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ANIMAL PRODUCTION |
,
* Department of Animal Science and Interdepartmental Nutrition Program, North Carolina State University, Raleigh 27695-7621;
and
Akey, Lewisburg, OH 45338; and
and
Animal and Poultry Waste Management Center, North Carolina State University, Raleigh 27695
Abstract
In each of two experiments, 924 pigs (4.99 kg BW; 16 to 18 d of age) were assigned to 1 of 42 pens based on BW and gender. Pens were allotted randomly to dietary copper (Cu) treatments that consisted of control (10 ppm Cu as cupric sulfate, CuSO4•5H2O) and supplemental dietary Cu concentrations of 15, 31, 62, or 125 ppm as cupric citrate (CuCit), or 62 (Exp. 2 only), 125 (Exp. 1 only), or 250 ppm as CuSO4. Live animal performance was determined at the end of the 45-d nursery phase in each experiment. On d 40 of Exp. 2, blood and fecal samples were collected from two randomly selected pigs per pen for evaluation of plasma and fecal Cu concentrations and fecal odor characteristics. In Exp. 1, ADG, ADFI, and G:F were increased (P < 0.05), relative to controls, when pigs were fed diets containing 250 ppm Cu as CuSO4. Pigs fed diets containing 125 ppm Cu as CuCit had increased (P < 0.05) ADG compared with pigs fed diets supplemented with 15 or 62 ppm Cu as CuCit. The ADG, ADFI, and G:F did not differ among pigs fed diets containing 125 and 250 ppm Cu as CuSO4 or 125 ppm Cu as CuCit. In Exp. 2, pigs fed diets containing 250 ppm Cu as CuSO4 had improved (P < 0.05) ADG, ADFI, and G:F compared with controls. In addition, ADG, ADFI, and G:F were similar when pigs were fed diets containing either 250 ppm Cu as CuSO4 or 125 ppm Cu as CuCit. Pigs fed diets containing 62 ppm Cu as CuSO4 or CuCit had similar ADG, ADFI, and G:F. Plasma Cu concentrations were not affected by dietary Cu source or concentration, but fecal Cu concentrations were increased (P < 0.05) as the dietary concentration of Cu increased. Pigs consuming diets supplemented with 125 ppm Cu as CuCit had fecal Cu concentrations that were lower (P < 0.05) than pigs consuming diets supplemented with 250 ppm Cu as CuSO4. Fecal Cu did not differ in pigs receiving diets supplemented with 62 ppm Cu as CuSO4 or CuCit. Odor characteristics of feces were not affected by Cu supplementation or source. These data indicate that 125 and 250 ppm Cu gave similar responses in growth, and that CuCit and CuSO4 were equally effective at stimulating growth and improving G:F in weanling pigs. Fecal Cu excretion was decreased when 125 ppm Cu as CuCit was fed compared with 250 ppm Cu as CuSO4. Therefore, 125 ppm of dietary Cu, regardless of source, may provide an effective environmental alternative to 250 ppm Cu as CuSO4 in weanling pigs.
Key Words: Copper • Cupric Citrate • Fecal Copper • Growth • Pigs • Odor
Introduction
Copper (Cu) is routinely supplemented to weanling pig diets at concentrations above the nutritional requirement of the animal because pharmacological concentrations of inorganic cupric sulfate (CuSO4) have been shown to have growth stimulatory properties in pigs (Barber et al., 1955
; Bunch et al., 1961; Hawbaker et al., 1961). Supplementation of 242 ppm Cu as CuSO4 resulted in maximal growth stimulation in pigs (Cromwell et al., 1989); however, pharmacological concentrations of dietary Cu present an environmental concern because excess Cu is excreted in feces (Kornegay and Harper, 1997).
Recent research has indicated that an organic form of Cu, cupric citrate (CuCit), can stimulate growth at lower concentrations than CuSO4 in broiler chickens (Pesti and Bakalli, 1996; Ewing et al., 1998) and weanling pigs (Dove, 1998). If CuCit could be used at dietary concentrations lower than those used with CuSO4, one could maintain the growth-promoting effects of Cu while decreasing fecal excretion of Cu. In addition, Cu supplementation improved odor characteristics of swine waste, and lower concentrations (125 ppm) of CuCit were as effective as 225 ppm CuSO4 (Armstrong et al., 2000a). If odor characteristics of swine waste can be improved via Cu supplementation, odor nuisance complaints might decrease and the public perception of swine production might improve. The objectives of these studies were to determine the commercial-scale efficacy of Cu source (CuCit and CuSO4) and dietary concentration on growth performance and fecal Cu excretion in weanling pigs, as well as the effect on odor characteristics of swine waste.
Materials and Methods
Animal Care and Experimental Design
Nine hundred twenty-four pigs (462 barrows and 462 gilts, PIC 337 x C22) were used in a 45-d nursery study in each of two experiments. Pigs were weaned at 16 to 18 d of age and transported approximately 850 km to the swine research facility of Akey in southwestern Ohio. On arrival, pigs were sorted and assigned to 1 of 42 pens based on BW and gender in each experiment. Three blocks were formed based on weight within each gender. There were 21 pens of barrows and 21 pens of gilts in each experiment. Pigs were housed at a stocking density of 22 pigs per pen, and the space allotment was approximately 0.24 m2 per pig. All procedures, care, and handling of animals followed the guidelines as established by FASS (1999).
Pigs were fed according to a four-phase feed budget in each experiment. On average, the feed budget provided each pig within a pen approximately 0.92 kg of Phase 1 feed, 2.95 kg of Phase 2 feed, and 6.35 kg of Phase 3 feed. The Phase 4 feed was fed from the end of Phase 3 until the end of the 45-d nursery period. Diets were changed when three of the six pens consumed the budgeted amount of feed. Within each experiment, all replicate pens were changed on the same day. However, if one pen consumed the entire budgeted amount of feed well in advance of the other six pens, that specific pen was given extra feed until the aforementioned criteria were met, in order to prevent pens from being without feed. These feed allotments resulted in average lengths of 5, 10, 11, and 19 d for Phases 1, 2, 3, and 4, respectively. Throughout the 45-d nursery period, including each of the four dietary phases, all pigs had ad libitum access to water and pelleted feed. The dietary formulations of the basal diets are presented in Table 1. The dietary lysine concentration was formulated to decrease by phase. Specifically, the dietary lysine concentration was formulated to be 1.59, 1.40, 1.30, and 1.22% for Phases 1, 2, 3, and 4, respectively. In each experiment, and in each phase of the four-phase nursery program, an odor control agent (Micro-Aid; DPI, Porterville, CA) was included in each diet, in order to reduce ammonia emissions from swine manure.
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Experiment 2
The average initial weight of the pigs was 4.99 kg (SEM = 0.06). Pens, within a gender, were assigned randomly to receive one of seven dietary treatments. Each dietary treatment was replicated three times within each gender. Dietary treatments (as-fed basis) were as follows: 1) control, 10 ppm Cu as CuSO4; 2) control + 62 ppm Cu as CuSO4; 3) control + 250 ppm Cu as CuSO4; 4) control + 15 ppm Cu as CuCit; 5) control + 31 ppm Cu as CuCit; 6) control + 62 ppm Cu as CuCit; and 7) control + 125 ppm Cu as CuCit. Pigs were fed according to a four-phase feed budget as previously described, and the test diets were initiated at the beginning of Phase 1, and continued until the end of the 45-d nursery period. At the completion of the 45-d nursery period, pigs were weighed and feed consumption was determined by pen to calculate ADG, ADFI, and G:F.
Fecal and venous blood samples were collected from two randomly selected pigs per pen on d 40 of the nursery period. Blood samples were collected in heparinized, trace mineral-free Vacutainer (Becton Dickinson and Company, Franklin Lakes, NJ) tubes. Plasma was obtained by centrifugation (1,670 x g) of the samples for 30 min at 4°C and stored at -20°C until analysis of plasma Cu concentrations. Fecal samples were individually frozen at -20°C until analysis for Cu concentrations and determination of odor characteristics.
Analytical Procedures
Plasma samples were diluted 1:2 (vol/vol) with 5% nitric acid and placed in a centrifuge for 30 min at 1,670 x g to precipitate protein. The supernatant was removed and analyzed for Cu concentrations by flame atomic absorption spectrophotometry (Shimadzu, AA-6701F, Japan). Fecal samples were pooled within each pen and aliquots were removed for odor evaluation. The remaining pooled fecal samples were dried at 100°C for 48 h, weighed, and ground through a 1-mm screen. Dried fecal samples were digested using a microwave digestion system (Model MDS-81D; CEM Corp., Matthews, NC) using a modified procedure as described by Ward et al. (1996). A 0.5-g representative sample of the dried feces was placed in Teflon vessels (CEM Corp.) with 10 mL of trace metal–grade nitric acid (Fisher Scientific, Pittsburgh, PA) and allowed to digest at room temperature (23°C) for 30 min. Vessels were sealed and placed in the microwave digester for 5 min at 50% power, followed by 15 min at 70% power, and for 10 min at 0% power. Vessels were vented, and 2 mL of 30% hydrogen peroxide (Sigma-Aldrich, St. Louis, MO) was added to each vessel. Open vessels were again placed in the microwave digester for 3 min at 50% power and cooled for 2 min at 0% power. Vessels were removed, samples were transferred to 25-mL volumetric flasks and allowed to cool, and samples were brought to final volume with deionized water. Copper concentration was determined using flame atomic absorption spectrophotometry.
Determination of Odor Characteristics of Swine Feces
The prepared fecal samples were evaluated by static olfactometry, using the human nose as the detector, in the form of an odor panel (Schiffman and Williams, 1999). Static olfactometry is the evaluation of compounds that are presented in a closed system. Fecal samples were prepared for evaluation by the odor panel as previously described (Armstrong et al., 2000a). The odor panel comprised 10 persons trained to identify and quantify odors. Each panelist was presented a separate amber glass bottle that contained the prepared fecal material. The individuals were asked to sniff the headspace in the bottle and to evaluate the odor intensity, irritation intensity, and odor quality on a 0-to-8 scale (Armstrong et al., 2000a).
For each of the odor characteristics measured (odor intensity, irritation intensity, and odor quality), the lower the score on the 0-to-8 scales, the more improved the response. Odor intensity was defined as the odor concentration of an individual sample, which is a measure of the response of the olfactory, or first cranial, nerve. Irritation intensity is related to the irritation of the nasal passages in response to the sample. Irritation intensity is a measure of the response of the trigeminal, or fifth cranial, nerve. Odor quality or pleasantness reflects the type of receptors to which the odorants bind. Odor pleasantness is influenced by genetics and learning. To minimize the potential of odor fatigue, the number of odor samples evaluated on any given day did not exceed a total of 20.
Statistical Analyses
Statistical analyses of data were performed by ANOVA for a randomized complete block (gender) design using the GLM procedure of SAS (SAS Inst., Cary, NC). The model contained dietary treatment, gender, and dietary treatment x gender interaction. There were no dietary treatment x gender interactions (P > 0.05); therefore, data were pooled across gender, which resulted in each mean comprising six replications within each experiment. Pen was the experimental unit. Differences between means for each dependent variable were determined using single-df orthogonal contrasts. Contrasts made in Exp. 1 were as follows: 1) control vs. 250 ppm Cu as CuSO4; 2) 125 ppm Cu as CuSO4 vs. 250 ppm Cu as CuSO4; 3) 125 ppm Cu as CuSO4 vs. 125 ppm Cu as CuCit; 4) 15 ppm Cu as CuCit vs. 125 ppm Cu as CuCit; 5) 31 ppm Cu as CuCit vs. 125 ppm Cu as CuCit; and 6) 62 ppm Cu as CuCit vs. 125 ppm Cu as CuCit. In Exp. 2, contrasts were 1) control vs. 250 ppm Cu as CuSO4; 2) 125 ppm Cu as CuCit vs. 250 ppm Cu as CuSO4; 3) 62 ppm Cu as CuSO4 vs. 62 ppm Cu as CuCit; 4) 15 ppm Cu as CuCit vs. 125 ppm Cu as CuCit; 5) 31 ppm Cu as CuCit vs. 125 ppm Cu as CuCit; and 6) 62 ppm Cu as CuCit vs. 125 ppm Cu as CuCit. Significance was declared at P < 0.05.
Results
Experiment 1
Over the entire 45-d nursery period, ADG, ADFI, and G:F were improved (P < 0.05) when pigs were fed diets supplemented with 250 ppm Cu as CuSO4 compared to the controls (Table 2). Pigs fed diets containing 125 ppm Cu as CuSO4 had similar ADG, ADFI, and G:F compared to pigs fed diets containing either 250 ppm Cu as CuSO4 or 125 ppm Cu as CuCit. Average daily gain and ADFI were higher (P < 0.05) when diets supplemented with 125 ppm Cu as CuCit were fed compared with feeding diets supplemented with 15 ppm Cu as CuCit. In addition, pigs receiving diets containing 125 ppm Cu as CuCit had higher (P < 0.05) ADG than pigs receiving diets containing 62 ppm Cu as CuCit. The dietary concentration of CuCit did not affect G:F.
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). Average daily gain, ADFI, and G:F did not differ among pigs receiving diets supplemented with either 250 ppm Cu as CuSO4 or 125 ppm Cu as CuCit. In addition, ADG, ADFI, and G:F did not differ when pigs were fed diets containing 62 ppm Cu as either source. Average daily gain was higher (P < 0.05) in pigs consuming diets containing 125 ppm Cu as CuCit compared with pigs receiving diets containing 15 ppm Cu as CuCit; however, ADG, ADFI, and G:F did not differ when pigs were fed diets supplemented with 31, 62, or 125 ppm Cu as CuCit.
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). Fecal Cu concentrations were increased (P < 0.05) as the dietary concentration of Cu increased (Table 4). Specifically, fecal Cu concentrations were increased (P < 0.05) when pigs were fed diets containing 250 ppm Cu as CuSO4 compared with the controls and pigs receiving diets containing 125 ppm Cu as CuCit. In addition, pigs consuming diets supplemented with 125 ppm Cu as CuCit had increased (P < 0.05) fecal Cu concentrations when compared to pigs consuming diets supplemented with 15, 31, or 62 ppm Cu as CuCit. Fecal Cu concentrations did not differ in pigs fed diets containing 62 ppm Cu from either CuSO4 or CuCit. None of the odor characteristics of the swine feces (odor intensity, irritation intensity, or odor quality) were affected by dietary Cu supplementation or source (Figure 1).
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In Exp. 1 and 2, feeding 250 ppm Cu as CuSO4 improved growth rate and feed efficiency over the 45-d nursery period. These data agree with previous studies in which supplementation of Cu as CuSO4 at concentrations of 125 to 250 ppm stimulated growth and improved feed efficiency in weanling pigs (Bunch et al., 1965; Stahly et al., 1980; Cromwell et al., 1989). Specifically, Cromwell et al. (1989) calculated that growth rate was maximized in weanling pigs when Cu from CuSO4 was supplemented at 242 ppm.
Of further interest in the current study was that lower dietary Cu concentrations (125 ppm), regardless of source, were as effective at stimulating gain during the 45-d nursery period as 250 ppm Cu from CuSO4. In agreement with these data, 100 to 125 ppm Cu has been shown to improve growth performance at rates similar to 250 ppm Cu (Roof and Mahan, 1982; Coffey et al., 1994; Apgar et al., 1995). In the current study, at the same dietary concentration, CuCit was as efficacious as CuSO4 with respect to growth performance. In contrast to these data, CuCit has been reported to increase gain at lower dietary concentrations than CuSO4 in broiler chickens (Pesti and Bakalli, 1996; Ewing et al., 1998) and weanling pigs (Dove et al., 1998). The current data represent the first commercial-scale study that has demonstrated the equal growth response of CuCit relative to CuSO4 supplementation in weanling pigs. Other Cu compounds besides CuCit have been studied with respect to growth stimulatory properties in weanling pigs. Compounds such as Cu-carbonate (Bunch et al., 1965), Cu-lysine (Coffey et al., 1994; Apgar et al., 1995), tribasic Cu-chloride (Cromwell et al., 1998), and organic Cu chelates (Zoubek et al., 1975; Stansbury et al., 1990) have been studied, and these compounds also seemed to be as effective as CuSO4 in stimulating growth of nursery pigs.
Previous research has indicated that pigs normally excrete 70 to 95% of the Cu consumed in diets (Kornegay and Harper, 1997). This poor retention of Cu by the pig when pharmacological concentrations of Cu are fed presents an environmental concern, because excess Cu in swine feces results in Cu accumulation in the soil. In the present study, pigs fed 125 ppm Cu from CuCit had a decreased fecal Cu excretion compared with 250 ppm Cu from CuSO4. However, this response probably relates more to dietary concentration rather than dietary source of Cu fed. Fecal Cu was not affected by Cu source when 62 ppm of Cu was supplemented.
Previous research has demonstrated that Cu supplemented to nursery diets improved the odor characteristics of swine waste, and lower dietary concentrations of CuCit were as effective as 225 ppm Cu as CuSO4 (Armstrong et al., 2000a). However, in the current study, there was no effect of dietary Cu, regardless of Cu source, on the odor characteristics of swine waste. This might be explained by the inclusion of sarsaponin extracts from the Yucca schidigera plant, an odor control agent (Micro-Aid), in the basal diets used in the current study. This specific odor control agent has been shown to aid in the control of ammonia emission from swine manure via an inhibition of urease activity (Asplund and Goodall, 1991; Sutton et al., 1992, 1999). As a result, the addition of an odor control agent may have masked any potential effect of Cu in improving the odor characteristics of swine waste.
Plasma Cu concentrations were not affected by dietary Cu source or concentration. These data disagree with a previous study from our laboratory that indicated an increase in plasma Cu when 225 ppm Cu as CuSO4 was supplemented to diets for nursery pigs (Armstrong et al., 2000b). In addition, plasma Cu was increased with supplemental dietary Cu concentrations of 100, 150, and 200 ppm (Apgar et al., 1995). However, Roof and Mahan (1982) reported an increase in plasma Cu concentrations only at supplemental dietary Cu concentrations of 375 and 500 ppm, but not at or below 250 ppm.
These data reveal that lower dietary Cu concentrations, specifically 125 ppm from either CuCit or CuSO4, were as effective as 250 ppm Cu from CuSO4 at stimulating growth of weanling pigs over a 45-d nursery period. In addition, fecal Cu excretion was decreased when 125 ppm Cu as CuCit was fed when compared to 250 ppm Cu as CuSO4. Moreover, these data demonstrate that 125 ppm dietary Cu, regardless of source, may be an effective environmental alternative to 250 ppm Cu from CuSO4 in the diets for nursery pigs.
Implications
Data from these commercial-scale trials indicate that the growth-stimulatory properties of 125 ppm copper as cupric sulfate or citrate and 250 ppm copper from cupric sulfate were equal. Results suggest that, as a result of the reduction in fecal copper concentrations, 125 ppm dietary copper may provide an effective environmental alternative to 250 ppm copper for weanling pigs. Further studies may be warranted to investigate the effects of dietary copper—either alone or in combination with dietary odor-control agents—on the odor characteristics of swine waste.
Footnotes
1 Use of trade names in this publication does not imply endorsement by the North Carolina ARS or criticism of similar products not mentioned. 
2 Appreciation is extended to K. E. Lloyd and L. Worley-Davis for technical assistance.
3 Present address: Elanco Animal Health, 2001 West Main Street, P.O. Box 708, Greenfield, IN 46140.
4 Correspondence: 220 Polk Hall, Box 7621 (phone: 919-515-4008; fax: 919-515-4463; e-mail: jerry_spears{at}ncsu.edu).
Received for publication August 13, 2003. Accepted for publication January 8, 2004.
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