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a Dep. of Veterinary Clinical Science, Purdue Univ., West Lafayette, IN 47907
b Dep. of Animal Science, Purdue Univ., West Lafayette, IN 47907
* Corresponding author (bjoern{at}purdue.edu)
Received for publication March 13, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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= 0.05) decreased fecal TP 19, 17, and 40%, respectively, compared with the control. Dissolved reactive P was 36% lower in the HAP + PHY diet compared with the other diets. Relative fractions (percent of TP) of DRP, DOP, ASOP, and PAP in slurry generally decreased with storage time up to 150 d, with the largest decreases occurring within 60 to 90 d. Diet-induced differences in relative fractions of DRP, DOP, ASRP, and PAP were significant when averaged across storage times, simulating a mixed-age slurry. Relative fractions of DRP in simulated mixed-age slurries were higher in HAP and HAP + PHY diets, indicating that diet may affect P losses under certain P-based application scenarios.
Abbreviations: ASOP, acid-soluble organic phosphorus • ASRP, acid-soluble reactive phosphorus • DM, dry matter • DOP, dissolved organic phosphorus • DRP, dissolved molybdate-reactive phosphorus • HAP, corn–soybean diet formulated with high-available-phosphorus corn • HAP + PHY, corn–soybean diet formulated with high-available-phosphorus corn and 600 phytase units kg-1 • PAP, phytate phosphorus • PHY, corn–soybean diet formulated with 600 phytase units kg-1, TP, total phosphorus
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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The high P content of pig manure is due to both dietary and physiological factors. Most pigs in the Midwestern USA are fed diets consisting of corn (Zea mays L.) and soybean [Glycine max (L.) Merr.] meal. Myo-inositol hexakisphosphate (phytate) is the major form of P in corn and soybean meal (Jongbloed and Kemme, 1990; Kasim and Edwards, 1998) and pigs do not have sufficient amounts of the phytase enzyme in their upper digestive tract to efficiently utilize P in this form (Pointillart, 1993; Jongbloed et al., 1992; Yi and Kornegay, 1996). Because of low phytate utilization, pig diets are often supplemented with inorganic P. While this practice is effective at meeting P needs, it further increases the P content of manure. Barnett (1994) reported that total P levels in pig manures collected from 16 herds were higher (19.7–40.0 g kg-1) than previously reported values (11.0 g kg-1, Peperzak et al., 1959; 14.8–18.0 g kg-1, Gerritse and Zugec, 1977), and concluded that this was probably due to increased use of inorganic P supplements.
Two products for meeting the P needs of swine without supplementing inorganic P are microbial phytase and high-available-P (HAP, also termed low-phytate) corn. Microbial phytase derived from the fungus Asperigillus niger catalyzes the hydrolysis of phytate in the upper digestive tract, making orthophosphate available for uptake. Phytase has been shown to be an effective way to improve P absorption and reduce P excretion in pigs (Jongbloed et al., 1992; Lei et al., 1993a,b; Cromwell et al., 1993, 1995). These studies show 25 to 30% increases in P utilization and up to 40% decreases in P excretion (depending on animal size and the amount of phytase added to the diet). A more recent approach to improving P utilization in livestock is replacing conventional corn with HAP corn in diets. High-available-P corn containing the lpa1-1 mutation has the same total P content as normal corn, but contains 50 to 75% less phytate (Raboy et al., 1990; Cromwell et al., 1998). Though not yet commercially available, HAP corn has promise for further reducing livestock P excretion. Diets formulated with HAP corn for pigs and chicks (Gallus gallus domesticus) have shown improved P utilization and decreased P excretion compared with diets formulated with conventional corn (Spencer et al., 2000; Ertl et al., 1998). Spencer et al. (2000) reported that young pigs fed HAP corn diets without supplemental inorganic P excreted 37% less P than pigs fed normal corn diets with supplemental inorganic P and 25% less P than pigs fed normal corn diets without inorganic P. They also reported similar P bioavailability among HAP corn diets and normal corn diets supplemented with inorganic P. Sands et al. (2001) showed that using HAP corn in pig diets improved P bioavailability and nutrient balance when compared with conventional corn. They also showed that when phytase was added to HAP corn diets, P digestibility was further increased.
The fact that HAP corn and phytase increase P digestibility and reduce total P excretion by pigs is well documented. However, there is little information on the effects of these diet modifications on the concentrations and forms of P in manure. While total P application to soils is a major environmental concern with manure and undoubtedly contributes to soil P loading, the forms of P present in manure may affect the short-term potential for P loss to surface waters via runoff or leaching.
Characterization of manure P traditionally has been performed by fractionation techniques that separate P into increasingly less soluble forms (Barnett, 1994; McAuliffe and Peech, 1949; Peperzak et al., 1959). Modifications of the sequential fractionation technique developed by Hedley et al. (1982) for use in soils have also been used to characterize the forms and availability of P in manures (Leinweber et al., 1997; Sharpley and Moyer, 2000; Dou et al., 2000; He and Honeycutt, 2001). Results from these studies indicate that total P, inorganic P, and organic P in manure varies widely by animal type and diet. Changes in the relative amounts of inorganic P and organic P in manures with storage have not been widely reported in literature. Gerritse and Zugec (1977) used 32P radioisotope techniques to measure P cycling in stored pig slurries and concluded that added inorganic P completely cycled through measured inorganic and organic P fractions within 10 to 20 wk.
While soil P fractionation can be related to plant availability and biogeochemical P cycling (Cross and Schlesinger, 1995), the usefulness of sequential fractionation techniques for estimating the potential for P losses from manure has not been clearly demonstrated. Sharpley and Moyer (2000) reported strong correlations between the water-extractable inorganic P and organic P fraction from dairy and poultry manure and the amount of inorganic P and organic P leached when subjected to simulated rainfall, but did not find highly significant correlations with other manure P fractions estimated by the Hedley procedure.
Dou et al. (2000) evaluated the use of the Hedley sequential fractionation procedure on dairy and poultry manures by investigating extraction times and relative strength of the various extractants. They found that water or bicarbonate extracted the majority of P from manure, and suggested a single water extraction to estimate P vulnerable for environmental losses. They also reported that 84 to 97% of total P was removed through repeated independent extraction with 5% trichloroacetic acid (TCA) or 1 M HCl and that the first extraction removed 94% of the cumulative total P removed by the repeated extractions. The acid-soluble P fraction is considered a potential source of P for plants, and may include Ca phosphates and hydrolyzable organic P forms such as phytate. Phytate P may be relatively unavailable in soils with high P sorption capacities, but can represent a significant source of P in soils with low P sorption capacities (Martin and Cartwright, 1971). Diet modifications like phytase and HAP corn alter the digestibility and forms of P present in feeds, and may affect the quantity and forms of P present in manure. These changes in manure P forms may affect the potential for P transport offsite.
Our objectives were to determine the effect of growing pig diets formulated with normal and HAP corn with and without phytase supplements on the relative contents of total phosphorus (TP), dissolved molybdate-reactive phosphorus (DRP), dissolved organic phosphorus (DOP), acid-soluble reactive phosphorus (ASRP), acid-soluble organic phosphorus (ASOP), and phytate phosphorus (PAP) in fresh excreta and evaluate changes in the relative contents of these P pools when stored up to 150 d as slurry. We also compared diet effects in slurries averaged across storage times to simulate a mixed-age slurry that may be more indicative of an actual storage pit. Detailed information relative to the effect of these diets on growth performance, P bioavailability, and nutrient balance in pigs is presented elsewhere (Sands et al., 2001).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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Complete diet formulations including analyzed digestible energy (DE), protein, calcium, TP, PAP, and nonphytate P are presented in Table 1 . Gross energy of diets and feces used to calculate DE was determined by adiabatic bomb calorimetry (Adeola and Bajjalieh, 1997). Protein (based on total N) and Ca were determined as described by Sands et al. (2001). Total P and PAP analyses of feeds are described below. Nonphytate P was determined as the difference between TP and PAP.
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Slurry Storage Experiment
From each composite sample, five subsamples of wet feces (approximately 50 g) were placed into 220-mL wide-mouth jars and deionized water was added to make a final volume of approximately 200 mL. The volume in the jars was not made up with urine because (i) urine samples were collected into a formaldehyde solution that would inhibit microbial growth and (ii) urine P made up less than 0.5% of the TP excreted. In total, 120 individual slurry samples (24 pigs x 5 sample times) were used in the experiment, with pigs being the experimental unit. Because the storage experiment was conducted immediately after homogenizing the samples, the actual mass of solids (dry weight) added to each jar was unknown at the time the experiment was set up and some variation occurred in the solids content among slurries from different pigs. Following moisture analyses of the fresh feces by lyophilization, it was determined that solids content among the slurry samples ranged from 10 to 15%. Slurry samples were mixed thoroughly, loosely capped, and randomly placed on shelves in a dark room maintained at 21 ± 5°C. Deionized water was added periodically to maintain a volume near 200 mL throughout the incubation periods. After 30, 60, 90, 120, and 150 d of storage, one jar of slurry from each pig was transferred to a 300-mL plastic container, frozen, lyophilized, and ground to pass a 1-mm sieve. Dry matter (DM) remaining after storage was calculated from the mass of solids after lyophilization relative to the mass of solids added to the jar at the start of incubation.
Analysis of Feeds, Feces, and Urine
Moist (as fed) feeds and lyophilized fresh fecal samples were ground to pass a 1-mm sieve. All chemical analyses were performed in triplicate on feeds, and in duplicate on urine and lyophilized fecal and slurry samples. All P analyses were made by the ascorbic acid–molybdate method of Murphy and Riley (1962). Total phosphorus (TP) in the feeds and feces was determined after wet-ashing samples (0.25 g feed, 0.2 g feces) in 5 mL of 18 M H2SO4 at 200°C with additions of 30% H2O2 until the solution was clear, diluted to 50 mL, and adjusted to pH = 6 before analysis. Urine TP was determined by evaporating 35 mL of urine to dryness, adding 5 mL of 16 M HNO3, heating at 140°C with additions of 30% H2O2 until the solution was clear, and adjusting to pH = 6 before analysis. Dissolved P was extracted by adding 0.25 g of feces to 50-mL high-speed centrifuge tubes, to which 25 mL deionized water and 0.1 mL chloroform (to suppress microbial activity) was added. The tubes were placed on a mechanical inline shaker for 24 h at 120 excursions per minute (epm) and centrifuged at 19800 x g for 15 min and the supernatant was immediately filtered through Fisherbrand P-5 filter paper to remove large floating particles. Centrifugation was used instead of 0.45-µm filtration because in preliminary work we found no detectable differences in inorganic and organic P levels due to filtration method in either water or acid extracts (data not presented).
Dissolved molybdate-reactive phosphorus (DRP) was determined directly in the filtered extracts. Dissolved total phosphorus (DTP) was determined after digesting 5-mL aliquots of the extract using the same method as for TP. Dissolved organic phosphorus (DOP) was calculated as the difference between DTP and DRP. A 1 M HCl extraction, similar to the method used by Chae and Tabatabai (1981) for determination of inorganic P in sewage sludges, was used to determine acid-soluble P in feces and stored slurry. Samples (0.2 g) were placed into 50-mL polypropylene screw-top centrifuge tubes to which 25 mL of 1 M HCl was added. Samples were shaken for 1 h at 120 epm, centrifuged, and filtered as described previously. Acid-soluble reactive phosphorus (ASRP) was determined directly in the filtered extracts. Acid-soluble total phosphorus (ASTP) was determined following digestion of 5-mL aliquots of extract using the same method as for TP. Acid-soluble organic phosphorus (ASOP) was calculated as the difference between ASTP and ASRP.
Phytate phosphorus (PAP) in feeds and feces was determined by the ferric-precipitate method used by de Boland et al. (1975) as modified by Raboy et al. (1984). This method was used to provide a general estimate of phytate present in feeds and feces, even though the precipitate may not be entirely specific for phytate at low concentrations (Peperzak et al., 1959). We chose this method because it requires a minimal amount of laboratory equipment and can be performed at a relatively low cost.
Statistical Analysis
All replicated analyses that did not agree within 10% were repeated. Manure and urine nutrient content data were analyzed as a randomized complete block design using the ANOVA procedure of SAS Institute (1989) with pigs as the experimental unit. A similar approach was used with the storage experiment data to determine the significance of the main effects, diet and storage time, with storage time included as a split plot treatment. Diet and storage time main effects were tested with combined error terms if error variances were homogeneous. Duncan's multiple range test was used to determine significant ( = 0.05) differences among diet means for fresh fecal and urine samples and among slurry samples averaged across storage times (Montgomery, 1997).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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Mean concentration of ASRP ranged from 11.7 to 23.5 g kg-1 DM and followed similar trends to the TP data. Compared with fecal DM from pigs fed the control diet, ASRP concentrations were 25, 29, and 50% lower from the PHY, HAP, and HAP + PHY diets, respectively. Acid-soluble organic P represented 7 to 8% of the total acid soluble P and was not significantly different among the diets. Because we used a single extraction with 1 M HCl, it is important to note that ASRP or ASOP determined in this study are not directly comparable with acid-soluble P fractions determined by sequential fractionation such as those reported by Barnett (1994), He and Honeycutt (2001), Leinweber et al. (1997), and Sharpley and Moyer (2000). The ASRP and ASOP pools we discuss include the less soluble forms that are removed before acid extraction in sequential procedures, and represent a composite of water- and/or bicarbonate-soluble, NaOH-soluble, and acid (HCl or H2SO4)-soluble P fractions discussed by the above-mentioned authors.
Phytate P ranged from 0.68 to 3.87 g kg-1 and was significantly greater in the control diet than all other diets (Table 2). The HAP + PHY diet produced the lowest mean fecal PAP concentration, and was lower than the HAP and PHY diets at = 0.06 and 0.16, respectively. Few studies have specifically measured PAP in pig feces but recent work by He and Honeycutt (2001) measured organic P in sequential fractions of pig and cattle (Bos taurus) manure using enzymatic characterization. They found the majority of "phytate-like" P in the water-soluble fraction, with little phytate in the other fractions measured. The total "phytate-like" P (0.35 g kg-1 DM) in pig manure reported by He and Honeycutt (2001) was much lower than the range of PAP reported in our study. However, the TP content they reported was also much lower (3.9 g kg-1 DM), which was probably due to their manure containing bedding material (straw). Even though phytate P is not thought to be absorbed by pigs, the PAP concentration in fresh feces was much lower (5–15% of TP, Table 2) than the PAP concentration of the diets (43–72% of TP, Table 1). This may be explained by hydrolysis of PAP to orthophosphate and lower inositol phosphates in the lower digestive tract where orthophosphate absorption does not occur. Wise and Gilburt (1982) showed that germ-free rats excreted significant amounts of phytate, while conventional rats did not, which they concluded was due to hydrolysis of phytate by endogenous bacteria in the digestive tract. In our study, the higher concentration of fecal PAP measured in the control diets reflects the amount of phytate entering the lower digestive tract. Though a portion of the phytate was probably hydrolyzed to orthophosphate or lower inositol phosphates as it passed through the lower intestine, the phytate present in the control diet was probably too large to be reduced to levels similar to the other diets.
The concentration of TP in urine was significantly higher in PHY and HAP + PHY diets compared with the control diet (Table 2). However, since average urine TP represented <0.5% of the TP excreted across diets, this finding had little effect on TP excretion. Due to dilution of urine samples caused by spillage from watering devices, the urine volumes and concentrations we report may not be compared with other studies where urine output was measured directly. Pigs generally absorb more P than is utilized in metabolism (Finco, 1989), with excess P being excreted via urine or as endogenous P in feces. High levels of urinary P excretion are most often a result of excess dietary P (Poulsen, 2000), and urine P levels may be used as an indicator of adequate dietary P (Dellaert et al., 1990). Spencer et al. (2000) showed elevated urine P with diets higher in available P due to formulation with HAP corn and supplemental inorganic P. Because the diets used in this experiment were considerably lower in available P than diets formulated to meet National Research Council P requirements, urine P values were considerably lower than would be expected for pigs under typical production conditions.
Influence of Storage Time on Slurry Phosphorus Pools
Table 3
shows mean DM recovery and relative fractions of DRP, DOP, ASRP, ASOP, and PAP as a percent of TP in slurry samples. Relative amounts of the P pools are presented since the nonhomogeneity of fresh feces resulted in slightly different amounts of TP added to the jars at the start of the experiment. No significant interactions between diet and storage time were observed for DM recovery or the P pools, indicating that the slurry from all four diets behaved similarly during storage.
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Storage time had significant effects on DRP and DOP as a fraction of TP. The DRP fraction was initially 47 to 56% of TP and decreased to about half of this value after 150 d of storage for all diets, with most of the reduction occurring between 30 and 90 d. The trend we observed with DRP over time agrees with that of Gerritse and Zugec (1977), who showed a 40% decrease in soluble inorganic P in aerated pig slurry after 63 d of storage. While the decrease in DRP after 30 d of storage may be explained by microbial assimilation or the formation of less soluble P compounds, another possible reason may be the conversion of readily hydrolyzable organic P in fresh fecal material to orthophosphate in the acidic matrix of the P analysis reagents, thereby giving a falsely high DRP measurement. Chardon et al. (1997), using gel fractionation techniques, observed decreases in DRP between fresh and stored (18 mo) pig slurry samples. They concluded that part of the DRP measured in fresh slurry was hydrolyzed from dissolved higher molecular weight organic compounds during analysis. It is possible in our experiment, that after storage and subsequent conversion of the hydrolyzable organic P to orthophosphate, some of the orthophosphate was assimilated into insoluble P compounds and no longer measured as part of the DRP pool. The DOP pool was initially 4 to 6% of TP and decreased the most during the first 30 d of storage. The DOP pool did not show an increase with a decrease in DRP at 30 and 90 d, indicating that increased storage time reduced both soluble inorganic and organic P.
The ASRP pool ranged from 77 to 92% of TP across diets and storage times and was not significantly affected by storage time. Although ASOP made up only a small portion of TP (0.8–8%), storage time did have a significant effect on the ASOP pool. The ASOP pool decreased from 0 to 30 d, then remained relatively stable in subsequent samplings. If ASRP represents a reasonable estimate of the less recalcitrant P pool, these data show that the majority of manure P is potentially bioavailable and that storage has little effect on the long-term availability of P in pig slurry.
The PAP pool ranged from 5 to 16% of TP across diets and storage times, and showed the largest decrease between the 0- and 30-d samples. The PAP pool fluctuated in the 60- to 90-d samples. The PAP data for the stored slurry samples were near the lower detection limits of the Fe(III)-precipitate procedure, and therefore may be subject to greater interference from other forms of organic P (Peperzak et al., 1959).
Estimated Diet Influences on Phosphorus Distribution in Mixed-Age Slurry
Average values for the P pools calculated across the six storage times are presented in Table 4
. These time-averaged values may be more indicative of relative P pools in a typical storage pit containing a mixture of different-aged materials. All discussion of significant differences in this section are based on mean separations performed at the = 0.05 level. Averaged across storage time, the DRP pool represented 33 to 40% of TP and was significantly higher in the HAP + PHY and HAP diets compared with the control diet. The DRP pool also was significantly greater in the HAP + PHY diet compared with the PHY diet. The DOP pool was significantly greater in the HAP + PHY diet (3.4% of TP) compared with the other diets (2.5–2.6% of TP), which were not significantly different from each other. In addition, the relative total dissolved P pool (sum of the DRP pool and the DOP pool) was greater in the HAP + PHY and HAP diets than the control diet and the HAP + PHY diet was also greater than the PHY diet (data not presented).
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The PAP pool averaged across storage times represented 2 to 10% of TP and was significantly lower in the PHY, HAP, and HAP + PHY diets compared with the control. The relative amount of TP present as PAP in the HAP + PHY diet was also significantly lower than both the PHY diet and HAP diet, which were not significantly different from each other. The relative fraction of PAP in stored slurry from the control diet averaged across time (10% of TP) agrees with values calculated from data reported by He and Honeycutt (2001) of "phytate-like" P as percent of total P (9%) in their pig manure. These data indicate that PAP constitutes a relatively small fraction of slurry TP, but it can be influenced by the feed phytate content and phytate utilization in the animal.
Implications
Our data show that diet formulation with phytase and/or HAP corn can effectively reduce the TP concentration of pig feces and when used together can also reduce DRP concentration. The 40% decrease in TP and 34% decrease in DRP observed when comparing the HAP + PHY diet with the control indicate that substantial environmental benefits can be gained from incorporating both HAP corn and phytase into pig diets. Though HAP corn is not yet commercially available, phytase is widely used and has been shown to be effective at reducing TP concentrations without raising DRP when supplemental P is reduced. In addition, the development of HAP (low phytate) soybeans (Wilcox et al., 2000) has the potential to further reduce P excretion by pigs fed corn–soybean meal diets.
The significant effects of diet on the relative amounts of DRP, DOP, ASOP, and PAP, averaged across storage time, indicate that diet may affect the forms and availability of P in slurry that is a mixture of different-aged material. This issue may become more important if P-based manure application strategies become more widely used. For example, if mixed-age slurries estimated from our study were applied to soils on an equal total P basis, the HAP + PHY diet would provide 23% more DRP and 18% more DOP than the control diet, which may increase the potential for runoff or leaching P losses under certain application scenarios (e.g., surface applications).
Moore et al. (2000) reported increased runoff DRP losses from pastures amended with untreated poultry litter compared with alum-treated litter with lower DRP. Similarly, Kleinman et al. (2002) reported a positive linear relationship between soluble P in manures and DRP losses in runoff when manures were applied at similar total P levels. Chardon et al. (1997) found that the majority of P leached from soil columns and lysimeters occurred in the soluble organic form, and that the fraction of TP present as DOP increased with depth. However, other research has shown that soluble or total P levels in pig slurry may have little effect on P transport in runoff when manure is incorporated (Gilley et al., 2001). Further research is needed to determine what effect the form of P applied in manure has on surface and subsurface P losses under various manure application scenarios.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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In our study, fecal TP concentration was reduced 17, 19, and 40% in PHY, HAP, and HAP + PHY diets, respectively, compared with the control diet and ASRP concentrations followed similar trends. Fecal DRP concentration was only significantly ( = 0.05) reduced in HAP + PHY diets compared with the control. Storage time up to 150 d reduced the relative pools of DRP, DOP, ASOP, and PAP across diets, with the largest changes occurring within the first 60 to 90 d. The relative ASRP pool was not significantly (P > 0.10) affected by storage time, indicating that the P cycled among the pools measured and did not form highly insoluble compounds. Despite changes in the various P pools with time, diet-induced differences in the relative DRP, DOP, ASRP, and PAP pools were significant when averaged across storage time up to 150 d, indicating that diet may affect P bioavailability in slurries containing a mixture of fresh and stored materials. Until recently, little attention has been paid to characterizing forms of P in manures, and even less to relating these forms to environmental P losses. The data presented here furthers our understanding of how diet manipulation with HAP corn and phytase can affect both the amount and forms of P in pig excreta, and the changes that may occur in these forms during storage. Additional studies are needed to determine if the effects we observed in this laboratory study also are observed with industry-standard diets under typical production and manure storage conditions.
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ACKNOWLEDGMENTS |
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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