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Effects of copper oxide bolus administration or high-level copper supplementation on forage utilization and copper status in beef cattle¹

University of Florida—IFAS, Range Cattle Research and Education Center, Ona 33865-9706

	Abstract

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Two experiments were conducted to study effects of high-level Cu supplementation on measures of Cu status and forage utilization in beef cattle. In Exp. 1, eight steers randomly received an intraruminal bolus containing 12.5 g of CuO needles (n = 4) or no bolus (n = 4). Steers were individually offered free-choice ground limpograss (Hemarthria altissima) hay. On d 12 (Period 1) and d 33 (Period 2) steers were placed in metabolism crates, and total forage refused and feces produced were collected for 7 d. Daily samples of forage offered and refused and of feces excreted for each steer within period were analyzed for DM, ash, NDF, ADF, and CP. Liver biopsies were collected on d 0, 12, and 33. Copper oxide bolus administration resulted in greater (P < 0.03) liver Cu (DM basis) accumulation in Period 1 (556 vs. 296 mg/kg) and Period 2 (640 vs. 327 ppm). Apparent digestibilities of NDF and CP were greater (P < 0.04) for steers receiving no bolus in Period 2 (62.2 vs. 57.1% and 50.2 vs. 43.4% for NDF and CP digestibility, respectively). In Exp. 2, 24 crossbred heifers were assigned to individual pens and received a molasses-cottonseed meal supplement fortified with 0, 15, 60, or 120 ppm of supplemental Cu (Cu sulfate; six pens per treatment). All heifers were offered free-choice access to ground stargrass (Cynodon spp.) hay. Heifer BW and liver biopsies were collected on d 0, 42, and 84. Forage refusal was determined daily, and diet DM digestibility was estimated over a 21-d period beginning on d 42. Heifers consuming 120 ppm of supplemental Cu gained less (P < 0.05; 0.04 kg/d) than heifers consuming 15 (0.19 kg/d) and 60 ppm of Cu (0.22 kg/d), but their ADG did not differ from that by heifers consuming no supplemental Cu (0.14 kg/d; pooled SEM = 0.07). Heifers supplemented with 15 ppm of Cu had greater (P < 0.05) liver Cu concentrations on d 84 than those on the 0-ppm treatment and the high-Cu treatments (60 and 120 ppm). Forage intake was less (P = 0.07) by heifers receiving no supplemental Cu than by heifers on all other treatments (6.6 vs. 5.8 ± 0.37 kg/d). Apparent forage digestibility was not affected by Cu treatment. These data suggest that high rates of Cu supplementation (Cu sulfate; > 60 ppm of total Cu) resulted in less liver Cu accumulation by beef heifers compared with heifers consuming diets supplemented with moderate dietary Cu concentrations (i.e., 15 ppm). As well, the administration of CuO boluses might depress the digestibility of forage nutrient fractions in steers.

Key Words: Beef • Copper • Forage Utilization

	Introduction

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Sulfur interferes with normal Cu absorption in cattle. This S-based antagonism is likely the result of the formation of ruminal thiomolybdates (Mason, 1981, 1990) or ruminal Cu-sulfide complexes (Suttle, 1974), both of which interfere with Cu metabolism in ruminants.

A potential method for overcoming S-based antagonisms in cattle might be a simple increase in the quantity of supplemental Cu provided; however, this management approach could affect animal performance negatively. The antimicrobial characteristics of Cu might affect the microbial environment of the rumen. Hubbert et al. (1958) suggested that relatively low concentrations of Cu were toxic to ruminal microbes in a culture system. In contrast, Lopez-Guisa and Satter (1992) suggested that the supplementation of Cu above NRC (1996) recommendations might improve the digestion of low-quality forages.

One alternative to the supplementation of Cu salts via the diet is the intraruminal administration of Cu-oxide boluses. Copper-oxide boluses are effective in rapidly increasing liver Cu stores in cattle (Rogers and Poole, 1988; Yost et al., 2002). In contrast, the effects of Cu oxide bolus administration on animal performance have been less documented. In one study, calves had a lower weaning weight at two commercial beef ranches when administered Cu oxide boluses (Arthington et al., 1995). In other studies, Cu toxicity was diagnosed in calves from Nebraska, Wyoming, and North Dakota beef herds receiving Cu oxide boluses (Hamar et al., 1997; Steffen et al., 1997).

Our hypothesis was that Cu antagonisms created by high-S diets might be overcome by management options that increase the quantity of supplemental Cu provided to the animal. To test this hypothesis, the current studies were initiated to examine the effect of high-level Cu supplementation (dietary inclusion or Cu-oxide bolus administration) on measures of Cu status and utilization of forage in beef cattle.

	Materials and Methods

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Animal Care, Handling, and Diet
The animals used in these experiments were cared for in accordance with acceptable practices (FASS, 1999), and the protocols were approved by the University of Florida Institutional Animal Care and Use Committee. Liver biopsy collections were performed by a trained technician using techniques described previously (Arthington and Corah, 1995).

In Exp. 1, eight crossbred steers (Brahman x British dams and Brangus sires; approximately 16 mo of age; average initial BW = 513 ± 49 kg) were obtained from the research herd at the University of Florida Range Cattle Research and Education Center, Ona. Steers were assigned randomly to one of two treatments, which provided 1) a single intraruminal, Copper oxide bolus (n = 4; 12.5 g of CuO needles; Copasure; Animax Ltd., Columbus, OH) or 2) non-bolus control (n = 4). Steers were housed individually in covered pens (15 m²). During the 40-d study, steers were provided access to ground limpograss (Hemarthria altissima) hay (Table 1) in quantities sufficient to ensure ad libitum consumption. To estimate apparent forage OM digestibility, total fecal production was measured in all steers during two 7-d fecal collection periods beginning on d 12 (Period 1) and d 33 (Period 2) after bolus administration. During the fecal collection periods, steers were placed into metabolism stalls (1 m x 3 m), and individual samples of daily forage offered and refused and samples of feces for each steer at each period were collected. To estimate the effect of Cu oxide bolus administration on Cu status of steers, individual liver biopsy samples were collected on d 0, 12, and 33.

Forage, Supplement, Feces, Plasma, and Liver Analysis
In Exp. 1, duplicate samples of forage offered, forage refused, and fecal samples were analyzed for DM, ash, and total N (AOAC, 1990). Duplicate samples for NDF and ADF were analyzed using methods described by Goering and Van Soest (1970). Hay mineral concentration was analyzed by a commercial laboratory using inductively coupled plasma-atomic emission spectroscopy (SDK Laboratories, Hutchinson, KS; Table 1).

In Exp. 2, random samples of forage offered, molasses, and ground corn were collected and analyzed for nutrient concentration by a commercial laboratory (SDK Laboratories; Table 1). Following collection of liver biopsies in Exp. 1 and 2, samples were frozen and sent to a commercial laboratory (SDK Laboratories) for determination of Cu concentration. Blood was collected by jugular venipuncture into heparin-coated, evacuated tubes. Plasma was harvested from blood following centrifugation at 2,400 x g for 20 min and then stored at –20° C. Plasma Cu concentrations were determined by atomic absorption spectrophotometry (AAS 5000; Perkin-Elmer, Wellesley, MA) using a 1:1 (vol:vol) dilution with deionized water (Miles et al., 2001).

Forage refusal was determined daily. Apparent diet DM digestibility was estimated over a 21-d period (beginning on d 42) by the determination of total fecal production using a sustained-release chromic oxide bolus (Captec, Auckland, NZ). Seven individual fecal samples were collected at 3-d intervals. This production lot of commercial boluses was validated in the researcher’s laboratory using growing steers placed in metabolism crates. Following collection of total feces produced, the average Cr release rate was determined to be 0.99 g/d.

Statistical Analyses
Analysis of liver Cu concentration (Exp. 1 and 2), plasma Cu concentration (Exp. 2), forage intake (Exp. 1 and 2), and digestibility (Exp. 2) was achieved by ANOVA for a repeated measures experiment within a completely randomized design using the MIXED procedure of SAS (SAS Inst., Inc., Cary, NC). The model statement contained the effects of treatment and time (day, week, or period) and the interaction of treatment x time. Data were analyzed using animal(treatment) as the random variable. Because treatments were delivered to individual animals, animal was the experimental unit. Analysis for overall change in liver Cu concentration (Exp. 2), fecal Cu concentration (Exp. 1), and ADG (Exp. 2) was achieved by ANOVA for a completely randomized design using PROC GLM of SAS, with animal(treatment) as the error term. Animal was the experimental unit. The model statement contained the effect of treatment.

With the exception of ADG in Exp. 2, there were no differences in any of the variables measured among steers receiving the 60 or 120 ppm of supplemental Cu; therefore, liver Cu data also were analyzed combining these treatments (60 and 120 ppm of Cu) into a single treatment (high Cu).

When treatment differences were observed (P < 0.05) in Exp. 2, differences among treatments were compared using single df orthogonal contrasts, which included the following comparisons: 1) Cu vs. no Cu, 2) no Cu vs. 15 ppm of Cu, and 3) 15 ppm of Cu vs. high Cu treatments (60 and 120 ppm of Cu).

	Results and Discussion

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Experiment 1
Administration of the Cu oxide bolus resulted in greater (P < 0.03) liver Cu accumulation compared with non-bolused steers (Figure 1). Increased liver Cu accumulation following administration of Cu oxide boluses is well documented (Rogers and Poole, 1988; Cameron et al., 1989; Yost et al., 2002). Excretion of Cu in the feces was also greater for bolused vs. nonbolused steers in both Period 1 (164 vs. 21 mg/d; SEM = 33.6) and Period 2 (79 vs. 23 mg/d; SEM = 8.6). Liver Cu concentration exceeded 600 ppm (DM basis) in bolused steers. Although no signs of clinical Cu toxicity were noted (McDowell, 2003), this accumulation of Cu exceeds that which has been suggested as normal for cattle in Florida (100 to 300 ppm, DM basis; Ammerman, 1969). Copper toxicity resulting from the administration of Cu oxide boluses has been reported in beef herds from Nebraska and Wyoming (Hamar et al., 1997). In the Hamar et al. (1997) survey, calves that died from Cu toxicity had liver Cu concentrations ranging from 474 to 6,370 ppm (DM basis) with an average value of 2,620 ± 1,520 (DM basis). This average value is considerably greater than the average liver Cu concentrations achieved in the current study. Nevertheless, even in the absence of clinical Cu toxicity, Cu-bolused cattle may experience decreased BW gain (Arthington et al., 1995).

View larger version (12K): [in this window] [in a new window]   Figure 1. The effect of Cu oxide bolus administration on the accumulation of liver Cu (DM basis) in growing beef steers (Exp. 1). Bolused calves received a single intraruminal administration of a bolus containing 12.5 g of Cuoxide on d 0. *P < 0.05 and **P < 0.01.

One explanation for the decrease in apparent digestibility of forage nutrients in bolused steers relates to the potential toxicity of Cu to the ruminal microorganisms. Hubbert et al. (1958) conducted in vitro studies aimed at determining the mineral requirements of ruminal microorganisms. In their study, Cu was found to be particularly toxic to ruminal microorganisms. Depression in forage digestion was noted with fermentation media containing 1.5 mg of Cu/L. Similarly, the ability of ruminal microorganisms to convert NPN into protein has been shown to be significantly decreased when ruminal fluid contained 10 mg of Cu/L (McNaught et al., 1950). In contrast to these studies, Lopez-Guisa and Satter (1992) found that the digestibility of low-quality forages was increased with the addition of a supplemental blend of Cu and Co at concentrations greater than NRC (1989) recommendations (12.22 and 0.25 ppm of supplemental Cu and Co, respectively). From the current literature, it is unclear what rate of dietary Cu is required to achieve the Cu toxicity threshold concentrations in ruminal fluid.

Experiment 2
Random allocation of heifers to Cu treatments resulted in a lesser initial BW for heifers assigned to the control treatment (0 ppm of Cu) than for heifers assigned to receive 15 ppm of Cu (P = 0.12) and 60 ppm of Cu (P = 0.05); therefore, initial BW was used as a covariate in the statistical model to test overall heifer ADG (average initial BW = 365, 386, 393, and 380 kg for treatments of 0, 15, 60, and 120 ppm of Cu, respectively; SEM = 9.7). Heifers consuming the greatest rate of supplemental Cu (120 ppm) had a lesser ADG (P < 0.05) compared with heifers consuming 15 and 60 ppm of Cu, but not in comparison with heifers consuming no supplemental Cu (0.14, 0.19, 0.22, and 0.04 kg/d for treatments of 0, 15, 60, and 120 ppm of Cu, respectively; SEM = 0.07). This decrease in BW gain agrees with the results of a study reported by Engle and Spears (2000) in which feedlot steers that were provided finishing diets fortified with 20 or 40 ppm of Cu, had decreased BW gain, feed intake, and feed efficiency compared with steers receiving no supplemental Cu. Furthermore, the results observed in Exp. 1 also can be applied to the forage-fed heifers in Exp. 2, in which a potential decrease in forage nutrient digestibility might have affected heifer BW gain.

Averaged over all four treatments (0, 15, 60, and 120 ppm of Cu), liver Cu concentrations decreased (P < 0.05) over time. Because no differences were observed among treatments providing 60 and 120 ppm of supplemental Cu, data were analyzed combining these heifers into a single treatment (high Cu). Heifers supplemented with 15 ppm of Cu had a greater (P < 0.05) increase in liver Cu concentration compared with heifers supplemented with 0 ppm and high Cu (60 and 120 ppm; Figure 2). An accumulation of Cu into the liver was expected, especially at the greater levels of supplementation offered in the present study. Other researchers have reported decreases in beef steer growth as a result of Cu supplementation (Engle and Spears, 2000). In that study, liver Cu concentrations reached a peak at the conclusion of a 56-d growing period and no longer increased after 84 d on a finishing diet, despite the inclusion of 20 and 40 ppm of supplemental Cu. Those reseachers suggested that an adaptive mechanism might be protecting these steers from Cu toxicity. In this manner, Cu absorption may be decreased, or alternatively, Cu excretion may be increased. Results of another study also support the existence of a protective mechanism against Cu toxicity (Felsman et al., 1973). In that study, young Holstein bull calves were fed a basal diet fortified with 0, 300, 600, and 900 ppm of Cu from Cu sulfate. Liver Cu accumulation increased in Cu-supplemented calves; however, no differences were observed among levels of Cu supplementation, despite a 300% difference between the least and greatest quantities of supplemental Cu provided. It is proposed that a similar protective mechanism might have affected the heifers in the current study that were consuming the high-Cu supplements. Through this proposed mechanism, the heifers supplemented with 60 and 120 ppm of Cu might have experienced decreased Cu absorption or increased Cu clearance through bile excretion, thereby protecting them from Cu toxicity.

View larger version (15K): [in this window] [in a new window]   Figure 2. The effect of varying rates of supplemental Cu on accumulation of liver Cu (DM basis) in growing beef heifers (Exp 2). a,bMeans with different superscripts differ, P < 0.05 (treatment x day; P = 0.11).

Another explanation for the lack of clinical Cu toxicity in the current study might be related to breed of cattle. Different cattle breeds metabolize Cu differently. In our study, Brahman x British crossbred heifers were used. This type of crossbred beef animal has previously been shown to tolerate very high doses of dietary Cu for long periods of time (Chapman et al., 1962). Ward et al. (1995) suggested that Simmental and Charolais steers have a greater Cu requirement than Angus steers because of lesser apparent absorption and retention of Cu. In a comparison among dairy cattle, Jersey cows were found to accumulate liver Cu faster and to a greater extent than Holstein cows fed a similar diet that contained 80 ppm of Cu. No symptoms of Cu toxicity were reported in their study; however, the diets were fed for only 60 d, a relatively short period of time (Du et al., 1996).

Initial plasma Cu concentrations were greatest (P < 0.05) for the treatment without supplemental Cu compared with each of the Cu supplementation treatments (1.21, 1.03, 1.06, and 0.97 ppm for 0, 15, 60, and 120 ppm, respectively; SEM = 0.05); therefore, initial plasma Cu concentrations were used as a covariate in the statistical analysis of plasma Cu at d 42 and 84. No treatment differences were detected in plasma Cu concentrations at d 42 (P = 0.90) and 84 (P = 0.79; average plasma Cu concentrations for all treatments were 0.82 and 0.86 ppm on d 42 and 84; SEM = 0.04 and 0.05, respectively).

Average weekly forage intake (as-fed basis) did not differ among treatments (treatment x week; P = 0.73). The single df contrast for no Cu vs. all three Cu supplementation treatments also did not differ over the 12-wk study (P = 0.27); however, over the first 2 wk of the study, average daily forage intake tended (P = 0.09) to be less by heifers provided no supplemental Cu vs. that of heifers on all three Cu supplementation treatments (1.40 vs. 1.63% of heifer BW; SEM = 0.09). These data suggest that supplemental Cu might be a factor affecting voluntary forage DMI. We have previously reported a similar response in heifers consuming grain-based supplements with and without supplemental Cu, whereas heifers provided no supplemental Cu had lesser voluntary forage DMI than heifers provided supplemental tri-basic Cu chloride (Arthington and Pate, 2004). In that study, the magnitude of difference among Cu-supplemented and nonsupplemented heifers was greatest during the initial weeks and lessened as the study progressed. These responses further support the proposed importance of dietary Cu on the digestion of forages in cattle (Lopez-Guisa and Satter, 1992); however, a mechanism might exist by which cattle partially adapt to the low-Cu diets over a short period of time. These results differ from those of Exp. 1, where a Cu-oxide bolus was used, further suggesting that the form of Cu supplementation is an important factor affecting Cu status and forage utilization.

Total fecal output was estimated using a sustained release Cr bolus as an internal marker over a 21-d fecal sampling period. During this time frame, forage DMI was not affected by Cu treatment (Table 4). Similar to Exp. 1, apparent digestibility of the total diet was not affected by Cu treatment (Table 4). Digestibility of the individual nutrient fractions was not analyzed in the feedstuffs from Exp. 2; therefore, comparisons between Cu treatment and nutrient digestibility, similar to those in Exp. 1, could not be made.

	Implications

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	Footnotes

 
¹ Contribution No. R-11044 from the Florida Agric. Exp. Stn. Appreciation is expressed to the American Feed Industry Association’s Liquid Feed Committee for their partial financial support of this research. Appreciation is also expressed to A. DiCostanzo (Univ. Minnesota) for laboratory assistance and to C. Piacitelli and T. Wood for their technical assistance during these experiments.

² Correspondence: 3401 Experiment Station (phone: 863-735-1314; fax: 863-735-1930; e-mail: jdarthington{at}ifas.ufl.edu).

Received for publication March 4, 2005. Accepted for publication July 25, 2005.

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