Journal of Environmental Quality 31:648-653 (2002)
© 2002 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
TECHNICAL REPORT
Plant and Environment Interactions
Jack Pine Growth and Elemental Composition Are Affected by Saline Tailings Water
Jennifer A. Franklina,
Sylvie Renaultb,
Clare Crosera,
Janusz J. Zwiazek*,a and
Michael MacKinnonc
a Department of Renewable Resources, 4-42 Earth Sciences Building, University of Alberta, Edmonton, AB, T5G 2E1 Canada
b Department of Botany, 505 Buller Building, University of Manitoba, Winnipeg, MB, R3T 2N2 Canada
c Syncrude Canada Ltd., Edmonton Research Centre, 9421-17 Avenue, Edmonton, AB, T6N 1H4 Canada
* Corresponding author (janusz.zwiazek{at}ualberta.ca)
Received for publication February 21, 2001.
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ABSTRACT
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In the processing of oil sands from Alberta's Athabasca formation, large quantities of alkaline, saline tailings and associated process-affected waters are produced. These waters may have a negative effect on plants used in reclamation of mined areas in this region of the northern boreal forest. In the present study, we examined the effects of process-affected water on the growth and elemental composition of jack pine (Pinus banksiana Lamb.) seedlings. Seedlings were grown in sand culture, and treated with tailings water to which mineral nutrients had been added. One-month-old seedlings were treated for 14 d, and all measured growth parameters were reduced. Growth and shoot elemental composition were also measured in seven-month-old seedlings that were treated for 10 wk with process-affected water. Shoots had significantly elevated levels of Na, Cl, S, P, B, and Sr, and significantly reduced levels of Fe, Mo, Ba, and K. The relationships between elemental composition and seedling growth and injury were examined using multiple regression. Growth rates, dry weights, and carotenoid content were reduced, but were not related to shoot elemental composition. Needle necrosis was positively related to tissue Na and Cl. Results indicate that reclamation planning must consider substrate Na and Cl levels when planting jack pine on tailings-affected sites.
Abbreviations: CT water, water contained in, and released from, a consolidated tailings deposit
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INTRODUCTION
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OIL SANDS, a newly emerging energy source, are found throughout the world, with large deposits occurring in the United States, Venezuela, Columbia, and the Peace River, Cold Lake, and Fort McMurray regions of Alberta, Canada. The Athabasca oil sands reserves north of Fort McMurray, Alberta consist of Cretaceous age fluvial, estuarine, and marine sand deposits that are saturated with heavy crude oil (bitumen) and are overlain by shale (Jardine, 1974). These reserves are being developed aggressively, with two commercial mining operations (Syncrude Canada Ltd. and Suncor Energy Inc.) currently in production, and several other companies in preproduction stages. The sands are recovered by surface mining, and bitumen is extracted and upgraded to synthetic crude oil. Large volumes of solid and aqueous tailings remain after the separation of bitumen from the oil sand ore, and this will necessitate the eventual reclamation of land areas in excess of 50000 ha. Much of the handled overburden and produced tailings materials will be more saline than the original soils, with some areas potentially providing challenging substrates in excess of 4 dS m-1 conductivity. Current tailings management practices involve the containment of the tailings within settling basins, as well as a new technology that entails the remixing of the fine and coarse components along with gypsum (CaSO4·2H2O at dosages of 7501200 g Mg-1 tailings) as a chemical coagulant to produce a nonsegregating material known as consolidated or composite tailings (CT) (Matthews et al., 2000). This mixture is deposited as a slurry from which solids-free water is released. The goal is to produce a deposit that becomes trafficable, and reclaimable, within a shorter period than without this treatment. A large volume of the CT water will remain in this material and is expected to be expressed over a number of years as the deposit settles and dewaters further. These tailings and associated pore waters (CT water) are relatively saline, with Na and Cl being derived primarily from the ore, while most of the SO4 comes from the gypsum treatment (MacKinnon et al., 2000).
Salinity may affect the growth of plants by altering water relations, by direct toxicity of ions, and by altering ionic balance resulting in nutrient deficiency. A reduction in water uptake may lead to a reduction in transpiration and photosynthesis, and therefore a reduction in growth. Nutrient imbalances may occur due to the inhibition or promotion of the uptake of nutritional elements under saline conditions (Alam, 1994), and by the relatively high pH of CT water. Injury to the plant tissues is also thought to occur due to the direct toxicity of ions (Greenway and Munns, 1980). Other components of CT water that may affect plant growth include B, Fl, Al, and Sr (Renault et al., 2001).
Reclamation goals for the sites of current mining operations include the establishment of a stable and self-sustaining landscape with a productive capability at least equivalent to the predisturbed area. The establishment of a productive forest on much of the reclaimed lands will be required. Jack pine is native to the Canadian boreal forest, with a range extending from Nova Scotia to northern British Columbia (Mirov, 1967, p. 188190). This pine is an early successional species commonly found on sandy, nutrient-poor sites, and may therefore be a suitable reclamation species for the oil sands mining areas. In our previous studies, lodgepole pine (Pinus contorta Dougl.) showed a high degree of interspecific variability in response to CT water (Renault et al., 1998). One possible explanation for this difference among individuals is a difference in the uptake or translocation of salt ions or nutrients. Therefore, in the present study, we related seedling injury to the shoot tissue concentration of essential and nonessential elements.
The main objective of this study was to assess the tolerance of jack pine to CT water. This assessment was made on seedlings of two age classes; seven-month-old seedlings of planting age, which would be expected to be exposed to CT water when planted directly on reclamation sites, and younger one-month-old seedlings, which may be affected by CT water shortly after germination in a future self-sustaining forest. The use of three seed sources reduced the possibility of testing an atypical population. The additional objective was to test the hypothesis that anticipated injury and growth reduction in seedlings treated with CT water are related to the shoot tissue concentration of salt ions or nutritional elements. Identification of factors related to injury will allow for more efficient and potentially successful selection of suitable reclamation sites for jack pine placement.
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MATERIALS AND METHODS
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Plant Material
Jack pine seed was collected from two sites approximately 60 km north of Fort McMurray, Alberta (57°05.95' N, 111°38.90' W and 56°56.06' N, 111°31.95' W), and a third site near Smoky Lake, Alberta (54°06.88' N, 112°10.38' W). Seed was germinated in Petri dishes. Seed, with emerged radicles approximately 10 mm long, was planted six days later in foam seedling blocks (Beaver Plastics, Edmonton, AB, Canada: 160 cavities per block, 60-mL volume per cavity) filled with quartzfeldspar sand (porosity of 28%) that had been washed with deionized water to eliminate silt and ions. Seedlings were grown in a controlled-environment chamber. Conditions during treatment and maintenance periods consisted of 70% relative humidity (RH), 24°C daytime temperature and 18°C nighttime temperature, and an 18-h photoperiod. A photosynthetically active radiation (PAR) of 300 to 350 µmol m-2 s-1 was provided by a combination of cool white fluorescent and tungsten lamps. Seedlings were rotated randomly within the growth chamber once per week. Plants were watered daily with a nutrient solution containing 80 mg L-1 N, 60 mg L-1 P, 104 mg L-1 K, 100 mg L-1 Ca, 60 mg L-1 Mg, 79 mg L-1 S, 3 mg L-1 Fe, 0.40 mg L-1 Mn, 0.25 mg L-1 B, 0.14 mg L-1 Zn, 0.50 mg L-1 Cu, and 0.10 mg L-1 Mo, as recommended for local pine seedling production (Wood, 1995). The containers with seedlings were flushed once a week with deionized water to prevent ion accumulation. For seven-month-old test material, budset was promoted at 10 wk of age by reducing relative humidity to 50%, and temperature to 14°C (day) and 10°C (night). At that time, watering was reduced to 2-d intervals, and nutrient solution was altered to contain 35 mg L-1 N, 80 mg L-1 P, and 50 mg L-1 Ca. Six weeks later, the photoperiod was reduced to 10 h to induce dormancy for a period of 4 wk prior to cold storage. Seedlings were stored for 8 wk at 3°C in darkness, and watered every 10 d with deionized water.
Consolidated Tailings Water
In 1995, Syncrude Canada created a test deposit of consolidated tailings at its Mildred Lake site in Fort McMurray, Alberta. Water released from this deposit was collected in an adjacent lined pond, from which the CT water used in this experiment was collected in October 1997. Water pH and conductivity were recorded, and samples were sent to Syncrude Research in Edmonton, Alberta for further analysis. Water samples filtered with 0.45-µm Millipore (Bedford, MA) filters were analyzed for anion composition using a Dionex (Sunnyvale, CA) DI 300 ion chromatograph, and cations and trace metals were quantified using an inductively coupled plasma optical emission spectrometer (ICPOES) (Vista-PRO RL; Varian Analytical Instruments, Victoria, Australia). A Syncrude Canada Ltd. method, based on analysis of methylene chloride extracts of acidified samples (Jivraj et al., 1996), was used to determine naphthenic acid concentrations. The composition of this CT water is shown in Table 1.
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Table 1. Chemical composition of consolidated tailings (CT) release water from the Syncrude's 1995 NST Field Test using gypsum treatment. The unit is mg L-1, unless otherwise specified.
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Treatments
One-month-old seedlings were exposed to CT water in two steps. Seedling blocks were continuously subirrigated by placing them in trays containing deionized water (control) or a mixture of deionized water and CT water (1:1 by volume) to which nutrients had been added as described above. After two days, solutions were changed and the concentration of CT water increased from 50 to 100%. The level of solution in the watering trays was maintained by the daily addition of deionized water, which countered the concentration of salts and other elements by evaporation. After one week of treatment, the sand was flushed with deionized water to prevent surface salt accumulation caused by evaporation, and treatment solutions were replaced. One week later, seedlings were again flushed with distilled water, then watered daily with nutrient solution for the following 30 d. This final one-month period without CT water additions was required to accurately assess mortality, as preliminary studies showed high seedling mortality during this period subsequent to salt treatment.
The effects of CT water on seedlings of planting age were investigated by treating seven-month-old seedlings. These seedlings were dormant at the beginning of the treatment period. Plants were removed from the cold room, and immediately placed in nutrient solutions made in deionized water (control) or 50% CT water, in a controlled environment chamber at 70% relative humidity, 24°C daytime temperature and 18°C nighttime temperature, and an 18-h photoperiod. As in the previous experiment, CT water was increased to a concentration of 100% after two days. Seedlings were subirrigated on a cycle of 24 h, followed by 24 h without irrigation, with treatment solutions for a period of 10 wk. Solutions were replaced weekly following flushing with deionized water, and the level of the solution in the watering trays was maintained by the daily addition of deionized water.
The experimental design for both one-month-old and seven-month-old studies was completely randomized, with the treatment unit of trays containing treatment solution being replicated four times, using 25 seedlings per replicate.
Measurements in One-Month-Old Seedlings
Survival was monitored every second day throughout the 14-d treatment period, and every fourth day for the following one-month recovery period. Five plants per replicate were randomly selected and harvested for growth measurements and ion analysis. Plants were separated into roots and shoots, rinsed three times with deionized water, and weighed. Shoot length was determined, and then tissue was freeze-dried to determine dry weights. Chlorophyll a and b were determined spectrophotometrically in methanol extracts of freeze-dried needles, and calculated using MacKinney equations (Sestak et al., 1971). Shoot and root Na and K concentrations of freeze-dried tissue were determined by atomic absorption spectrophotometry (PerkinElmer 503 [Wellesley, MA]) after digestion with sulfuric acid and hydrogen peroxide at 350°C (Richards, 1993).
Measurements in Seven-Month-Old Seedlings
Terminal bud flushing and survival were monitored every four days throughout the 10-wk treatment period. At the end of this period, all shoots were harvested and washed three times with deionized water. Plants were weighed, stem length was determined, and needles were separated into living (green) and necrotic (brown) portions. The tissue was freeze-dried prior to dry weight measurements and pigment and ion analysis. The percentage of needle necrosis was calculated based on the dry weight ratio of living and necrotic needles. Relative growth rate was determined from measurements taken at the beginning and end of the treatment period. Chlorophyll a and b were determined as described above, and total carotenoid content was measured spectrophotometrically in acetone extracts as described by Davies (1976).
For analyses of tissue mineral elements, 5 plants from the control group and 15 plants from the CT treatment group were randomly selected from within a single seed source (57°05.95' N, 111°38.90' W). The smaller sample size of control plants was found to be sufficient due to a low variance within the control group. Previously separated green needles, brown needles, and stem from each shoot were recombined and homogenized. Mineral element analyses were performed by Envirotest Laboratory (Edmonton, AB, Canada) using an inductively coupled plasma optical emission spectrometer, as described by Renault et al. (1999). Tissue chloride concentrations were determined after extraction with 0.5 M HNO3 for 30 min (Rieger and Litvin, 1998) using an Accumet chloride selective electrode (Fisher Scientific, Edmonton, AB, Canada).
Data Analysis
A general linear model (GLM) was used to test for interaction of seed source with treatment. No such interaction was found, and data from the three seed sources were combined for further analyses. Means of control and CT water treatment groups were compared by t test. A correlation matrix was used to determine the factors most closely related to needle necrosis, shoot dry weight, and chlorophyll a content of seven-month-old seedlings.
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RESULTS
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One-Month-Old Seedlings
Survival of treated plants was greater than 95% over the two-week treatment period and subsequent one-month recovery period. All measured growth parameters and needle chlorophyll a concentration were significantly reduced by CT water treatment (Table 2). The relative reduction of growth was greater in roots (70% of control) than in shoots (80% of control). The reduction in needle chlorophyll b concentration in plants treated with CT water was not significant (Table 2). Tissue Na levels increased in shoots and roots of CT-treated plants by more than seven- and fivefold, respectively, above those of control plants (Table 3).
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Table 2. Means and standard errors (in parentheses) for growth parameters and needle chlorophyll concentration of 30-day-old seedlings treated for 14 d with deionized water (control) or consolidated tailings (CT) water, followed by a 30-d recovery period. N = 100.
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Table 3. Means and standard errors (in parentheses) of tissue Na and K concentration of 30-day-old seedlings treated for 14 d with deionized water (control) or consolidated tailings (CT) water, followed by a 30-d recovery period. N = 12.
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Seven-Month-Old Seedlings
Survival was greater than 95% over the 10-wk treatment period. Needle and stem dry weights and shoot growth rate were significantly reduced by CT water treatment (Table 4). Flushing of the terminal bud was delayed by three days in CT-treated plants, but this delay was not significant and analysis of covariance showed that it was not significantly related to the reduction in shoot weight. Needle necrosis varied greatly among seedlings of the CT treatment group, ranging from 1 to 29% with a mean of approximately 9% of the total needle weight, compared with 2% in control plants. Chlorophyll a and total carotenoid concentrations were significantly reduced by CT treatment; however, chlorophyll b concentration was not affected. Assuming that the necrotic (brown) portion of the needles contained no pigments, pigment concentrations were recalculated using the dry weight ratio of green to brown needles to reflect only the living needle pigment concentration. The significance of chlorophyll a and carotenoid reduction was maintained, indicating that the observed reduction in chlorophyll a and carotenoid content was not simply due to dilution of pigment concentrations by necrotic tissue in the sample.
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Table 4. Means and standard errors (in parentheses) of growth parameters and injury indicators (needle necrosis and pigment concentration) of 28-week-old seedlings treated for 10 wk with deionized water (control) or consolidated tailings (CT) water. N = 16.
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Seedlings treated with CT water had significantly reduced levels of Fe, Mo, K, and Ba in shoot tissue (Table 5). Shoot P, S, B, Cl, Na, and Sr were significantly increased by treatment. Correlation of elemental concentration with needle necrosis showed Na and Cl concentrations to be strongly related to needle necrosis (r2 = 0.65 and r2 = 0.59, respectively) (Fig. 1)
. No relationship was found between shoot elemental concentrations and shoot dry weight or needle pigment concentrations.
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Table 5. Means and standard errors (in parentheses) of elemental shoot tissue concentration of 28-week-old seedlings treated for 10 wk with deionized water. N = 5 (control) or N = 15 (consolidated tailings [CT] water).
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Fig. 1. Regression of needle necrosis with shoot sodium and chloride concentrations, in 28-wk-old jack pine seedlings treated for 10 wk with consolidated tailings (CT) water. Solid squares represent Na concentrations, with a solid line indicating the regression line (y = -14.02 + 0.00336x, r2 = 0.65). Open circles represent Cl concentrations, with a broken line indicating the regression line (y = -15.99 + 0.00391x, r2 = 0.59).
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DISCUSSION
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Although survival of jack pine seedlings treated with CT water was relatively high, both one-month-old and seven-month-old seedlings exhibited growth reduction and visible signs of injury. Under saline conditions, shoot growth is often found to be more affected than root growth, which may be due to altered plant hormonal relations (Poljakoff-Mayber and Lerner, 1994). In contrast, in the present study, one-month-old seedlings showed a greater growth reduction of roots than of shoots. Direct root damage could result from a high Na+ to Ca2+ ratio, which is thought to cause displacement of calcium from the plasma membrane (Cramer et al., 1985) and increased membrane permeability (Greenway and Munns, 1980). Root growth may also have been inhibited by factors other than salinity. One potential such factor is Al, which is known to affect root physiology (Cizkova, 1995), and has been found to accumulate in the roots of red-osier dogwood (Cornus stolonifera Michx.) treated with CT water (Renault et al., 2001). The observed reduction in shoot growth rate is a common response to salinity, and may result, in part, from osmotic stress that leads to a reduction in transpiration that subsequently limits photosynthesis. Growth reduction under saline conditions has also been attributed to a reduction in cell size due to decreased cell wall extensibility (Naqvi, 1994).
While reduced growth rates and dry weights are consistent with salinity stress, our results suggest that this growth reduction does not result from insufficient nutrient availability. Nutrient status is a concern due to the alkalinity of CT water, which reduces the solubility of N, P, Mn, Fe, and Mo. Although Fe, K, and Mo concentrations were significantly reduced in CT treated plants, no relationship was found with plant dry weight. Altered ratios of K+ to Na+ may affect growth, and this ratio is higher in more salt-tolerant provenances of cluster pine (Pinus pinaster Aiton) (Saur et al., 1995). However, no relationship was found between the growth of pine seedlings and K+ to Na+ ratios in this study. A slight increase in shoot K concentration of one-month-old seedlings occurred, in contrast with the significant decrease in seven-month-old seedlings after CT treatment. This difference could be due to differences in physiology or treatment duration of the two age groups, as different effects predominate in short-term and long-term salt exposure (Greenway and Munns, 1980).
The effect of salinity on tissue Fe content varies widely among species (Grattan and Grieve, 1994), but our previous (unpublished) study showed no effect of NaCl or Na2SO4 on shoot Fe concentration in jack pine. The reduced shoot Fe concentration observed in this study could be the result of the high pH of CT water. Deficiencies in Fe and Mo are known to result in chlorosis (Salisbury and Ross, 1992), and this may have contributed to the observed chlorophyll reduction in treated jack pine, although no direct relationship was found. Similarly, nutrient status may have contributed to the observed reduction in carotenoid content, as total carotenoids have been found to decrease under Fe and K deficiency (Young and Britton, 1990). Tissue nitrogen content was not determined in this study, and could have been limiting, as high levels of Cl can inhibit NO3 uptake (Grattan and Grieve, 1994).
Several elements were present in elevated levels in the shoot tissue of CT-treated seedlings. The most notable increases were in tissue Na and Cl. No relationship was found between needle dry weight and needle Na or Cl concentration, in contrast to the findings of Rogers et al. (1998), who found dry weight to be negatively correlated with shoot Na, Cl, and S concentration in alfalfa (Medicago sativa L.) treated with NaCl and Na2SO4. Although not related to seedling growth, shoot Na and Cl concentrations were strongly associated with needle necrosis. Similar relationships between foliar NaCl and necrosis have been reported in red pine (Pinus resinosa Aiton) (Sucoff et al., 1975) and white pine (Pinus strobus L.) (Hall and Hofstra, 1972). Exposure to NaCl has been found to result in a loss of chlorophyll in many crop species including tomato (Lycopersicon esculentum Mill.) (Khavari-Nejad and Mostofi, 1998) and alfalfa (Khavari-Nejad and Chaparzadeh, 1998). However, chlorosis is not a typical symptom of salt-affected woody plants (Bernstein, 1975), and no relationship was found between needle pigment content of CT-treated seedlings and Na or Cl concentrations. Sodium and Cl ions can cause toxicity at high concentrations in plant tissues, but the mechanism of this toxicity is not fully understood. Martin and Koebner (1995) reported that Cl may be more toxic than Na, but that the effects of Na and Cl together were greater than the effects attributable to either ion alone in salt-treated wheat (Triticum aestivum L.). Sodium concentrations of CT-treated jack pine roots were nearly twice those in shoots of treated one-month-old seedlings, indicating that jack pine possesses some mechanism to restrict Na translocation. The ability to limit Na accumulation by restricting uptake or translocation has also been reported for Monterey pine (Pinus radiata D. Don) (Myers et al., 1998).
We found significantly increased tissue S levels in the shoots of treated plants, reflecting the high SO4 level present in CT water. Known effects of SO4 include a disruption of N metabolism, and the promotion of toxic sulfoxide formation in leaves and roots of plants (Strogonov, 1973). An inhibition of cell division by sulfoxides may be a factor in the reduced growth of treated jack pine seedlings. In our study, CT-treated plants also contained elevated levels of P. Salinity has been found to alter plant P status, with increases in tissue P observed for salt-treated Canary Island pine (Pinus canariensis C. Sm.) (Tausz et al., 1998) and soybean [Glycine max (L.) Merr.] (Grattan and Maas, 1988), and a decrease found in leaves of bean (Phaseolus vulgaris L.) (Carbonell-Barrachina et al., 1997).
Shoot tissue in CT-treated plants was also found to contain elevated levels of B and Sr. Shoot B in the control seedlings was well within the range of 11 to 32 mg kg-1 reported for pine species (Stone, 1990), while CT-treated seedlings had tissue B above the levels reported to result in tip necrosis in red pine and Scotch pine (Pinus sylvestris L.). On sites with high soil B and salinity levels, pecan [Carya illinoinensis (Wangenh.) K. Koch] showed a reduction in yield and a disruption of N and P translocation (Picchioni et al., 2000). Although elevated levels of B were found in the shoot tissue, these were not directly related to growth reduction or injury in jack pine. An accumulation of Sr in pea (Pisum sativum L.) has been found to result in growth reduction (Burstrom, 1983). Although Sr concentrations of CT-treated plants were significantly higher than controls, no correlation was found between tissue strontium and growth or injury. Small increases in tissue Sr, such as those found here, may have little effect on plant growth or injury due to possible compartmentalization within the shoot tissue, which has been demonstrated in European larch (Larix decidua Mill.) (Gierth et al., 1998). The somewhat-elevated Fl in CT water may also have contributed to seedling injury and growth reduction. Sodium fluoride has been found to inhibit the growth of jack pine at concentrations as low as 1 mmol L-1 (Zwiazek and Shay, 1988), but tissue fluoride was not determined in this study.
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SUMMARY
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The alteration in nutrient status of plants treated with CT water appears to be related both to high pH and salinity. The observed reduction of shoot concentrations of several essential nutrients could potentially affect plant growth in the long term. Nutrient deficiency was not found to be directly related to plant growth or injury, and the factors responsible for growth reduction of CT-treated plants could not be identified in this study. The greatest concern is that of ion toxicity. The high sodium and chloride levels in CT water were associated with needle necrosis, and salinity must, therefore, be considered in the development of reclamation plans for CT-affected areas. The loss of carotenoids is a potential problem, as one function of carotenoids is to protect the chloroplast from oxidative damage (Young and Britton, 1990). Resulting damage to the photosynthetic apparatus and the observed loss of chlorophyll a may reduce long-term growth. Future research with jack pine should examine the interactions of CT water chemistry with the physical properties of CT, and investigate the potential of mycorrhizae to alleviate toxicity due to CT water chemistry.
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ACKNOWLEDGMENTS
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This study was funded by the Environmental Science and Technology Alliance Canada, Natural Sciences and Engineering Research Council of Canada, Suncor Energy, Inc., and Scynrude Canada Ltd. We would like to thank S. Tuttle and D. Sheeran (Suncor Energy Inc.) and M. Fung (Syncrude Canada Ltd.) for their valuable advice. The authors would also like to thank M. Chomokovsky, E. Redfield, and M. Molina for technical assistance.
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S. Renault, M. MacKinnon, and C. Qualizza
Barley, a Potential Species for Initial Reclamation of Saline Composite Tailings of Oil Sands
J. Environ. Qual.,
November 1, 2003;
32(6):
2245 - 2253.
[Abstract]
[Full Text]
[PDF]
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