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Department of Plant and Soil Sciences, University of Delaware, Newark, DE 19717-1303
* Corresponding author (ashober{at}udel.edu).
Received for publication December 31, 2002.
ABSTRACT
The application of biosolids (sewage sludge) to agricultural soils provides P in excess of crop needs when applied to meet the N needs of most agronomic crops. These overapplications can result in the buildup of P in soils to values well above those needed for optimum crop yields and also may increase risk of P losses to surface and ground waters. Because of concerns regarding the influence of P on water quality in the USA, many state and federal agencies now recommend or require P-based nutrient management plans for animal manures. Similar actions are now under consideration for the land application of biosolids. We reviewed the literature on this subject and conducted a national survey to determine if states had restrictions on P levels in biosolids-amended soils. The literature review indicates that while the current N-based approach to biosolids management does result in increases of soil P, some properties of biosolids may mitigate the environmental risk to water quality associated with land application of P in biosolids. Results of the survey showed that 24 states have regulations or guidelines that can be imposed to restrict land application of biosolids based on P. Many of these states use numerical thresholds for P in biosolids-amended soils that are based on soil test phosphorus (STP) values that are much greater than the values considered to be agronomically beneficial. We suggest there is the need for a comprehensive environmental risk assessment of biosolids P. If risk assessment suggests the need for regulation of biosolids application, we suggest regulations be based on the P Site Index (PSI), which is the method being used by most states for animal manure management.
Abbreviations: BPR, biological phosphorus removal • FeO-P, iron oxide strip–extractable phosphorus • PSI, P Site Index • STP, soil test phosphorus • TSP, triple superphosphate • WSP, water-soluble phosphorus • WWTP, wastewater treatment plant
NONPOINT-SOURCE POLLUTION of surface waters by agricultural P is a major environmental concern in many areas of the USA (Vanden Bossche et al., 2000; Parry, 1998; Sharpley et al., 2000; United States Geological Survey, 1999; USEPA, 2000; Withers et al., 2000). Many of the most serious concerns with nonpoint P pollution are found in areas of intensive animal production, where farm- and watershed-scale P surpluses commonly occur (Kellogg et al., 2000). Consequently, a number of U.S. states have passed laws or established guidelines restricting the application of P in animal manures and/or fertilizers, such as those in Delaware (1999), Maryland (1998), and Virginia (1999) that restrict manure P applications and require some form of "P-based" nutrient management when STP exceeds a certain value (Coale et al., 2002; Sims, 1999; Sims et al., 2002). Of considerable importance to municipalities in the Mid-Atlantic region of the USA is the fact that the Maryland regulations also apply to land application of municipal biosolids (sewage sludge). Changes in the approach to P management for organic by-products have also occurred at the national level. For example, to receive financial assistance from the USDA Natural Resources Conservation Service (NRCS), all lands receiving soil amendments are required to implement a nutrient management plan in accordance with the NRCS Code 590 standard. Code 590 requires adoption of P-based manure management plans in fields with high or very high soil test P ratings, or when soil test P equals or exceeds threshold levels, or when a PSI assessment (Lemunyon and Gilbert, 1993) indicates a high risk of P loss to water (USDA Natural Resources Conservation Service, 2002). Additionally, the USEPA has recently promulgated new regulations for concentrated animal feeding operations (CAFOs) that will require some form of P-based management for the land application of manures and wastewaters (USEPA, 2003).
The widespread changes in P management for animal manures have brought attention to the need for similar approaches for the land application of biosolids, as was done in Maryland due to pressure from the agricultural community for equal regulation of agricultural and municipal organic by-products (Simpson, 1998). Nationally, agronomic application of biosolids represents a secondary, but still significant, input of P to soils when compared with manures and inorganic P fertilizers. Wright et al. (1998) reported that approximately 2.3 million Mg of manure P are generated annually in the USA and that 1.6 million Mg of fertilizer P are applied annually. In comparison, Millner et al. (1998) estimated that 0.15 million Mg of biosolids P are generated in the USA each year. The Federal biosolids regulations (40 CFR Part 503) promulgated by the USEPA in 1993 do not directly limit the amount of biosolids P that can be land-applied (USEPA, 1993). Instead, the Part 503 rule follows the long-term approach used with animal manures, requiring that biosolids and wastewaters be applied at a rate that is equal to or less than the agronomic N rate for the crops to be grown. At the time the Part 503 regulations were developed, there was limited information available on nonpoint-source pollution of surface waters by P in biosolids and biosolids-amended soils. The omission of P from the Part 503 regulations stemmed from this lack of information and the belief that N, not P, was the nutrient of greatest environmental concern in most regions of the USA. Phosphorus was considered to be less of an issue because it was believed that best management practices for erosion control required by the USEPA would minimize the effects of P on surface water quality (Alan Rubin, USEPA, personal communication, 2002).
We believe that the emerging question about the need for a more regulatory approach to biosolids P management is an important environmental issue in the USA today. Specifically, will application of biosolids in accordance with current N-based regulations increase the risk of P loss to water sufficiently to justify the adoption of similar approaches to biosolids P management as are now being required for animal manures? Or, are there fundamental differences in the forms of soil P or the physical properties of biosolids-amended soils that mitigate the risk of P loss and require a different approach to P management than is needed for manures and fertilizers? Consequently, our objectives in this paper are to (i) provide an overview of the current issues that should be considered as we evaluate the need for P-based management of biosolids and (ii) summarize and critically analyze, based on a national survey we conducted, the current approaches used by U.S. states to control land application of biosolids based on P.
NATURE OF THE BIOSOLIDS PHOSPHORUS ENVIRONMENTAL ISSUE
Previous research suggests that some of the factors that lead to the more restrictive approaches now used for animal manure P also apply to biosolids. For instance, as with manures, N-based biosolids applications add more P to soils than is removed in crop harvest. Stehouwer et al. (2000) reported that biosolids applied to meet the N requirements for corn (Zea mays L.) added 93 to 294 kg P ha-1, much more than is removed in harvested corn grain (approximately 25 kg P ha-1). Phosphorus removal in the harvested portion of most other agronomic crops is also usually lower than the amount added in biosolids, ranging at typical yields for 10 major crops from 10 to 71 kg P ha-1 (average = 28 kg P ha-1; Pierzynski and Logan, 1993). This planned overapplication of biosolids P increases the concentrations of most forms of soil P, which has been shown in research with manures to increase the risk of P loss to surface and shallow ground waters (Sharpley, 2000; Tunney et al., 1997). Chang et al. (1983) reported that five continuous years of biosolids compost applications at 22.5, 45, or 90 Mg ha-1 (total P added in the five years was 1650–6582 kg P ha-1) to two California soils increased soil total P (0–15 cm) from initial values of 515 to 540 mg kg-1, to 1092 to 1312, 1657 to 2163, and 2617 to 3470 mg kg-1, respectively. Maguire et al. (2000b) conducted an on-farm survey of biosolids use in the Mid-Atlantic USA, where biosolids applications to meet crop N needs are usually made at two- to three-year intervals. They found that concentrations of total soil P (0–20 cm) in biosolids-amended soils (738 mg kg-1) were nearly double the values in soils from unamended setback areas (403 mg kg-1). Increases in bioavailable1 forms of soil P (e.g., STP, water-soluble phosphorus [WSP], and iron oxide strip–extractable phosphorus [FeO-P]) from biosolids applications have also been shown. In a study of the effects of applying biosolids at an N-based rate (mean P addition per application of 197 kg P ha-1) on the extractability of P in 11 Mid-Atlantic soils (seven Ultisols, two Entisols, and two Alfisols), Maguire et al. (2000a) found that average concentrations of WSP, FeO-P, STP (Mehlich 1), and ammonium oxalate–extractable P were higher in biosolids-amended soils (0–20 cm; 7.4, 54.4, 106, and 589 mg kg-1) than in unamended setback areas (4.9, 34.0, 80, and 296 mg kg-1). The degree of P saturation was also higher in soils receiving biosolids (50%) than unamended soils (44%). Reported environmental threshold values for Mehlich-1 P and degree of P saturation are 75 mg kg-1 and 20 to 30% (Breeuwsma et al., 1995; Sims et al., 2002).
There can be advantages to the increases in bioavailable P in biosolids-amended soils, such as improved plant growth as soil P deficiencies are corrected, and disadvantages, such as an increased potential for the loss of WSP and soil particles that are enriched in bioavailable P. Most research shows that, although STP usually increases when biosolids are applied, they are often less effective sources of bioavailable P than fertilizers and that plant availability of P in biosolids varies with wastewater treatment plant (WWTP) processes (Cavallaro et al., 1993; DeHaan, 1980; McLaughlin and Champion, 1987; McCoy et al., 1986; Peterson et al., 1994; Wen et al., 1997). Kelling et al. (1977) conducted a three-year field study of the N and P value of anaerobically digested liquid biosolids as a soil amendment for corn, rye (Secale cereale L.), and sorghum–sudan (Sorghum bicolor L. Moench x S. sudanese P. Stapf). Biosolids increased crop yields and P concentration and uptake for rye and sorghum–sudan in all years; for corn, biosolids increased P uptake, but not P concentrations. Crop recoveries of biosolids P were from 1 to 5%. At optimum rates for crop production (7.5–15 Mg ha-1, dry weight basis), STP (Bray P1) 26 mo after application had increased from 24 (no biosolids) to 35 to 55 mg kg-1 in a silt loam soil (0–15 cm) and from 39 (no biosolids) to 69 to 86 mg kg-1 in a sandy loam soil. Soil test P at the highest biosolids rate (60 Mg ha-1) had increased to 129 to 135 mg kg-1. Economically optimum Bray P1 values range from 25 to 30 mg kg-1. Frossard et al. (1996) compared P uptake by ryegrass (Lolium perenne L.) grown in two French soils amended with fertilizer P and four types of biosolids (primary; aerobically digested flocculated with FeSO4 and an organo–cationic polymer; and two aerobically digested biosolids treated with FeSO4). Plant P concentrations were 0.22 to 0.26% with the unamended soils, 0.35 to 0.36% with the fertilized soils, and 0.29 to 0.36% in biosolids-amended soils. Lowest P availability was found with biosolids produced using FeSO4. Corey (1992) evaluated the effect of the (Al + Fe) to P ratio in biosolids on P uptake by soybean (Glycine spp.) relative to mineral forms of Ca-P, Al-P, and Fe-P. He found that as the (Al + Fe) to P ratio increased, there was a trend for decreased biological availability of P, as indicated by lower plant P concentrations.
The risk of P loss to water with biosolids relative to manures and fertilizer P has also been investigated, either by measuring changes in soil P or by directly investigating P losses by erosion, runoff, or leaching. Some studies have found lower risks for P loss when biosolids are applied, at least in the short-term, due to the use of chemical amendments (e.g., alum, Fe-salts) added at some WWTPs (Elliott et al., 2002; Maguire et al., 2001; Penn and Sims, 2002; Withers et al., 2001). Kyle and McClintock (1995) found that the addition of Fe and Al to biosolids decreased P solubility in an Inceptisol compared with biosolids generated by a biological phosphorus removal (BPR) process. They reported leachate P concentrations of 0.13, 0.23, 0.22, 0.62, and 1.38 mg L-1 for the unamended soil and soils amended with digested Al biosolids, digested Fe biosolids, digested BPR biosolids, and digested untreated biosolids, respectively. Maguire et al. (2001) found that the concentrations of WSP, FeO-P, and Mehlich-1 P were lowest in soils receiving biosolids (0–20 cm) amended with Fe or Al salts followed by biosolids treated with Al or Fe salts and lime, with the highest P concentrations in soils receiving biosolids treated without lime, Al, or Fe salts. Jokinen (1990) reported that biosolids treated with Al salts had lower concentrations of extractable P than biosolids treated with Fe and Al salts, Ca (lime), and Fe and lime, although results varied somewhat with soil type.
Withers et al. (2001) measured P in runoff from Alfisols in the United Kingdom that received surface applications of triple superphosphate (TSP), liquid cattle manure, liquid digested biosolids, dewatered biosolids cake, and no treatment under field conditions. Addition of all P sources increased dissolved unreactive P and in runoff when compared with no treatment with the largest increases occurring in the first runoff event after amendment addition. Release of P in runoff was related to the amount of P extracted from the different amendments by NaHCO3 or H2O, with the highest P solubility found in TSP and lowest P solubility found in biosolids. Based on total P applied to the sites, the risk of P transfer to surface waters was reported to be less for biosolids-amended soils than for soils that received manure or TSP. This study also showed that risk of P loss was greatest just after application and decreased with time, suggesting that measures to reduce P loss (i.e., erosion control) are most beneficial immediately after application. Penn and Sims (2002) conducted a runoff study using two Ultisols with "medium" (21 mg kg-1) and "excessive" (124 mg kg-1) STP (Mehlich 1) concentrations that were amended with eight biosolids and poultry litter. They found that soils receiving BPR or Fe–Lime biosolids (0–5 cm) had the largest increases in bioavailable P (Mehlich-1 P, Mehlich-3 P, FeO-P, and WSP) compared with unamended soils, while soils receiving Fe-biosolids had the smallest increases. Concentrations of dissolved reactive P and FeO-P in runoff were highest for soils amended with BPR biosolids and decreased in the following order: BPR > Fe–lime > no Fe–no lime > poultry litter > Fe–no lime.
Rydin and Otabbong (1997) conducted a laboratory study with Al or Fe stabilized biosolids from WWTPs in Sweden and three soils (sandy clay loam, sandy loam, and sandy clay). They measured P release in small columns leached with simulated rainfall (pH 5.0). Their results showed that 20 to 40% of the biosolids P was considered to be mobile, as measured by loss in leaching from the columns, and that soils amended with Al-biosolids had higher P losses (37%) than those treated with Fe-biosolids (20%). Elliott et al. (2002) assessed P leaching from Florida sandy soils using repacked soil columns and the A horizon of an Immokalee soil (sandy, siliceous, hyperthermic Arenic Alaquods; low P-sorption capacity) or a Candler soil (hyperthermic, uncoated Typic Quartzipsamments; moderate P-sorption capacity) placed over 28 cm of Myakka E horizon (sandy, siliceous, hyperthermic Aeric Alaquods; negligible P-sorption capacity). Soils were amended with eight different biosolids, chicken manure, and TSP at P-based (56 kg P ha-1) and N-based (224 kg P ha-1) application rates. Biosolids represented a variety of treatment processes including BPR, BPR and alum [Al2(SO4)3], activated biosolids with Fe salts, and activated biosolids with codisposal of water treatment residuals. Leachate P concentrations from Immokalee soils amended with BPR biosolids (no Fe salts) and TSP were significantly higher than from unamended soils, representing a worst-case scenario for P leaching. Phosphorus losses from the Candler soil were significant only for the high rate of TSP (P loss 1.7–21.7%) compared with other treatments and control. Shepherd and Withers (2001) conducted a study to determine if regular application of biosolids increased the risk of P leaching from sandy soils in the United Kingdom. Liquid digested biosolids were added (60 and 240 kg P ha-1 rates) to loamy sand and sandy loam soils in 12 monolith lysimeters with no crop cover. Surface soil (20 cm) was removed from the lysimeter and mixed with biosolids to simulate injection. There were no reported treatment effects on losses of molybdate-reactive P and total P from both soils and no effects on total dissolved P losses from the sandy loam soil. There was, however, a small but significant effect of biosolids treatment on losses of total dissolved P from the loamy sand soil with the soil receiving the high biosolids rate losing the most total dissolved P.
The application of biosolids to soils, as with manures, adds a significant amount of organic matter to the soil, which tends to improve infiltration and reduce erosion, hence reducing runoff volume and sediment load. Research has shown that, while biosolids application can lead to increases in the concentration of dissolved forms of P in runoff it can also reduce runoff volume and sediment load (Diezman et al., 1989; Vanden Bossche et al., 2000; Bundy et al., 2001; Harris-Pierce et al., 1995). Harris-Pierce et al. (1995) reported that surface application of biosolids decreased runoff in semiarid grasslands due to the increased surface roughness from the physical presence of the biosolids on the soil surface. Bundy et al. (2001) reported that sediment load and concentration in runoff were significantly lower in biosolids and manure treatments when compared with control. This was due to the physical properties of the organic matter in the amendments that increased infiltration and reduced runoff. Vanden Bossche et al. (2000) indicated that application of liquid biosolids could also reduce runoff and sediment load leading to a decrease in total P exported from the biosolids-treated soil when compared with control. This was attributed to the formation of a film over existing soil aggregates by the liquid biosolids.
Other research has shown that tillage and biosolids application methods can have an effect on soil physical properties and P losses in runoff. Diezman et al. (1989) found that surface application of biosolids to conventional till plots lead to 25% reduction in runoff volume and significantly less sediment loss when compared with incorporated biosolids. Application of biosolids reduced sediment yield and runoff in both no-till and conventional tillage (surface-applied and incorporated) systems when compared with control. Again the authors attributed these results to improvement of soil physical properties from addition of organic matter in the biosolids. It has also been shown that incorporating biosolids into soils decreases soluble P losses in runoff relative to surface application (Withers et al., 2001). Improvement of soil physical properties by addition of biosolids may not warrant that biosolids be regulated differently than manures, which ultimately have the same effect on soil due to organic matter composition (McDowell and Sharpley, 2003; Gilley and Risse, 2000). It does, however, suggest that organic P amendments should be treated differently than inorganic P sources when assessing the potential risk of P loss to water.
CURRENT STATUS OF PHOSPHORUS-BASED BIOSOLIDS MANAGEMENT IN THE USA: RESULTS OF A NATIONAL STUDY
Given the emerging interest and growing body of research on the potential environmental effect of P from the land application of biosolids, we conducted a national survey in 2002 to determine which U.S. states have already implemented, or are considering, restrictions on the land application of biosolids based on concerns about the environmental effects of P. Biosolids coordinators associated with the agency responsible for the regulation of land application of biosolids in each state and U.S. territory were contacted and asked to answer a survey indicating soil or biosolids monitoring requirements, land application siting and management restrictions, and state biosolids P research (Table 1). Biosolids coordinators were asked to answer the questions to the best of their ability or to refer the survey to individuals from other state agencies or land-grant universities who could provide more information on biosolids P management.
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All 13 states that have numerical criteria for STP require biosolids and soils to be analyzed for P (Fig. 2) . Ten of the other 11 states with regulations or guidelines that can restrict biosolids application based on P require that all types of biosolids be analyzed for total P. Mississippi requires that all composts be analyzed for total P with no requirement for monitoring of noncomposted biosolids. In addition, eight of these 11 states require monitoring of STP concentrations in soils at sites where biosolids are land-applied, and Florida requires soil testing for P in designated areas where P applications are restricted (Fig. 2). Of the remaining states that do not include P restrictions in their guidelines, regulations, or legislation, 15 states require that biosolids and/or soils be analyzed for P (Table 1). Of these 15 states, 11 require that biosolids and soils be analyzed, three only require biosolids analyses, and one only requires soil testing. Overall, of all 51 respondents to our survey, 30 require biosolids and soils monitoring, six require biosolids monitoring only, one requires soil monitoring only, and 12 do not require any monitoring of biosolids or soils for P (Fig. 2).
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Ten states (20% of respondents) indicated they are conducting research or know of someone in their state who is conducting research on the topic of P loss at sites where biosolids are land-applied. The states that are involved in this type of research include: Delaware, Florida, Maryland, Michigan, Minnesota, New Hampshire, Oregon, Pennsylvania, Virginia, and Wisconsin. We know from personal communications with colleagues at universities and government research agencies that some states were erroneously omitted from this category. This probably occurred because the biosolids coordinator for that state was unaware of ongoing or previously published biosolids research specific to their state. This is evidence of an information gap between state agencies and research institutions on this subject and suggests the need for greater communication between those involved in research, management, and regulation of biosolids with respect to P.
In summary, the national biosolids survey we conducted indicates that almost one-half of U.S. states (47% of the 51 respondents) have established regulations, guidelines, or legislation that can be used to limit land application of biosolids based on some measure of soil or biosolids P. However, only 13 states have established numeric limits for maximum P concentrations in soils. For most of these states, application of biosolids must cease when these numerical limits on STP are exceeded. The remaining states that address P restrictions have an allowance in their regulations or guidelines to determine the maximum amount of P loading. A few of these states, such as Indiana, Oklahoma, and New Jersey, have language in their regulations that directly specifies that P limits could be implemented; however, the current regulatory focus is on meeting the agronomic needs of the crops as opposed to limiting P loadings. Almost 65% of the survey respondents (33 states) require biosolids to be analyzed for P if they are going to be land-applied, and almost 55% of the survey respondents (28 states) require soils at land application sites to be tested for P.
PHOSPHORUS-BASED NUTRIENT MANAGEMENT PLANNING FOR BIOSOLIDS: FUTURE DIRECTIONS
The advent of laws, regulations, and guidelines on the management of P in animal manures in the USA has raised the question about the need for similar actions with biosolids. In keeping with U.S. environmental policy, such regulations would ideally be based on a comprehensive body of research that emphasizes an understanding of the basic principles involved and also includes multisite, multiyear field studies. Unfortunately, at this point in time, there is a rather limited, somewhat contradictory body of research on the fate in soils and loss to water of biosolids P. Some of the research cited above suggests that the reasons given for the increased regulation of animal manures based on P also apply to biosolids. The most direct similarity between manures and biosolids is the buildup of soil P to values above those needed for crop production when an N-based approach is used to determine land application rates. Other research, however, suggests that P in biosolids may be less of a risk to water quality than P in manures and fertilizers, usually because of the effects of WWTP on P solubility in biosolids.
There are several significant consequences of adopting across the board P-based management for biosolids as has already been done by a number of U.S. states (Fig. 2; Table 3). First, regulation of biosolids applications based on P using an environmental or agronomic STP threshold will drastically increase the amount of land necessary to apply the same amount of biosolids produced by a WWTP when compared with application based on the appropriate agronomic N rate. Increases in the amount of land required will directly increase the costs associated with biosolids application and transportation. Additionally, in some cases, P-based biosolids management will result in the application of less biosolids N than is needed to meet crop N requirements, or no biosolids N at all. This increases the likelihood that additional chemical N fertilizers must be applied, costs that will need to be borne by someone, be it the farmer, the municipality, or the responsible state agency. Also, the alternatives to land application of biosolids as beneficial soil amendments are extremely limited (e.g., incineration, landfilling) and often very unpopular. Finally, once states have incorporated numerical STP threshold values into their regulations, it is extremely difficult to have them removed or even replaced with a different approach to identify the situations where P-based management of biosolids should be practiced.
Given the changes and concerns discussed above, we believe that there is a need for a thorough, carefully conducted risk assessment before more widespread implementation of regulations limiting biosolids application based on the potential environmental effects of P on water quality. The overall goal of this risk assessment would be to determine if it is environmentally beneficial and economically feasible to shift to some form of P-based biosolids management, as opposed to the current practice (N-based agronomic rates). To be most effective, this risk assessment should be conducted at the national level and led by USEPA, which has the overall responsibility for the land application of biosolids in the USA. Should this risk assessment indicate the need for P-based management for biosolids, we suggest use of the PSI approach, now widely used in the USA for manures and fertilizers to identify situations where such management should be required. One specific area that should be addressed in the risk assessment, and in the development of a PSI for biosolids, would be the need to include the WWTP process used to generate the biosolids in any regulations or guidelines, given past research suggesting that biosolids produced from processes using metal salts may have lower risks of P loss. For example, P source coefficients (also referred to as P availability coefficients) have been suggested in some PSI as a means to quantify the relative potential for P loss to water due to the physicochemical properties of different organic P sources including biosolids (Coale, 2000; Leytem et al., 2003). The use of P source coefficients is currently being researched by several states and has already been incorporated into the Pennsylvania PSI (Pasture Systems and Watershed Management Research Laboratory, 2003). Another issue is the need for a consistent national approach to determine plant-available P in biosolids, should an agronomic need for P exist. Plant availability of biosolids is usually estimated to be approximately 50% but, as indicated by the research discussed earlier, this can vary as a function of biosolids type and WWTP process (Evanylo, 1999).
ACKNOWLEDGMENTS
The authors would like to thank Cynthia Greene for her work on the national survey in 1998 for the Delaware Water Resources Center, Alan Rubin from the USEPA for his knowledge and insight on the Part 503 regulations, and the state biosolids coordinators who participated in the study and provided valuable information regarding their biosolids programs.
NOTES
Paper no. 03-01-1737 in the journal series of the Delaware Agricultural Experiment Station.
1 Forms of P in soils or eroded sediments that are available for uptake by terrestrial plants or aquatic organisms. 
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