes N losses through ammonia volatilization and denitrification (Choi et al., 2001).



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  		Fig. 2. Total 15N recovery expressed as a percentage of added 15N in plant, growth media, and those that were unaccounted for. Error bars are standard errors of the means (n = 4). The same lowercase letters in the same N pool indicate statistically nonsignificant differences (P > 0.05). Compost age significantly (P < 0.05) affected 15N recovery in growth media and total recovery but not in plant (P = 0.056). Treatment codes indicate different ages (1, 2, 3, and 4 yr old) of compost without N addition (1YN0, 2YN0, 3YN0, and 4YN0, respectively) or with N addition (1YN1, 2YN1, 3YN1, and 4YN1, respectively), and soil represents the soil-based growth media.

 
Foliar Carbon Isotope Abundance and Seedling Growth
Plant {delta}13C is a time-integrating measure of gas exchange responses to environmental conditions affecting CO2 diffusion and carboxylation efficiency (e.g., O'Leary, 1981; Warren et al., 2001). As such many studies have been conducted to examine plant responses to changing growth conditions using the relationship of {delta}13C with gas exchanges (e.g., Korol et al., 1999; Livingston et al., 1999). However, to our knowledge, this is the first attempt to apply the {delta}13C technique to evaluate plant responses to HC-contaminated soil amendments.

The relationship between plants {delta}13C and carbon isotope discrimination ({Delta}) can described using the following equation (Farquhar et al., 1989):

[4]
where ({delta}a) is {delta}13C of air (normally approximately –8{per thousand}). A more negative {delta}13C indicates an increase of {Delta} and vice versa. In this study, foliar {delta}13C values of seedlings grown in the compost media were less negative (decreased carbon isotope discrimination), ranging from –27.3 to –26.7{per thousand}, than that of seedlings grown in the soil media (–27.9{per thousand}) (Fig. 3) . According to the model of Farquhar et al. (1989)(Eq. [1]), a decrease in {Delta} generally reflects decreased CO2 diffusion or increased carboxylation efficiency, which decreases the Ci/Ca ratio. However, in our study, seedling growth and N uptake significantly decreased in the compost media (Table 2), making increased carboxylation efficiencies unlikely, because increased carboxylation efficiencies tend to increase plant growth. Therefore, we attribute the less negative foliar {delta}13C values to the decreased rate of CO2 diffusion via stomatal and/or mesophyll cells caused by water limitation that resulted from root growth inhibition in the HC-contaminated composts (Korol et al., 1999; Warren et al., 2001). This hypothesis does not preclude the growth limitation by nutrient (particularly N) deficiencies, but suggests that water limitation prevailed over nutrient limitation as compared with seedlings grown in the soil treatment. However, because data on shoot water potentials were not measured, we cannot provide conclusive evidence to explain the {delta}13C pattern in relation to water limitation. Hence, gas exchange and water potential measures (although these measurements are time consuming and labor intensive) may be helpful in interpreting the {delta}13C data toward better delineating of the effects of HC contamination on plant physiology.



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  		Fig. 3. Foliar {delta}13C of seedlings grown for 18 wk in co-composted drilling wastes or in soil growth media. Error bars are standard errors of the means (n = 4). The same lowercase letters indicate statistically nonsignificant differences (P > 0.05). Foliar {delta}13C was significantly affected by compost age and N fertilization (P < 0.01). Treatment codes indicate different ages (1, 2, 3, and 4 yr old) of compost without N addition (1YN0, 2YN0, 3YN0, and 4YN0, respectively) or with N addition (1YN1, 2YN1, 3YN1, and 4YN1, respectively), and soil represents the soil-based growth media.

 
Within the compost treatments, the {delta}13C values were significantly (P < 0.05) affected by compost age and N addition. Overall, foliar {delta}13C values became less negative in the N fertilization treatments. The effect of N addition on foliar {delta}13C was greater in the 3Y (–27.3 to –26.8{per thousand}) and 4Y composts (–27.1 to –26.7{per thousand}) as compared with the 1Y (–27.4 to –27.2{per thousand}) and 2Y composts (–27.5 to –27.3{per thousand}). Foliar {delta}13C values were positively correlated with foliar N concentrations (Fig. 4) , but were neither correlated with biomass production (R2 = 0.030, P = 0.38 for the whole plant and R2 = 0.004, P = 0.74 for the foliage component) nor dry weight (R2 = 0.010, P = 0.59 for the whole plant and R2 = 0.001, P = 0.84 for the foliage component) at harvest. These results suggest that at given water limitations, improved N nutrition further decreased {Delta} (O'Leary, 1981) by increasing carboxylation efficiencies (Livingston et al., 1999). Although increased water demand by enhanced tree growth may also result in the same {delta}13C pattern, it is generally not true for seedlings because of their small size (Munger et al., 2003).



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  		Fig. 4. Correlation between foliar {delta}13C and foliar N concentration of seedlings grown for 18 weeks in co-composted drilling wastes (n = 32).

 

   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
Seedling height and diameter growth, biomass accumulation, and N uptake decreased in the HC-contaminated composts as compared with the noncontaminated soil treatment mainly via impairment of root growth. Height growth and production of foliar and stem plus branch biomass were significantly (P < 0.05) affected by compost age, but not by N fertilization. However, the different growth responses could not be attributed solely to HC concentration since the compost material and soil also differ in several of their physicochemical properties as well. Plant N uptake significantly (P < 0.05) increased with compost age and by N fertilization except in the root component. Differences in plant N uptake among compost treatments were primarily attributable to different indigenous mineral N concentrations, because higher plant uptake of N was associated with higher mineral N concentration in the composts. Plant N uptake response to N fertilization was affected by both the indigenous mineral N concentration and microbial activity in composts. Composts with high microbial activity showed greater retention of applied 15N in the growth media–plant system, suggesting that immobilization decreased N loss. Foliar {delta}13C data suggests that limitation on water uptake caused by impairment of root growth rather than nutrient deficiency affected seedling growth in the compost treatments. Water rather than nutrient management would be more important in the successful use of co-composted drilling wastes as a growth medium; however, whether this conclusion is equally applicable to field conditions needs to be studied.


   ACKNOWLEDGMENTS
 
This work was supported by an Izaak Walton Killam Memorial Postdoctoral Fellowship from the University of Alberta. Financial support for this project was also provided by Petro-Canada. We gratefully acknowledge the assistance of Newpark Environmental Services in collecting co-composted drilling waste samples. Young-Hui Shin assisted in sample preparation. Ms. Pamela Caffyn and Mr. Clarence Gilbertson performed the 15N and 13C analyses. We thank the associate editor and two anonymous reviewers for their helpful comments.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 





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