Published online 20 April 2005
Published in J Environ Qual 34:782-792 (2005)
DOI: 10.2134/jeq2004.0126
© 2005 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
TECHNICAL REPORTS
Ecosystem Restoration
Effect of Water Table on Willows Grown in Amended Mine Tailing
M. M. Bourreta,
J. E. Brummerb,*,
W. C. Leiningera and
D. M. Heilc
a Department of Forest, Rangeland, and Watershed Stewardship, Colorado State University, Fort Collins, CO 80523
b Western Colorado Research Center, P.O. Box 598, Gunnison, CO 81230
c Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO 80523
* Corresponding author (jbrummer{at}lamar.colostate.edu)
Received for publication March 29, 2004.
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ABSTRACT
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Survival and growth characteristics of two montane riparian willow species, Geyer willow (Salix geyeriana Andersson) and mountain willow (Salix monticola Bebb), grown in amended fluvial mine tailing were investigated in a greenhouse study. Willow stem cuttings were planted in lysimeters that simulated a 60-cm amended tailing profile with three static water depths (20, 40, and 60 cm) and a fluctuating water table for a total of four water table treatments. Species and water table treatments affected plant biomass and chemical composition of the soil and plant tissue. Mountain willow leaf, stem, and root biomass were 62, 95, and 164% greater, respectively, than for Geyer willow. Averaging across species, the fluctuating water table negatively affected leaf and stem biomass compared with the 20- and 60-cm water table treatments. Manganese was the only metal in plant tissue to strongly respond to water table treatments. Manganese concentrations in mountain willow leaf tissue were approximately twofold higher in the two most saturated water table treatments (20 cm and fluctuating) than in the least saturated water table treatment (60 cm). This trend was consistent with chemical analyses of the growth media, which reflected higher bioavailable Mn in the saturated tailing profile compared with the unsaturated profile. Results from this study indicate that mountain willow is a more vigorous and possibly more metal-tolerant species than Geyer willow when grown in amended mine tailing and that a fluctuating water table negatively affects willow growth.
Abbreviations: AB–DTPA, ammonium bicarbonate–diethylenetriaminepentaacetic acid • EC, electrical conductivity
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INTRODUCTION
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MINING, SMELTING, and the disposal of sewage sludge have increased the release of heavy metals into the environment (Nriagu and Pacyna, 1988). Heavy metals tend to accumulate in soils and aquatic sediments because they are not readily removed or degraded by chemical processes (Punshon and Dickinson, 1997). Mining activities adversely impact approximately 2000 km of streams and rivers in Colorado and 19000 km in the United States (National Research Council, 1992). The Leadville area in the central Colorado Rockies has been mined for gold, silver, lead, and zinc for more than 100 years. These past activities and several historic flood events have resulted in tailing material containing toxic levels of metals being fluvially deposited in the riparian zone along an 18-km stretch of the upper Arkansas River (Swayze et al., 1996). These tailing deposits are devoid of vegetation (URS Operating Services, 1999; Walton-Day et al., 2000) and toxic material continually erodes into the river, which may adversely impact water quality (Colorado Water Control Division, 1988; Walton-Day et al., 2000).
A fundamental element in the restoration of many riparian areas is the establishment of woody plant species such as willows (Salix spp.) (Volny, 1984). The greatest success in revegetation of tailing material has been achieved when natural pioneer species such as alders (Alnus spp.), birches (Betula spp.), willows, larches (Larix spp.), and pines (Pinus spp.) have been planted (Good et al., 1985). Willows are particularly important in revegetation efforts because they are an extremely hardy genus that opportunistically colonizes disturbed and industrially contaminated soils (Grime et al., 1988; Punshon, 1996), which makes them ideal for restoration of riparian systems impacted by mining. In addition, their vast root system and fast growth help to stabilize stream banks (Gray and Sotir, 1992) and create critical habitat and resources for a number of wildlife species (Sommerville, 1992).
In 1997, a field study was initiated to determine the viability of revegetating fluvial tailing deposits on the Arkansas River near Leadville, Colorado (Fisher, 1999). Results from this study indicated that herbaceous vegetation and Geyer willow can easily establish on these deposits by first amending with lime, organic matter, and phosphorous before seeding and staking (Fisher, 1999). Chemical analyses of the growth media indicated that the lime amendment increased pH of the mine tailing such that trace metals became less bioavailable, which reduced phytotoxic effects. The addition of organic matter to the lime amendment further reduced bioavailability of some metals and proved to be beneficial for herbaceous plant growth (Fisher, 1999). During the third growing season of the study initiated by Fisher (1999), Geyer willow survival averaged 28% in the lime-amended plots and 40% in the lime with organic matter plots (Brummer et al., 2001). However, all surviving Geyer willows exhibited signs of chlorosis and slow leader growth. This is in contrast to a greenhouse study on Geyer willows grown in the same amended fluvial mine tailing that produced significant aboveground current year's growth (Fisher et al., 2000). The amendments that resulted in significant willow growth in the greenhouse did not elicit the same response in the field. This suggested that other environmental factors in the field negatively affected willow establishment and growth.
The objective of this greenhouse study was to determine factors that may be contributing to the chlorosis, slow leader growth, and ultimate survival of willows established in the field. The effect of different ground water levels on Geyer and mountain willow grown in amended fluvial mine tailing was investigated as a possible factor. The natural fluctuation of the water table in the amended tailing could be affecting metal bioavailability and negatively impacting growth of the willows. These willow species were chosen for study because they are the two most prevalent willow species in the 18-km riparian zone of the upper Arkansas River near Leadville, CO, that has been contaminated with fluvial mine tailing deposits.
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MATERIALS AND METHODS
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Study Material Collection
Approximately 750 L of mine tailing was collected in July 2001 from a fluvial deposit on the east bank of the Arkansas River approximately 8 km south of Leadville, CO (39°12' N, 106°21' W). The tailing material was placed in 120-L plastic trash cans and transported to the Mountain Meadow Research Center in Gunnison, CO. It was then homogenized in a cement mixer and a sample was taken for characterization (Table 1). The tailing material was subsequently stored in the plastic trash cans in a cool, dry shed until the study was initiated the next spring.
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Table 1. Physical and chemical properties of fluvially deposited mine tailing collected on the bank of the Arkansas River and composted biosolids from Buena Vista, CO.
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Dormant stem cuttings approximately 90 cm in length and 1.5 cm in diameter were collected in mid-March 2002 at random from native populations of Geyer and mountain willows growing in the vicinity of the tailing collection. The cuttings were made perpendicular to the stem, bundled together in plastic mesh bags, and transported to the Mountain Meadow Research Center where they were placed in cold storage at 2°C for about 45 d.
Experimental Design and Setup
A completely randomized factorial design was used to test the interactive effects that four water table treatments had on growth of two willow species. An individual lysimeter was used as the experimental unit for each water table–willow species combination. Each treatment combination was replicated six times for a total of 48 experimental units.
Lysimeters were constructed from 15-cm-diameter polyvinyl chloride (PVC) pipe that was 83 cm in height and sealed with a PVC cap at the bottom (Fig. 1)
. A single 12.7-mm-diameter hole was drilled in the PVC pipe approximately 18 cm from the bottom of each lysimeter. A PVC nipple with a 12.7-mm-diameter threaded end was then screwed into the hole and sealed with silicon caulking. The nipples had either single or double (T-shaped configuration) 10-mm barb connectors on the other end. Clear flexible plastic tubing (10-mm i.d.) was slipped over the barbed end of the nipples and secured using stainless steel hose clamps. The six lysimeters that made up the same water table–willow species combination (e.g., all mountain willow 20-cm water table treatments) were then connected to each other using the flexible plastic tubing. Once constructed, the lysimeters were held upright by placing them in a wooden rack that measured 3.50 by 1.05 by 0.45 m. The lysimeters were spaced 15 cm apart by cross-hatching the rack every 15 cm with a wooden board that was 15 cm wide.
To regulate the water table depth within lysimeters, eight tanks were constructed that had the same dimensions and were made of the same material as the lysimeters. A 10-mm-diameter by 83-cm-long aluminum rod was attached to the inside of each tank to which a simple livestock float valve ("Little Giant" Trough-O-Matic, Model TM830T; Miller Manufacturing Co., Eagan, MN) was mounted. The float valve could be adjusted up and down to change or fine tune the water table depth within lysimeters. These float tanks were connected to one of the six lysimeters within a given treatment combination using the flexible plastic tubing attached to the barbed PVC nipples. Tap water from the city of Gunnison, CO, was supplied to the float tanks by placing eight 76-L plastic tanks with lids and spigots on a greenhouse bench and connecting the spigot to a barbed connector in the top of the float valve with flexible plastic tubing. Finally, a wooden lid was added to the float tanks to reduce evaporative water losses.
The stored tailing material was amended with lime (CaCO3, less than 200 mesh size; Calco, Salida, CO) and organic matter (composted biosolids characterized in Table 1) at a rate of 0.87 and 1.0 kg, respectively, per 30 kg of tailing. The lime application rate was determined by taking the Shoemaker–McLean–Pratt (SMP) buffer capacity plus the acid–base potential value based on the pyritic sulfur content (calculated as: 31.25 [% pyritic S] = Mg CaCO3 per 907.2 Mg of material) of the tailing (Table 1) and adding an additional 25% to the lime requirement. The organic matter application rate was comparable with that used in the Fisher et al. (2000) study, which was based on literature values (Brown and Trlica, 1996). The amended tailing was homogenized in a cement mixer.
Before filling each lysimeter, a piece of 20-mm-i.d. by 83-cm-long PVC pipe was placed along the inside edge to allow periodic measurement of the water table depth. The bottom of these access pipes was cut at a 45° angle and covered with a piece of landscape fabric that allowed water to flow through, but kept roots and soil out. The top of the access pipe was covered with a rubber plug to prevent evaporative water losses. The lysimeters were then filled by first adding sand to a depth of 20 cm, lightly tapping on the pipe to aid settling, and then topping off the sand layer at 20 cm. Amended tailing was placed on top of the sand layer to a depth of 60 cm using a similar procedure to ensure settling. Both the sand and tailing material were added dry. The sand and tailing combination represented 60 cm of fluvially deposited mine tailing on top of a cobble layer that was characteristic of the field site (Fisher, 1999).
Water table treatments included three static (saturated to 20, 40, or 60 cm below the soil surface) and one fluctuating water table (Fig. 2)
. The 20-cm water table had the highest level of saturation, while the 60-cm water table had the lowest level of saturation. The fluctuating water table treatment simulated the natural hydrograph at the study site where the ground water table rises in the spring as the river level comes up with snowmelt and then falls as the river recedes (Walton-Day et al., 2000). From the time that the water table begins to rise in the spring, water is moving from the river into the riparian zone (i.e., loosing river). As the water table falls, water is moving from the riparian zone to the river (i.e., gaining river). To simulate these natural changes, the lysimeters in the fluctuating treatment were operated as follows: 31 d at 40 cm (May), 46 d at 20 cm (June and first half of July), 31 d at 40 cm (second half of July and first half of August), and 32 d at 60 cm (second half of August and first half of September).
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Fig. 2. Schematic of experimental units illustrating the four water table treatments (20, 40, 60 cm, and fluctuating). The fluctuating water table simulated the natural hydrograph in the field: May (40 cm), June and first half of July (20 cm), second half of July and first half of August (40 cm), and second half of August and first half of September (60 cm).
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Mountain and Geyer willow stakes were randomly selected from the dormant cuttings and two stakes per lysimeter were planted to a depth of 70 cm on 30 Apr. 2002. Lysimeters were arranged randomly in a greenhouse without artificial lighting with an average daytime temperature of 23°C and average nighttime temperature of 6°C. The least vigorous willow cutting in each lysimeter was clipped below the soil surface on Day 53 of the experiment to maintain homogeneity among willows. The remaining stake of both willow species had an average of four leaders on 2 July 2002 (10 d after the other stake was removed) that were 32 and 53 cm in length for Geyer and mountain willow, respectively, when averaged across water table treatments. Since willow cuttings rely on stored nutrients in the early stages of development, it took about 50 d to identify those willows that were not viable or were inherently weak. It should be noted that none of the terminated willow cuttings exhibited any signs of regrowth or residual root mass when harvested.
Data Collection and Chemical Analyses
Survival, shoot length, and shoot number were assessed monthly throughout the experiment. All aboveground growth was harvested and separated into shoots and leaves 20 wk after planting on 17 Sept. 2002. At the time of harvest, both willow species averaged four leaders per stake with an average leader length of 91 and 118 cm for Geyer and mountain willow, respectively, when averaged across water table treatments. Plant samples were placed in labeled paper bags, dried at 60°C for 72 h, weighed, and ground through a 2-mm screen in a Wiley mill. The ground plant material was stored in 120-mL plastic cups that were tightly capped with screw lids until analyzed for metals concentrations 2 to 3 mo later. Metals in the leaf and stem tissue were determined by digesting 1 g of sample in a solution containing 2 mL of perchloric acid and 6 mL of nitric acid at 200°C for 2 h (Miller, 1996). Trace metals were analyzed using inductively coupled plasma–atomic emission spectroscopy (ICP–AES).
Soil cores were extracted by laying the lysimeters on their side, splitting them down their vertical axis on opposite sides using an air hammer with a panel cutting bit (this bit cut the PVC with very little disturbance of the underlying soil), and placing the soil core on 6-mm screens. The cores were divided into four sections (0–20, 20–40, 40–60, and 60–80 cm from the top) and soil samples were taken from the top three portions. The bottom 60- to 80-cm section was not sampled because it did not contain mine tailing (Fig. 2). Soil samples were air-dried, finely ground, sieved through a 2-mm screen, and analyzed for pH, electrical conductivity (EC), and ammonium bicarbonate–diethylenetriaminepentaacetic acid (AB–DTPA)-extractable metals (Soltanpour, 1991) using ICP–AES.
Belowground biomass was determined by washing roots from the four sections free of soil and particulates using a gentle stream of water, clipping the roots from the willow stake (the stake was then discarded), and collecting the roots on 0.5-mm screens. Roots were oven-dried at 60°C for 72 h and weighed.
Statistical Analyses
Statistical analyses were conducted using SAS Version 8.2 software (SAS Institute, 2002). The PROC MIXED analysis of variance (ANOVA) procedure was used to determine statistical differences among water table treatments and species. This model was used for parameters that were measured a single time per lysimeter: leaf and stem tissue metals, and leaf and stem biomass. The PROC MIXED repeated measures procedure was used when parameters required more than one measurement. Repeated measures by depth included root biomass, AB–DTPA-extractable metals, EC, and pH. The least square means method was used to test parameters for significant treatment differences at P 
0.05. Data were tested for homogeneity of variance and normality (Ott, 1993) and some metal and biomass data were log-transformed to meet these assumptions. All means were reported as nontransformed values for ease of interpretation.
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RESULTS
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Soil Chemical Responses
The bioavailability of the heavy metals evaluated in this study depended on the degree of saturation of the amended tailing within a given water table treatment (Table 2). For example, the amended tailing at the 0- to 20-cm soil depth of the 20-cm water table treatment was wetted from capillary rise, but the tailing at the 20- to 40- and 40- to 60-cm soil depths was totally saturated. Averaged across the 20- to 40- and 40- to 60-cm soil depths, this led to a 10.4, 9.5, and 109.5% increase in bioavailability of Cd, Cu, and Pb, respectively, and a 4.6% decrease in Zn when compared with the 0- to 20-cm soil depth. These changes amounted to 1.7, 12.8, 45.0, and 3.4 mg kg–1 for Cd, Cu, Pb, and Zn, respectively. The trend and magnitude of these changes in bioavailability were similar for the other water table treatments when the soil depths with unsaturated tailing were compared with the soil depths with saturated tailing. Additionally, bioavailability of Pb tended to increase in the soil depths that were wetted by capillary rise. The bioavailability of all metals was least affected in the 60-cm water table treatment since none of the amended tailing was saturated at any time.
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Table 2. Ammonium bicarbonate–diethylenetriaminepentaacetic acid (AB–DTPA)-extractable metal concentrations in amended mine tailing as affected by soil depth and one fluctuating and three static water table treatments. The species of willow, Geyer willow or mountain willow, growing in the amended mine tailing did not influence these metal concentrations, so the data were pooled over willow species.
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Trends observed in bioavailability of Mn were similar to those of the other four metals evaluated except that the species of willow grown in the amended tailing had an influence on the concentration of Mn at some of the different soil depths, so the two species are presented separately (Fig. 3)
. Differences in Mn concentration were measured among water table treatments at the 0- to 20-cm soil depth for the lysimeters with Geyer willow, but not for those with mountain willow. The 0- to 20-cm soil depth of the 20-cm water table treatment with Geyer willow had about 50% more bioavailable Mn compared with the 40- and 60-cm water table treatments. The biggest difference between the two species occurred at the 20- to 40-cm soil depth of the 20-cm water table treatment. Manganese was highly responsive to the degree of saturation of the amended tailing, which was further influenced by the species of willow grown in the tailing. For the 20-cm water table treatment, the 20- to 40-cm saturated soil depth for lysimeters with Geyer and mountain willows was 435 (26.1 mg kg–1) and 1097% (35.1 mg kg–1) higher in Mn concentration, respectively, when compared with the respective unsaturated soil depth (0–20 cm).
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Fig. 3. Manganese concentrations at different soil depths in amended mine tailing as affected by water table treatments and species of willow grown in the tailing. Water table treatments within a soil depth with different lowercase letters are significantly different at P 0.05 for a given willow species.
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The amended tailing that was directly above the saturated soil depths and was influenced by capillary rise of the water had higher soil pH than the saturated tailing below (Table 3). The magnitude of this increase in pH was further affected by the species of willow grown in the amended tailing. In the zone directly above the saturated soil depths, the pH was 0.1 to 0.2 units higher in the amended tailing with mountain willow grown in it compared with that with Geyer willow.
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Table 3. Soil pH and electrical conductivity (EC) of amended mine tailing as affected by soil depth and one fluctuating and three static water table treatments. The species of willow growing in the amended mine tailing influenced these soil variables, so the data are presented by willow species.
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Table 4. Electrical conductivity (EC) of amended mine tailing as affected by soil depth or one fluctuating and three static water table treatments. Main effect means are presented for Geyer willow because the water table by soil depth interation was not significant at P 0.05.
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Soil EC was affected by the interaction of the water table treatments, soil depths, and species of willow that were grown in the amended tailing (Table 3). However, the water table treatment by soil depth interaction was not significant for Geyer willow when the species were analyzed separately, so only main effects are presented for this species (Table 4). In the tailing with Geyer willow, the EC in the least saturated water table treatment (60 cm) was about 36% higher than the rest of the water table treatments when averaged over soil depths. Among soil depths, the tailing with Geyer willow at the 0- to 20-cm depth had 42 and 108% higher EC compared with the 20- to 40- and 40- to 60-cm depths, respectively, when averaged over water table treatments. For the tailing with mountain willow, soil EC followed a similar trend as for Geyer willow with levels at the 0- to 20-cm depth ranging from 129 to 686% higher when compared with the 40- to 60-cm depth. The smallest difference (1.8 S m–1) was associated with the least saturated water table treatment (60 cm) while the largest difference (4.8 S m–1) was associated with the most saturated treatment (20 cm). At the 0- to 20-cm soil depth, EC averaged 2.3 S m–1 higher in the amended tailing of the 20-cm water table treatment compared with the other three treatments.
Metal Concentrations in Plant Tissue
In general, Geyer and mountain willows concentrated metals in their leaf tissue preferentially over stem tissue (Table 5, Fig. 4)
. However, Cu concentrations in the leaf tissue of both species did not differ from concentrations in the stem tissue. Out of the potentially phytotoxic metals found in this experiment (Cd, Cu, Mn, Pb, and Zn), Cd was the only metal that had a higher concentration in the leaves of mountain willow compared with Geyer willow, differing by 7.6 mg kg–1. The other metals were either higher in Geyer willow or not different between the two species. Stem concentrations of Cd, Cu, and Zn were 6.4, 2.0, and 46.5 mg kg–1 higher, respectively, in Geyer willow than in mountain willow. Concentrations of Pb in the stems of both willow species were small (average of 1.1 mg kg–1) with no discernable trends among the water table treatments (data not shown).
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Table 5. Concentrations of cadmium (Cd), copper (Cu), lead (Pb), and Zinc (Zn) in leaf and stem tissue of two willow species grown in amended mine tailing.
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Fig. 4. Manganese concentrations in leaf and stem tissue of two willow species grown in amended mine tailing as affected by water table treatments. Water table treatments within a willow species with different lowercase letters are significantly different at P 0.05 for a given tissue type.
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Manganese was the only metal to show a clear response to the various water table treatments and this response differed between the two willow species (Fig. 4). Manganese concentrations in mountain willow leaf tissue averaged more than 200% or 246 mg kg–1 higher in the two most saturated water table treatments (20 cm and flux) compared with the least saturated treatment (60 cm). The concentration of Mn in Geyer willow leaf tissue was higher and varied less with water table treatment compared with mountain willow. Geyer willows grown in the 20-cm water table treatment had 33% or 109 mg kg–1 higher Mn concentrations in their leaves compared with those grown in the 60-cm treatment. Similar trends were measured in concentration of Mn in stem tissues of both willow species, with mountain willow being more responsive to differences among the water table treatments. Manganese concentrations in mountain willow stem tissue averaged 216% or 58 mg kg–1 higher in willows grown in the 20-cm and fluctuating treatments compared with the 60-cm water table treatment.
Total metal concentrations (mg plant–1) were calculated to determine how the water table treatments affected total uptake of each metal by the two willow species (Table 6). Since biomass yields (see below) were greater in mountain willow, this species accumulated more total Cd, Cu, and Zn in both leaves and stems, as well as Pb in the stems, compared with Geyer willow. Zinc was the metal that accumulated to the greatest degree in aboveground tissues of both species, but averaged 4.28 (68.5%) and 2.17 mg plant–1 (56.8%) higher in mountain willow leaves and stems, respectively, compared with Geyer willow. Willows grown with the fluctuating water table typically accumulated fewer total metals than the willows grown in the other water table treatments. A notable exception occurred in the total amount of Mn that accumulated in the leaves of mountain willow (Fig. 5) and stems of both species (Table 6). The leaves of mountain willows grown in the 20-cm and fluctuating water table treatments accumulated 3.13 (135%) and 2.41 mg plant–1 (104%) more Mn, respectively, than the leaves of those grown in the 60-cm treatment. A similar trend in accumulation of Mn occurred in the stems of both species where the 60-cm water table treatment accounted for the lowest uptake (0.98 mg plant–1) of Mn and the 20-cm treatment the highest (2.51 mg plant–1). Similar to the other metals evaluated, Mn accumulation in the leaves of Geyer willow was least in the fluctuating water table treatment.
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Table 6. Total metals in leaf and stem tissue of two willow species grown in amended mine tailing as affected by one fluctuating and three static water table treatments.
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Fig. 5. Total manganese contained in leaves of two willow species grown in amended mine tailing as affected by water table treatments. Water table treatments within a willow species with different lowercase letters are significantly different at P 0.05.
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Growth Responses
Leaf, stem, and root biomass of mountain willow was 62, 95, and 164% greater, respectively, than Geyer willow (Tables 7 and 8). Leaf and stem biomass, averaged across species, was lowest for willows grown in the fluctuating water table compared with all other water table treatments, although the 40-cm water table treatment was not statistically different from any other treatment. Root biomass of both species was concentrated in the depths directly above the saturated zone. For example, willows of both species grown in the 20-cm water table treatment concentrated approximately 86% of their roots in the 0- to 20-cm soil depth (unsaturated portion of the lysimeter).
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Table 7. Root biomass of two willow species grown in amended mine tailing as affected by soil depth and one fluctuating and three static water table treatments. The species of willow growing in the amended mine tailing influenced root biomass, so the data are presented by willow species.
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Table 8. Leaf and stem biomass of two willow species grown in amended mine tailing as affected by one fluctuating and three static water table treatments.
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DISCUSSION
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Soil Chemical Responses
Natural fluctuations of the water table in the field fill soil pore spaces and create anaerobic conditions, causing a decrease in the oxidation–reduction (redox) potential. Changes in soil redox conditions are known to affect Mn solubility in soils (Sposito, 1989). Significant portions of Mn oxides have been shown to dissolve within 3 d following saturation (Xiang and Banin, 1996; Green, 2001). Once Mn oxides are reduced, Mn becomes soluble and remains in solution, which can cause Mn toxicity in plants (Smith, 1990). These findings are consistent with the extractable Mn trends found in the amended mine tailing evaluated in this study. The saturated tailing had up to 12-fold greater concentrations of Mn than the unsaturated tailing (Fig. 3). Concentrations of available Mn in the tailing did not reach levels considered phytotoxic to plants (1500–3000 mg kg–1; Alloway, 1990). However, the Mn levels in the leaf tissue did reach phytotoxic levels (Fig. 4; 300–500 mg kg–1; Alloway, 1990).
Manganese oxides associate with trace metals, including Pb, Zn, Cu, and Ni, through specific surface adsorption, substitution, and coprecipitation (McKenzie, 1989; Sposito, 1989). Coprecipitation and substitution of metals with Mn oxides occur when soils experience alternate wetting and drying cycles (McBride, 1994). Soil reduction releases metals associated with Mn and Fe oxides, which are susceptible to reductive dissolution (Charlatchka and Cambier, 2000; Davranche and Bollinger, 2000). Oxides dissolve and the metals are released into the soil solution and become bioavailable to plants. Therefore, fluctuations in anaerobic conditions found in riparian areas may promote the dissolution of heavy metals bound to Mn and Fe oxides in pyritic mine tailing (Svendsen, 2002). This process explains the trend of higher extractable concentrations of Cu and Pb in the saturated tailing compared with the unsaturated tailing. Elevated soil EC in the unsaturated tailing was due to capillary rise of water from the water table, which carried the soluble metal salts to the surface. The water then evaporated and the salts were left behind.
Plant-available concentrations of metals in the tailing did not reach phytotoxic levels, with the exception of Cd and Cu. Cadmium and Cu concentrations were in the phytotoxic range (
10 and 125 mg kg–1, respectively; Alloway, 1990) in all water table treatments at all tailing depths for both willow species.
Metal Concentrations in Plant Tissue
With the exception of Cd, Mn, and Zn, trace element concentrations in willow leaf and stem tissues were below levels considered toxic to agronomic plants in all water table treatments for both species (Table 5, Fig. 4; Kabata-Pendias and Pendias, 1992). Although Cu concentrations were in the phytotoxic range (125 mg kg–1; Alloway, 1990) in the tailing, the willows did not contain toxic concentrations (20–100 mg kg–1; Alloway, 1990) in their aboveground tissue. This is consistent with other studies and suggests willows exclude Cu from their aboveground biomass with the lowest accumulation in foliage and the highest accumulation in roots (Punshon, 1996; Nissen and Lepp, 1997). Dickinson et al. (1994) found Cu concentrations to be 14 times higher, on average, in the roots than in the aboveground biomass of willows grown in a nutrient solution of 0.5 mg L–1 Cu. In addition, willows may be more sensitive to Cu toxicity than other heavy metals, in particular Cd and Zn (Dickinson et al., 1994; Punshon, 1996). Considering that concentrations of Cu in the tailing were within the phytotoxic range, and Cu concentration in the roots was not analyzed in this study, the potential for Cu toxicity cannot be eliminated as a possible growth inhibitor.
In contrast to Cu, Cd concentrations were in the phytotoxic range (3 mg kg–1; Kabata-Pendias and Pendias, 1992) in both leaves and stems in all water table treatments for both willow species. Willows are thought to have a high uptake and tolerance to Cd compared with other heavy metals (Brieger et al., 1992; Ostman, 1994; Riddel-Black, 1994; Punshon and Dickinson, 1997). They are often unaffected or stimulated by Cd in contrast to Ni, Cu, and Zn (Punshon and Dickinson, 1999). Consequently, it seems unlikely that Cd toxicity was a factor in the depressed growth of Geyer willow.
Leaf tissue concentrations of Zn were in the phytotoxic range (300 mg kg–1) when averaged across water table treatments and willow species. These high Zn concentrations are similar to those found in other studies, due in part to Zn mobility and compartmentalization within leaf tissue (Nissen and Lepp, 1997; Punshon and Dickinson, 1999). Punshon and Dickinson (1999) examined several species of willows and reported that willow sensitivity to metal toxicity was Ni > Cu > Zn > Cd, and Fisher et al. (2000) found Geyer willow with plant tissue Zn concentrations in the range of 1130 to 1280 mg kg–1 to be vigorous and healthy. The concentrations in the Fisher et al. (2000) greenhouse experiment were 98% higher than the Zn plant tissue concentrations in this experiment, suggesting that a direct link to Zn toxicity is not likely to be contributing to the stunted growth of Geyer willow.
Manganese concentrations in the mountain willow leaves were highest in the two most saturated water table treatments (20 cm and flux) and were at phytotoxic concentrations ( 300 mg kg–1; Alloway, 1990). Manganese concentrations in Geyer willow leaf tissue exceeded the phytotoxic range in all water table treatments. However, the only significant water table effect was that the 20-cm treatment (most saturated) was higher than the 60-cm treatment (least saturated). These data are consistent with the extractable Mn in the soil in which Mn concentrations were highest in the most saturated treatment and lowest in the least saturated treatment. No published data on the sensitivity of willows to high concentrations of Mn in the soil or plant tissue is currently available, and consequently Mn toxicity remains a possibility for the stunted growth of Geyer willow.
The growth of mountain willow was not greatly impacted by any of the water table treatments, despite potentially phytotoxic concentrations of Cd, Mn, and Zn. Results of past studies have shown that considerable variation exists among response of different willow species to elevated metals (Landberg and Greger, 1994; Punshon and Dickinson, 1999), and the poor growth of Geyer willow compared with mountain willow might be attributed to this variation in susceptibility to metals.
Growth Responses
The large growth response differences between mountain and Geyer willow were especially pronounced in root biomass. The superior root system of mountain willow is important in revegetation efforts for tailing stabilization and subsequent prevention of surface water contamination. Dickinson et al. (1994) reported that only Cu and Ni produced significant differences in willow root growth between treatments of nutrient solutions containing Cu, Cd, Zn, and Ni. In a separate pot experiment, Dickinson et al. (1994) also noted the largest detrimental effect on willow root growth was from Cu-contaminated soil. Copper toxicity results in growth reduction, especially root growth (Greger et al., 1991). Heavy metal transport to the shoots is low, whereas roots are the first plant structure to encounter metal ions in the soil and, consequently, are more likely to be strongly affected by heavy metals (Greger et al., 1991). The noted differences in root biomass between the two willow species in the present study may be due to mountain willow's ability to either tolerate certain heavy metals or exclude them from uptake.
In this study, willows preferentially rooted directly above the saturated zones of the tailing and poor root growth was observed below the unsaturated–saturated interface in all water table treatments for both species. This indicates intolerance to the anaerobic conditions or elevated metals in the saturated zones, or some combination of the two. Although the fluctuating water table was not statistically different from the 40-cm water table treatment (P = 0.1395), this treatment negatively affected leaf and stem biomass compared with all other water table treatments for both species. Initially, the water table in the fluctuating treatment was at 40 cm, allowing for root growth to occur directly above this depth. The water table was then raised to 20 cm, forcing the newly established roots into the saturated zone and any new root growth to be concentrated above this zone. The process of lowering the water table back down to 60 cm caused the roots that were growing in the upper profiles while the water table was high to be without a water source. Swenson (1988) reported that dormant cuttings of willows planted in areas with a naturally fluctuating water table had lower survival rates than those with stable water levels. This finding and results from the present study suggest that the natural rise and fall of the ground water levels in the field could have a negative effect on growth of willow species.
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CONCLUSIONS
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Results from this greenhouse experiment indicate that substantial variability exists in uptake and potential tolerance to heavy metals between the two dominant willow species found near Leadville, Colorado. Mountain willow is a more vigorous and possibly more metal-tolerant species than Geyer willow when grown in amended mine tailing from this area. Potentially phytotoxic levels of Cd, Mn, and Zn in the leaf tissue and phytotoxic levels of Cu and Cd in the soil had little effect on growth of mountain willow. However, a combination of phytotoxic levels of metals could have contributed to reduced growth of Geyer willow in this greenhouse experiment and the Fisher (1999) field trial. Published data suggested that Cu toxicity might have occurred (Dickinson et al., 1994; Punshon and Dickinson, 1999) in these studies. Manganese toxicity is also a possible cause of reduced growth of Geyer willow; however, there is no published data on Mn toxicity in willows to support this claim.
Even though the fluctuating water table negatively influenced growth of both willow species, mountain willow responded more favorably to all water table treatments as compared with Geyer willow. The superior growth of mountain willow observed in this greenhouse study is supported by results from the field in which survival and growth of mountain willow were greater than for Geyer willow (Bourret, 2004). Therefore, establishment of mountain willow on mine tailing deposits along the Arkansas River should be considered in future revegetation projects to stabilize stream banks and reduce surface water contamination, thereby improving critical habitat for wildlife.
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NOTES
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Funding for this research was provided by the Colorado Agricultural Experiment Station.
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