Published online 3 April 2006
Published in J Environ Qual 35:858-865 (2006)
DOI: 10.2134/jeq2005.0435
© 2006 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
TECHNICAL REPORTS
Waste Management
Impact of Diet, Moisture, Location, and Storage on Soluble Phosphorus in Broiler Breeder Manure
R. O. Maguirea,*,
P. W. Plumsteadb and
J. Brakeb
a Department of Soil Science, North Carolina State University, Raleigh, NC 27695
b Department of Poultry Science, North Carolina State University, Raleigh, NC 27695
* Corresponding author (rory_maguire{at}ncsu.edu)
Received for publication November 21, 2005.
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ABSTRACT
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Decreasing dietary phosphorus (P) has the potential to reduce P excreted in manure and therefore alleviate the environmental degradations associated with intensive animal farming. We evaluated reducing dietary P for broiler breeders as an aid to reduce manure total and water soluble phosphorus (WSP). Broiler breeders were fed diets high and low in dietary P, with and without phytase, from 22 to 64 wk of age. At the end of the 42-wk production period, manure was collected from four locations in each two-thirds slat, one-third litter breeder pen: the litter scratch area, under the drinker in the slat area, under the feeder in the slat area, and in a clean area of the slat area away from feeder or drinker. After the initial sampling, all manure was removed from pens and representative samples were stored for 6 mo with and without feed mixed in to simulate the effect of spilled feed. Total P was determined on all pen samples, and moisture and WSP determined on the pen and stored samples. The manure collected under the drinker had much greater moisture due to spilled water. This was associated with much greater WSP in this location, showing the importance of good water management. The manure from under the feeder had similar WSP as manure from the clean area, so spilled feed did not significantly affect WSP. Dietary phytase either had no effect or significantly decreased manure WSP. However, addition of dietary phytase to the feed led to slightly elevated manure moisture. Since moisture was correlated with manure WSP this may explain some of the variability in WSP results between studies. Over 6 mo of storage WSP increased and generally followed the same ranking order at 168 d as at 1 d among the dietary treatments (high > high + phytase > low > low + phytase). Combining decreased dietary P and phytase reduced both manure total P and WSP by 42%. As total P and WSP are indicators of the long and short term impacts manure applications can have on P losses from manured soils, diet modification should be seen as environmentally beneficial.
Abbreviations: AvP, dietary available phosphorus • HAP, high available phosphorus • NPP, non-phytate phosphorus • WSP, water soluble phosphorus
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INTRODUCTION
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MODERN INTENSIVE ANIMAL production can lead to more nutrients entering a region in animal feeds than may be exported in animal products (Kellogg et al., 2000). The excess P is normally applied to crop land, often at rates above crop requirements leading to the buildup of soil test P. Due to concerns over P losses from agricultural activities decreasing the quality of surface waters, some recent efforts have been directed toward decreasing the P in animal feeds and therefore P excreted in manure.
In a review article, Maguire et al. (2005) reported that feeding P closer to animal requirement could decrease total P in manure by up to 33% in poultry. Combining this with other feeding strategies, such as using phytase and high available phosphorus (HAP) corn, could decrease total P in poultry and swine by approximately 40%. It has been suggested that by using currently available technologies, it should be possible to reduce total P in manure by 40% for poultry, 50% for swine, and 30% for dairy cattle, and future developments could lead to further decreases (Council for Agricultural Science and Technology, 2002). Decreasing total P applications to agricultural land by reducing total P in manure will help control buildup of soil test P in the long term. However, dietary strategies not only change the total P concentration in the manures produced, but also the forms of P that are present. Of particular concern is WSP in manures, as this has been linked to the potential for soluble P losses in runoff immediately after land application of manures (Kleinman et al., 2002; Smith et al., 2004).
Most dietary strategies have decreased WSP in the manures produced. Studies have shown that feeding P closer to animal requirements and HAP corn have consistently led to reductions in WSP in addition to decreasing total P, although the magnitude of decreases has varied between studies (Maguire et al., 2005). For example, Smith et al. (2004) reported that changing from normal to HAP corn in broiler diets decreased WSP by 35% and total P by 18%. In a study with three flocks of broilers on the same bed of litter, feeding closer to requirement decreased WSP by 52% and total P by 17% (Maguire et al., 2004). However, phytase additions to feeds have had inconsistent effects on WSP in manures. Most studies show a decrease or no significant effect of dietary phytase on WSP in manure, but Vadas et al. (2004) reported that phytase increased WSP in poultry manure.
Most studies that reported WSP in manures from modified diets measured WSP in manure immediately following the feeding trial, but in agricultural situations manure is often stored before it is land applied. McGrath et al. (2005) stored broiler litters from diets high and low in dietary P, with and without phytase, at initial dry (24%) and wet (40%) moisture and measured WSP during 1 yr of storage. In the dry litter, WSP was stable over the year of storage, but in the wet litter WSP increased substantially. This translated into greater soluble P in runoff when these wet manures were land applied and rained on (McGrath et al., 2005). Baxter et al. (2003) stored swine manure from diets with and without phytase and HAP corn for 150 d. The WSP to total P ratio in the manures decreased with increasing storage time for all manures and there was no significant difference between the treatments after 150 d. Dietary phytase had no impact on WSP in stored manures in either study.
Despite the recent research efforts focusing on decreasing dietary P, there is limited research available on the impact of diet modification on P in broiler breeder manure. Breeder manure accumulates for much longer than broiler litter and in a purer form (no dilution by bedding such as wood chips), due to the longer life and management of these birds. Therefore, this study was conducted to investigate the influence on WSP in broiler breeder manure of (i) reducing dietary P and using phytase, (ii) location in pens, as moisture is much greater under the drinker, (iii) feed spillage, and (iv) storage time.
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MATERIALS AND METHODS
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Breeder Study
Ross 308 female and male Ross 344 broiler breeders were fed diets with or without phytase and 0.1% non-phytate phosphorus (NPP; from dicalcium phosphate) was removed from the phytase amended diets. High and low available NPP diets were also evaluated, with the high diet being equivalent to the National Research Council (1994) recommendations and the low diet created in a manner such that when phytase was added no supplemental NPP from dicalcium phosphate was required. This provided the four dietary treatments described in Table 1. Calcium level was maintained at 2.7% of the diet by weight by substituting calcium carbonate for dicalcium phosphate in the reduced P diets.
While not always well defined in animal feeding experiments, the dietary NPP and available phosphorus (AvP) content of diets fed to poultry have been determined not to be the same and have often been erroneously interchanged (Angel and Applegate, 2001). The use of the term AvP in this experiment represents the relative bioavailable P fraction as determined using a slope ratio assay with monocalcium phosphate as the reference standard (Apke et al., 1987; Soares, 1995). The NPP was calculated by subtracting the analyzed phytate P content of ingredients from their analyzed total P content. The importance of differentiating between AvP and NPP was emphasized in data from Van der Klis and Versteegn (1996) that showed poultry to be capable of digesting a variable portion of the phytate bound phosphorus that differed considerably between ingredients. The general industry practice of maintaining the same level of AvP by replacing 0.1% NPP from monocalcium phosphate with 500 FTU of phytase was applied (Van der Klis and Versteegn, 1996). The phytase enzyme used was Allzyme SSF (Alltech, Nicholasville, KY) with an analyzed activity of 1098 FTU g–1.
There were 6 male and 60 female breeders placed in each 3.96- x 3.96-m pen, with each pen having a litter scratch area of one third of the pen and raised plastic slats for the remainder. Clean pine wood shavings were placed in the scratch area to a depth of 10 cm (4 inches) while no shavings were placed under the slats. There were five female tube feeders with male exclusion grills and one automatic waterer located above the slats, and one male tube feeder located over the scratch area. Birds were introduced to the pens after the 21-wk rearing period and stayed there for the 42-wk production period, during which time all manure generated accumulated within the pens. Each treatment was replicated four times, for a total of 16 pens. All eggs laid by the birds were collected twice daily and fertility determined by incubating sets of eggs periodically throughout the production period. More details on the diet formulations and management applied during the rearing and breeding phase was reported by Plumstead et al. (2005).
Manure Collection and Analysis
Immediately following removal of the birds at the end of the production phase, manure samples were collected from four locations in each pen (i) the scratch area, (ii) under the feeder, (iii) under the drinker, and (iv) around the edge of the pen away from the feeders and drinkers to avoid spillage effects of either feed or water. These samples were called scratch, feeder, drinker, and clean, respectively. Moisture content was measured by drying subsamples at 105°C overnight. Fresh (undried) manure samples were then extracted for WSP at an equivalent dry weight to water ratio of 1:10. The extract was centrifuged at 1000 x g and filtered through Whatman (Brentford, UK) #40 filter papers. Phosphorus in the extract was measured by inductively coupled plasma–atomic emission spectrometry (ICP–AES). To determine total P, 8 mL of concentrated nitric acid was added to 2.5-g sample, dried on a steam plate, and combusted at 500°C in a muffle furnace overnight. Once the samples had cooled, 4 mL of 6 M HCl was added, dried on a steam plate, then rehydrated with 4 mL of 6 M HCl and warmed before being transferred into a volumetric flask and diluted with deionized water. The resulting solution was filtered through Whatman #40 filter paper, and then analyzed for P by ICP–AES.
Storage Study
Following collection of samples from each of the four locations in each pen as described above, all remaining manure was consolidated by dietary treatment. After thorough mixing, 10-kg subsamples were taken for the storage study. Moisture contents ranged from 55 to 60%, so deionized water was added to raise the moisture content of all samples to 60% for consistency. The storage study had two parts, both of which were initiated on 14 Feb. 2005: (i) storage of manure samples as collected, and (ii) storage of manure with feed mixed in to simulate feed spillage. Each of the four treatments had four replicate samples stored for 168 d. For the simulation of spilled feed, feed was mixed in at 3% by weight (thought to be a reasonable feed spillage rate from experience) and each treatment was replicated four times. A 2 x 3 factorial design was used, with three feeds (high P, high P + phytase, and low P) mixed with each of two manures (high P and high P + phytase). The three feeds used gave combinations of the same NPP (0.27%) or the same available P (0.40%), depending on phytase and dicalcium phosphate supplements (Table 1). Subsamples were collected weekly for the first half and every 3 wk for the second half of the 6-mo study. These samples were analyzed for moisture and WSP as described earlier.
Statistical Analysis
Manure samples from breeder laying pens were analyzed using a split-plot design with breeder treatment as the main plot and sample area within each pen as the sub-plot. Variations within pens in the breeder manure analyses were not considered in the calculation of differences between dietary treatments. Data were interpreted using the mixed procedure of SAS Institute (1998). Means were partitioned using LSMEANS and statements of statistical significance were based on P 
0.05, unless otherwise stated.
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RESULTS AND DISCUSSION
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Effect of Diet and Location in a Pen on Breeder Manure Parameters
Moisture
When the moisture for all locations within a pen was averaged by treatment, diet had no significant impact on manure moisture (Table 2). However, when the consolidated samples were collected for the storage part of this study from the total pen cleanout and moisture determined on four replicates, there was significantly (P < 0.01) more moisture in the manures from the phytase diets. No results for the effect of phytase on manure moisture content are available in the literature, so this observation deserves more study.
The moisture content of the breeder manure for the four locations significantly decreased in the following order: drinker (69%) > clean (52%) > feeder (39%) > scratch (16%) (Table 2). The higher percentage moisture of the breeder manure collected from under the drinker can be explained by spilled water dropping onto the manure beneath it. The low moisture in the scratch area can be explained by dilution of the manure with wood chips and greater ventilation, as this area was not covered by slats. The moisture in the manure under the feeder and in the clean area were intermediate to these two extremes as expected, but the reason there was more moisture in the clean area was not clear. These two areas were similar distances from the drinker and the manure was of similar depth, but the clean manure was collected from around the outside of the pen. It is possible that accumulation of condensation against the brick edges, or some other unexpected process, led to slightly elevated moisture in that location.
Total Phosphorus
The breeder manure was diluted by wood chips in the scratch area, but not at any of the three locations under the slats. Therefore, it was not surprising that when total P was averaged across all diets, it was lowest in the scratch area (13 983 mg kg–1) compared to the feeder, clean, or drinker areas under the slats (Table 3). The total P in the manures from under the slats was of a similar magnitude, but it was significantly greater under the drinker (30 446 mg kg–1) than the clean location (26 893 mg kg–1), with the manure under the feeder being intermediate (27 365 mg kg–1). The greater moisture in the manure under the drinker (Table 2) may have increased microbial activity, reducing carbon content by driving off carbon dioxide and concentrating the remaining P. Increased microbial activity in manures with greater moisture content has been suggested by McGrath et al. (2005). Manure under the drinkers had turned black, which may indicate anaerobic conditions due to increased oxygen use by microbes. Manure was not black in any other location.
When averaged across locations, total P in the manure decreased in the order high P (32 341 mg kg–1) > high P + phytase (27 905 mg kg–1) > low P (19 729 mg kg–1) > low P + phytase (18 713 mg kg–1) (Table 3). This trend applied to all locations, with minor exceptions probably due to sample variability. The manures from the phytase diets on average had numerically lower total P (14% for the high P diet and 5% for the low P diet). However, dietary phytase had no significant effect on manure total P, probably due to the variability between pen locations. Other researchers have shown that dietary phytase significantly decreased manure total P in poultry, when NPP supplements were decreased to allow for phytase increasing phytate-P digestibility. For example, Applegate et al. (2003) reported phytase decreased total P in broiler litter by 24%. For turkeys, Angel et al. (2005) showed that dietary phytase decreased total P in litter by 45% and Maguire et al. (2004) reported a drop in litter total P of 7 to 24%. The only significant differences in our study were between the high P and low P diets, unrelated to whether or not dietary phytase was included (Table 3). This showed the importance of feeding P closer to the birds' requirement by decreasing overfeeding of supplemental inorganic dietary P.
Total P in manure is important in the long term, as it is the total manure P application rate that determines long term trends in soil test P (Sims et al., 2000). Total P is particularly important when manures are applied on N-based nutrient management rates, which is the normal practice in many areas. Therefore, decreased manure total P through diet modification will be environmentally beneficial in the long term, regardless of whether achieved through feeding phytase to replace some supplemental dietary P, or minimizing overfeeding of P.
Water Soluble Phosphorus
Water soluble P varied greatly across location and diets, from a minimum of 473 mg kg–1 for the low P diet in the scratch area, to a maximum of 1899 mg kg–1 for the high P diet under the drinker (Table 4). Across all diets, WSP was greatest in manure from under the drinker and lowest in the litter from the scratch area, which followed the same pattern as manure moisture (Table 2). When averaged across all diets for each location, WSP in the manure significantly decreased in the following order: drinker (1279 mg kg–1) > feeder (912 mg kg–1) 
clean (907 mg kg–1) > scratch (661 mg kg–1). McGrath et al. (2005) reported similar results, and attributed this to elevated microbial activity resulting in the degradation of usually insoluble P forms such as phytate P. As manure under the feeder had similar WSP to the manure in the clean area, spilled feed appeared to have had no effect on manure WSP. As soluble P in runoff from manured soils has been linked to WSP in manures (Smith et al., 2004), this shows the potentially large impact that dietary P and bird pen management can have on controlling P losses in runoff. The elevated WSP in manure from under the drinker emphasizes the importance of reducing manure moisture levels by implementation of water restriction programs in broiler breeders combined with dietary feed formulation strategies to reduce urinary water losses.
Most research has shown that dietary phytase either decreased or has no significant effect on WSP in manures (Maguire et al., 2005), although in a study by Vadas et al. (2004) dietary phytase increased WSP in poultry manure. This study had four locations and two levels of available dietary P with and without phytase, making for eight possible comparisons of equivalent manures from diets with and without phytase (Table 4). Out of these eight comparisons, dietary phytase significantly decreased WSP twice (under the feeder and drinker for the high P diet), and had no significant effect on the other six comparisons. When averaged across all pen locations, phytase significantly decreased WSP for the high P diet (from 1316 to 940 mg kg–1), but had no significant effect on the low P diet. Therefore, these results suggest that dietary phytase will not increase soluble P losses in runoff following land application of broiler breeder manure, and may even decrease them for manure applied on an equivalent mass or nitrogen basis. It was interesting that the slightly elevated moisture content of the manures from phytase diets did not result in elevated WSP (Tables 2 and 4), but this may be due to manures from phytase diets having a lower concentration of phytate-P (Maguire et al., 2004) for microbes to breakdown into more soluble P. This elevated moisture in manures from phytase diets may also explain, at least in part, why results on the effect of phytase on WSP reported in the literature have been variable. It would be helpful if future studies on dietary phytase reported the moisture in the resulting manure.
The four locations and two levels of available dietary P with and without phytase also make it possible to have eight comparisons where supplemental P was reduced to feed P closer to the birds' requirement (high P vs. low P and high P + phytase vs. low P + phytase for all four locations). For all of these comparisons, the manure from the low available P diet had numerically less WSP than the manure from the equivalent high available P diet, and these decreases were significant on three occasions. When averaged across all locations, WSP decreased in manures from the high P (1316 mg kg–1) to the low P (743 mg kg–1) diets, but there were no significant differences for manures from the high P + phytase and low P + phytase diets. These equivalent manures from high P and low P diets were achieved by removing some supplemental dicalcium phosphate from high P diets. As this consistently decreased manure WSP, it shows the importance of minimizing supplemental dietary inorganic P to help reduce WSP losses in runoff following land application of manure. Consistent decreases in manure WSP of 21 to 52% when supplemental dietary P was removed have also been reported for broilers and turkeys (McGrath et al., 2005; Maguire et al., 2004).
Water Soluble Phosphorus to Total Phosphorus Ratio
Manure management has started to shift from nitrogen based nutrient management plans to P based plans (Sharpley et al., 2003). If manures are applied at the same rate of P, rather than N, then the WSP to total P ratio shows how variations in manure WSP and total P will combine to affect the WSP application rate and potential for soluble P losses in runoff. When averaged across all diets the WSP to total P ratio was greatest for the scratch area, indicating that the dilution by wood chips led to greater decreases in total P than WSP, despite the low moisture content of this area compared to the other three locations (Tables 2 and 5). This may have been an effect of extraction ratio, as a wider extraction ratio leads to more WSP being extracted (Kleinman et al., 2002). For example, if the litter from the scratch area was half wood chips (by weight), then only half the sample would have been manure and the effective water to manure extraction ratio would have been 20:1 instead of 10:1. When averaged across all diets, under the slats the WSP to total P ratio was numerically greater (although not significantly) in manure from under the drinker (0.041) and similar between the feeder (0.034) and clean (0.034) areas. This again shows the importance of minimizing water spillage to control WSP, and the lack of effect of feed spillage on WSP.
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Table 5. Effect of breeder diet and spatial location on water soluble P to total P ratio in broiler breeder manures.
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Out of the eight comparisons of equivalent manures with and without phytase, three showed an increase in the WSP to total P ratio with dietary phytase, one showed no effect, and four had a decrease, showing no overall effect of phytase on the WSP to total P ratio. When averaged across all locations, phytase greatly decreased the WSP to total P ratio from the high P (0.044) to high P + phytase (0.035) manure, but slightly increased it (although not significantly) from the low P (0.038) to low P + phytase (0.041) manure. This agrees with the results of Angel et al. (2005) who reported that phytase use should not increase WSP or WSP to total P ratio in manures when it "is used properly, i.e., with a simultaneous reduction of dietary NPP." Meanwhile, feeding P closer to the requirement of the bird also had an inconsistent effect on the WSP to total P ratio, with no consistent trends between manures from high P and low P diets at the four pen locations.
Relationship between Water Soluble Phosphorus in Manures and Their Moisture Content
Despite differences in dietary P, when WSP in manure from all diets and all pen locations was plotted against manure moisture content, there was a significant (P < 0.001) positive relationship (Fig. 1). Therefore, increased manure moisture led to greater manure WSP. However, the regression coefficient was relatively low (0.23), almost certainly due to the different concentrations of P in the diets fed to the broiler breeders. This again demonstrates the importance of preventing water spillage from drinkers, which was the single main factor that increased manure moisture and hence WSP.
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Fig. 1. Relationship between water soluble P in manure samples from all locations in the pens and their moisture content.
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Change in Water Soluble Phosphorus with Time during Storage
Without Spilled Feed
The WSP in the consolidated pen samples for each treatment followed the same pattern as the means across locations reported in Table 4, with WSP on Day 1 of storage showing the following order: high P > high P + phytase low P = low P + phytase (P < 0.05) (Fig. 2). After Day 1, there was a general increase in WSP for manures from all diets until about Day 50. During this time, the manure from the high P diet had the greatest WSP, manure from the low P diet had least WSP, and the two phytase diets had WSP intermediate to these two treatments. From about Day 50 to Day 125, there was a high degree of variability in manure WSP caused by large variations between replicates within treatments, despite sample retesting. The reason for this was not clear, as the sampling procedure was consistent throughout the study. However, from Day 125 to the end of the storage study on Day 168, the variability in WSP decreased, and during this time WSP consistently followed the trend high P > high P + phytase > low P > low P + phytase. Therefore, dietary phytase did not lead to increased WSP during manure storage for 168 d and frequently decreased manure WSP. This agreed with the results of McGrath et al. (2005). Angel et al. (2005) reported that dietary phytase should not affect breakdown of organic P (phytate-P), as increases in WSP during a 3-d incubation could be prevented by adding antibiotics, showing that the increased WSP was microbially mediated. However, as manure from the high P diets generally had greater WSP than the equivalent low diets, this showed the importance of feeding P closer to the requirements of the birds.
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Fig. 2. Trends in water soluble P with time for broiler breeder manure from the four dietary P treatments (showing standard error bars).  Values followed by different letters are significantly different at the 0.05 probability level.
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With Spilled Feed
For the manure containing 3% feed to simulate spilled feed, the phytase feed had the same available P as the 0.37% NPP feed and the same NPP as the 0.27% NPP feed (Table 1). The manures from the high P diet generally had greater WSP than those of the high P + phytase diet, irrespective of spilled feed (Fig. 3). This was similar to the results reported for the manures stored with no spilled feed (Fig. 2). Throughout the 168-d incubation, the manures that contained spilled feed had greater or equal concentrations of WSP. As for the manures with no spilled feed (Fig. 2), the manures that had feed mixed in at 3% showed a general increase in WSP over the first 50 d of storage (Fig. 3). Over this period of time the type of spilled feed had no consistent significant effect on WSP. As for the manures with no spilled feed, there was a high degree of variability in WSP between 50 and 125 d before stabilizing for the last two measurements at 147 and 168 d. By 168 d, the high P or high P + phytase manure with no spilled feed had numerically lower WSP than any of those with spilled feed for both manures (not significant). This agreed with WSP in the pen samples, where manure under the feeder did not have significantly greater WSP than manure in the clean area (Table 4). The fact that spilled feed sometimes increased WSP shows the importance of preventing feed spillage. However, the lack of effect of phytase or dietary NPP on WSP limits concern over this potentially negative side effect of modifying diets. As Angel et al. (2005) reported that increases in WSP were microbially mediated, it may be the extra carbon added in the feed, rather than the added P, that controlled WSP when feed was added to these manures.
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Fig. 3. Trends in water soluble P with time for manure from (a) the high P diet and (b) the high P + phytase diet, with feed from the high P, high P + phytase, and low P diets mixed in to simulate feed spillage (showing standard error bars).
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CONCLUSIONS
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With increased intensification of animal production and concerns over P losses from manured soils, reducing dietary P represents a cost-effective way to decrease excreted P. However, there are many interactions between changes in dietary P, bird management, and total and WSP in manures produced to be considered. Several studies have reported that total P in manure can be decreased through diet modification. The present study showed that combining feeding P closer to bird requirements and phytase led to a 42% decrease in total P. As the total P applied in manure controls long term changes in soil test P, diet modification can therefore address concerns over long term buildup of P in soils by decreasing P excreted. However, manure WSP is an indicator for soluble P losses in runoff immediately following land application of manure. We found that water management within pens greatly affected WSP, as spilled water led to elevated moisture under the drinker and this location was where WSP was greatest. Therefore, all efforts should be made to maximize drinker efficiency to minimize spillage and hence manure WSP. Feeding to the P requirement consistently decreased WSP, and phytase either decreased or had no significant effect on manure WSP. Comparing manure from under the feeder to manure from a clean area away from the feeder showed that spilled feed does not have a great effect on manure WSP. Storage of manures from the four diets showed that there should be no concern over feed ingredients such as phytase increasing WSP during storage, although there was a high degree of variability. Therefore, all efforts should be made to encourage implementation of reduced P diets and improve water management to decrease concerns over the environmental impact of manure applications.
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ABSTRACT
INTRODUCTION
