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Poult Sci 2007. 86:225-231
© 2007 Poultry Science Association
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ENVIRONMENT, WELL-BEING, AND BEHAVIOR

Effects of Phosphorus Level and Phytase in Broiler Breeder Rearing and Laying Diets on Live Performance and Phosphorus Excretion1

P. W. Plumstead*, H. Romero-Sanchez{dagger}, R. O. Maguire{ddagger}, A. G. Gernat§ and J. Brake*,2

* Department of Poultry Science, College of Agriculture and Life Sciences, North Carolina State University, Raleigh 27695-7608; {dagger} Grupo Grica, Faculty of Agriculture, University of Antioquia, Medellin, Colombia; {ddagger} Department of Crop and Soil Environmental Sciences, Virginia Tech, Blacksburg 24061; and § Escuela Agrìcola Panamericana, Zamorano, Center for Poultry Research and Teaching, Tegucigalpa, Honduras

2 Corresponding author: jbrake{at}ncsu.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The effects of a reduced dietary nonphytate phosphorus (NPP) level and inclusion of phytase on broiler breeder performance and P concentrations in the litter and manure were investigated. Ross 308 broiler breeder pullets and Ross 344 cockerels were placed sex-separate in a blackout growing house and fed standard starter and grower diets to 9 wk of age. At 10 wk of age, 4 treatments (A, B, C, D) were assigned to each of 4 floor pens of 68 pullets and 1 pen of 50 cockerels. From 10 to 21 wk, treatments A to D contained 0.37, 0.27, 0.27, and 0.17% NPP, respectively, with 300 phytase units (FTU)/ kg of phytase added to treatments B and D. At 21 wk of age, birds were photostimulated and transferred to a two-thirds slat-litter breeder house with 16 pens of 60 pullets and 6 cockerels. A laying diet was fed from 22 to 64 wk and NPP levels of treatments A to D were adjusted to 0.37, 0.27, 0.19, and 0.09%, respectively, and phytase addition to treatments B and D was increased to 500 FTU/ kg. Analysis of the litter from growing pens showed no effect on litter total P when phytase replaced 0.1% of NPP. However, decreasing the dietary NPP by 0.1% without phytase reduced the litter total P by 18%. Water-soluble P (WSP) and the WSP:total P ratio decreased when the grower dietary NPP level was reduced to 0.17% with added phytase and was correlated with litter moisture levels in growing pens. During the laying period, a reduction in NPP from 0.37 to 0.09% with added phytase reduced both the manure total P and WSP by 42%. Hen-day egg production was highest on the lowest NPP diet with phytase, but fertility decreased when the dietary NPP was reduced below 0.37%. Results showed that phytase inclusion in a broiler breeder laying diet at the expense of all added P from dicalcium phosphate reduced the manure total P and WSP concentrations by 42%, with no effect on the number of chicks produced per hen housed.

Key Words: broiler breeder • phosphorus • phytase • environment • litter


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The application of animal manures to land remains the most efficient method of using the large quantities of manure generated by confined animal feeding operations (Olson and Paterson, 2005). However, because of an unfavorable nitrogen:total P ratio relative to crop requirements, the continual application of manures to soils often leads to an accumulation of soil test P concentrations (Sims et al., 2000), which in turn has led to federal regulations that limit the amount of P from manure that can be applied to soils (Environmental Protection Agency, 2003). Further, in addition to total P in poultry litter, the water-soluble P (WSP) fraction has been identified as an important environmental risk factor because P losses in runoff following land application of litter have been related to WSP in the litter applied (Maguire et al., 2005). To date, strategies to decrease P accumulation in soils have focused primarily on reducing both total P and WSP fractions in the litter by reducing levels of inorganic P supplementation to diets in combination with added phytase enzymes (Applegate et al., 2003; Angel et al., 2005). Angel et al. (2000a, b) showed that the dietary nonphytate phosphorus (NPP) levels of broiler diets could be reduced substantially from NRC (1994) recommendations without affecting broiler performance. Applegate et al. (2003) further showed that when combined with phytase, the revised NPP regimens reduced the litter total P and WSP fractions by as much as 30 and 50%, respectively. However, in spite of extensive research investigating the combined effects of NPP and phytase in broilers, comparably few reports have described similar effects on the total P and WSP fractions in manure from broiler breeders. Studies have shown that combinations of reduced dietary NPP and added phytase had either no effect or, in some instances, increased egg production from broiler breeder hens (Berry et al., 2000, 2003; Li et al., 2002; Brake et al., 2003). Because these previous authors did not describe the treatment effects on total P and WSP in the manure or litter, the objectives of the present study were to further evaluate the effects of reduced dietary NPP and phytase on the performance of broiler breeders while also quantifying the potential benefits of these strategies to reduce the total P or WSP concentrations in pullet-rearing litter and broiler breeder manure.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Definitions
Because the dietary NPP and available P (AvP) contents of diets fed to poultry have often been erroneously interchanged, the term AvP, as used in this experiment, refers to relative bioavailable P as determined using a slope ratio assay with monocalcium P as the reference standard (Apke et al., 1987; Soares, 1995), and NPP represents a chemically defined entity calculated by subtracting the analyzed P content of ingredients from their analyzed phytate P content (Angel and Applegate, 2001).

Pullet and Breeder Management
A total of 1,088 1-d-old Ross 308 breeder pullets and 200 one-day-old Ross 344 cockerels were placed in a blackout growing house and reared sex-separate, with either 68 female or 50 male chicks randomly assigned to each of 16 female or 4 male pens of 3.96 x 3.96 m. The lighting program consisted of 23 h of light per day for 1 wk, followed by 8L:16D to 21 wk of age. The management and house infrastructure were as generally described by Brake and Baughman (1989). At 21 wk, 60 pullets from each of the 16 female rearing pens as well as 6 cockerels from the pens of males on the same treatment were moved to each of 16 breeder pens located within a curtain-sided breeder house. The laying pen dimensions were similar to those of the growing house, whereas two-thirds of each breeder pen was covered with raised plastic slats and a scratch area with fresh pine shavings constituted the remaining one-third of each pen. Each pen contained one automatic waterer, one 12-hole galvanized nest box, 5 tube feeders with male exclusion grills for females that were located above the slats, and one tube feeder for males, located over the scratch area. At 20 and 22 wk, the photoperiod was increased to 14 and 15 h, respectively, after which it was further increased to 15.5 h at 5% lay and again to 16 h at 50% lay. All eggs laid were collected twice daily and stored at 18.6°C and 70% RH until incubated in Jamesway 252B incubators (Jamesway Incubator Company, Ft. Atkinson, WI). The fertility of eggs was determined from sets of 60 eggs per pen, which were incubated biweekly from 28 to 64 wk of age. The treatment identity of hatching eggs was maintained by breeder pen throughout the incubation and hatching process. After 21.5 d of incubation, all eggs that did not hatch were broken out and examined macroscopically, and the percentage of fertility and stage of embryonic mortality were calculated. All eggs that were accidentally cracked were deleted from the analyses.

Pullet and Breeder Diets
From placement to 3 wk of age, all chicks received a common pullet starter diet (2,925 kcal/kg of ME and 17.66% CP), followed by a common grower diet (2,925 kcal/kg of ME and 15.96% CP) to 9 wk of age (Table 1Go). From 10 wk of age, 4 female pens and 1 male pen were randomly assigned to 1 of 4 treatment groups (A, B, C, D) that received diets with different combinations of AvP or NPP in the presence or absence of a fungal-derived phytase (Allzyme SSF; Alltech Inc., Nicholasville, KY) during the growing (10 to 21 wk) and laying period (22 to 64 wk; Table 2Go). For the grower period, diets fed to treatment A contained 0.37% NPP with no added phytase. Treatment B contained 0.27% NPP with 300 FTU of phytase. Treatment C contained 0.27% NPP but with no added phytase. The reductions in NPP between treatments A and B were based on the recommendation of the phytase manufacturer that the addition of 300 FTU of phytase in pullet-rearing diets was able to replace the equivalent of 0.10% NPP from dicalcium phosphate. In a similar manner, the NPP level of the grower diet fed to treatment D was reduced by 0.10% from that in treatment C (to 0.17%) while simultaneously adding 300 FTU of phytase. Further, to reduce the phytase contribution from endogenous sources, the wheat bran and a portion of the corn, poultry fat, and vermiculite was removed from the diet formulation and pelleted separately as a premix, which consisted of 37% corn, 58% wheat bran, 1.6% poultry fat, and 3.4% vermiculite. The reduction in basal phytase activity of the pelleted bran premix was confirmed prior to mixing it back into the diets at levels that reflected the original ingredient quantities in each formulation. The treatment identity of pens was maintained during transfer from the rearing facility to the production facility. During the 42-wk breeder phase, the NPP level of treatment A was 0.37% with no added phytase, whereas treatment B contained 0.27% NPP and 500 FTU of added phytase. The NPP level of treatment C was further reduced to 0.19% with no added phytase. Breeder treatment D, with 0.09% NPP, was created by removing all remaining dicalcium phosphate from the breeder diets fed to treatment C while adding 500 FTU of phytase. The phytase included in breeder diets B and D was increased to 500 FTU/kg during the breeder layer phase to increase the likelihood of detecting potentially deleterious effects of phytase on the performance of the broiler breeder progeny, as had been reported previously (Brake et al., 2003).


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  		Table 1. Formulation and calculated analyses of the common broiler breeder starter and grower diets1 fed to 9 wk of age
 

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  		Table 2. Formulation and calculated analyses of dietary treatments fed during the rearing and production phases
 
Manure Collection
Litter samples were collected at 21 wk from 5 locations within each of the 20 growing pens and from 4 locations from each of the 16 breeder pens at 65 wk after the birds had been removed. Sampling areas in the growing pens consisted of 4 areas 1 m from each corner along the diagonal tangent of the pen and 1 area in the center of the pen. Samples from the breeder house consisted of 3 samples from beneath the slatted floor area and 1 sample from the scratch area. The sampling location under the slated floor area was the same in each pen and consisted of 1 sample drawn from under the drinker, 1 sample drawn from under a feeder, and 1 sample drawn from an area not directly under a feeder or drinker. The 5 samples from each growing pen were mixed and a composite sample was prepared, whereas the 4 samples from each breeder pen were analyzed individually. The moisture content of all litter and manure samples was determined by drying samples overnight at 105°C. The analytical procedure for total P and WSP analyses of the litter was as described by Maguire et al. (2006).

Statistical Methods
A pen of birds was the experimental unit for all live production measurements. Egg production, fertility, and hatchability data were analyzed on a cumulative basis from 29 to 64 wk. Litter data from the rearing phase were subjected to one-way ANOVA using a completely randomized design with 5 replicate pens per treatment. Upon initial analysis of the data, a significant correlation was found between litter moisture and litter WSP (r = 0.74, P ≤0.001). To account for this correlation, the percentage of litter moisture was log transformed and then included as a covariate in the subsequent statistical analyses to assess treatment effects on WSP and the ratio of WSP:total P in the rearing litter. Manure samples from breeder pens were analyzed using a split-plot design, with treatment as the main plot and sample area within each pen as the subplot. Because pen was the experimental unit, within-pen variation in the manure analyses was not considered in the estimation of treatment effects during the breeder phase, and spatial effects within individual pens were reported previously by Maguire et al. (2006). The GLM procedure of SAS (SAS Institute, 1996) was used to analyze the continuous variables of the broiler breeder production data. Fertility data were analyzed as categorical data, where each individual egg was taken as a binomial event, either fertile or infertile, using the generalized model (GENMOD) procedure of SAS (SAS Institute, 1996). The results of the rearing litter and breeder manure analyses were interpreted using the MIXED procedure of SAS (SAS Institute, 1996). Means were partitioned using protected LSMEANS, and statements of statistical significance were based on P ≤0.05 unless otherwise stated.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Effect of Treatment on P Excretion
Analyses of the rearing litter showed no reduction in the total P concentration of the litter when 300 FTU of phytase was added to pullet grower diets at the expense of 0.1% NPP at either the 0.37 or 0.27% NPP level (treatments A vs. B and C vs. D; Table 3Go). However, a 0.1% reduction in NPP without the simultaneous addition of phytase decreased the litter total P by 18% with no effects on the WSP (treatments A vs. C). Treatment D exhibited the lowest WSP and also had the lowest WSP:total P ratio because there was a strong correlation between the percentage of litter moisture and WSP concentration (r = 0.74, P ≤0.001), whereas the moisture level in the litter showed no correlation with the litter total P concentration (Table 3Go).


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  		Table 3. Total P and water-soluble P (WSP) in broiler breeder pullet-rearing litter as affected by changes in dietary nonphytate P (NPP) level in pullet grower diets with or without phytase enzyme1 and fed from 10 to 21 wk of age
 
In the breeder manure, a reduction of 0.10% NPP (from 0.37 to 0.27%) with 500 FTU of phytase had no effect on total P or the WSP:total P ratio but decreased the WSP by 28.6% (treatments A vs. B; Table 4Go). The further reduction in NPP from 0.27 to 0.19% without added phytase decreased the manure total P concentration by an additional 29% but had no effect on WSP or the WSP:total P ratio (treatments B vs. C). A somewhat surprising result was that the further reduction in dietary NPP, from 0.19 to 0.09%, in combination with 500 FTU of phytase had no additional effect on either the litter total P or percentage of WSP (treatments C vs. D; Table 4Go). The overall reduction in dietary NPP, from 0.37 to 0.09%, with 500 FTU of added phytase decreased both the total P and WSP by 42% without altering the relative proportion of WSP, as judged by the WSP:total P ratio (treatments A vs. D; Table 4Go).


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  		Table 4. Total phosphorus (P) and water-soluble P (WSP) in manure from breeders as affected by changes in nonphytate P (NPP) level of breeder layer diets with or without phytase enzyme1 and fed from 22 to 64 wk of age
 
Treatment Effects on Broiler Breeder Performance
The removal of all added dicalcium phosphate with the simultaneous addition of 500 FTU of phytase (treatment D) increased hen-day egg production relative to all other treatments (Table 5Go), whereas there was no effect of dietary treatment on the percentage of female or male breeder mortality (data not shown). The percentage of fertility decreased when dietary NPP was reduced below 0.37% (treatments B, C, D), but there was no treatment effect on the number of eggs or chicks produced per hen housed. The increased hen-day egg production of hens that received the 0.09% NPP + phytase treatment (treatment D) contributed to a reduction of feed consumed per dozen eggs produced (P = 0.059).


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  		Table 5. Effect of varying dietary nonphytate P (NPP) level with or without added phytase enzyme1 on performance variables of broiler breeders from 29 to 64 wk of age
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Although the authors are not aware of previous research that reported effects of the level of NPP and inclusion of phytase on broiler breeder pullets housed in floor pens, comparable research in broilers has shown that phytase addition, in combination with a reduction in dietary NPP closer to broiler requirements, decreases both total P and WSP in the broiler litter by as much as 30 and 50%, respectively (Applegate et al., 2003). In one of the few research papers that investigated these effects in broiler breeder pullets, Lilburn et al. (2004) reported that replacing 0.10% NPP with phytase in 6-wk-old broiler breeder pullets housed in battery cages decreased fecal P by 17% during a 48-h collection study. However, these results cannot be extrapolated to breeder pullets reared on litter because of the considerable recycling of fecal P by birds housed on litter (Harms et al., 1984). In contrast to the results of Applegate et al. (2003), our investigation using broiler breeder pullets reared on litter showed no effect on litter total P when phytase replaced 0.10% of the NPP in diets with either 0.37 or 0.27% NPP (Table 3Go). Importantly, the same reduction of 0.1% NPP (from 0.37 to 0.27% NPP) without adding phytase decreased the litter total P concentration by 18.0% (Table 3Go). This lack of an effect of phytase on reducing the litter total P can most likely be explained on the basis of the recycling of P from the litter. Tamin et al. (2004) showed that, in the absence of dietary calcium, broilers had a high inherent capacity to hydrolyze phytate P, as evidenced by its disappearance from the small intestine. Because these breeder pullets were feed-restricted and housed in floor pens over a 22-wk period, they could also be expected to be able to hydrolyze a considerable amount of the residual phytate P in the litter they consumed. Even though we did not verify this mechanism by means of a mass balance study, one could expect that the digestion of residual bound phytate in the litter would, over time, effectively ameliorate the potential benefits of phytase, and that this would also explain why a reduction in litter total P was observed only when dietary NPP was reduced without the simultaneous addition of phytase. However, although reductions in litter total P may potentially be explained on this basis, previous reports on WSP showed the effects of reduced dietary NPP with or without phytase to be variable at best (Angel and Applegate, 2001). Results from some broiler studies showed that phytase application in combination with reduced NPP did not alter the proportion of WSP in the litter (Applegate et al., 2003), whereas other studies reported a decrease in the proportion of WSP (Saylor et al., 2001), and in one case, phytase supplementation even increased the proportion of WSP in broiler litter (Vadas et al., 2004). To help explain these conflicting results, Leytem et al. (2006) showed that a 94% correlation existed between the proportion of manure total P that was WSP and the amount of manure P that was present as phytate P. Microbial fermentation of the phytate P fraction was also shown to increase WSP in the feces (Angel et al., 2005), whereas the proportion of WSP was further influenced by the manure moisture level (Maguire et al., 2006). The effects of microbial fermentation of the phytate P fraction over time were also previously demonstrated by the work of McGrath et al. (2005), who showed that the proportion of WSP increased during long-term storage of wet, but not dry, broiler litter. Because litter from the broiler breeder pullets was kept in the rearing house for 22 wk, the effects of moisture and the extent of microbial degradation of the phytate P fraction may have been greater than in conventional broiler studies conducted over a much shorter time period. These effects of moisture on litter WSP were suggested by our data, which showed a highly significant correlation (74%) between the percentage of litter moisture and the WSP concentration. Further, when moisture was included as a covariate in a model to explain treatment differences in the WSP fraction, both the moisture level and the dietary treatment had significant effects on the percentage of WSP, but only the litter moisture level was influential in altering the WSP as a proportion of litter total P (Table 3Go). After correcting for the effects of litter moisture, our data supported the previous findings of Applegate et al. (2003), specifically, that reduced-NPP diets in combination with phytase reduced the percentage of WSP in the litter but had no effect on the relative proportion of WSP:total P.

In a similar manner, reductions in the dietary NPP with or without phytase did not affect the proportion of WSP in manure produced from 22 to 64 wk of age. The concentrations of total P and WSP in the breeder manure again reflected the positive benefits that could be obtained by decreasing dietary NPP levels, either alone or in combination with dietary phytase enzymes, and showed a potential reduction in total P of 39 or 42% when NPP was reduced from 0.37% to either 0.19 or 0.09% without or with phytase, respectively (Table 4Go). Although the reduction in NPP from 0.19 to 0.09% while adding phytase provided no additional benefits in further reducing the manure total P, this did allow for the complete removal of all added inorganic phosphate from the diet while also having a positive effect on the percentage of hen-day egg production. Li et al. (2002) previously reported an increased egg production of 0.55% from 26 to 40 wk of age and a 2% improvement in hatchability when NPP was reduced from 0.30 to 0.10% and phytase was added to the diets of broiler breeders housed in slat-litter pens. However, because there were only 2 dietary treatments in their study, it was not possible to differentiate between the effects of NPP and phytase. In contrast to the positive effect on egg production that was shown in our study and in the study by Li et al. (2002), Brake et al. (2003) were unable to find any change in broiler breeder performance when all added inorganic P was replaced by phytase in 2 previous studies. The reduction in fertility that occurred in our study when dietary NPP was reduced below 0.37% has not been previously reported in broiler breeders. The effect of NPP level on fertility in our study might have been related to the early start (10 wk of age) of the reduced NPP treatments and warrants further study. Nevertheless, in spite of the potentially detrimental effect on fertility, the slightly higher egg production of treatments that had received less than 0.37% NPP, although not statistically significant, contributed to there being no treatment differences in the number of chicks produced per hen.

Our calculations showed that a broiler breeder hen housed to 64 wk of age consumed 397 g of total dietary P, of which approximately 41%, or 165 g/bird, was excreted in the litter and manure produced (Plumstead et al., 2005). Data from the present study suggest that the replacement of 0.10% dietary NPP with phytase had little effect on reducing the total litter P in diets fed to pullets that had been reared on litter. However, once transferred to a two-thirds slat-litter breeder house, the replacement of all added inorganic P in the diets fed to broiler breeders with 500 FTU of phytase could provide substantial benefits to producers by reducing the concentrations of P in manure from broiler breeders by as much as 42% without affecting the number of chicks produced per breeder hen housed.


   ACKNOWLEDGMENTS
 
This research was partially funded by the United Soybean Board and the North Carolina Agricultural Foundation.


   FOOTNOTES
 
1 The use of trade names in this publication does not imply endorsement of the products mentioned or criticism of similar products not mentioned. Back

Received for publication June 20, 2006. Accepted for publication October 13, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Angel, R., and T. Applegate. 2001. Phytase use—What do we know? Pages 250–263 in Proc. 62nd Minnesota Nutrition Conf. and Minnesota Corn Growers Assoc. Technol. Symp., Bloomington, MN. Minnesota Corn Growers Assoc., Shakopee.

Angel, R., T. J. Applegate, and M. Christman. 2000a. Effects of dietary non-phytate phosphorus (nPP) on performance and bone measurements in broilers fed on a four phase feeding system. Poult. Sci. 79(Suppl. 1):21–22. (Abstr.)

Angel, R., T. J. Applegate, M. Christman, and A. D. Mitchell. 2000b. Effect of dietary non-phytate phosphorus (nPP) level on broiler performance and bone measurements in the starter and grower phase. Poult. Sci. 79(Suppl. 1):22. (Abstr.)

Angel, R., W. J. Powers, T. J. Applegate, N. M. Tamin, and M. C. Christman. 2005. Influence of phytase on WSP in poultry and swine manure. J. Environ. Qual. 34:563–571.[Abstract/Free Full Text]

Apke, M. P., P. E. Waibel, K. Larntz, L. Metz, S. L. Noll, and M. Walser. 1987. Phosphorus availability bioassay using bone ash and bone densitometry as response criteria. Poult. Sci. 66:713–720.[ISI][Medline]

Applegate, T. J., B. C. Joern, D. L. Nussbaum-Wagler, and R. Angel. 2003. Water soluble phosphorus in fresh broiler litter is dependent upon phosphorus concentration fed but not on fungal phytase supplementation. Poult. Sci. 82:1024–1029.[Abstract/Free Full Text]

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Brake, J., and G. R. Baughman. 1989. Comparison of lighting regimens during growth on subsequent seasonal reproductive performance of broiler breeders. Poult. Sci. 68:79–85.

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