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a Department of Poultry Science, North Carolina State University, Raleigh, NC 27695
b School of Veterinary Medicine, University of Pennsylvania, Kennett Square, PA 19348
c Department of Plant and Soil Science, University of Delaware, Newark, DE 19716
d Department of Agronomy, Purdue University, West Lafayette, IN 47907
* Corresponding author (rory_maguire{at}ncsu.edu)
Received for publication October 29, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSTRATEGIES TO REDUCE THE...IMPACT OF DIET STRATEGIES...IMPACT OF STORAGE ON...ENVIRONMENTAL IMPACT OF DIET...CONCLUSIONSREFERENCES |
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Abbreviations: DRP, dissolved reactive phosphorus • HAP, high available phosphorus • NPP, non-phytate phosphorus • WSP, water-soluble phosphorus
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSTRATEGIES TO REDUCE THE...IMPACT OF DIET STRATEGIES...IMPACT OF STORAGE ON...ENVIRONMENTAL IMPACT OF DIET...CONCLUSIONSREFERENCES |
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STRATEGIES TO REDUCE THE PHOSPHORUS CONCENTRATION IN DIETS |
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TOPABSTRACTINTRODUCTIONSTRATEGIES TO REDUCE THE...IMPACT OF DIET STRATEGIES...IMPACT OF STORAGE ON...ENVIRONMENTAL IMPACT OF DIET...CONCLUSIONSREFERENCES |
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Reducing overfeeding of P involves clearly identifying critical levels of P for individual species and then formulating feeds as closely as possible to these requirements, such as guidelines issued by the National Research Council (1994)(1998). But actual diets formulated and implemented often contain more P than NRC recommendations. For instance, several surveys of dairy farms have shown that P concentrations in lactating cow rations were 20 to 40% greater than NRC recommendations (Shaver and Howard, 1995; Sansinena et al., 1999; Satter and Wu, 1999; Sink et al., 2000; Dou et al., 2003). Furthermore, NRC recommendations have not always kept pace with rapidly emerging new information on dietary requirements or changing animal genetics. For example, in a recent review article, the Council for Agricultural Science and Technology (2002) stated that "it is clear that the NRC's 1994 recommendations for nonphytate P concentrations no longer apply to today's poultry genotypes." The review also states that today's poultry require less NPP than the NRC recommends (Council for Agricultural Science and Technology, 2002). As animals age, they generally require less P as their bone development matures. Increasing the number of feeding phases with a decreasing of the P concentration in each successive phase as the animals mature, especially in the case of swine and poultry, can therefore reduce overfeeding of P.
There are several strategies now used to increase P utilization by monogastrics, including (i) adding the enzyme phytase to increase digestion of dietary phytate-P, (ii) adding citric acid to reduce gut pH and increase the effectiveness of phytase, (iii) adding vitamin D3 or its derivatives to increase uptake of P from the gut, and (iv) breeding of HAP crops (sometimes called low phytate-P) for animal feeds that decrease the need for NPP supplements (Council for Agricultural Science and Technology, 2002; Harper et al., 1997; Huff et al., 1998; Cromwell, 1996). These strategies and their impact on animal performance have been covered in depth elsewhere so they will not be elaborated on here. However, these strategies can reduce dietary P without negatively impacting animal performance (Council for Agricultural Science and Technology, 2002; Dou et al., 2002; Applegate et al., 2003; Miles et al., 2003; Overturf et al., 2003).
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IMPACT OF DIET STRATEGIES ON PHOSPHORUS FORMS IN MANURE |
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For dairy cattle, feeding strategies to decrease fecal P excretion have focused on reducing P overfeeding, because they have the ability to digest phytate-P. Data summarized in Table 2 include three types of investigations: (i) research feeding trials with total collections measuring the mass of feed P intake and/or fecal P excretion, reported as g P intake and/or excretion per cow per day (Experiments 1–4 in Table 2); (ii) research feeding trials with grab sample collection measuring the concentration, not the mass, of P in feeds and/or feces, reported as g kg–1 dry matter (Experiments 5 and 6); and (iii) farm-based sampling and analysis (Experiments 7 and 8) measuring P concentrations, also reported as g kg–1 dry matter.
Some of the research feeding trials exhibited apparent P deficiency at the lowest P level (Experiments 1, 4, and 5), whereas the trial in Experiment 3 included a diet that was near the greater end of the P feeding spectrum. Regardless of the range of dietary P included in the individual trials or the commercial farms, greater dietary P clearly and consistently resulted in greater fecal P in all investigations (Table 2). Based on farm-based data (Experiments 7 and 8), the reduction of P overfeeding from a commonly fed level of 4.5 to an adequate level of 3.5 g kg–1 led to fecal total P reduction of 20% or more (Table 3).
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The effects of phytase inclusion in poultry and swine diets on manure WSP have also shown promise. In most studies, phytase use, which is always done in combination with a reduction in dietary NPP to account for increased digestion of phytate P, has decreased or had no significant impact on WSP in litters and manures (Table 1). For WSP in litter sampled after two flocks of turkeys and after three flocks of broilers, Maguire et al. (2004) reported no significant difference between diets formulated with and without phytase. Penn et al. (2004) reported that WSP in turkey manure was decreased by approximately 50% in phytase diets compared with a standard turkey diet. In a study with 8- to 15-d-old turkeys, Maguire et al. (2003) reported that inclusion of dietary phytase had no significant effect on WSP in turkey manures. For a full flock of broilers, Applegate et al. (2003) concluded that "phytase supplementation did not affect solubility of P in the litter regardless of P feeding program." Experiments with swine have also shown that proper use of phytase either decreases or has no effect on manure WSP. Smith et al. (2004a) reported that phytase significantly decreased WSP in swine manures by 17%. Baxter et al. (2003) showed that phytase did not increase swine manure WSP and even decreased manure WSP in one of two dietary comparisons. Finally, in a paper that reported results from three broiler, one turkey, and one swine experiment, Angel et al. (2005) concluded that dietary phytase does not affect WSP when used properly (i.e., with appropriate reductions in dietary NPP). Microbial activity in the lower gut (where the animal does not derive benefit from P) can lead to hydrolysis of dietary phytate-P, leading to nonsoluble P becoming soluble without dietary phytase additions. For example, Ajskaiye et al. (2003) reported a two- to fourfold increase in the WSP content between ileal digesta and excreta for swine.
A few studies, however, have shown that diets including phytase may increase manure WSP and this has generated some controversy about the environmental benefits of this dietary amendment (DeLaune et al., 2001, 2004; Vadas et al., 2004; Waldroup, 2002). Miles et al. (2003) reported that phytase increased WSP after one flock, but not after two or three flocks of broilers grown on the same bed of litter. In fresh broiler excreta, Vadas et al. (2004) reported that phytase increased WSP, but after composting, phytase had no consistent effect on manure WSP. DeLaune et al. (2001)( 2004), using broiler litters from a three-flock floor pen study in Delaware, reported that phytase increased WSP in litter from a normal broiler diet, but decreased WSP in litter from a diet formulated with phytase and HAP corn. However, analyses of these same litters conducted immediately after litter removal from the floor pens had not shown an increase in litter WSP due to phytase use (Saylor et al., 2001). One explanation may be that after the end of the Delaware floor pen studies, the litters were stored outside for six to eight months. During this time, plastic covers blew off some of the litter stockpiles, resulting in rainfall wetting some, but not all, of the stockpiled litters (G.W. Malone, University of Delaware, personal communication, 2004). Recent research has shown that WSP increases in broiler litter samples stored under wet conditions (McGrath et al., 2005).
Combining HAP corn and phytase use has usually been more effective, reducing manure WSP 27 to 49% with broilers, 47% with turkeys, and 34% with swine (Table 1). Miles et al. (2003) reported that after three flocks of broilers fed a HAP corn diet were grown on the same litter, inclusion of dietary phytase decreased WSP in broiler litters. In broiler experiments, Smith et al. (2004b) reported that phytase had no significant effect on litter WSP in a normal diet, but decreased WSP in litter from a HAP corn diet. Comparing diets with HAP corn to those with HAP plus phytase, Moore et al. (1998) showed no significant differences in WSP between these diets throughout two flocks. While the use of HAP corn in combination with phytase appears to be a very promising approach to reduce total and WSP excretions by poultry and swine, the potential for widespread use of HAP corn, or the more recently developed HAP soybean, is uncertain today. Full-scale commercial production has been limited thus far by ongoing concerns about decreased yield potentials with HAP feed grains (Raboy, 2002). There are also logistical concerns, such as the need for most grain producers to primarily grow HAP grains to produce a quantity sufficient to modify animal diets enough to impact manure P production.
Similar benefits of dietary modification were reported for dairy cattle, where feeding trials using diets containing reduced P concentrations resulted in linear decreases in manure WSP (Table 2; Dou et al., 2002). On-farm sampling conducted at 33 commercial dairies further confirmed that decreasing dietary P leads to less WSP in dairy feces (Chapuis-Lardy et al., 2004; Table 2). As indicated by the slopes of the linear regression equations (Experiments 7 and 8 in Table 2), each unit of dietary P decrease (g P kg–1 feed dry matter) resulted in a decrease of about 1 g WSP kg–1 dry matter in feces. Therefore, if dietary P were reduced from a commonly fed level of 4.5 to an adequate level of 3.5 g kg–1, fecal WSP would be reduced by approximately 25% (Table 3). It needs to be noted that the linear regression derived from the feeding trials (Experiment 6 in Table 2) has a slope of 1.37, which is greater than the farm-based results. The difference could be partially attributed to the fact that feeding trials usually maximize treatment (dietary P) effects by controlling other animal health and nutritional factors as much as possible while commercial farms often cannot maintain such strict controls. Also, the laboratory procedures for determining WSP differed between experiments; in Experiment 6, 0.3-g dried-ground samples were extracted in 30 mL of water, whereas Experiments 7 and 8 used 2-g wet samples in 98 mL of water.
Soluble Phosphorus to Total Phosphorus Ratio in Manure
The WSP to total P ratio could be very important if manure applications move away from nitrogen and toward P-based nutrient management plans, as is becoming more common in areas of intensive animal production. If diet manipulation leads to increasing WSP to total P ratios (despite decreasing manure total P) and manures are applied at a P-based rate, then the greater WSP application could lead to increased concerns about dissolved reactive phosphorus (DRP) losses in runoff immediately following manure application.
Feeding P to requirement greatly decreased the WSP to total P ratio in broiler litter, but increased it in turkey litter (Table 1). Combining feeding to requirement and dietary phytase led to decreasing the percent of total P that was soluble in broilers while increasing it in turkeys. For poultry, four studies showed that phytase alone reduced the WSP to total P ratio, while two studies suggested phytase increased the WSP to total P ratio and two studies showed little effect. For swine, results for the impact of phytase alone and HAP corn alone on the WSP to total P ratio were similarly mixed. When phytase was combined with HAP corn, one study reported an increase of 5% in the WSP to total P ratio (Baxter et al., 2003), while the other six studies showed little impact or a decrease in the solubility of total P.
Although there were some studies that indicated that feed strategies increased the WSP to total P ratio of manure produced, there was no consistent trend for any feeding strategy that suggested this strategy could increase DRP losses in runoff following land application of manure according to a P-based nutrient management plan. However, the variability in the data suggests that there is still work to be done on refining diets to ensure that diet modification to reduce manure P consistently decreases P losses in runoff immediately following manure applications.
In the case of dairy, less dietary P led to a reduced ratio of WSP to total P in feces. This was true for all studies (feeding trials as well as farm-based results) where data are available. This point is clearly shown in Fig. 2 , where there was a highly significant (P < 0.01) relationship between dietary P and the WSP to total P ratio in feces for data from studies in Table 2. Therefore, less dietary P for dairy will decrease the application rate of WSP even when manures are applied at a P-based rate, decreasing the risks of DRP losses in runoff.
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IMPACT OF STORAGE ON PHOSPHORUS FORMS AND SOLUBILITY IN LITTER AND MANURE |
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Baxter et al. (2003) evaluated the impact of diet modification on changes in P solubility in swine manure stored over 150 d. The percentage of total P that was WSP decreased with increasing storage time from an average of 51.7% initially to 27.3% after 150 d of storage, with most of this reduction occurring between 30 and 90 d (P < 0.001). These trends in reducing WSP with time were consistent for all diets with and without phytase and HAP corn (Baxter et al., 2003). Changing from a normal diet to one with phytase and/or HAP corn had little effect on the WSP to total P ratio in swine manure, with the ratio ranging from 47 to 55% for all manures. After 150 d of storage, there were no significant differences in the WSP to total P ratios for these manures (Baxter et al., 2003).
McGrath et al. (2005) stored broiler litters from diets high and low in NPP with and without phytase at 20 and 40% moisture for 440 d and analyzed P forms. Trends in P forms remained similar for the dry litters (20% moisture) over 440 d of storage, with inorganic P being greater in litters from diets that received more NPP supplementation. However, in the litters stored wet WSP increased significantly in all litters, although trends between treatments remained the same. McGrath et al. (2005) attributed this increase in WSP to microbial degradation of phytate-P, as inorganic P increased at the expense of phytate-P.
Vadas et al. (2004) measured WSP in fresh broiler manure from several diets with and without phytase and again several months later after storing frozen in the laboratory with several freeze–thaw cycles. They reported that WSP averaged 52% less in the fresh samples than in the ones stored for several months, "but the trends for the effect of diet on WSP were the same at both times." Composting broiler manures with straw and wood chips decreased total P on average by 61% and WSP by 82%, with the decreases in WSP being greater in manures from diets that included phytase (Vadas et al., 2004). Angel et al. (2005) investigated the impact of microbial activity versus added dietary phytase on the solubility of P in litters and manures from four poultry and swine studies during a 72-h lab incubation, by using boiling and adding antibiotics to manures. They concluded that "any increase in WSP content following excretion is due to microbial activity" (Angel et al., 2005).
These studies indicate that dietary amendment did not significantly alter processes that control WSP during storage. For example, there was no carryover effect of dietary phytase continuing to release soluble P from phytate-P in stored manure. The high degree of temporal variability of WSP in manures during storage indicates the importance of sampling WSP as close to time of application as possible.
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ENVIRONMENTAL IMPACT OF DIET STRATEGIES TO REDUCE PHOSPHORUS |
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Phosphorus Losses in Runoff
As previously mentioned, DRP in runoff from soils immediately following manure-amendment has been linked to WSP in the manure applied (Kleinman et al., 2002). However, concerns over DRP losses following manure applications have been shown to be generally short-term as WSP additions have had the greatest impact on the first runoff event, with the impact of WSP additions decreasing with increasing number and duration of rain events (Maguire et al., 2004; Penn et al., 2004; Vadas et al., 2004; Gilley et al., 2001). This decrease in DRP loss with increasing number of runoff events is probably due to removal of soluble P in runoff as well as adsorption of P by soils. Total P in runoff has been shown to be not as sensitive as DRP to changes in P in manure due to dietary modification, as sediment loss and hence soil total P controls total P loss to a large extent (Vadas et al., 2004).
Swine
For swine manure from diets with and without phytase, Smith et al. (2004a) reported that even though the phytase diet reduced WSP in the manure there were no significant differences in the DRP concentrations in runoff from soils amended with these two manures. For three soils amended with swine manure, Gilley et al. (2001) observed that the phytase diet led to consistently lower concentrations of DRP in runoff initially than HAP corn or traditional corn diets, although this was not always significant. There was no consistent trend in total P loss between soils amended with manure from HAP corn, phytase, or traditional corn diets (Gilley et al., 2001). All of these studies have reported either a significant decrease in P (especially DRP) in runoff or no significant difference between reduced P and standard diets, suggesting that diet modification in swine can have a beneficial impact on reducing P losses from swine manure-amended soils.
Poultry
Penn et al. (2004) reported runoff DRP and total P from soils amended with turkey manure from diets with combinations of reduced P, phytase, and HAP corn. The DRP and total P concentrations in runoff were generally similar between treatments throughout three runoff events, although the HAP corn treatment had a greater DRP concentration in the first runoff event and in spite of the fact that diet modification reduced manure WSP to total P and thus manure WSP applied (Penn et al., 2004). Vadas et al. (2004) reported that even though dietary phytase increased WSP in broiler manure, runoff DRP and total P from soils amended with manure from normal and phytase diets were not significantly different. Smith et al. (2004b) reported that runoff DRP concentrations were less from plots amended with broiler litter from a phytase diet than a normal diet, although this was no longer significant after three rainfall events. Comparing plots amended with broiler litter from diets including HAP corn with and without phytase, the phytase did not affect runoff DRP concentrations, which were similar to the phytase diet without HAP corn (Smith et al., 2004b). Maguire et al. (2005) incorporated turkey litter into soils at the same rate of plant available nitrogen. They reported that in six comparisons between equivalent treatments with and without phytase, phytase significantly increased DRP in the first runoff event once, decreased DRP once and had no significant effect on four comparisons. For the second runoff event on Day 7, DRP concentrations were greatly reduced and statistically identical for turkey litter–amended soils from all diets (Maguire et al., 2005). Feeding P closer to requirement in turkeys consistently led to reductions in DRP in runoff (Maguire et al., 2005). McGrath et al. (2005) conducted box runoff studies under simulated rainfall with broiler litter from diets high and low in dietary NPP, with and without phytase, incorporated into soils at the same rate of total P. The litters from the high P diets led to greater application rates of WSP to the soils than litters from the low NPP diets, and this greater WSP application rate led to slightly greater DRP in runoff from soils amended with litters from the high P diets, although not significant. Dietary phytase had no impact on DRP in runoff from litter-amended soils (McGrath et al., 2005).
Some runoff studies showed small increases in runoff DRP that were not significant (Vadas et al., 2004; Smith et al., 2004a). However, runoff studies generally showed a decrease in DRP concentration or no significant difference in runoff DRP and total P concentrations from soils amended with manures from reduced P diets compared with normal diets. This suggests that diet modification to reduce dietary P will not increase DRP or total P losses and in some cases will decrease DRP in runoff in the short term immediately following manure and litter applications. In particular, reducing overfeeding of P shows promise.
Dairy
For dairy, the effect of low vs. high P diets on P runoff was investigated by Ebeling et al. (2002) in a field study with no till corn. Dairy manures (feces only, no bedding) from a low P diet (3.1 g kg–1) vs. a high P diet (4.9 g kg–1) were applied at the same manure rate (56 wet Mg h–1), resulting in 40 and 108 kg P ha–1, respectively. In addition, manure from the high P diet was also applied at a reduced rate (21 wet Mg ha–1) to result in an equivalent P rate of 40 kg P ha–1. Runoff was generated using simulated rainfall and runoff samples collected in June (approximately 10 d after manure application) and once again in September after corn silage harvest. Natural runoff was collected from November to July in the following year. At equal manure application rates, DRP in June runoff from the high P diet manure was 10 times greater than the low P diet manure, and four times greater at the equivalent P rates. Phosphorus losses in September and the natural runoff samples afterward were less than June samples, but treatment effect was the same as in June. Clearly manure from a high P diet had greater DRP in runoff, even applied at the same P rate, presumably because of greater manure WSP (although the study did not measure WSP in the manure samples).
Soil Test Phosphorus
Over the long term, total P application controls changes in soil test P that, in turn, exerts a strong influence on P losses in runoff (Sims et al., 2000). Several studies have linked soil test P to P losses in runoff when there has been no recent manure application (Pote et al., 1999). As land application of manure has been generally the only economic way to use manure, the surplus of P in manure in areas of intensive animal production tends to accumulate in agricultural soils (Sims et al., 2000). As previously discussed, diet modification can be used to decrease total P in manure and associated P surpluses, so modifying diets should be able to limit soil test P levels if the P in manure from modified diets affects soil test P in the same way as total P in standard manures.
Few studies have reported the impact of diet modification on soil test P in soils amended with manure from modified diets. Maguire et al. (2004) performed an incubation experiment with four soils and turkey and broiler litter from diets high and low in P, with and without phytase, with the litters incorporated into the soils at the same total P rate (150 kg P ha–1). After one month, the Mehlich-3 P concentrations in soils were very similar between treatments indicating that it was the total P application rate that controlled changes in Mehlich-3 P rather than the form in the manure (Maguire et al., 2004). Maguire et al. (2003) also found that Mehlich-3 P in soils was affected by total P application rate for soils amended with turkey manure. However, under nitrogen-based management, applications of litter from traditional diets led to greater increases in Mehlich-3 P than adding litter from reduced P diets, due to greater total P rate (Maguire et al., 2004). Toor et al. (2005b) added dairy manure from high and low P diets to soils at a rate of 150 kg P ha–1, and measured WSP and Mehlich-3 P after 21 d. There were no significant differences in WSP or Mehlich-3 P between soils amended with manures from the high and low P diets after 21 d. Toor et al. (2005b) concluded that when manures are added to soils at the same rate of total P, the solubility or bioavailability of P in soils will be the same.
Maguire et al. (2005) amended soils with turkey litter high and low in P with and without phytase at the same rate of total nitrogen (which applied different rates of total P). Mehlich-3 P and WSP were measured in the soils immediately before runoff generation under simulated rainfall 1 and 7 d after litter application. Increases in both WSP and Mehlich-3 P following litter additions followed the same trend as total P additions and phytase in the diet had no impact on the WSP in soils (Maguire et al., 2005). McGrath et al. (2005) applied broiler litter from high and low P diets with and without phytase to soils at the same rate of total P, and measured WSP and Mehlich-3 P after one day. A greater application of WSP in the litter from the high P diet (22.6 kg WSP ha–1) than the low P plus phytase diet (14.4 kg WSP ha–1) did not result in any significant differences in soil WSP or Mehlich-3 P, again suggesting that the total P application rate is the determining factor. Maguire et al. (2003) reported that WSP in soils was initially controlled by WSP additions in turkey manure, but this dependence decreased with time. Therefore, any dietary strategy that could decrease WSP in manure generated could reduce WSP in amended soils.
As the P in manures from modified diets has tended to affect soil test P values in the same way as total P in manures from modified diets, implementing diet modification could go a long way toward decreasing P losses from manure-amended soils in the long-term by reducing P surpluses and hence buildup of soil test P.
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CONCLUSIONS |
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As regulations push manure applications away from N and toward P-based nutrient management plans, the importance of the WSP to total P ratio becomes very important. Most strategies to reduce dietary P did not increase the WSP to total P ratio, but the results for phytase were variable because total P reductions sometimes exceeded WSP reductions. Therefore, further research should be undertaken to maximize reductions in both total and particularly WSP in manures produced. Corn and soybeans make up the majority of feed concentrates and future development of HAP versions of these and other grains, in combination with feed additives such as phytase, seem to promise great benefits in terms of reducing not only total P but also WSP in manures from poultry and swine. These reductions in manure total P production will be able to completely remove surpluses of P in some cases, preventing accumulation of soil test P and excessive losses of P. However, some geographical areas will require other approaches in addition to dietary amendment (such as transporting of manure, stabilization of manure P) to achieve P mass balance and/or environmental protection. However, dietary modification to reduce P was shown to be cost effective and can save money in some cases, making this a more attractive best management practice to reduce P losses from agriculture than most other approaches.
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