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TECHNICAL REPORT
Plant and Environment Interactions

Bioavailability of Biosolids Molybdenum to Soybean Grain

^a Soil and Water Science Dep., Univ. of Florida, Gainesville, FL 32611-0510
^b Metro. Water Reclamation District Greater Chicago, 6001 W. Pershing Rd., Cicero, IL 60804
^c Dep. of Plant Soil Sciences, Oklahoma State Univ., Stillwater, OK 74078

* Corresponding author (gao{at}ufl.edu)

Received for publication October 16, 2000.

	ABSTRACT

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

 
Legumes grown in biosolids-amended soils and then fed to ruminants can represent problematic sources of molybdenum (Mo), but few field data are available to quantify the risk. We used a set of fields amended to high cumulative biosolids Mo loads (>18 kg ha^-1) over 27 yr to generate additional data. Soybean [Glycine max (L.) Merr.] was grown on 29 fields (pH values >6.8) amended to a wide range of soil Mo loads. Soybean grain harvested from each field was analyzed for Mo and the concentrations regressed against soil Mo loads estimated from actual soil Mo concentrations in the 0- to 15-cm depth. Slopes of such linear regressions represent uptake coefficients (UC values) used by the USEPA to assess risk of biosolids Mo to ruminants fed forage grown on biosolids-amended land. The UC value for all 29 fields was estimated as 1.66, which agrees with the few soybean grain data in the literature. The UC value, however, is well below a conservative UC value of 4, recently recommended for all fresh legume materials fed to cattle. Soybean grain can contain high concentrations of Mo (>10 mg kg^-1) and have low (<2:1) Cu to Mo ratios, which can exacerbate molybdenosis problems in cattle. However, soybean grain normally constitutes only 10% of dairy cattle diet, and other constituents (e.g., corn grain, stover, mineral supplements) are sufficient, or can be manipulated, to control molybdenosis.

Abbreviations: HEI, highly exposed individual • RPc, reference pollutant load • UC, uptake coefficient

	INTRODUCTION

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

 
IN 1993, THE USEPA promulgated regulations (40 CFR Part 503) that, along with state regulations, govern biosolids recycling (USEPA, 1993). The federal rule is risk-based and assesses exposure of highly exposed individuals (HEI)—animals, humans, and the environment—to 10 biosolids metals through 14 exposure pathways. A reference pollutant load (RPc, kg ha^-1) is calculated for each metal in each pathway, which is designed to avoid detrimental effects on the HEI (USEPA, 1995). The smallest RPc for any of the investigated pathways becomes the limiting value for a particular metal, and is in turn used to calculate an allowable pollutant concentration (APL, mg kg^-1) in biosolids for each metal. The accumulated APL values represent Table 3 of Part 503.

Pathway 6 (biosolids soil plant animal) is the limiting pathway for Mo. The HEI is a ruminant that develops molybdenosis (a Mo-induced Cu deficiency) as a result of consuming excessive amounts of Mo in the diet. The allowable (RPc) Mo load in Pathway 6 is calculated from an algorithm that includes an uptake coefficient (UC value) representing the ratio of plant Mo (mg Mo kg^-1) to soil Mo (kg Mo ha^-1). Uptake (transfer of soil Mo to plant) is assumed to be linearly related to soil Mo load, and the numerous factors known to affect plant uptake of Mo and utilization of plant Mo by ruminants (Gupta, 1997b; O'Connor and McDowell, 1999) are not directly considered. O'Connor et al. (2001a) recommended several changes to the algorithm, including consideration of typical cattle diets, which vary among regions of the country (Mowrey and Spain, 1999), and with ruminant type and feeding management (Etgen et al., 1987; Ensiminger et al., 1990). O'Connor et al. (2001a) recommended using a diet-weighted UC value that allotted 50% of animal diet to nonlegumes and 50% to legumes. The distinction is important because nonlegumes generally accumulate much less Mo than legumes (e.g., Gupta, 1997b; Johansen et al., 1997; Kabata-Pendias and Pendias, 1991; Vlek and Lindsay, 1977). Recognition of such variations in Mo concentrations among plant species—at the same soil Mo load—form the historic basis (Cameron and Goss, 1948; Ferguson et al., 1943) for management of cattle Mo intake on (known) high soil Mo areas. Ranchers are advised to plant nonaccumulating grasses or grains, rather than accumulators such as legumes.

The UC value database for nonlegumes is relatively rich (including a diverse suite of plant species) and documents minimal Mo accumulation (O'Connor et al., 2001b). The UC value database for legumes, however, is less diverse (three plant species), and is dominated by data from one source (Pierzynski and Jacobs, 1986). These researchers used an industrial sludge containing 1500 mg Mo kg^-1 total Mo, attained soil Mo loads as great as 300 kg Mo ha^-1, and included greenhouse pot data in their extensive study of Mo uptake. Current regulations (USEPA, 1993) disallow land application of biosolids containing >75 mg Mo kg^-1, and the mean concentration of Mo in modern biosolids is 20 to 30 mg Mo kg^-1 (R.B. Brobst, personal communication, 2000). Applying typical modern biosolids at typical loading rates (5 to 10 Mg ha^-1) would require about 1000 yr to attain the maximal loads investigated by Pierzynski and Jacobs (1986). Greenhouse pot studies are recognized to result in much greater plant accumulation of trace elements than measured under field conditions (USEPA, 1992). Thus, although the Pierzynski and Jacobs (1986) data represented an important (and extensive) database in the original risk assessment for Mo in Pathway 6, additional legume-based data are needed to fully assess molybdenosis risk.

McBride et al. (2000) recently reported Mo uptake data for red clover (Trifolium pratense L.) grown in greenhouse columns, and for several other legume forages at field sites. Values of Mo uptake coeffecients for biosolids-amended treatments varied with plant species and with soil pH (affected by biosolids source), and ranged from <1 for field-grown pea (Pisum sativum L.) to >4 for greenhouse-grown red clover. A limited sampling of alfalfa (Medicago sativa L.) grown on biosolids-amended land suggested UC values ranging from about 1.5 to 8.6. The McBride et al. (2000) data reemphasize the potential for problematic Mo concentrations in some legumes, especially at high soil pH.

The objective of our study was to provide additional field data for legume uptake of Mo to improve legume UC value estimation. Data were collected for soybean grain produced on fields amended with high cumulative rates of typical (nonindustrial) biosolids. Soybean was grown in 1998 in soils amended with biosolids 3 to 24 yr earlier. All soil pH values were >6.8, so Mo availability was expected to be high (Gupta, 1997a,b; Pierzynski and Jacobs, 1986; Williams and Gogna, 1981).

	MATERIALS AND METHODS

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

 
The Metropolitan Water Reclamation District of Greater Chicago has applied biosolids to a site in Fulton County, IL for more than 25 yr. The site consists of about 6000 ha, of which approximately 2000 ha are currently developed for biosolids application and crop production. The major soil types of the site are Typic Hapludalfs and Aric Ochraqualfs, but much of the site consists of calcareous strip-mine spoil (mined soil). The biosolids application area is divided into 70 fields averaging about 20 ha in size. Anaerobically digested biosolids were applied to the fields as liquid material (3 to 5% solids) and disk-incorporated from 1972 through 1979. From 1980 through 1988, biosolids were applied as dewatered cake (15 to 30% solids) through side-shoot manure spreaders, with subsequent disk incorporation. Since 1988, biosolids additions have been as surface applications of air-dried material (65% solids), followed by disk incorporation. Historic biosolids Mo concentrations are unknown. Modern biosolids contain about 12 mg Mo kg^-1. Details of the fields and biosolids application methodology are given in Granato et al. (1991). Biosolids application rates to individual fields have varied over the years, and there has been no attempt to equalize biosolids application rates to certain fields. Thus, there are no treatment replicates, per se, and some fields vary in time since their last biosolids applications from 3 to 24 yr (Table 1). The maximum annual biosolids application rate for liquid and dewatered cake biosolids was 56 Mg ha^-1, and 128 Mg ha^-1 for air-dried biosolids, in accordance with permit requirements.

Soil samples archived from a 0- to 15-cm sampling of the fields in 1998 were analyzed for total soil Mo. Typically, about 85 to 90% of soybean root mass occurs in the 0- to 15-cm depth. (Raper and Barber, 1970; Mitchell and Russell, 1971). Each field was divided into halves, and 20 cores taken from each half. Resulting samples from each half-field were then further composited to yield the samples analyzed. Bulk densities of individual fields varied, but averaged about 1.3 g cm^-3. Composited soil samples were air-dried, sieved (<2 mm), and digested according to USEPA Method 3050A (USEPA, 1986). Digests were analyzed for Mo by simultaneous multielement atomic absorption spectrophotometery, with a graphite furnace (PerkinElmer [Norwalk, CT] SIMMA 6000). Quality assurance for Mo analysis included spike (QC 21, 100 µg Mo L^-1; SPEX-Certiprip, Meutchin, NJ) recoveries and analysis of a priority pollutant inorganic soil (TM/CLP, 35 mg Mo kg^-1; Environmental Resource Assoc., Arvada, CO). Spike and certified standard sample recoveries were within 10% of expected values.

Soybean was grown in 29 fields in 1998. This growing season represents the only year in which many of the entire 70 fields (biosolids-amended and controls—little or no amendment) shared a common soybean crop. Different farmers lease different fields and impose different (and incompletely documented) cultural practices. Thus, Agrow 3002, Pioneer STS, and Stein 3264 soybean varieties are represented in our soybean database. Herbicide applications varied with grower: some used glyphosate [N-(phosphonomethyl)glycine] alone; some used glyphosate and 2,4-D (2,4-dichlorophenoxyacetic acid) ester; and some used glyphosate, 2,4-D ester, and sulfentrazone [N-[2,4-dichloro-5-[4-(difluoromethyl)-4,5-dihydro-3-methyl-5-oxo-1H-1,2,4-triazol-1-yl]phenyl]methanesulfonamide]. Some farmers applied P and K fertilizers, but some did not. No attempt has been made to separately identify varietal, herbicidal, or fertilizer effects in our analysis of plant response to biosolids Mo. Rather, we regard the collective data as representative of regional soybean grain production practices.

Samples of grain for Mo analysis were composites of beans collected from each field at harvest. Grain samples were dried at 65°C for 48 h, then ground (20 mesh) in a Wiley mill prior to storage (room temperature) in glass jars with teflon-lined lids. Ground tissue (2 g) was digested in concentrated HNO₃, then evaporated to dryness, and brought to final volume (50 mL) in 1% HCl. Molybdenum and copper in grain digests were analyzed by high resolution inductively coupled plasma atomic emission spectroscopy (Thermo-Jarrell Ash [Franklin, MA] IRIS ICP) Good agreement of <5% relative standard deviation between the two analytical wavelengths of 202.030 nm and 204.598 nm was found for Mo analysis. Excellent recoveries of 94.5% of the 1.46 mg kg^-1 Mo in the certified rice flour SRM 1568a (National Institute of Standards and Technology, Gaithersburg, MD) were obtained. Molybdenum and copper control and spike samples were within 5% of actual values. Detection and practical quantitation limits for Mo were 0.005 mg L^-1 and 0.025 mg L^-1, respectively.

Paired soybean grain Mo concentrations and soil Mo loads (estimated from total soil Mo concentrations) for each field in 1998 were used in a regression analysis computed using SAS (SAS Institute, 1996). The linear regression slopes are defined by the USEPA (USEPA, 1995) as the uptake coefficients (UC values), irrespective of statistical significance. It is within this context, and in accordance with our objectives of improving legume UC value estimation, that the data are discussed.

	RESULTS AND DISCUSSION

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

 
Molybdenum concentrations in composited soybean grain samples from each field are plotted against estimated soil Mo loads in Fig. 1. Soil Mo loads were estimated from total Mo concentrations in composite soil samples taken in the same year (1998) that soybean was grown. Historic biosolids Mo concentrations are unknown, so soil Mo loads could not be estimated from cumulative biosolids loads. Estimates of soil Mo load based on actual soil Mo concentrations are preferred, as estimates based on biosolids loads would be confounded by Mo leaching losses that are likely in these high pH systems (O'Connor et al., 2001a). Soil Mo loads were estimated from the product of soil Mo concentration in the 0- to 15-cm depth samples and the sum of biosolids masses applied to each hectare (Table 1) and the mass of soil in a hectare-15 cm, using the average bulk density of 1.3 g cm^-3 (2240 Mg) as described by Granato et al. (1999). Thus, for Field 1, in which the soil Mo concentration is 4.68 mg Mo kg^-1 and biosolids load (Table 1) is 1546 Mg ha^-1, the estimated soil Mo load (kg ha^-1) is calculated as follows:

View larger version (15K): [in this window] [in a new window]   Fig. 1. Effect of soil Mo loading in biosolids on Mo concentration in soybean grain (all points).

The linear regression of soybean Mo to soil Mo load is significant (P = 0.0014), but accounts for only about 30% of the variability in soybean grain Mo concentration by variations in estimated soil Mo load. Similar regressions of soybean Mo to soil Mo concentrations accounted for about 20% of the variability (data not presented). Undoubtedly, the variability in cultural practices and cultivars grown on different soils by the different lesees over many years contributed to the unexplained variability. Nevertheless, the data set represented in Fig. 1 represents additional field data of legume response to biosolids Mo that can be used to estimate legume UC values needed for risk assessment. Especially significant is the extensive range of soil Mo loads represented, some of which exceed the allowable reference pollutant load (RPc) value of 18 kg Mo ha^-1 originally calculated by the USEPA for Pathway 6 (the limiting pathway for biosolids Mo). Studies conducted with modern biosolids (mean Mo concentrations of 20 to 30 mg Mo kg^-1), applied at agronomic (N-based) rates, would require many decades to attain such high soil Mo loads. The pH values (6.6 to 7.8; Table 1) of spoil materials and "placed" (natural) soils involved in this study also pertain to the situation where Mo bioavailability is greatest (Pierzynski and Jacobs, 1986; O'Connor et al., 2001a), and represent typical agricultural settings for soybean.

The USEPA uses the slopes of the linear regressions of plant Mo to soil Mo as estimates of UC values (USEPA, 1995). Thus, the UC value for soybean grain derived from data in Fig. 1 is 1.66. This value is similar to UC values (1.6 to 1.7) for soybean grain reported by Pierzynski and Jacobs (1986), who used an industrial sludge (1500 mg Mo kg^-1) that resulted in soil Mo loads as great as 141 kg Mo ha^-1 for the soybean grain experiments. O'Connor et al. (2001a) recently suggested a UC value of 4 be used by the USEPA for all fresh legume materials fed to cattle. This conservative value was chosen because of the limited legume UC database. A UC value of 4 appears to greatly overestimate Mo accumulation for soybean grain.

The fields used in this study are unique because of the biosolids Mo loads applied and because the high cumulative loads were achieved with an average of 13 applications spread over 27 yr. Thus, there had probably been sufficient time for the biosolids and soil to reach at least a quasiequilibrium with respect to soil Mo reactions. This is even true for fields amended with >1000 Mg biosolids ha^-1. In these fields, biosolids were applied in 14 to 21 annual applications, and there has been at least 3 yr since the last biosolids application. The high soil Mo loadings observed in this study were produced through applications of a typical municipal biosolids over decades of time.

To examine possible differences in biosolids Mo bioavailability and time of reaction, we separated the data set into "new" and "old" data. "New" data represented grain Mo and soil Mo pairs from fields amended with biosolids <3 yr before soybean was grown (includes fields with 1 Mg ha^-1 biosolids, as controls). "Old" fields had biosolids last applied at least 6 yr before soybean was grown (includes fields with 1 Mg ha^-1 biosolids, as controls). Response curves of plant Mo to soil Mo loads for the new and old data sets are presented in Fig. 2 and 3, respectively. Slopes of linear regressions (UC values) for the "new" data were greater than for the "old" data, but an F test of the slopes was not significant at P = 0.05. Thus, there was no evidence of long-term differences in bioavailability of biosolids Mo to soybean grain associated with time of reaction of biosolids Mo with soil.

View larger version (12K): [in this window] [in a new window]   Fig. 2. Effect of soil Mo loading with biosolids on Mo concentration in soybean grain ("new" points represent fields last treated <3 yr before crop).

View larger version (12K): [in this window] [in a new window]   Fig. 3. Effects of soil Mo loading with biosolids on Mo concentration in soybean grain ("old" points represent fields last treated >6 yr before crop).

Soybean grain Cu, Mo, and Cu to Mo ratio data are given in Table 2, and indicate extremely low Cu to Mo ratios in grain produced from almost all fields. Exceptions are grain produced in the control plots (Fields 18, 24, 29, and 75). Thus, when such soybean grain is part of a cow's diet, other dietary components with higher Cu to Mo ratios (e.g., corn stover or grain, grasses, Cu mineral supplements) should be included. Lactating dairy cows (prime targets for molybdenosis) are typically fed diets containing between 40 and 60% concentrates and the remainder as forage (Ensminger et al., 1990). Concentrates typically consist of 50% grain (e.g., corn or barley), 20% by-product feeds (e.g., whole cotton seeds, beet pulp, and wheat mill run), and 20% protein supplement (e.g., soybean meal, alfalfa), with the remaining 10% being molasses, sodium bicarbonate, mineral and vitamin supplements, and various other ingredients (Ensminger et al., 1990; O'Connor et al., 2001a). Thus, the potential effect of low Cu to Mo ratios of soybean grain is normally minimized by the other dietary components, or can be intentionally minimized by Cu mineral supplements to increase the Cu to Mo ratio of the whole diet to >2:1. Molybdenosis is easily recognized in the early stages by characteristic changes in animal coat color (O'Connor and McDowell, 1999). Farmers, ranchers, and dairymen have long been advised to add Cu mineral supplements to compensate for low dietary Cu availability and to correct Mo problems (Allaway, 1977; Gooneratne et al., 1989).

	SUMMARY AND CONCLUSIONS

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

The resulting UC value for 29 fields, amended over many years at biosolids loads as great as 1500 Mg ha^-1, was 1.66. There was no evidence of long-term differences in Mo phytoavailability associated with time of reaction of biosolids with soil. Our UC value is similar to the values reported by Pierzynski and Jacobs (1986) of 1.6 to 1.7, but is much less than the conservative UC value of 4 recently estimated by O'Connor et al. (2001a) for all fresh legume materials likely to be fed to cattle. A UC value of 4 appears to greatly overestimate Mo accumulation in soybean grain. Nevertheless, soybean grain use in cattle diets should be cautiously noted, as grain Mo concentrations can easily exceed 10 mg Mo kg^-1, and Cu to Mo ratios can be much lower than the recommended minimum of 2:1. Cattle diets can contain 10% soybean meal, and cattlemen should ensure that total cow diets contain typical low-Mo material (e.g., corn grain and stover) and Cu mineral supplements to avoid, or correct, molybdenosis problems.

	ACKNOWLEDGMENTS

 
We express our special appreciation to J.B. Sartain for his statistical assistance and to Angela Choate, Hai Nguyen, and Jack Schroder for their analytical support. The authors also appreciate the support of Richard Pietz, Prakasam Tata, Cecil Lue-Hing, and Richard Lanyon for this work.

	NOTES

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

 
Florida Agric. Exp. Stn. Journal Series no. R-07816.

	REFERENCES

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

 

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