Journal of Environmental Quality 32:834-840 (2003)
© 2003 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
TECHNICAL REPORTS
Heavy Metals in the Environment
Root Growth and Metal Uptake in Four Grasses Grown on Zinc-Contaminated Soils
Antonio J. Palazzo*,a,
Timothy J. Carya,
Susan E. Hardya and
C. Richard Leeb
a U.S. Army Engineer Research and Development Center, Cold Regions Research and Engineering Laboratory, 72 Lyme Road, Hanover, NH 03755
b U.S. Army Engineer Research and Development Center, Environmental Laboratory, 3909 Halls Ferry Road, Vicksburg, MS 39180
* Corresponding author (antonio.j.palazzo{at}erdc.usace.army.mil)
Received for publication July 11, 2001.
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ABSTRACT
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Depth and area of rooting are important to long-term survival of plants on metal-contaminated, steep-slope soils. We evaluated shoot and root growth and metal uptake of four cool-season grasses grown on a high-Zn soil in a greenhouse. A mixture of biosolids, fly ash, and burnt lime was placed either directly over a Zn-contaminated soil or over a clean, fine-grained topsoil and then the Zn-contaminated soil; the control was the clean topsoil. The grasses were ‘Reliant’ hard fescue (Festuca brevipila R. Tracey), ‘Oahe’ intermediate wheatgrass [Elytrigia intermedia (Host) Nevski subsp. intermedia], ‘Ruebens’ Canada bluegrass (Poa compressa L.), and ‘K-31’ tall fescue (Festuca arundinacea Schreb.). Root growth in the clean soil and biosolids corresponded to the characteristic rooting ability of each species, while rooting into the Zn-contaminated soil was related to the species' tolerance to Zn. While wheatgrass and tall fescue had the strongest root growth in the surface layers (0–5 cm) of clean soil or biosolids, wheatgrass roots were at least two times more dense than those of the other grasses in the second layer (5–27 cm) of Zn-contaminated soil. When grown over Zn-contaminated soil in the second layer, hard fescue (with 422 mg/kg Zn) was the only species not to have phytotoxic levels of Zn in shoots; tall fescue had the highest Zn uptake (1553 mg/kg). Thus, the best long-term survivors in high-Zn soils should be wheatgrass, due to its ability to root deeply into Zn-contaminated soils, and hard fescue, with its ability to effectively exclude toxic Zn uptake.
Abbreviations: BCP, biosolids mixture over clean topsoil and zinc-contaminated soil • BPP, mixture of biosolids, fly ash, and burnt lime over zinc-contaminated soil • CCC, control treatment with clean soil
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INTRODUCTION
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METAL TOXICITY limits plant growth around many smelters and nonferrous mine-waste storage areas in the United States and other countries (Chaney et al., 1988). In the Borough of Palmerton, Pennsylvania, more than 800 ha of forest vegetation on Blue Mountain are dead due to emissions of Zn, Cd, Cu, Pb, and SO2 from a Zn smelter operating since 1898 (Sopper, 1989; Buchnauer, 1973). Soil contaminated by atmospheric releases of S, Zn, Cd, and Pb caused the USEPA to include the immediate area at Palmerton as a Superfund Site in 1984 (Washington, 1985). Over the past 50 yr, about 30 cm of the original surface soil have been removed through erosion. In addition, the area was subjected to extensive logging and frequent fires (Jordan, 1975). Natural revegetation has been hampered primarily by the high Zn concentrations in the surface mineral soil and by the steep slopes. The soil depth of adverse contamination is 5 to 30 cm (Sopper, 1989). Chaney et al. (1989) reported that Zn toxicity to grasses is so severe at Palmerton that many homeowners have covered their lawns with stones or other mulch materials. The soils below these lawns contain as high as 10000 mg total Zn/kg and 100 mg total Cd/kg. Zinc phytotoxicity is the most extensive microelement phytotoxicity after the "natural" phytotoxicity caused by Al and Mn in strongly acidic soil. Li et al. (2000) reported that on the steep hillsides in the vicinity of the smelter, soil concentrations of Zn reached 26000 to 80000 mg/kg.
Contaminated hillsides are difficult to revegetate because the slopes are inaccessible to agronomic equipment needed to incorporate soil amendments for ameliorating the effects of toxic elements. This is a problem even though the contamination is only in the upper 30 cm of soil (Sopper, 1989). Oyler (1988) and Sopper (1989) found that surface applications of sewage sludge (biosolids) and fly ash were successful in promoting plant growth for up to two years and that tall fescue had good growth in those conditions. Questions remain, however, as to how long the surface applications of organic materials can sustain growth due to the retardation of rooting into the contaminated soil. Also, surface applications are subject to depletion and runoff, so plants must be able to grow into and tolerate the contaminated soil if the vegetation is to survive. Johnson et al. (1977) reported that vegetation sown on surface applications of sewage sludge to stabilize toxic spoil heaps is usually only temporary, and swards will deteriorate unless tolerant plant populations are sown. Haghiri and Sutton (1982) found that yields of tall fescue increased one year after seeding with sewage sludge application but then decreased the following year due to depletion of the readily mineralizable portion of the sludge's organic N. Identifying plants that can root through the surface-applied biosolids and contaminated soil layers will be beneficial for long-term survival. Grasses with deep root systems will have an increased capability to extract soil water and survive longer periods of drought than grasses with shallow root systems (Beard, 1973; Kneebone et al., 1992; Watschke and Schmidt, 1992).
Chaney et al. (1989) screened cultivars of several cool-season grass species for their ability to grow in Zn-contaminated soils and to take up Zn from the soils. They found differences in both growth and Zn concentration in shoots between cultivars of red fescue (Festuca rubra L.), tall fescue, and perennial ryegrass (Lolium perenne L.) in soil Zn levels of 1740 and 3480 mg/kg. ‘Merlin’ red fescue was the only cultivar tested that tolerated the higher soil Zn level. This was accomplished through the exclusion of Zn uptake to shoots. The cultivar ‘Hounddog’ was the more tolerant tall fescue tested in terms of yield and shoot Zn. In general, the tall fescue cultivars took up more Zn than the red fescue cultivars. In a study on Zn mine soil in Sweden, Bergholm and Steen (1989) reported that, two years after planting, red fescue and Kentucky bluegrass (Poa pratensis L.) were the two most dominant species at the site. After 10 yr, red fescue and the natural invasion of colonial bentgrass (Agrostis capillaris L.) dominated the plots. Merlin was the dominant cultivar of the red fescue species planted. Tall fescue constituted only a minor portion of the stand. Merlin red fescue and ‘Spbel’ creeping bentgrass [Agrostis stolonifera L. var. palustris (Huds.) Farw.] contained the lowest shoot Zn concentrations of the species at the site. These studies indicate that tolerance of grasses to Zn-contaminated soils may be related to low Zn uptake into the shoots.
Compared with shoot growth, much less is known about the rooting characteristics of plants grown on high-Zn soils. Likewise, little is known of how the root and shoot growths of different species are affected by high-Zn soil. We believe that depth and area of rooting are major factors in the long-term survival of plants grown on contaminated soils covered with a clean soil or organic material. Brar and Palazzo (1995) showed that some grasses root more deeply than others and hypothesized that deeper-rooting plants tolerant of Zn will be more likely to be successful in long-term survival following a one-time surface amendment. Another requirement for survival on surface-amended soil is a plant's ability to root through a change in substrate. Inhibition of root growth from a soil amendment layer into a toxic metal substrate below could cause plant dieback or injury (Johnson et al., 1977).
The objective of this research was to evaluate shoot morphology, rooting ability, and metal uptake of four cool-season grasses grown on a high-Zn soil. The contaminated soil was covered with either a mixture of biosolids, fly ash, and burnt lime or the biosolids mixture plus a fine-grained topsoil with a texture similar to that of the contaminated soil.
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MATERIALS AND METHODS
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We used a slant-tube technique, described by Taylor et al. (1978), to evaluate shoot and root growth and Zn uptake of four grasses grown in a Zn-contaminated soil. Each clear acrylic tube (4.8-cm i.d., 60-cm length, and 6-mm wall thickness) had a total volume of 1085 cm3. The tubes were placed in three racks that held the tubes at 15 degrees from vertical (Brar et al., 1990). The wooden racks were insulated with 2.5-cm-thick polystyrene sheets to decrease temperature fluctuations and prevent exposure of roots to direct sunlight in the greenhouse.
We used a completely randomized factorial design, containing four replications each of four grasses and three soil treatments. Soil in each tube was arranged in three layers over approximately 10 cm of sand: Layer 1 was 0 to 5 cm from the surface; Layer 2, 5 to 27.5 cm; and Layer 3, 27.5 to 50 cm (Fig. 1)
. Treatment BPP contained a 12:6:1 mixture of biosolids, fly ash, and burnt lime (B) in Layer 1 over Zn-contaminated soil (P) in Layers 2 and 3. Treatment BCP contained the biosolids mixture (B) in Layer 1 over clean topsoil (C) in Layer 2 and Zn-contaminated soil (P) in Layer 3. The control treatment (CCC) had clean soil (C) in all three layers. Sand packed to a bulk density of 1.65 g/cm3 filled the bottom of all tubes. The tubes were closed at the base with an aluminum cap containing holes to allow free drainage. After the three soil treatments were placed in the tubes, the soil was saturated repeatedly with distilled water and allowed to settle.
The Zn-contaminated soil was collected from the top 10 cm of soil at the Palmerton Smelter Site in Palmerton, Pennsylvania. Soils at the site are classified as a Klinesville very stoney silt loam (loamy-skeletal, mixed, active, mesic Lithic Dystrudept). Soils were placed in plastic barrels for storage and shipping to the Cold Regions Research and Engineering Laboratory, Hanover, New Hampshire, and were maintained field moist at 4°C. Before they were placed in the tubes, all soils were sieved through a 5-mm stainless steel mesh and maintained at the moisture level at which they had been collected. The uncontaminated or clean topsoil was a Hanover silty loam (fine-loamy, mixed, mesic Typic Fragiudult), which is similar in texture to the contaminated Palmerton soil. The biosolids (aerobically digested material), fly ash, and burnt lime (CaO2) material, called Ecoloam (Zinc Corporation of America, Palmerton, PA)1, was from the Palmerton site where it was being applied as a revegetation soil treatment; Ecoloam has a volume ratio of 12:6:1 of biosolids, fly ash, and lime. Soil analyses were performed using the methods in the Northeast Regional Publication 493 (Northeast Coordinating Committee on Soil Testing, 1995), except for soil metals, which were analyzed using the methods cited by Sparks (1996). The chemical properties of the Palmerton soil, the clean topsoil, and the biosolids are shown in Table 1. The sand that was placed in the bottom of each tube contained 16, 1, and 33 mg/kg of total N, P, and K, respectively.
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Table 1. Chemical and physical characteristics of the Hanover silty loam topsoil (clean soil), Palmerton contaminated soil, and the biosolids.
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The grasses studied were Reliant hard fescue, Oahe intermediate wheatgrass, Ruebens Canada bluegrass, and K-31 tall fescue. These grasses represent the dominant species sown and existing at the Palmerton site. To improve germination, seeds of the selected species were primed for two days on filter paper in Petri dishes containing distilled water. We planted four seeds of one cultivar per tube and covered the tubes with aluminum foil to reduce soil moisture loss. After emergence, we removed the foil and thinned the plants to two uniform seedlings per tube. Every day, the plants were watered with 50 mL per tube of distilled water; every 14 d, they were watered with 50 mL per tube of a modified half-strength nutrient solution (Johnson et al., 1957).
An unshielded thermocouple recorded air temperature inside the greenhouse. Data were logged hourly with a Model CR-10X data recorder (Campbell Scientific, Logan, UT). The average daily air temperatures varied between 12.8 and 24.4°C.
The grasses were harvested 67 d after planting, when the first root touched the bottom of the acrylic tube. We cut the plant shoots above the crown and washed them with distilled water, using a paper towel to remove excess surface water. The roots were sectioned at the 5.0-, 27.5-, and 50.0-cm depths and were washed free of soil over a 60-mesh nylon screen by both spraying and immersion in water as described by Brar and Palazzo (1995).
Total shoot area and total root area and length were measured with an AgVision root and leaf imaging system (Decagon Devices, Pullman, WA). Dry weights of roots and shoots were recorded after oven-drying at 80°C for 48 h to a constant weight. Root length, area, and weight densities for each soil depth range were determined by taking the root length, area, or weight divided by the soil volume. All measurements were taken on both plants in each tube, averaged, and then reported as if there were a single plant per tube. Analyses of variance (ANOVA) of the data were conducted using SAS Version 8.0 (SAS Institute, 1999), and the means were separated using least significant differences at the 0.05 probability level.
Plant shoots were analyzed for zinc using the methods described by Lindsay and Norvell (1978). No statistical analyses were performed on the tissue analysis data because replications had to be combined to obtain sufficient tissue for analysis.
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RESULTS
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Shoot Growth
Greater shoot weights were found in the BCP and BPP treatments than in the control treatment (CCC), but the only statistically significant difference was between BCP and CCC (Table 2). The greatest shoot area was noted in the BPP treatment. The two species with the normally greater leaf size, wheatgrass and tall fescue, exhibited the greatest shoot areas, while wheatgrass had the greatest shoot weight. Though not significantly different, tall fescue had slightly greater shoot area than did wheatgrass, indicating that wheatgrass, with significantly greater shoot weight, had wider or thicker leaves than the tall fescue.
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Table 2. Combined effects of soil treatment and grass species on mean plant shoot area and weight of four grasses.
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Root Growth
Significant differences were found for most soil treatments and species in all three soil layers for root length, area, and weight densities (Table 3). The interaction of species and soil treatment was found to be significant in Layers 1 and 2, but not Layer 3. Soil Layer 3 was at a depth of 27.5 to 50.0 cm and contained few plant roots. Few grass roots normally grow to this depth.
Soil Layer 1
Soil Layer 1 (0–5 cm) consisted of one treatment of control soil over two layers of the control soil (CCC) and two treatments of biosolids, one over contaminated Palmerton soil (BPP) and the other over a control soil and then contaminated soil (BCP) (Fig. 1).
Mean root weight, length, and area densities in Layer 1 were greater in the BPP treatment, followed by the BCP treatment and then the CCC treatment (Table 4). The means of all species growing in a biosolids surface layer (treatments BPP or BCP) had about four to seven times greater root weight, length, and area densities in the surface 0 to 5 cm as compared with the control soil (treatment CCC).
The only significant differences between species were in the biosolids treatments (Table 4). Tall fescue and wheatgrass produced greater root weight, length, and area densities than Canada bluegrass and hard fescue.
Soil Layer 2
Soil Layer 2 (5–27.5 cm) consisted of two treatments of clean soil—one under and over clean soil (CCC) and one under biosolids and over contaminated Palmerton soil (BCP)—and one treatment of contaminated Palmerton soil below biosolids and over more Palmerton soil (BPP) (Fig. 1).
In the CCC soil treatment, tall fescue produced greater root weight, length, and area densities than the other species (Table 5). In the BCP treatment, tall fescue again had greater weight and area densities than the other three species, and wheatgrass and tall fescue produced greater root length density than Canada bluegrass and hard fescue. In the contaminated soils of the BPP treatment, wheatgrass had significantly greater root length densities than the other species, and, although not significant, the weight densities were also two times greater for wheatgrass.
Soil Layer 3
Soil Layer 3 consisted of one treatment of clean soil under clean soil (CCC) and two treatments of contaminated Palmerton soil, one below biosolids and contaminated Palmerton soil (BPP) and one below biosolids and clean soil (BCP) (Fig. 1).
Few roots in any of the treatments were able to penetrate to this soil depth (27.5 cm), and relatively few differences were found between treatments (Table 6). Tall fescue was the only species with any noticeable growth into Layer 3 of the CCC or BCP treatments. No roots of any species were able to penetrate into Layer 3 when there was contaminated soil above (treatment BPP).
Plant Zinc Concentrations
Mean plant Zn concentrations of shoots are shown in Table 7. Plants grown in the BPP soil treatment had greater Zn concentrations than the plants grown in either the CCC or BCP treatments. Except for hard fescue (at 422 mg/kg), Zn concentrations of plants grown in the BPP treatment were all in the toxic range (greater than 500 mg/kg) for plant growth, yet we saw no signs of Zn phytotoxicity in any of the plants.
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DISCUSSION
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Shoot and Root Growth
Of the four grasses in this study, two are rapid-growing, larger-structured plants (tall fescue and wheatgrass) and the other two are more petite species (hard fescue and Canada bluegrass). As expected, greater shoot growth was found for tall fescue and wheatgrass than for Canada bluegrass and hard fescue. The lower shoot areas and weights recorded for Canada bluegrass and hard fescue (Table 2) are related to their shorter leaves and slower growth rates compared with tall fescue and wheatgrass. The quantity of root growth in the biosolids in Layer 1 (treatments BCP and BPP, Table 4) also followed the growth-rate characteristics (strong vs. weak rooting capability) of the individual species: tall fescue and wheatgrass were stronger-rooting plants than either Canada bluegrass or hard fescue in both biosolids treatments. These results agree with those of Palazzo and Brar (1997), who reported that tall fescue had greater shoot weights and area and root weight densities than hard fescue grown in acrylic tubes in the greenhouse.
In Layer 1, three of the four grasses had significantly greater root weight, length, and area densities in the biosolids treatments (BCP and BPP) than in the clean soil (CCC) (Table 4). Although not statistically significant, the fourth grass, hard fescue, also had greater root weight, length, and area densities in the biosolids. Although most differences were not significant, three of the four grasses also had greater root growth in the second layer of clean soil below the biosolids (BCP) compared with the clean soil with no biosolids (CCC) (Table 5). These results are to be expected because of the added nutrients and moisture provided by the biosolids.
For the stronger-growing grasses (tall fescue and wheatgrass) in Layer 2 below the biosolids, tall fescue had significantly less growth in the contaminated soil (BPP) than in the clean soil (BCP), while wheatgrass showed no significant differences between those two treatments (Table 5). These findings indicate that wheatgrass is more tolerant of rooting into Zn-contaminated soil than is tall fescue. Tall fescue did equally well or slightly better than wheatgrass in the biosolids of Layer 1, and both species were able to grow through a change of substrate into the clean soils of Layer 2, but tall fescue was apparently inhibited by the contaminated substrate. Johnson et al. (1977) also reported the cessation of grass root growth at an interface between sewage sludge and a high-Zn colliery spoil. This inability of tall fescue to grow into the contaminated substrate suggests that, while it may do well initially, as observed by Oyler (1988) and Sopper (1989), it may not be able to sustain growth once the biosolids have broken down. Of the two strong-growing grasses we tested, wheatgrass appears to be the best candidate for sustained growth because of its deep-rooting ability and tolerance of rooting in Zn-contaminated soil.
Zinc Uptake
The shallow depth of the contaminated soil (5 cm) in the BPP treatment resulted in greater shoot Zn concentrations in all species (Table 7). Johnson et al. (1977) reported that the highest concentrations of Zn in plants occurred when the maximum root penetration for a particular plant was equivalent to the depth of the contaminant. The normal range for plant Zn is 10 to 300 mg/kg (Allaway, 1968), and Chaney (1993) found that Zn levels of 500 mg/kg in plants reduced plant yield. Hard fescue was the only grass in our study that was not well above the 500 mg/kg level in the BPP treatment. Our finding that tall fescue had the greatest Zn concentration (1553 mg/kg) agrees with Sopper (1989), who reported that tall fescue had higher concentrations of Zn than did wheatgrass when grown in surface applications of biosolids over the contaminated Palmerton soil. Our observations also agree with Sopper's (1989) in that there were no symptoms of phytotoxicity despite the high foliar concentrations.
The low uptake we saw in hard fescue (422 mg/kg) agrees with the results of Chaney (1993) and Chaney et al. (1989), who reported that red fescue, another fine fescue, excludes the uptake of Zn. Johnson et al. (1977) and Bergholm and Steen (1989) also reported that red fescue is tolerant of soils with high metal concentrations, and Bergholm and Steen (1989) found that red fescue was more dominant than tall fescue when sown on high-Zn soils.
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ACKNOWLEDGMENTS
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The authors thank Dr. A. Page, University of California-Riverside, and Dr. K. Asay and Dr. K. Jensen, USDA, Logan, UT, for technical reviews. The authors also thank Larry Piazza, John Lombardo, and James Moore, Baltimore District, U.S. Army Corps of Engineers, and Fred McMillian, USEPA, Philadelphia, PA, for advice and John Oyler and Robert Thompson, Zinc Corporation of America, for their assistance in soil collection. The authors thank the USEPA and the Strategic Environmental Research and Development Program for funding this study.
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NOTES
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1 The use of trade names is necessary to report factually on available data. However, the U.S. Army neither guarantees nor warrants the standard of the product, and the use of the name by the U.S. Army implies no approval of the product to the exclusion of others that may also be suitable. 
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ABSTRACT
INTRODUCTION
