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TECHNICAL REPORTS

Surface Water Quality

Influence of Phytase on Water-Soluble Phosphorus in Poultry and Swine Manure

^a Department of Animal and Avian Sciences, University of Maryland, College Park, MD 20742
^b Department of Animal Science, Iowa State University, Ames, IA 50011
^c Department of Animal Science, Purdue University, West Lafayette, IN 47907

^* Corresponding author (wpowers{at}iastate.edu)

Received for publication March 27, 2004.

	ABSTRACT

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The effect of dietary non-phytin phosphorus (NPP) and phytase (PHY) concentration on total phosphorus (TP) and water-soluble phosphorus (WSP) excretion was determined. Diets tested in broiler experiments were: National Research Council nutrient requirements for non-phytin phosphorus (NRC), NRC + PHY, reduced non-phytin phosphorus (RED), and RED + PHY. Turkey and swine experiment diets included NRC, RED, and RED + PHY. For all experiments, except broiler Experiment 1, excreta were: (i) boiled, antibiotic added, then frozen; (ii) boiled, antibiotic added, incubated (37°C for 72 h), then frozen; and (iii) incubated, boiled, antibiotic added, then frozen. In Experiment 1, excreta were collected and frozen or incubated for 24 or 48 h. In broiler Experiment 1, WSP was not affected by phytase but increased with post-excretion incubation. In a broiler Experiment 2, reducing NPP resulted in reduced excreta TP and WSP (11.3 to 8.3 and 5.3 to 2.7 g kg^–1). Feeding RED + PHY diets resulted in less TP and WSP (7.6 and 0.6 g kg^–1) as compared with NRC + PHY (11.2 and 3.9 g kg^–1, Experiment 3). Incubation resulted in increased WSP, irrespective of phytase addition such that WSP as a percent of TP was similar among treatments. Addition of antibiotics before incubation prevented the increase in WSP. Similar results were observed with turkey and swine. Therefore, when phytase is used properly (i.e., with a simultaneous reduction of NPP), WSP or WSP as a percent of TP are not affected. The increase in WSP as a percent of TP post-excretion is a function of excreta microbial activity and not dietary phytase addition.

Abbreviations: F, manure frozen without incubation • I, manure incubated for 72 h at 37°C • IA, manure incubated with an antibiotic • NPP, non-phytin phosphorus • NRC, National Research Council • PHY, phytase • PHYb, phytase with Natuphos 1200 phytase source • PHYr, phytase with Ronozyme phytase source • RED, reduced non-phytin phosphorus diets • TP, total phosphorus • WSP, water-soluble phosphorus

	INTRODUCTION

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CONCERNS REGARDING excessive phosphorus in surface waters that leads to eutrophic conditions have resulted in animal agriculture adopting practices to curtail the excretion of P. One of the most commonly adopted practices in the swine and poultry industries has been the inclusion of exogenous phytase in the diet. Phytase enzyme, a phosphatase capable of catalyzing the hydrolysis of phospho-ester bonds, releases phosphate groups from the phytate molecule that can be readily absorbed by the animal. The use of phytase in the diets of monogastric animals has gained importance in recent years because phytate is the predominant form of P found in most seed-based ingredients used in nonruminant diets (Taylor, 1965; Nelson et al., 1968; Pallauf and Rinbach, 1996), and these animals have a limited ability to utilize this form of P (Pointillart et al., 1987; Sebastian et al., 1996; Radcliffe et al., 1998; Zanini and Sazzad, 1999; Tamim and Angel, 2003). Seed-based ingredients account for the largest proportion of diets commercially used in poultry and swine production. As a result of proper inclusion of phytase in swine and poultry diets, more of the phytic acid P present in the seed-based ingredients is absorbed by the animal, reducing the need for supplementation of inorganic dietary sources of NPP such as dicalcium phosphate, hence reducing the TP concentration of the diet (Cromwell et al., 1995; Waldroup et al., 2000).

Phytase releases phosphate groups from the phytate molecule, making the P available to the animal, raising the concern that P excreted is more soluble and subject to higher potential of environmental loss. This would suggest that the use of phytase may actually increase and/or accelerate the potential mobility of excreted P to surface waters. Much of the controversy extends from a report by DeLaune et al. (2001). In that report, runoff from tall fescue (Festuca arundinacea Schreb.) field plots fertilized with litter from broilers fed diets with phytase exhibited greater WSP concentrations during a rainfall simulation.

Contrary to the report of DeLaune et al. (2001), Moore et al. (1998) noted numerical, but nonsignificant reductions in both TP and WSP concentrations in broiler litter when phytase was added to either normal corn (Zea mays L.) or low-phytate corn diets for two flocks. The litter was then applied to fescue test plots at similar application rates. Total P and WSP in runoff from the plots, on the day of application or 7 d after application, were not significantly different between litters from birds fed normal or low-phytate corn with or without phytase. Applegate et al. (2003) concluded that phytase supplementation did not affect the solubility of P in the litter regardless of the P feeding program when dietary P content was reduced to accommodate the estimated sparing effect of phytase inclusion.

The hypotheses of the current work were that (i) when used correctly, phytase does not increase WSP in the excreta, and (ii) WSP in manure after excretion increases due to microbial activity regardless of whether or not phytase is exogenously included in the diet. The objectives of the current work were to determine in broilers, turkeys, and swine: (i) if dietary inclusion of exogenous phytase influenced WSP and WSP as a percentage of TP; (ii) if WSP changed in manure post-excretion; (iii) the mechanisms behind WSP changes post-excretion; and (iv) if the method of dietary P content, when phytase was included in the diet, affected the WSP excreted.

	MATERIALS AND METHODS

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Experimental Design
Five independent studies were performed with broiler, turkey, and swine fed different diets (Table 1). Each experiment included a diet formulated to meet the NRC nutrient requirements for NPP (NRC), a reduced NPP diet that accounted for that accounted for the improved P utilization when phytase was supplemented (RED), and one or two diets at reduced NPP with the addition of commercial phytase, either Natuphos 1200 (BASF, Mt. Olive, NJ) (PHYb) or Ronozyme P (CT) 2500 (DSM Nutritional Products, Basel, Switzerland) (PHYr). The units of phytase addition, the NPP concentrations of the various diets, and the ages of the animals in the study are listed in Table 1.

Sample Treatments
Excreta from Experiment 1 was either frozen immediately (0 h) or incubated at 37°C for 24 or 48 h before freezing in liquid nitrogen. For Experiments 2 to 5, samples were treated with antibiotics in the following schemes: (i) boiled for 10 min in a water bath before antibiotics addition and then frozen (F); (ii) boiled for 10 min, followed by antibiotics addition, incubated for 72 h at 37°C (IA), and then frozen; or (iii) incubated for 72 h, boiled for 10 min followed by antibiotics addition, and then frozen (I). The antibiotics applied in Experiments 2 to 5 consisted of consisted of two antibiotics: Gentamycin (Sigma #G 1272; Sigma-Aldrich, St. Louis, MO), containing 10 mg gentamycin mL^–1 deionized water, and an antibiotic–antimycotic solution (Sigma #A 4668), containing 10000 U penicillin, 10 mg streptomycin, and 25 µg amphotericin B per mL of 154 mmol L^–1 NaCl. Samples from Experiment 2 received 1 mL of antibiotics solution, which resulted in a low and inconsistent level of microbial inhibition (45–90%). The application rate was then increased to 4 mL per sample for Experiments 3 to 5. Also, to enhance the effect of the antibiotics, deionized water was added to samples from Experiments 3 to 5 (30 g sample + 90 mL for Experiments 3 and 4; 60 g + 170 mL for Experiment 5) before the treatments. Efficacy of microbial inhibition by antibiotics in Experiment 3 was 97.5% (SD = 6.25).

Sample Analyses
Following treatments, excreta samples were freeze-dried, then analyzed for excreta total P as described for the diets and for WSP following a modified Self-Davis and Moore (2000) procedure, using 2 g of a dry ground (1-mm screen) sample into 25 mL of deionized water, a 1-h extraction, and a 0.45-µm filter. While no uniform procedure has been established for determining WSP, the conditions used fell within the procedural conditions required by Kleinman et al. (2002).

Microbiological analyses were performed after incubation on samples from Experiments 2 and 3. For each analysis, a 10-g sample was weighed into a blender and 90 mL of 1 g L^–1 sterile peptone (Sigma #P 5905) was added. The mixture was homogenized for one minute and then serial dilutions (10-fold) were prepared in 1 g L^–1 peptone water. The pour plate method (Vanderzant and Splittstoesser, 1992) was used for the estimation of total aerobic count using total plate count agar (#0479-17; Difco Laboratories, Detroit, MI). All plates were incubated at 37°C for 48 h. A colony counter was used to count the colony forming units (cfu) in plates that contained between 0 and 250 colonies. All samples were tested in duplicate.

Formulated diets were subsampled at the time of mixing for TP and NPP content and phytase activity analysis. All diets were fed as mash. Total P in the diet was determined by a wet acid digestion, followed by colorimetric determination (Method 7.123; AOAC International, 1980). High-pressure liquid chromatography was used to determine phytin P content (Latta and Eskin, 1980). The NPP content was calculated by subtracting phytin P from TP. Phytase activity of each diet was analyzed by a commercial laboratory (DSM Nutritional Products, Technical Marketing Analytical Services, Belvidere, NJ). A unit of phytase is defined as the amount of phytase needed to liberate 1 µmol of inorganic P per min from 5.1 mmol L^–1 of sodium phytate at pH 5.5 and 37°C.

Statistical Analyses
Each of the five experiments was analyzed as a randomized split-plot design in which the dietary treatment was the whole plot and the excreta treatment was the subplot and the factor of interest was the dietary treatment. In Experiments 2 and 3, the diet treatments formed a complete two-way factorial arrangement of NPP content and phytase source and were analyzed as such. The NPP–PHY combinations in the other experiments were treated as one-way designs. Assumptions of normality and homogeneous variance were checked and were met for all experiments except for Experiment 2, which had unequal variances among excreta treatments. As a result, for Experiment 2, a weighted analysis was performed to allow for the unequal variances (Neter et al., 1990). Pairwise means comparisons were performed using Tukey's method (Tukey, 1991) to control experiment-wise error rate. All analyses were done using SAS Version 8.2 (SAS Institute, 1999).

	RESULTS

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Animal performance data for all experiments will be published elsewhere. However, diets and duration of the experiments were designed to not have negative effects on performance. Consequently, feed consumption and weight gains were similar between treatments for all experiments.

Broiler Experiment 1
Reducing dietary P content resulted in decreased excreta TP, WSP, and ratio of WSP to TP for some incubation treatments (Table 2). Addition of phytase to the RED diets further reduced TP in excreta (9.0 vs. 8.1 g kg^–1; Table 2) with no effect on WSP or the WSP as a percent of TP. Excreta TP, WSP, or WSP as a percent of TP were not different between excreta from birds fed the two phytase sources (RED + PHYb vs. RED + PHYr).

Broiler Experiment 2
Reducing dietary P content below NRC nutrient requirements resulted in a decrease in excreta TP, from 17 to 14 g kg^–1 P (P = 0.0015; Table 3). No differences were observed in WSP content of excreta as a result of dietary NPP concentration. Inclusion of phytase further reduced TP in excreta (17 vs. 15 g kg^–1; Table 3) with no effect on WSP or the WSP as a percent of TP.

Broiler Experiment 3
In broiler Experiment 3, TP, WSP, and WSP as a percent of TP were reduced in excreta from birds fed the RED diets versus the NRC diet (P < 0.0001). Inclusion of phytase tended to further reduce TP in excreta (9.4 vs. 10.1 g kg^–1 TP, P = 0.059; Table 4) with no effect on WSP. The WSP as a percent of TP was greater in excreta from birds fed diets containing phytase (42.3 vs. 38.0%, P = 0.02; Table 4).

Turkey Experiment 4
Consistent with the findings of broiler Experiment 1 (Table 2), diet effects were observed on all measurements studied. Reducing dietary NPP resulted in reduced excreta TP and WSP (Table 5). Excreta TP content decreased 25% (8.1 vs. 10.8 g kg^–1 TP) while WSP content decreased 38% (2.3 vs. 3.7 g kg^–1 WSP) leading to a 20% reduction in the WSP as a percent of TP. Inclusion of phytase in the diet decreased TP and WSP in the excreta even further, 25 and 30%, respectively. However, the WSP as a percent of TP was not different between excreta from birds fed diets with and without exogenous phytase (Table 5),

Swine Experiment 5
Diet fed did not result in significant differences in feces composition of TP content, WSP content, or WSP as a percent of TP (P = 0.085, 0.16, and 0.76, respectively; Table 6). The TP content of feces pooled across feces treatments was 17.3 g kg^–1 (18.0, 18.1, and 15.9 g kg^–1 P in feces from pigs fed the NRC, RED, and RED + PHYb diets, respectively). Lack of statistical difference in TP excretion as a result of dietary treatment was probably due to not formulating the RED and RED + PHYb diets sufficiently low in dietary P to see a sparing effect that occurs when animals are fed below their requirement. However, feces from pigs fed the RED + PHYb diets tended to be lower in P content (P = 0.0850). Excreta WSP, pooled across dietary treatments, was 5.9 g kg^–1 (5.7, 6.5, and 5.4 g kg^–1 WSP in feces from pigs offered the NRC, RED, and RED + PHYb diets, respectively) with a corresponding WSP as a percent of TP of 33.96 (31.69, 35.95, and 34.25 for the NRC, RED, and RED + PHYb diets). Analyzing a subset of the data that included only feces from pigs fed the RED and the RED + PHYb diets indicated no effect of phytase on TP, WSP, or WSP as a percent of TP.

	DISCUSSION

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Diet Effects
Non-Phytin Phosphorus Content
In practice, producers typically feed phosphorus at the NRC required level or, in some cases, exceed NRC requirements. With the exception of the swine study (Experiment 5), reducing dietary NPP content resulted in reduced TP and WSP content in excreta. In the swine study, it is likely that the RED diet was formulated still higher than the animal's NPP requirement, preventing a statistical reduction in excreta TP. The findings demonstrate that dietary management to avoid overfeeding P has environmental benefits in that TP excreted is reduced and the mass of P excreted that is water soluble is reduced as well. Furthermore, in broiler Experiments 1 and 3 and turkey Experiment 4, the fraction of excreted P that was WSP was greater in the NRC diets than in the RED diets, supporting the basis for the experimental design where NRC diets are at or above requirements and RED diets are below requirements. As in the present study (Experiments 1, 2, 3, and 4), Applegate et al. (2003) and Waldroup and Fritts (2003) reported a decrease in excreta P concentration when dietary P concentrations were reduced to below National Research Council (1994) levels in broilers. Omogbenigun et al. (2003) reported that reductions in dietary P below requirements in weanling pigs resulted in improved digestibility of phosphorus as well as in a decrease in P excretion. Similarly, Bruce and Sundstol (1995) found lower P excretion in growing–finishing pigs fed diets with P content below requirements. Requirements for P in the diet decrease through the growth phase as the animal increases in weight (National Research Council, 1998).

Phytase Inclusion
In Experiments 1, 2, and 4, inclusion of phytase to the RED diets resulted in a further reduction in excreta TP, demonstrating the benefits of phytase inclusion when diets are formulated correctly (i.e., diets P-formulated to be at or close to the NPP requirements of the animal and to reflect the amount of P made available by the phytase). Main effect means results for Experiment 3 showed a tendency for this effect, though nonsignificant (P = 0.059). Comparison of WSP content in excreta from either birds or pigs fed diets with and without exogenous phytase showed no differences, supporting the hypothesis that the increase in WSP is independent of dietary phytase inclusion. These results agree with prior work in broilers by Applegate et al. (2003) and Maguire et al. (2003) with turkey excreta. Work with broilers showed that the addition of phytase to diets with reduced concentrations of NPP (below requirements) led to a reduction in litter TP and WSP and no change in WSP as a percent of TP (Applegate et al., 2003). Maguire et al. (2003) also reported decreases in TP and WSP in excreta from turkey poults fed diets that met National Research Council (1994) requirements for NPP and diets containing phytase with NPP levels below requirements. Maguire et al. (2003) showed a decrease in WSP as a percent of TP when phytase was added, possibly due to the large reduction [42% versus National Research Council (1994) NPP requirement] in NPP (Angel et al., 2002). As with poultry, work with swine also supports the findings in the present study. Oryschak et al. (2002) found a 28% decrease in excreted P from 23-kg pigs fed diets containing 0.12% available P with no phytase versus that from diets supplemented with 374 U phytase kg^–1 diet. Similarly, Harper et al. (1997) observed a 27% decrease. Data on the WSP in the manure of pigs fed diets containing phytase are scarce.

Excreta Treatment Effects
Dietary phytase activity is negligible when the digesta reaches the lower small intestine (Jongbloed et al., 1992; Liebert et al., 1993; Rapp et al., 2001). It is well known that microbes present in the digesta in the intestinal tract and primarily found in high numbers in the ceca and colon can change nonsoluble P to WSP (Fan et al., 2000; Sandberg and Andlid, 2002; Ajskaiye et al., 2003). Ajskaiye et al. (2003) reported an increase (two- to fourfold) in the WSP content between ileal digesta and excreted feces. Some of the microbes present in the digesta will flow out of the animal with feces and thus be present in manure. This research was designed to separate changes that occur within the animal from changes that occur after excretion and to better understand what is mediating the changes that occur post-excretion.

Incubation Time
Findings from Experiment 1 illustrate that incubation of excreta at 37°C resulted in increased water solubility of P. Excreta that was frozen with no incubation exhibited WSP content that was only 42% of the WSP content in excreta following 24 h of incubation. These findings were confirmed in Experiments 2, 3, 4, and 5 with the effect ranging from a 44% increase in WSP (Experiment 5) to a 750% increase in WSP (Experiment 4) following incubation. Incubation for 48 h did not increase WSP content further, indicating that the solubilization process primarily occurred within the first 24 h post-incubation (Experiment 1).

Antibiotic Addition
Antibiotics were added to excreta at freezing (0 incubation time, F), before 72 h of incubation (IA), or following 72 h of incubation (I) to decrease any microbial activity that might contribute to solubilization of TP to WSP in the excreta. This was done to try and elucidate whether changes post-excretion were being mediated, completely or in part by added dietary phytase or by microbes. Results from all four studies that included the antibiotics in the treatment (Experiments 2, 3, 4, and 5) clearly demonstrate that by adding the antibiotic, solubilization of P was greatly reduced to the extent that WSP was no different from excreta that was immediately frozen (Experiments 2, 3, and 4) or only 10% greater than feces that had been frozen (F, Experiment 5), whereas incubating before antibiotic addition (I) resulted in increased WSP relative to freezing (F). Manure was boiled just before antibiotic addition, so boiling effects are indistinguishable from antibiotic effects. However, the purpose of boiling was to stop phytase activity. Antibiotics were added to prevent microbial activity. These findings support the hypothesis that any increase in WSP content following excretion is due to microbial activity. Others have found that microbial activity in digesta, especially in the ceca and colon, increases hydrolysis of phytate P (Wise and Gilbert, 1982; Wise et al., 1983) and thus solubility of P. No literature published in a scientific journal to date could be found that directly implicates dietary phytase in changing P form or solubility post-excretion.

	CONCLUSIONS

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The five studies, when combined, demonstrated that (i) dietary inclusion of exogenous phytase decreased mass of WSP excreted in broiler chickens, turkeys, and swine, but increased the WSP as a percent of TP in one broiler chicken study; (ii) the P in excreta changes post-excretion by becoming more soluble; (iii) solubilization post-excretion is the result of microbial activity from microbes that are inherently present in the excreta itself and thus, any treatment of excreta or manure post-excretion that minimizes microbial activity (reduction of moisture or water activity in litter or use of antimicrobials) will decrease P solubilization; and (iv) proper management of dietary P and exogenous phytase addition can positively affect P excretion by reducing the mass of TP and WSP excreted in addition to reducing the fraction of TP excreted that is water soluble.

	ACKNOWLEDGMENTS

 
The authors wish to acknowledge DSM Nutritional Products, Basel, Switzerland (phytase and vitamin premix); BASF, Mt. Olive, NJ (phytase); PCS Sales, Feed Products, Raleigh, NC (monocalcium phosphate); Degussa Corp., Charlotte, NC (methionine); and BCP Ingredients (choline chloride) for their contribution of feed ingredients and diet analyses. The authors also acknowledge Sarah Newman for her help with Experiment 1 and Tim Shellem and Martha Jeffrey for help with animal work and laboratory analysis.

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