Soil Science Society of America Journal 64:955-962 (2000)
© 2000 Soil Science Society of America
DIVISION S-4-SOIL FERTILITY & PLANT NUTRITION
Soil pH Affects Copper Fractionation and Phytotoxicity
A.K. Alvaa,
B. Huangb and
S. Paramasivamc
a USDA-ARS-PWA, 24106 N. Bunn Rd., Prosser, WA 99350 USA
b Institute of Soil Science, Academia Sinica, Nanjing, 210008, People's Republic of China
c Univ. of Florida, Institute of Food and Agricultural Sciences, Citrus Research and Education Center, 700 Experiment Station Rd., Lake Alfred, FL 33850 USA
aalva{at}tricity.wsu.edu
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ABSTRACT
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Phytotoxicity of copper (Cu) depends on the relative distribution of different chemical forms, which is a function of soil properties, such as soil pH and organic matter content. Sequential fractionation was conducted to partition the total Cu into exchangeable, sorbed, organically bound, precipitate, and residual forms. Three soils were sampled from existing citrus groves and 0 to 400 mg Cu kg-1 were added. The soils used were: Myakka fine sand (sandy, siliceous, hyperthermic Aeric Haplaquods; pH = 5.7), Candler fine sand (hyperthermic, uncoated, Typic Quartzipsamments; pH = 6.5), and Oldsmar fine sand (sandy, siliceous, hyperthermic Alfic Arenic Haplaquods; pH = 8.2). Phytotoxicity of added Cu was evaluated using citrus rootstock (Swingle citrumelo) seedlings grown for 330 d. In Cu-unamended soils, the major portion of the total Cu was in the organically bound form in the low pH soils. However, in the high pH soil, the precipitate form was the dominant form. As the rate of Cu increased, the concentration of the readily soluble Cu forms (exchangeable + sorbed forms) increased in the low pH soils, that is, from 0.8 to 89.5 mg kg-1 (8.4–25.3% of total Cu) in the Myakka soil, and from 2.2 to 70.3 mg kg-1 (3.1–20.3% of total Cu) in the Candler soil. In the high pH Oldsmar soil, however, the concentration of readily soluble Cu forms increased only from 1.1 to 5.3 mg kg-1. In relation to the total Cu content this was equivalent to a decrease from 5.2 to 1.5%. The citrus seedling growth was negatively correlated with Cu concentrations in the readily soluble forms and positively correlated with those of the precipitate form. A 20% decrease in the top and root weights occurred at 2.5 mg kg-1 of readily soluble Cu in the Candler soil (pH = 6.5). The critical concentration was lower (1.7 mg kg-1) for root growth on the Myakka soil (pH = 5.7). The critical Cu concentration in the leaves varied from 60 to 68 mg kg-1, while that in the roots was 62 mg kg-1 in the Myakka soil, but increased to 270 mg kg-1 in the Candler soil. This study demonstrated that the readily soluble form of Cu is the most phytotoxic, and an increase in the precipitate form is, thus, responsible for a reduction in Cu phytotoxicity.
Abbreviations: ICPAES, inductively coupled plasma argon emission spectrometer
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INTRODUCTION
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COPPER is an essential element for plant growth. However, its presence in the soil in quantities lower or greater than the optimal amount could adversely affect plant growth. For citrus, deficiency of Cu can result in dieback (Tucker et al., 1995) while excess Cu may cause iron chlorosis (Reuther and Smith, 1952, 1953; Reuther et al., 1953; Alva and Graham, 1991). The Cu concentration in mineral soils of central Florida is naturally lower than that in other regions of the USA (Holmgren et al., 1993). For new citrus plantings on virgin soils (mainly Spodosols and Alfisols) in the southern part of Florida, addition of Cu to young trees is necessary for several years (Tucker et al., 1995). Since Cu mobility in soils is quite low, Cu which is not taken up by the trees tends to accumulate in the top few centimeters of soil, due to binding of Cu by organic matter.
Many sandy soils, which have been under citrus production since the 1940s, show considerable accumulation of Cu (Alva, 1993). This is due to heavy rates of Cu application in the early 1940s, because Cu was recommended to control citrus dieback. During those early years, the N/Cu ratio in young citrus tree fertilizer blend was 8:1. In addition, Cu was also contributed annually by the pesticide applied routinely as foliar sprays (Reuther and Smith, 1952, 1953; Reuther et al., 1953). A part of the Cu-based pesticides applied on the foliage could run off from the leaves, thus contributing to Cu accumulation in the soil. Although the annual contribution of this Cu is very small, its cumulative effects over several years can be substantial. Therefore, Cu concentration in soils with long-term citrus production is significantly greater than that in the similar soil series under native vegetation (Alva et al., 1993; Zhu and Alva, 1993a; Alva and Obreza, 1994). The total Cu concentrations in some citrus grove soils varied from 100 to 380 mg kg-1 (Alva, 1992; Zhu and Alva, 1993b; Zhang et al., 1997). This represents Cu accumulation in small quantities over a number of years. When an old grove site is replanted with young trees, the effects of Cu toxicity may be evident in some cases, depending on the soil pH as well as the Cu sensitivity of the rootstock used (Alva et al., 1995).
The phytotoxicity of Cu depends on its bioavailability, which is closely related to the distribution of Cu in different chemical forms. Copper in soils may exist in the following forms: (i) water soluble, (ii) exchangeable, (iii) organically bound, (iv) associated with carbonates and hydrous oxides of Fe, Mn, and Al, and (v) residual (Shuman, 1985). Copper fractionation studies have shown that Cu exists in soils predominantly as organically bound and residual forms (McLaren and Crawford, 1973; Shuman, 1979; Hickey and Kittrick, 1984; Saha et al., 1991), as organically bound and precipitate forms (Zhu and Alva, 1993b), or as acid-soluble forms (Berti and Jacobs, 1996).
The relative distribution of various chemical forms of heavy metals appear to depend, to some extent, on the fractionation procedure employed. Due to differences in fractionation procedures, it is rather difficult to assign specific geochemical identities of each metal to the various fractions that are being extracted. Studies conducted with a variety of soils ranging in pH from 4.6 to 6.4 have shown that organic and exchangeable forms of Cu are the major forms taken up by various crop species, including corn (Zea mays L.) and wheat (Triticum aestivum L.) (Viets, 1962; Martens, 1968; McLaren and Crawford, 1973; Jarvis, 1981; Sims, 1986).
Several soil properties such as pH, redox potential (Eh), cation exchange capacity, organic matter, texture, oxide content, and clay mineralogy influence the relative distribution of Cu in different chemical forms (Viets, 1962; Martens, 1968; Sims and Patrick, 1978; McLaren et al., 1983; Sims, 1986). An increase in soil pH, for example, increases the precipitate form of Cu while decreasing the organically bound form (Sims, 1986; Sims and Kline, 1991; Zhu and Alva, 1993b).
The objectives of this study were: (i) to examine the relative distribution of various forms of Cu in three soils with different pH values and amended with different rates of Cu, and (ii) to evaluate the relationship between the growth response and Cu concentration of Cu-sensitive citrus rootstock (Swingle citrumelo; Castle et al., 1993) seedlings as affected by the relative distribution of Cu forms in different soils.
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Materials and methods
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Three soils selected to represent the major soils used in different citrus production regions of Florida, that is, Myakka fine sand (pH = 5.7, organic matter = 1.0%), Candler fine sand (pH = 6.5, organic matter = 0.4%), and Oldsmar fine sand (pH = 8.2, organic matter = 1.7%), were sampled from 0 to 30 cm depth. The soil samples were taken from existing citrus groves in each of the three sampling locations. The soil samples were air dried and sieved to collect particle size <2 mm. Each soil was divided into six subsamples and each of the subsamples was amended with either 0, 25, 50, 100, 200, or 400 mg kg-1 of Cu as CuSO4·5H2O. A dry granular fertilizer blend containing 80, 30, and 100 g kg-1 of N, P, and K, respectively was mixed with the soil at a rate equivalent to 0.05 mg N g-1 across all treatments and soils. Amended soils were incubated for 47 d at field capacity soil moisture content.
At the end of the incubation period, 3.0-kg portions of amended soils were weighed into plastic pots (16.5 cm height and 17 cm top diameter) with four replicate pots per treatment. One 5-mo-old seedling of Swingle citrumelo rootstock was transplanted into each pot. The pots were then placed in a greenhouse and arranged in a completely randomized design. The seedlings were grown for 330 d, at a mean temperature of 25 ± 2°C. Soil water content was maintained close to field capacity by weighing the pots daily and adding water to replenish the moisture deficit.
At the end of the experiment, each plant was harvested by clipping the shoot at the soil level. The leaves were separated from the stem, washed in dilute detergent solution, followed by several rinses in distilled water. The root system was separated from the soil and washed in distilled water. All plant parts were dried in an oven at 70°C for 72 h, and the dry weights were recorded. The seedling parts, including the leaves and roots, were ground and ashed at 500°C for 5 h. The ash was dissolved in 20 mL of 1 M HCl solution. The Cu concentration was measured by using an inductively coupled plasma argon emission spectrometer (ICPAES, Plasma 40, Perkin-Elmer Corp, Norwalk, CT).
Soil pH was measured in water (1:2 w/v) at the end of the incubation period. The soil samples from each pot at the end of the seedling growth experiment were used for fractionation of Cu chemical forms. The procedure of Sposito et al. (1982) was adapted to fractionate total Cu into exchangeable, sorbed, organically bound, and precipitated forms. Each 2 g soil sample was weighed into 50-mL centrifuge tubes, and 25 g each of following reagents were sequentially added and shaken for the time specified for each extractant in the order listed: 0.5 M KNO3 for 16 h (exchangeable); three extractions in deionized water for 2 h each (sorbed); 0.5 M NaOH for 16 h (organically bound); 0.05 M Na2 EDTA for 6 h (precipitated). At the end of each extraction period, the soil suspension was centrifuged for 15 min and filtered through Whatman no. 42 filter paper. The tube with soil was weighed once after the addition of the extractant and again after the solution was filtered, to estimate the quantity of entrained solution. The quantity of each subsequent extractant was adjusted to account for the entrained solution from the previous extraction. The concentration of Cu was measured in each filtrate using ICPAES. The Cu content in the entrained solution is carried over into the subsequent extraction. The contribution of Cu in the entrained solution from the previous extraction was used to correct calculations of Cu content in the subsequent extraction.
The concentration of total Cu in the soil was determined by USEPA Method no. 3050 (USEPA, 1986). This method involved digestion of 1.0 g soil in 10 mL of 8 M HNO3 at 95°C for 15 min. The solution was cooled and 5 mL of concentrated HNO3 was added and refluxed twice for 30 min each. The solution was then evaporated to 5 mL. After cooling the solution, 2 mL of deionized water and 3 mL of 30% H2O2 were carefully added and refluxing was continued on a hot plate. The addition of H2O2 was repeated (total quantity of H2O2 addition did not exceed 10 mL) until the solution became clear, followed by addition of 10 mL of deionized water and 5 mL of concentrated HCl, and 15 min of reflux without boiling. The solution was cooled and filtered through Whatman no. 42 filter paper, and the volume was adjusted to 100 mL with distilled water. The concentration of Cu was determined using ICPAES. Residual Cu was calculated by the difference between total Cu and the sum of other four forms (i.e., exchangeable + sorbed + organically bound + precipitate). This procedure was previously used by Bell et al. (1991) and Luo and Christie (1998).
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Results and discussion
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Fractionation of Copper in Copper-Unamended Soils
Copper contents in unamended soils represent the accumulation of Cu over several years of Cu additions in small doses through pesticides and fertilizers. Under these conditions, the major Cu fractions were the organically bound, that is, 7.4 to 25.9 mg kg-1 (28.1–73.5% of total Cu) and the precipitate forms, that is, 1.4 to 32.3 mg kg-1 (14.2–65.2% of total Cu; Fig. 1 and 2)
. The sum of these two forms accounted for 81 to 93% of the total Cu. The organically bound form of Cu was 7.4 mg kg-1 (73.5% of the total Cu) in the low pH (5.7) Myakka soil. The proportion of the organically bound form decreased along with an increase in that of the precipitate form in the higher pH soils. The readily soluble forms (exchangeable + sorbed) varied from 0.8 to 2.2 mg kg-1, which accounted for a small portion of the total Cu (i.e., 3.1–8.4%). Several studies have shown a very low content of Cu in readily soluble forms (McLaren and Crawford, 1973; Hickey and Kittrick, 1984; Saha et al., 1991; Berti and Jacobs, 1996). Likewise, the residual form of Cu among the three soils in this study represented only 1.6 to 16.1% of total Cu among the three soils (Fig. 2).
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Fig. 1 Concentrations of different chemical forms of Cu in three soils with different rates of Cu amendments as CuSO4 · 5H2O. Readily soluble fraction = (exchangeable + sorbed) forms
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Fig. 2 Relative distribution of total Cu into different chemical forms. The similar letters on the top of histograms for each Cu rate within each Cu form indicate that the mean values are not significantly different according to Duncan Multiple Range test at P  0.05. Readily soluble fraction = (exchangeable + sorbed) forms
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Fractionation of Copper in Copper-Amended Soils
Readily Soluble Form
Concentrations of readily soluble Cu increased from 0.8 to 89.5 and from 2.2 to 70.3 mg kg-1 with increasing Cu rate in the Myakka and Candler soils, but decreased in the Oldsmar soil (Fig. 1 and 2). In the Myakka and Candler soils, the soil pH decreased significantly with an increase in Cu rate, which could be primarily due to a "salt effect." The increase in proportion of the readily soluble Cu with an increase in Cu rate in the Myakka and Candler soils could be, in part, due to the decrease in soil pH. Increased rates of Cu additions had negligible effects on the soil pH and readily soluble Cu in the Oldsmar soil.
Organically Bound Form
With an increase in the Cu rate, the proportion of the organically bound form of Cu decreased in all three soils (Fig. 2). The low organic matter content of these soils may not have been adequate to bind high rates of Cu additions. In contrast, in studies with Cu application in organic sources such as Cu-enriched swine manure (Payne et al., 1988) or Cu-rich-sewage sludge (Sposito et al., 1982; Sims and Kline, 1991), the proportion of total Cu in the organically bound form increased with an increase in Cu amendment. Organically bound Cu concentrations were significantly greater in the Myakka soil compared to the other two soils (Fig. 2). This is due to a combination of low pH and high organic matter content. Although the organic matter content was greater in the Oldsmar soil (1.7%), as compared to that in the Myakka soil (1.0%), the greater pH of the Oldsmar soil resulted in an increased proportion of total Cu in the precipitated form than in the Myakka soil.
Precipitate and Residual Forms
Increased rates of Cu increased concentrations of precipitate Cu in all soils (Fig. 1). This increase in precipitate Cu was greater in the high pH Oldsmar soil (14.3–271.2 mg kg-1) compared to the other soils (1.4–105.5 mg kg-1 in the Myakka soil and 32.3–175.9 mg kg-1 in the Candler soil). The slopes of the linear regression between the concentration of precipitate form and the Cu rates were 0.26, 0.36, and 0.64, respectively, for the Myakka, Candler, and Oldsmar soils (Fig. 3) . There was also a positive correlation (r = 0.81***) between the proportion of the precipitate form and the soil pH. This is further evidence that an increased soil pH resulted in an increase in the proportion of Cu in the precipitate form.
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Fig. 3 Relationship between the concentration of precipitate Cu and rates of Cu. The r2 value followed by *** indicates significance of the regression at P 0.001
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Residual Cu was quite low in the Oldsmar soil, that is, 0.4 to 16.3 mg kg-1, which was equivalent to 1.5 to 5.6% of the total Cu (Fig. 1). The proportion of total Cu in the residual form peaked (27–32%) at the 100 mg kg-1 Cu rate for both the Myakka and Candler soils. A further increase in Cu rates decreased the proportion of the residual Cu (Fig. 2).
Effects of Chemical Forms of Soil Copper on Phytotoxicity to Citrus Seedlings
Effects on Dry Weight of Citrus Seedlings
Increased rates of Cu significantly decreased leaf, stem, and root dry weight of citrus seedlings in the low pH Myakka and Candler soils; however, no clear effects were observed on seedling growth in the high pH Oldsmar soil (Fig. 4)
. In the unamended soils, both the leaf and stem dry weights of the seedlings grown in the Oldsmar soil were greater than those in the Myakka and Candler soils. However, this difference was negligible for the root dry weight. The correlation coefficients between soil pH vs. leaf, stem, and root dry weights were 0.87, 0.89, and 0.77, respectively (Table 1)
. The dry weights of all seedling parts were negatively correlated with the readily soluble form of Cu (Table 1), thus suggesting that the seedling growth was most sensitive to an increase in the readily soluble form of Cu in the soil. The concentration of this form of Cu in the soil increased with a decrease in soil pH.
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Fig. 4 Dry weights of leaves, stem, and roots of Swingle citrumelo seedlings as influenced by various rates of Cu additions. The significance of the regression at P 0.05, 0.01, and 0.001 is shown by *, **, and ***, respectively
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Table 1 Correlation coefficients (r) between dry weight of citrus seedling parts and soil pH as well as the proportion of various Cu forms in the soil as a percentage of total Cu
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Seedling growth response to concentrations of readily soluble Cu was evaluated on the basis of relative dry weight of seedling tops or roots (Fig. 5)
. The concentration of readily soluble Cu was low in the Oldsmar soil compared to the other soils despite applications of up to 400 mg kg-1 Cu (Fig. 1). Accordingly, effects of increased Cu addition on seedling growth were minimal in the Oldsmar soil (Fig. 4 and 5). In the other soils, there was a negative exponential relationship between the relative dry weight of tops and roots and concentration of readily soluble Cu (Fig. 5). On the basis of these relationships, a 20% decrease in the growth of tops occurred at 2.2 and 2.5 mg kg-1 readily soluble Cu in the Myakka and Candler soils, respectively. A similar decrease in root growth occurred at 1.7 and 2.5 mg kg-1 readily soluble Cu in the Myakka and Candler soils.
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Fig. 5 Relative dry weights of Swingle citrumelo rootstock seedling tops or roots in relation to concentration of readily soluble Cu. The significance of the regression at P 0.05, 0.01, and 0.001 is shown by *, **, and ***, respectively
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Concentrations of precipitate Cu were positively correlated with dry weight of leaves and stems (Table 1). This suggests a decrease in Cu toxicity with an increase in the precipitate form. Precipitation of Cu was the basis for the reported decrease in Cu toxicity by liming (Reuther et al., 1953). Accordingly, soil management to increase the proportion of precipitate Cu is an important consideration to mitigate Cu phytotoxicity.
Effects of Copper Amendments on Tissue Copper Concentration of Citrus Seedlings
The leaf and root Cu concentrations increased significantly with an increase in readily soluble soil Cu (Fig. 6 and 7)
. The rates of increase in both leaf and root Cu concentrations were greater in the Myakka and Candler soils than in the Oldsmar soil. It is important to underscore the fact that with an increase in Cu rate from 0 to 400 mg kg-1, the concentrations of the readily soluble Cu forms increased from 0.8 to 89.5 mg kg-1 in the Myakka and Candler soils, and only 1.1 to 5.3 mg kg-1 in the Oldsmar soil (Fig. 1). This was clearly reflected in the lower concentrations of Cu in the leaves and roots of the seedlings grown in the Oldsmar soil compared to those of the other soils. The root Cu concentrations at the 400 mg kg-1 treatment were greater by 45- and 118-fold, respectively, for the Myakka and Candler fine sands, compared to those in the unamended treatment. In the Oldsmar soil, the corresponding increase in root Cu concentration was only fourfold.
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Fig. 6 Copper concentrations in the leaves of Swingle citrumelo rootstock seedlings as a function of total Cu measured in three soils with different pH which received various rates of Cu amendment. The significance of the regression at P 0.05, 0.01, and 0.001 is shown by *, **, and ***, respectively
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Fig. 7 Copper concentrations in the roots of Swingle citrumelo rootstock seedlings as a function of total Cu measured in three soils with different pH which received various rates of Cu amendment. The significance of the regression at P 0.05, 0.01, and 0.001 is shown by *, **, and ***, respectively
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The leaf and root Cu concentrations were substantially lower in the seedlings grown in the Oldsmar soil compared to those of the seedlings grown in the other two soils (Fig. 6 and 7). This is related to the extremely low concentration of the readily soluble form of Cu in the former soil. A 20% reduction in seedling top weight occurred at leaf Cu concentration of 60 and 68 mg kg-1 in the seedlings grown in the Myakka and the Candler soils, respectively (Fig. 8)
. A similar magnitude of decrease in root growth occurred at 62 and 271 mg kg-1 Cu in the roots of the seedlings grown in the Myakka and Candler soils, respectively. The critical Cu concentration in the roots showed dependency on the soil pH. It appears that at higher pH the roots can tolerate increased levels of external Cu for the same degree of growth suppression. However, the leaf critical Cu concentration showed little variation between the two pH levels. Further research is necessary to understand the mechanism for these differences.
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Fig. 8 Relative dry weights of tops and roots as a function of Cu concentration in the leaves and roots, respectively, of Swingle citrumelo rootstock seedlings. The significance of the regression at P 0.05, 0.01, and 0.001 is shown by *, **, and ***, respectively
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Conclusions
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This study demonstrates that soil pH influences the phytotoxicity of Cu primarily due to differential distribution of Cu chemical forms. Readily soluble Cu (exchangeable and sorbed) is the most phytotoxic form, and its concentration decreases considerably with an increase in soil pH above 6.5. The critical concentration of readily soluble Cu varied from 1.7 to 2.5 mg kg-1 in soils with pH 5.7 to 6.5. On the basis of the relative dry matter weights of the seedling tops, a 20% reduction in dry matter weight occurred at about 60 to 68 mg kg-1 leaf Cu in seedlings grown in soils with pH 6.5. In contrast, a 20% reduction in root weight occurred at 62 and 271 mg kg-1 Cu in the roots of seedlings grown in soils with pH 5.7 and 6.5, respectively. Soil pH plays a major role in determining Cu phytotoxicity. The roots can accumulate greater concentrations of Cu when grown in a higher pH than in a lower pH soil for a given degree of growth suppression.U.S. Environmental Protection Agency 1986
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ACKNOWLEDGMENTS
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One of the authors, B. Huang, is grateful to the financial support of K.C. Wong Education Foundation, Hong Kong, China, for his study leave in the USA.
Received for publication October 27, 1998.
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R. Vulkan, U. Mingelgrin, J. Ben-Asher, and H. Frenkel
Copper and Zinc Speciation in the Solution of a Soil-Sludge Mixture
J. Environ. Qual.,
January 1, 2002;
31(1):
193 - 203.
[Abstract]
[Full Text]
[PDF]
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ABSTRACT
INTRODUCTION
