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Effects of Dietary Fiber and Reduced Crude Protein on Ammonia Emission from Laying-Hen Manure¹

S. A. Roberts^*, H. Xin, B. J. Kerr, J. R. Russell^* and K. Bregendahl^*,2

^* Department of Animal Science, and Department of Agricultural and Biosystems Engineering, Iowa State University, Ames 50011; and Swine Odor and Manure Management Research Unit, Agricultural Research Service, USDA, Ames, IA 50011

² Corresponding author: kristjan{at}iastate.edu

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Ammonia (NH₃) emission is a major concern for the poultry industry. The objective of this research was to determine whether inclusion of dietary fiber and a reduced dietary CP content would decrease NH₃ emission from laying-hen manure. A total of 256 Hy-Line W-36 hens were fed diets with 2 levels of CP (normal and reduced) and 4 fiber treatments in a 2 x 4 factorial arrangement. The fiber treatments included a corn and soybean meal-based control diet and diets formulated with either 10.0% corn dried distillers grains with solubles (DDGS), 7.3% wheat middlings (WM), or 4.8% soybean hulls (SH) to contribute equal amounts of additional neutral detergent fiber. The CP contents of the reduced-CP diets were approximately 1 percentage unit lower than those of the normal-CP diets. All diets were formulated on the basis of digestible amino acid content and were formulated to be isoenergetic. Fresh manure was collected such that pH, uric acid, and Kjeldahl N contents could be measured. The NH₃ emission from manure was measured over 7 d by placing pooled 24-h manure samples in NH₃ emission vessels. Data were analyzed by ANOVA with Dunnett’s multiple-comparisons procedure to compare results from the fiber treatments with the control, whereas the main effect of protein was used to compare the normal- and reduced-CP treatments. Dietary corn DDGS, WM, or SH lowered (P 0.01) the 7-d cumulative manure NH₃ emission from 3.9 g/kg of DM manure for the control to 1.9, 2.1, and 2.3 g/kg of DM manure, respectively, and lowered (P < 0.05) the daily NH₃ emission rate. Results of this study showed that dietary inclusion of 10.0% corn DDGS, 7.3% WM, or 4.8% SH lowered NH₃ emission from laying-hen manure; however, reducing the CP content by 1 percentage unit had no measurable effect on NH₃ emission.

Key Words: ammonia emission • corn dried distillers grains with solubles • reduced-protein diet • soybean hull • wheat middlings

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Ammonia is a major aerial pollutant lost from livestock operations, with domestic animals being the largest global contributor of atmospheric NH₃ emissions (Aneja et al., 2006) and poultry (including laying hens) being the largest contributor among domestic animals in the United States (EPA, 2004). Not only can NH₃ adversely affect health and production by contributing to corneal ulcers, deciliation of the trachea, impaired macrophage function, decreased lung function, lower egg production, and lower BW gains (Kling and Quarles, 1974; Nagaraja et al., 1983; Carlile, 1984; Deaton et al., 1984; Omland, 2002), but it may also cause eutrophication of surface water resources and nuisance odors (De Boer et al., 2000; Angus et al., 2003; Ritz et al., 2004). The Federal Comprehensive Environmental Response, Compensation, and Liability Act (CERCLA) and Emergency Planning and Community Right to Know Act (EPCRA) require reporting of NH₃ releases above 45 kg/d per animal-housing site. The Occupational Safety and Health Administration (OSHA) has set the NH₃-exposure threshold at 50 ppm averaged over an 8-h workday, whereas the National Institute of Occupational Safety and Health (NIOSH) has established a threshold limit of 25 ppm averaged over 8 h. The United Egg Producers 2006 Animal Husbandry Guidelines state that atmospheric concentrations of NH₃ should ideally be below 25 ppm and should not exceed 50 ppm (United Egg Producers, 2006). Maintaining air NH₃ concentrations below these maximum allowable amounts is difficult in high-rise laying-hen houses, especially during winter when ventilation is decreased (Liang et al., 2005). To comply with government and industry-group regulations, minimize health risks, and optimize egg-production potential, egg producers need to either decrease hen numbers at each production site or develop methods to lower NH₃ emission with current hen populations.

Adjusting the diet composition may decrease the amount of NH₃ that is lost from laying-hen facilities. Inclusion of feed ingredients with high concentrations of fiber has been shown to lower NH₃ emission from pigs, and reduced-CP diets have been shown to decrease N excretion from pigs, broilers, and laying hens (Summers, 1993; Canh et al., 1997, 1998b; Bregendahl et al., 2002; Shriver et al., 2003). We hypothesized that reducing the dietary CP content and including high-fiber feed ingredients would lower NH₃ emission from laying-hen manure. The objectives of this research were to feed diets with a reduced-CP content and additional high-fiber ingredients to laying hens and measure manure NH₃ emission, egg production, and N balance. The effects of the dietary treatments on NH₃ emission are presented here, with production and N balance data presented separately (Roberts, 2007).

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Animals and Diets
A total of 256 Hy-Line W-36 laying hens, 17 wk of age, were obtained from a commercial facility and placed in completely enclosed, fan-ventilated, light (12:12 L:D) and temperature (20°C) controlled room. Hens were housed 2 per cage, corresponding to 619 cm² (96 in.²) per hen, in wire-bottomed cages (Chore-Time, Milford, IN), each equipped with a plastic self-feeder and a nipple drinker. Feeders were fitted with a wire grate to minimize waste of feed but not restrict feed consumption. The photoperiod was increased incrementally according to the W-36 Commercial Management Guide (Hy-Line International, Des Moines, IA) to 16:8 L:D at 25 wk of age. Prelay and prepeak diets were formulated according to recommendations in the W-36 Commercial Management Guide for 17 to 18 and 19 to 22 wk of age, respectively, and fed to all hens before commencement of the trial. At 23 wk of age (corresponding to 95% production and denoted as wk 1 of the study) hens were reassigned to cages according to a randomized complete block design, with BW and cage location within the barn as blocking criteria, and were fed the treatment diets. Hens were phase-fed to account for changes in nutrient requirements and feed consumption, with 3 phases from 23 to 31 (phase 1), 32 to 44 (phase 2), and 45 to 58 (phase 3) wk of age. Manure was collected only during phase 3, so phases 1 and 2 will not be discussed in this paper. The 8 dietary treatments were arranged in a 2 x 4 factorial arrangement with 2 contents of CP and 4 fiber diets. The normal-CP diet simulated a diet typically used in industry and the reduced-CP content was achieved by lowering CP by approximately 1 percentage unit with supplemental crystalline amino acids. The 4 fiber diets included a corn- and soybean meal-based control diet and 3 higher fiber diets formulated with 10.0% corn dried distillers grains with solubles (DDGS), 7.3% wheat middlings (WM), or 4.8% soybean hulls (SH). Corn DDGS, WM, and SH were chosen for their high neutral detergent fiber content and availability in the Midwest. Diets were formulated using corn, soybean meal, and meat and bone meal to contain equal amounts of ME_n and digestible TSAA and Lys (Table 1). All diets contained Celite (Celite Corporation, Lompoc, CA) as a source of acid-insoluble ash (AIA), which was used as an indigestible marker, and NaHCO₃ (American Soda, Parachute, CO) to equalize the calculated dietary electrolyte balance. The Iowa State University Institutional Animal Care and Use Committee approved all techniques and procedures involving birds.

Contents of SCFA, phenol, and indole were measured using GLC on 1 fresh manure sample per diet, pooled from 16 cages. Briefly, 4 g of manure was transferred into a tared 15-mL polypropylene centrifuge tube, after which 1 mL of HPLC-grade water (Fisher Scientific) and 5 mL of HPLC-grade acetone (Fisher Scientific) were added, and each tube was sonicated for 15 s. After sonication, 100 µL of 85% o-phosphoric acid (Fisher Scientific) was added and the contents of the tube were mixed using a vortex mixer. Tubes were then centrifuged at 21,000 x g for 23 min at 4°C. The supernatant was filtered through a 0.2-µm syringe filter and analyzed on an Agilent 6890 gas chromatograph equipped with a flame-ionization detector and DB-FFAP column (30 m x 0.25 mm x 0.25 µm; Agilent Technologies, Wilmington, DE). The following gas chromatograph parameters were used: split mode, 20:1; inlet temperature, 220°C; initial inlet pressure, 168 kPa; injection volume, 1 µL; constant column flow (He), 1.4 mL/min; and detector temperature, 250°C. The oven temperature program was initial temperature 35°C, 0.5 min hold; 90°C, 2.0 min hold; increase by 10°C/min; final temperature 230°C, hold for 6 min; increase by 12°C/min.

For the second collection, manure was collected during wk 33 (birds at 56 wk of age) over 3 consecutive 24-h periods on plastic trays placed 15 cm below each cage. To obtain sufficient quantities for NH₃ emission analysis, manure from each of the 24-h periods was pooled within diet and stored at –20°C until analysis. Manure was thawed at 4°C and analyzed for contents of DM by oven drying a 2-g subsample at 70°C for 24 h and for NH₃ emission and NH₃ emission rate by placing 2.5 kg of manure in NH₃ emission vessels. The 8 NH₃ emission vessels were made of 19-L (5-gal) plastic containers, which were lined with Teflon FEP100 film (200A, DuPont Teflon Films, Wilmington, DE). The air inlet and outlet were located in the airtight Teflon-lined lid. Teflon tubing (0.64 cm diameter) and manifold, along with poly(vinyl chloride) compression fittings, were used in constructing the emission vessel system. The vessels were operated under positive pressure with a diaphragm pump (model DOA-P104-AA, Gast Manufacturing, Inc., Benton Harbor, MI) to supply fresh air to the vessels. Flow rate of the fresh air was controlled and measured using an air mass-flow controller (0 to 30 L/min, stainless steel wetted part, AAlborg Instruments and Control Inc., Orangeburg, NY). The supply air was connected to a distribution manifold in which air was divided via 8 identical flow meters (0.2 to 4 L/min, stainless steel valve, VFB-65-SSV, Dwyer Instruments, Inc., Michigan City, IN). A flow rate of 3 L/ min was provided to each vessel, resulting in an air-exchange rate of 11 air changes/h. Each vessel was equipped with a stirring fan (12 V DC, Radio Shack, Fort Worth, TX) located 6 cm below the lid for uniform mixing of the headspace. Gas exhausted from the vessels was connected to a common 5-cm plastic pipe that was routed to the building vent outlet. Exhaust air from the head-space of each of the 8 vessels, incoming air, and room air were sampled sequentially at 6-min intervals, with the first 4 min for stabilization and the last 2 min for measurement. This yielded a measurement cycle of 1 h. A photo-acoustic infrared analyzer (Chillgard RT Refrigerant Monitor, MSA, Pittsburgh, PA) was used to measure NH₃ concentration. The analyzer uses an internal pump to draw air at a flow rate of approximately 1.0 L/min. Eight solenoid valves (Type 6014, 24 V, stainless steel valve body, Burkert Contromatic USA, Irvine, CA) controlled the sequential sampling. A Teflon filter was placed in front of each solenoid valve. Analog outputs from the NH₃ analyzer and mass-flow controller were recorded at 20-s intervals with a measurement and control module (model CR10, Campbell Scientific, Inc., Logan, UT).

Calculations
The AIA contents of feed and manure were used to calculate total DM manure excretion as:

where DM_manure is the DM manure excreted (g/d), AIA_feed and AIA_manure are the analyzed contents (%) of AIA in feed and manure, respectively, and DM_feed is the DM feed consumption (g/d) of the hen. The NH₃ emission per kilogram of manure was determined in the NH₃ emission vessels and the NH₃ emitted from the hens was calculated as:

where A_hen is the NH₃ emitted (g/d) from the hens and A_manure is the NH₃ emitted (g/g) from manure on a DM basis. The total N excretion of each hen was calculated as:

where N_excretion is the total N excretion (g/d) and N_manure is the N content (%) of the manure on a DM basis. Uric acid excretion was calculated as:

where UA_excretion is the uric acid excreted (g/d) and UA_ma-nure is the uric acid content (%) of the manure on a DM basis. The proportion of N in manure from uric acid was calculated as:

where %UAN_excretion is the uric acid N excreted, expressed as a percentage of total N excretion and 1/3 is the N content of uric acid by weight.

Statistical Analyses
Statistical analyses were performed with JMP (version 5.1.2, SAS Institute, Inc., Cary, NC). Data were analyzed by ANOVA appropriate for a randomized complete block design with 16 blocks and 8 dietary treatments in a 2 x 4 factorial arrangement (Morris, 1999). The ANOVA model included effects of block, protein, fiber, and the interaction of protein and fiber. Dunnett’s multiple-comparisons procedure (Dunnett, 1955) was used to compare the results from each of the fiber treatments with the results from the control; the main effect of protein was used to compare the reduced- and normal-CP diets. The experimental unit for analysis of fresh manure was a cage with 2 hens, whereas the experimental unit for NH₃ emission was the pooled manure sample for each diet; P-values 0.05 were considered significant and P 0.10 considered a trend.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS AND DISCUSSION REFERENCES

 
Including high-fiber ingredients in pig diets has been shown to decrease NH₃ emission because dietary fiber increases the metabolism and growth of bacterial populations in the large intestine (Kirchgessner et al., 1994). In addition to the energy provided by the fiber, the bacteria also require N, part of which may be acquired from N that would otherwise be excreted as uric acid, thereby shifting the N excretion from uric acid to bacterial protein. Indeed, when Shriver et al. (2003) fed SH or beet pulp to pigs, N excretion was repartitioned from the urine to the feces. Bacterial enzymes in manure readily degrade uric acid to NH₃, which is volatilized (Mackie et al., 1998). In contrast, bacterial protein in the feces is more stable compared with uric acid such that the N will remain in the manure for a longer period of time, thereby lowering NH₃ volatilization and improving the fertilizer value of the manure (Canh et al., 1998c).

In the present study, NH₃ emission from manure was lowered (P < 0.01) by dietary inclusion of 10.0% corn DDGS, 7.3% WM, or 4.8% SH when measured per kilogram of manure over 7 d compared with manure of hens fed the control diet, with the diet containing corn DDGS resulting in a 50% decrease in NH₃ emission (Table 2). Canh et al. (1998b) found that pigs fed high-fiber diets excreted more DM manure than pigs fed a control diet. Inclusion of high-fiber feed ingredients in laying-hen diets may also cause an increase in DM manure excretion because of the possibility of lower DM digestibility (Jaroni et al., 1999; Hogberg and Lindberg, 2004; Holt et al., 2006). Although the DM digestibilities of the diets were not affected by the inclusion of fiber in the present study (Roberts, 2007), NH₃ emission was calculated on a per hen basis to account for any potential differences in manure excretion between control- and fiber-fed hens. Regardless of this adjustment, NH₃ emission was lower (P 0.05) from hens fed the fiber diets compared with emission from hens fed the control diet (Table 2).

The bacterial fermentation of fiber produces SCFA, which are readily absorbed across the mucosal membranes of the digestive tract (Bergman, 1990). However, when pigs are fed a high-fiber diet, the slurry contains considerably more SCFA compared with the slurry from pigs fed a common grain-based diet, and these SCFA cause a lower slurry pH (Canh et al., 1997, 1998c; Hogberg and Lindberg, 2004; Kerr et al., 2006). The pH of slurry is a major determinant of the rate and extent of NH₃ volatilization from animal waste because lower manure pH shifts the NH₃ equilibrium (pKa = 9.2) toward NH₄⁺, which is more water soluble and therefore less volatile than NH₃. Additionally, bacterial enzymes that are involved in the breakdown of uric acid to NH₃ have a relatively high optimum pH and are therefore less active when manure pH is decreased (Mobley and Hausinger, 1989). Indeed, Canh et al. (1998a) and Panetta et al. (2005) showed that the pH of slurry and NH₃ emission are inversely related. Compared with manure from hens fed the control diet, the pH of manure from hens fed corn DDGS or WM was lower (P < 0.05), whereas the manure from SH-fed hens tended (P = 0.10) to have a lower pH (Table 2). Because the manure N was not repartitioned from uric acid to bacterial protein, the lower pH was probably responsible for the lower NH₃ emission that was observed from the manure of the fiber-fed hens. Higher contents of acetic, propionic, isobutyric, butyric, isovaleric, and valeric acids were observed in the manure from hens fed each of the 3 high-fiber diets compared with manure from the control-fed hens (Table 4). Although only 1 manure sample was measured from each diet, the observed higher contents of these SCFA indicate that the lower pH was caused by increased contents of SCFA in the manure.

Standard corn-soybean meal diets, balanced for the first- and second-limiting amino acids (TSAA and Lys, respectively), contain contents of the other amino acids above hen requirements. Hens do not have the ability to store excess dietary amino acids, which are instead excreted, mainly as uric acid. Formulating a diet based on amino acid requirements with no CP minimum and including supplemental amino acids lowers the CP and N contents of the diet. We hypothesized that reduced dietary CP content would cause a decrease in total N and uric acid excretion, and therefore have less potential for microbial conversion of uric acid to NH₃. Typically, when the dietary CP content is lowered by using crystalline amino acids, N excretion is lowered by 8 to 10% for each 1 percentage unit decrease in dietary CP (Kerr and Easter, 1995; Canh et al., 1998c). Indeed, in the present study, the reduced-CP diets caused a 10% decrease (P < 0.05) in total N excretion compared with the normal-CP diet (Table 2). In addition, lower uric acid excretion, and therefore lower NH₃ emission, was expected from hens fed the reduced-CP diets. However, NH₃ emission was not lower from the manure of hens fed the reduced-CP diets, contrary to previous studies, which showed approximately 7 to 10% lower NH₃ emission for each 1 percentage unit lower dietary CP in pigs (Canh et al., 1998b). Not only was NH₃ emission higher than expected from the hens fed the reduced-CP diets, but egg production and egg mass also were lower compared with hens fed the normal-CP diets (Roberts, 2007), indicating a possible amino acid deficiency in the reduced-CP diets. If the reduced-CP diets were indeed deficient in 1 or more individual amino acids, the other dietary amino acids, now in excess, would have been deaminated and the N would have been excreted as uric acid, which could explain both the higher than expected uric acid excretion and NH₃ emission from the reduced-CP fed hens.

Results of this study showed that inclusion of 10% corn DDGS, 7% WM, or 5% SH in laying-hen diets lowered total manure NH₃ emission and the NH₃ emission rate by up to 50%. This effect was mainly through a decrease in manure pH. When corn DDGS, WM, or SH are included in a commercial laying-hen diet, it is typically because of their contribution of nutrients to the diet or their relatively low cost in least-cost feed formulations. However, this study showed that, in addition to the essential amino acids, minerals, and other nutrients provided by the corn DDGS, WM, and SH, these ingredients also function to lower NH₃ emission.

	ACKNOWLEDGMENTS

 
The authors would like to thank the Midwest Poultry Consortium (St. Paul, MN) and Novus International Inc. (St. Louis, MO) for financial support. Additionally, we would like to acknowledge the Feed Energy Company (Des Moines, IA) and ADM (Des Moines, IA) for in-kind contributions and Novus International Inc. for amino acid analysis. The assistance provided by personnel in the laboratories of Xin, Kerr, and Bregendahl and at the Iowa State University Poultry Science Research Center, as well as statistical guidance from Philip Dixon, Department of Statistics, Iowa State University, are greatly appreciated.

	FOOTNOTES

 
¹ Mention of trade names, proprietary products, or specific equipment does not constitute a guarantee or warranty by Iowa State University or the USDA and does not imply approval to the exclusion of other products that may be suitable.

Received for publication October 16, 2006. Accepted for publication April 15, 2007.

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