Productive and metabolic parameters in lambs fed diets with castor seed meal

Livestock Science ∎ (∎∎∎∎) ∎∎∎–∎∎∎

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Productive and metabolic parameters in lambs fed diets with castor seed meal Isis Miranda Carvalho Nicory a,n, Gleidson Giordano Pinto de Carvalho a, Ossival Lolato Ribeiro a, Stefanie Alvarenga Santos a, Fabiano Ferreira da Silva b, Robério Rodrigues Silva b, Lívia Santos Costa Lopes b, Fábio Nicory Costa Souza a, José Esler de Freitas Jr. a a b

Federal University of Bahia, Salvador, BA, Brazil Southwest State University of Bahia, Itapetinga, BA, Brazil

art ic l e i nf o

a b s t r a c t

Article history: Received 16 January 2015 Received in revised form 7 August 2015 Accepted 21 September 2015

The objective of this study was to evaluate replacing levels of soybean meal with castor meal in diets for lambs on the productive and metabolic parameters. Fifty uncastrated Santa Inês lambs with an initial body weight of 26.52 74.76 kg and four-to-six months of age were confined in feedlots and fed diets containing castor seed meal (0, 25, 50, 75 and 100%) replacing soybean meal. The experimental design was completely randomized, with five treatments and ten replicates. The intakes of dry matter, organic matter, crude protein, ether extract, non-fibrous carbohydrates and total digestible nutrients decreased linearly (Po 0.05), whereas the intake of neutral detergent fiber corrected for ash and protein, both in body weight or metabolic weight basis increased linearly (Po 0.05). The digestibility coefficients of dry matter, organic matter, neutral detergent fiber corrected for ash and protein, non-fibrous carbohydrates, total carbohydrates and total digestible nutrients decreased linearly (Po 0.05), and the digestibility of crude protein was not influenced (P 40.05). There was no effect (P4 0.05) on the daily and total weight gains and feed conversion. Hepatic parameters were not affected. The consumed-, absorbed- and retained-nitrogen values decreased linearly (P o0.05), but had no effect on the liver metabolism. Despite the decreased intake, nutrient digestibility and nitrogen balance, castor seed meal can replace up to 50% of soybean meal without changing lambs’ blood parameters or performance. & 2015 Elsevier B.V. All rights reserved.

Keywords: Alternative feed Ricinus communis Sheep Body weight gain

1. Introduction The global energy production is based on petroleum, a nonrenewable source; thus, seeking renewable alternatives to produce fuels is a constant need. In this scenario, cereal grains began to be used in biodiesel production, e.g., corn and soy, which are currently used on a larger scale. Ethanol production from corn in USA is 13.3 billion gallons per year (RFA, 2013), whereas Brazil produces 242.5 m3/mo (ANP, 2014), and 80% of the latter is from soy. The use of these cereals, however, competes with human feeding and may limit the production of biofuels, requiring the use of other sources such as the castor oil plant (Pompeu et al., 2012; Andrade et al., 2013). Castor is a promising alternative in that it does not compete with human feeding, has a high yield—2.5 t/ha, on average—and every ton of castor produced generates 44% oil and 56% of residue. The castor seed meal, obtained after the extraction of the residual n Correspondence to: Federal University of Bahia, Avenida Ademar de Barros, 500, Ondina, CEP 40170-110, Brazil. E-mail address: [email protected] (I.M.C. Nicory).

oil from the cake through the use of solvents, may contain up to 55.83% crude protein (Carrera et al., 2012), and has the potential to be used as a protein source (Diniz et al., 2010). Nevertheless, its use requires caution, because this product contains ricin as an anti-nutritive factor (Audi et al., 2005; Aslani et al., 2007). Reduction or elimination of the toxin is achieved by various types of seed processing (Anandan et al., 2005; Barnes et al., 2009; Mckeon et al., 2013). Some studies have demonstrated the feasibility of using the meal or cake of castor seed in diets for large ruminants. Diniz et al. (2011) observed that the cake treated with 60 g kg–1 Ca(OH)2 can fully replace soybean meal in diets for finishing crossbred cattle. Cobianchi et al. (2012) concluded that castor seed meal treated with 60 g kg
1 of Ca(OH)2 can replace one-third (33%) of soybean meal in diets (inclusion of 50 g kg
1 DM) for lactating cows with a milk yield of 20 kg/day, because it will not affect the productive performance of these animals. Oliveira et al. (2010) studied the effect of ricin on the ruminal microbiota, nutrient digestibility, nitrogen metabolism, and hepatic function in sheep. Still, further information is necessary in order to validate the use of castor seed meal in diets for animals of this species.

http://dx.doi.org/10.1016/j.livsci.2015.09.015 1871-1413/& 2015 Elsevier B.V. All rights reserved.

Please cite this article as: Nicory, I.M.C., et al., Productive and metabolic parameters in lambs fed diets with castor seed meal. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.09.015i

I.M.C. Nicory et al. / Livestock Science ∎ (∎∎∎∎) ∎∎∎–∎∎∎

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Therefore, it was hypothesized in this study that castor seed meal detoxified with calcium oxide (Ca(OH) 40 g kg
1) can totally replace soybean meal in diets for growing lambs without compromising their productive performance or their protein and hepatic metabolism. The objective was thus to evaluate replacing levels of soybean meal with detoxified castor seed meal in diets for lambs and the effects of this replacement on intake and digestibility of nutritional components, nitrogen balance, hepatic metabolism, and body weight gain of these animals.

2. Materials and methods The experiment was carried out according to guide lines of the Ethics Committee on Animal care and handling for experimental trials of School of Veterinary Medicine and Animal Science of the Federal University of Bahia (protocol 08/2013). 2.1. Animals, experimental design and diets The experiment was conducted at the Experimental Farm of the School of Veterinary Medicine and Animal Science of Universidade Federal da Bahia, located in the municipality of São Gonçalo dos Campos/BA, Brazil, from March to June 2012. As treatments, five levels (0%, 25%, 50%, 75%, and 100%) of castor seed meal (CSM) were used to substitute soybean meal in the concentrate (Table 2), corresponding to 0%, 6.75%, 13.50%, 20.25%, and 27% of the total diet, respectively. Fifty uncastrated Santa Inês lambs at four-to-six months of age, with an average initial body weight and standard error mean of 27.78 kg 71.64 kg, 25.37 kg 7 1.90 kg, 26.34 kg 71.61 kg, 27.08 kg 71.95 kg and 23.83 kg 71.44 kg, for the treatments 0%, 25%, 50%, 75%, and 100%, respectively, were distributed in a completely randomized design with five treatments and ten replicates. The diets were formulated to be isonitrogenous, so as to meet the nutritional requirements of lambs with a weight gain of 200 g/day estimated by the National Research Council (NRC, 2007). Tifton 85 (Cynodon sp.) hay chopped to particles of approximately 5 cm was used as roughage source. 2.2. Detoxification and measurement of ricin The castor seed meal was detoxified with a Ca(OH)2 solution consisting of 1 kg/9 L of water, applied at the proportion of 40 g Ca(OH)2 for every kilogram of the concentrate, as described by Anandan et al. (2005). The material was then kept covered overnight (12 h), and on the next day it was spread and dried in the sun, and stirred at every two hours for 48 h. The proteins present in the CSM treated and untreated with calcium hydroxide were extracted by boiling with distilled water, at the rate of 1 g of meal/10 mL of water, followed by a boiling bath for 5 min. The extract was centrifuged for 5 min at 4100g, and the sediment was discarded. The ricin was evaluated qualitatively by separating fractions A (36 kDa) and B (29 kDa) in polyacrylamide gel 12% under denaturing conditions (SDS-PAGE), according to the methodology proposed by Laemmli (1970). For the revelation, the gel was placed in a 0.1% coomassie blue solution in 40% methanol and 10% acetic acid. The protein bands in the gel were visualized by discoloration with a 40% methanol solution containing 10% acetic acid. The molecular weights of the stained ricin bands extracted in the control and in the (treated and untreated) meal were determined using markers of known molecular weight (Sigma, USA), according to Anandan et al. (2005). The treatment of CSM was considered effective when there were no visible ricin bands in the standard gels. The analysis was repeated with three dilutions (5, 2 and 1 mL) of the sample to confirm the absence of protein (Fig. 1).

Fig. 1. Polyacrylamide gel electrophoresis of castor seed meal treated or untreated with Ca(OH)2.t(1) -treated castor seed meal, t(2) -treated castor seed meal (replicate), u/t -untreated castor seed meal.

2.3. Experimental procedures, sample collections and chemical analysis The animals were housed in individual, covered stalls with suspended slatted floor provided with feed and water toughs so that there would be free access to water and diets throughout the experimental period. The lambs were maintained in a confinement system for 72 h preceded by 13 days to adapt to the facilities, diets and the daily management. In this phase, the animals received forage (Tifton 85 hay ad libitum) and the experimental diets. The experimental phase consisted of three consecutive 24-day periods designed for sample and data collection to evaluate intake, nutrient digestibility, nitrogen balance, protein metabolisms and productive performance. The feed was supplied to the animals twice daily, at 09h00 an 16h00, as a total mixed ration, with a roughage:concentrate ratio of 50:50 to reduce feed selection. The amount of feed supplied was calculated daily so that to allow orts between 10% and 20% (as fresh fed), as compared with intake of the previous days. The amounts of feed supplied and leftovers were recorded daily to determine intake. Body Weight gain was determined by weighing the animals (fasted) at the beginning and end of the experiment. The feed supplied and orts were sampled weekly. The daily samples of forage and orts were grouped proportionally as dry basis every seven days, thus forming composite weekly samples per animal, during the three experimental periods. The samples were conditioned in labeled plastic bags and stored in a freezer at
20 °C. After thawing, samples of roughage, concentrate and leftovers were pre-dried in a forced ventilation oven at 55 °C for 72 h. Next, they were ground in Wiley mills (Model 4, Laboratory Mill, Philadelphia, USA) with 1-mm sieve and stored in labeled plastic jars with lids, ready for laboratory analyses. The chemical composition of the feeds and diets is shown in Tables 1 and 2. Thus, by following the methodologies proposed by AOAC (1990), the dry matter (DM), mineral matter (MM) and crude protein (CP) contents were determined in all samples, and the ether extract (EE) content was measured by Goldfish extraction in petroleum ether. The contents of neutral detergent fiber (NDFap) corrected for ash (according to Mertens (2002)), and protein (according to Licitra et al. (1996)), and acid detergent fiber (ADF) (as described by Van Soest et al. (1991)) were determined in all samples. Lignin was determined by treating the acid detergent fiber residue with 72% sulfuric acid. The bags for indigestible NDF

Please cite this article as: Nicory, I.M.C., et al., Productive and metabolic parameters in lambs fed diets with castor seed meal. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.09.015i

I.M.C. Nicory et al. / Livestock Science ∎ (∎∎∎∎) ∎∎∎–∎∎∎ Table 1 Chemical composition of the ingredients used in the experimental diets. Item

Dry matter Organic mattera Mineral mattera Crude proteina Ether extracta NDFapa Acid detergent fibera Lignina Cellulosea Hemicellulosea Non-fiber carbohydratesa iNDF ADIN (%TN) NDIN (%TN)

Ingredient Tifton 85 hay

Ground corn Soybean meal

Castor seed meal

87.44 92.52 7.48 5.89 1.23 71.35 45.00 7.91 37.08 26.35 14.05

85.95 98.56 1.44 7.24 3.50 10.70 5.07 2.24 2.83 5.63 77.12

87.84 93.41 6.59 40.01 2.20 9.83 8.48 2.17 6.60 1.35 41.38

88.50 88.24 11.76 38.02 2.00 43.55 40.00 29.71 10.45 3.55 4.69

24.75 13.73 44.94

2.45 9.53 7.74

2.17 3.82 3.50

31.30 5.25 7.23

NDFap¼ neutral detergent fiber corrected for ash and protein; iNDF ¼ indigestible neutral detergent fiber; ADIN (%TN) ¼acid detergent insoluble nitrogen; NDIN (% TN) ¼neutral detergent insoluble nitrogen; TN¼ total nitrogen. a

Expressed in % of dry matter.

Table 2 Percentage composition of the ingredients and chemical composition of the experimental diets. Ingredient (% DM)

Ground corn grain Soybean meal Castor seed meal Mineral supplementa Tifton 85 hay Chemical composition Dry matter Organic matterb Mineral matterb Crude proteinb Ether extractb NDFapb iNDFb ADFb Ligninb Celluloseb Hemicelluloseb Non-fiber carbohydratesb

Castor seed meal (%) 0

25

50

75

100

21.50 27.00 0.00 1.50 50.00

21.50 20.25 6.75 1.50 50.00

21.50 13.50 13.50 1.50 50.00

21.50 6.75 20.25 1.50 50.00

21.50 0.00 27.00 1.50 50.00

87.15 93.19 6.81 15.30 1.96 40.32 13.56 25.64 4.81 20.82 14.68 35.61

87.11 92.83 7.17 15.17 1.95 42.72 14.82 28.01 6.72 21.27 14.71 33.00

87.66 92.50 7.50 15.03 1.94 44.88 17.78 30.86 9.14 21.70 14.02 30.66

87.71 91.96 8.04 14.90 1.92 47.34 19.01 33.28 11.52 21.75 14.06 27.81

87.82 91.55 8.45 14.76 1.91 49.34 20.15 35.19 13.27 21.91 14.15 25.55

Analyses conducted at the Animal Nutrition Laboratory (Laboratório de Nutrição Animal, LANA) at UFBA. NDFap¼ neutral detergent fiber corrected for ash and protein; iNDF ¼ indigestible neutral detergent fiber; ADF (%TN)¼ acid detergent fiber. a Guaranteed levels (per kg, in active elements): calcium
120 g; phosphorus
87 g; sodium
147 g; sulfur
18 g; copper
590 mg; cobalt
40 mg; chromium
20 mg; iron
1,800 mg; iodine
80 mg; manganese
1300 mg; selenium
15 mg; zinc
3800 mg; molybdenum
300 mg; maximum fluorine
870 mg; phosphorus (P) solubility in citric acid 2% minimum-95%. b Expressed in % of dry matter.

(iNDF) analyses were incubated in the rumen of a cannulated animal for 240 h, according to the methodology described by Casali et al. (2008). The concentration of total digestible nutrients was estimated by the formula proposed by Weiss (1999). The trial to evaluate the digestibility of dietary nutrients was conducted with 20 lambs (four lambs from each treatment), by adopting the total fecal collection method. From the 16th day of each experimental period, collector bags were placed on the animals. The first three days were designed for adaptation, and the remaining five days were used for total collection of feces. The

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material was harvested directly from the collector bags twice daily, at 08h00 and 15h00. Subsequently, after the total feces from each animal were recorded, samples of approximately 10% of the total and samples of the feed supplied were collected and conditioned in individual labeled plastic bags and stored in a freezer. These samples were later thawed, dried in a forced-ventilation oven at 60 °C for 72 h and processed in a Wiley mill with 1-mm sieve, thus forming composite samples per animal (Detmann et al., 2012). At the end of the experimental period, urine was collected as spot samples during spontaneous urination, approximately four hours after the supply of the morning feeding. These samples were filtered through gauze, and a 10-mL aliquot was separated and diluted with 40 mL sulfuric acid (0.036 N) (Valadares et al., 1999) to prevent precipitation of uric acid and bacterial activity on the purine derivatives. The nitrogen input (Consumed N) and output (Fecal N) were quantified in orts, feed supplied and feces by estimating the amount of dry matter and, on a DM basis, the nitrogen content. The nitrogen in the urine was quantified by using 5 mL of urine (AOAC, 1990); and the total nitrogen in feces and urine, according to the methodology described by Silva and Queiroz (2002). The absorbed nitrogen was estimated by the following formula: Absorbed N ¼Consumed N
Fecal N. The retained nitrogen, which represents the nitrogen balance, was calculated by the formula given by Decandia et al. (2000): Retained N¼ Consumed N
(Fecal Nþ Urine N). To evaluate the hepatic metabolism, blood samples were collected by jugular venipuncture on the 72nd experimental day, approximately four hours after the morning feeding, using bloodcollection tubes (Vacutainers, São Paulo, Brazil). Samples were immediately centrifuged at 2800g for 15 min to remove plasma samples, which were conditioned in mini-tubes (Eppendorf, São Paulo, Brazil) and frozen at
15 °C for subsequent analyses. The activities of the alanine-aminotransferase (ALT), aspartateaminotransferase (AST) and gamma-glutamyltransferase (GGT) enzymes to evaluate the hepatic metabolism were measured by colorimetry using commercial kits (Bioclin, Minas Gerais). The catalytic activity was read on a spectrometer (Celm, SBA 2000, São Paulo) with temperature between 20 and 30 °C, with values expressed in IU/L. Serum albumin levels were analyzed by green bromocresol method, and total protein by the Biuret method, using commercial kits and a spectrophotometer (reading). The globulin content was calculated as the mathematical difference between the total protein content and the serum albumin, and the values were expressed in g/dL. The serum urea levels were determined through the enzymatic-colorimetric system, by using commercial kits (LABTEST, Minas Gerais, Brazil) and a spectrophotometer with 600-nm wavelength (reading), considering that 47% of this urea is composed of nitrogen, and the values were expressed in mg/dL. The lambs’ performance was evaluated by their average daily gain, which was calculated as the difference between their final and initial weights divided by the number of days in the experimental period (72 days), with values expressed in kg/day. 2.4. Statistical analysis The results about the effect of the CSM levels on the evaluated variables were interpreted statistically by analyses of variance and regression via orthogonal polynomials, by decomposing the sum of squares of the interval into linear, quadratic and cubic effects, using the PROC GLM procedure of SAS (2005) (Statistical Analysis System, version 9.4) software, allowing 5% probability of occurrence of type-I error. The initial BW of lambs was considered to be a covariate in the statistical model, according to the following

Please cite this article as: Nicory, I.M.C., et al., Productive and metabolic parameters in lambs fed diets with castor seed meal. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.09.015i

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nitrogen ratio decreased linearly (Po 0.05) with the increased CSM levels. The retained-nitrogen in relation to the absorbed nitrogen (retainedN/absorbedN), urine nitrogen, fecal nitrogen and CP were not influenced (P 40.05) by the CSM levels (Table 5). The gamma-glutamyltransferase(GGT), aspartate aminotransferase (AST) and alanine aminotransferase (ALT) enzymes values were not influenced (P 40.05) by the levels of CSM (Table 6). The mean values of total proteins, albumin, globulin and urea were not influenced (P 40.05) by the CSM levels in the diet (Table 7). These results stated the absence of a residual effect of ricin on the protein profile of the animals, indicating an adequate status for animals' health. There was no effect (P 40.05) of CSM levels on total weight gain (TWG), average daily gain (ADG) or feed conversion (FC) (Table 8), which averaged 11.03 g/kg BW, 0.16 kg/d and 7.85 kg DM intake/kg BW gain, respectively.

model:

(

)

Yi = μ + Ti β Xi − X¯ + ei where: Yi¼dependent variable corresponding to experimental observations; μ ¼general mean; Ti ¼fixed effect of treatments i; β ¼ regression coefficient or functional relationship with covariate; Xi¼ observed value of covariate applied to experimental unit; X̅ ¼ mean value for covariate; and ei¼random error assuming normal independent distribution (NID) (0; s²ε).

3. Results The intakes of DM, non-fibrous carbohydrates (NFC) and total digestible nutrients (TDN) reduced linearly (P o0.05) as the CSM levels were increased. The intakes of CP and EE also reduced linearly (P o0.05), with every 25% of substitution resulting in a reduction of 10.79 and 1.23 g/day for these variables, respectively. The NDFap intake in kg/day, g/kg BW and g/kg BW0.75, and the iNDF intake increased linearly (Po 0.05). The treatments did not affect (P 40.05) the DM intakes (g/kg BW and BW0.75) or the TC intake (g/day), which averaged 2.95, 72.65, and 812, respectively (Table 3). The digestibility of DM, OM, NDFap, TC, NFC and TDN decreased linearly as the CSM levels in the diets were increased. Each 25% of substitution caused a reduction of 3.74%, 3.41%, 2.54%, 3.97%, 2.27% and 4.41%, respectively. The EE digestibility showed a quadratic response, with maximum value of 81.41% at the CSM level of 81.14%. The digestibility of CP was not influenced (P4 0.05), averaging 74.23% (Table 4). Nitrogen intake (g/day), absorbed nitrogen (g/day), nitrogen balance, retained nitrogen (g/kg MW) and the retained/consumed

4. Discussion Despite the decrease in DMI, the average intake was 1.0 kg/day for diet with 100% substitution, which is close to 1.05 kg/day recommended by the NRC (2007). Thus, it is suggested that detoxification of CSM with Ca(OH) was efficient in reducing the ricin contents of feed, because high levels of this glycoprotein might affect the dietary organoleptic traits. According to Cooper and Johnson (1984), the lethal experimental oral dose of ricin for sheep varies from 1 to 2 g/kg. The greater presence of iNDF in the CSM in relation to soybean meal (Table 1) limited DM intake, possibly because of its characteristic of reducing the ruminal degradation rate of fibrous

Table 3 Daily intake of the nutritional components,in kg, g kg–1 BW and in g kg–1 BW0.75, in lambs fed diets containing castor seed meal in substitution of soybean meal. Item

Castor seed meal (%) 0

25

SEM 50

75

100

1.14 1.07 0.19 0.024 0.45 0.46 0.203 0.84 0.74

1.08 1.00 0.18 0.023 0.46 0.40 0.205 0.81 0.63

1.00 0.93 0.16 0.021 0.47 0.34 0.201 0.77 0.51

3.02 1.19

2.98 1.27

74.85 29.48

72.93 30.95

P-valuen L

Q

0.02 0.02 0.00 0.00 0.01 0.01 0.00 0.02 0.02

0.0016 0.0008 0.0002 0.0006 0.0059 o 0.0001 o 0.0001 0.1992 0.0175

0.3617 0.3989 0.3462 0.7202 0.8141 0.3885 0.0674 0.8124 0.2652

2.91 1.36

0.03 0.01

0.6384 o 0.0001

0.0538 0.4196

70.25 32.86

0.81 0.33

0.5663 o 0.0001

0.0842 0.3901

–1

DM OM CP EE NDFap NFC iNDF TC TDN DM NDFap DM NDFap

Intake in kg day 1.19 1.15 1.12 1.08 0.21 0.19 0.026 0.024 0.40 0.40 0.55 0.50 0.155 0.163 0.85 0.80 0.76 0.72 Intake in g kg–1BW 2.86 2.99 0.97 1.09 Intake in g kg–1BW0.75 71.82 73.39 24.30 26.77

Regression equations DM NDFap (g kg–1BW) OM CP (kg day–1) EE (kg day–1) NDFap (kg day–1) NDFap (g kg–1BW0.75) iNDF NFC (kg day–1) TDN

Ŷ ¼1.20124–0.00180215X (R²¼ 0.91) Ŷ ¼2.46043 þ0.00854747X (R²¼ 0.99) Ŷ ¼1.12999–0.00180370X (R²¼0.93) Ŷ ¼0.206115–0.000431440X (R²¼ 0.84) Ŷ ¼0.0261326–0.0000493894X (R²¼ 0.88) Ŷ ¼0.398242þ 0.000742708X (R²¼ 0.86) Ŷ ¼24.6043 þ 0.0854747X (R²¼ 0.99) Y ¼ 0.158154 þ0.000543814X (R2 ¼0.76) Ŷ ¼0.553969–0.00206457X (R²¼ 0.99) Ŷ ¼0.787837–0.00230087X (R²¼ 0.80)

DM¼ dry matter; OM ¼organic matter; CP¼ crude protein; EE ¼ether extract; NDFap ¼neutral detergent fiber corrected for ash and protein; NFC¼ non-fiber carbohydrates; TC¼ total carbohydrates; TDN ¼ total digestible nutrients; SEM¼ standard error of the mean; L ¼significance for linear effect; Q¼significance for quadratic effect; P-value. n

¼significant probability at 5%

Please cite this article as: Nicory, I.M.C., et al., Productive and metabolic parameters in lambs fed diets with castor seed meal. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.09.015i

I.M.C. Nicory et al. / Livestock Science ∎ (∎∎∎∎) ∎∎∎–∎∎∎ Table 4 Digestibility of the nutritional fractions (%) of diets containing castor seed meal in substitution of soybean meal for lambs. Item

Castor seed meal (%)

SEM

Table 6 Mean values for the gamma-glutamyl transferase (GGT), aspartate-aminotransferase (AST) and alanine-aminotransferase (ALT) enzymes in lambs fed diets containing castor seed meal in substitution of soybean meal.

P-valuen Item

0

25

50

75

100

DM OM CP EE NDFap TC NFC TDN

67.80 70.58 76.21 71.42 50.32 68.00 87.00 74.25

65.34 68.33 75.57 75.84 47.96 65.50 85.85 71.70

59.76 62.53 72.45 79.83 43.45 57.63 81.87 66.20

59.06 62.49 74.50 82.08 44.13 59.53 81.97 65.77

52.58 56.44 72.43 80.51 39.53 51.16 77.59 55.17

DM OM EE NDFap TC NFC TDN

Regression equation Ŷ ¼68.2542–0.149607X (R² ¼0.96) Ŷ ¼70.8988–0.136526X (R²¼ 0.94) Ŷ ¼71.0954 þ0.254298X–0.00156697  2 (R² ¼0.98) Ŷ ¼50.1626–0.101691X (R² ¼0.92) Ŷ ¼68.2937–0.158610X (R²¼ 0.89) Ŷ ¼87.3915–0.0907281X (R² ¼0.93) Ŷ ¼75.4372–0.176396X (R² ¼0.90)

0.42 0.42 0.44 0.41 0.71 0.61 0.27 0.72

L

Q

o 0.0001 o 0.0001 0.0907 0.0001 0.0051 o 0.0001 o 0.0001 0.0001

0.5696 0.7392 0.6894 0.0201 0.9393 0.8052 0.5017 0.2549

GGT (IU/L) AST (IU/L) ALT (IU/L)

Castor seed meal (%)

SEM

0

25

50

75

100

61.62 170.63 15.75

55.56 170.67 14.89

58.67 186.33 18.83

65.25 173.63 15.63

63.57 178.29 18.43

2.31 3.19 0.68

P-valuen L

Q

0.4433 0.4584 0.2591

0.5649 0.6169 0.8262

SEM¼ standard error of the mean; L¼ significance for linear effect; Q¼ significance for quadratic effect; P-value. n

¼significant probability at 5%.

Table 7 Mean values for urea, total proteins (TP), albumin and globulin in lambs fed diets containing castor seed meal in substitution of soybean meal. Item

DM ¼dry matter; OM¼ organic matter; CP¼ crude protein; EE ¼ ether extract; NDFap¼ neutral detergent fiber corrected for ash and protein; NFC ¼non-fiber carbohydrates; TC ¼total carbohydrates; TDN ¼total digestible nutrients.SEM ¼ standard error of the mean; L¼ significance for linear effect. Q ¼significance for quadratic effect; P-value n

5

¼ significant probability at 5%.

Urea (mg/dL) TP (g/dL) Albumin (g/dL) Globulin (g/dL)

Castor seed meal (%)

SEM

0

25

50

75

100

68.50 6.22 3.34 2.89

62.11 6.50 3.36 3.14

63.00 7.28 3.60 3.68

61.50 5.99 3.39 2.60

63.14 6.61 3.44 3.17

1.42 0.15 0.03 0.14

P-valuen L

Q

0.3136 0.8389 0.2139 1.0000

0.2903 0.4437 0.2107 0.5424

SEM¼ standard error of the mean; L¼ significance for linear effect; Q¼ significance for quadratic effect;P-value. n

fraction and increasing the feed retention time in the rumen and reducing intake (Muniz et al., 2012). The increase in NDFap and iNDF intakes were likely due to their concentrations in the CSM as compared with soybean meal, which were, respectively, 43.55% and 9.83% for NDFap and 31.30% and 2.17% for iNDF (Table 1).The high NDFap content of the CSM might have influenced negatively the intakes of DM and OM, given that voluntary intake decreases as a result of the physical effect of bulking, which is associated with the rumen distension capacity and to the NDF content of the diet (Mertens, 1994). In the evaluation of NDFap intake it was observed that this fraction varied from 0.97% to 1.36% of their body weight (BW), which is consistent with the 1.27% (Carvalho et al., 2013), 1.48% (Gomes et al., 2012) and 1.97% (Silva et al., 2009)

¼significant probability at 5%.

reported for tropical climate. The linear decrease in NFC intake can be explained by the lower contents of this component in CSM (4.69%), as compared with soybean meal (41.38%) (Table 1). Although the diets were isonitrogenous, there was a decrease in DM intake, which consequently reduced the CP intake (Table 3), and although the latter decreased, it was still higher than the 0.125 kg/day recommended by the NRC for lambs with same weight range gaining 200 g/day. The reduction in DM intake probably reduced EE intake, because the EE contents of the diets were similar. The reduction in energy intake was caused by the high NDFap and iNDF contents in diets (Table 2). Another piece of evidence of the impact of CSM on TDN intake is the reduction in the intakes of

Table 5 Nitrogen balance in lambs fed diets containing castor seed meal in substitution of soybean meal. Item

Castor seed meal (%)

SEM

0

25

50

75

100

CsmN (g day ) Fecal N (g day–1) AbsN (g day–1) Urine N (g day–1) RetN/day (g kg–1MW) RetN/CsmN RetN/AbsN N balance

35.00 7.04 27.96 2.14 1.75 0.74 0.92 25.82

34.68 7.04 27.64 3.32 1.74 0.70 0.88 24.32

36.56 7.76 28.80 2.97 1.73 0.70 0.90 25.84

27.04 6.40 20.64 1.48 1.42 0.71 0.93 19.16

24.12 6.64 17.48 2.30 1.17 0.63 0.87 15.18

CsmN(g day–1) AbsN(g day–1) RetN/day (g kg–1MW) RetN/CsmN N balance

Regression equation Ŷ ¼37.3600–0.117600X (R² ¼0.71) Ŷ ¼30.0960–0.111840X (R² ¼0.75) Ŷ ¼1.85489–0.00588989X (R²¼ 0.81) Ŷ ¼0.735731–0.000798596X (R² ¼0.70) Ŷ ¼ 27.3547–0.105808X (R²¼ 0.78)

–1

0.84 0.25 0.75 0.15 0.03 0.01 0.01 0.73

P-valuen L

Q

0.0048 0.5987 0.0032 0.3439 0.0005 0.0412 0.3996 0.0037

0.1352 0.6209 0.1337 0.3315 0.0647 0.4981 0.8404 0.1693

CsmN¼ consumed nitrogen; AbsN ¼ absorbed nitrogen; N balance ¼nitrogen balance (g/day); RetN/day (g/kg MW) ¼retained nitrogen (g/kg of metabolic weight); RetN/ CsmN¼ ratio between retained and consumed nitrogen; RetN/AbsN ¼ratio between retained and absorbed nitrogen; SEM¼ standard error of the mean; L ¼significance for linear effect; Q¼ significance for quadratic effect; P-value. n

¼ significant probability at 5%.

Please cite this article as: Nicory, I.M.C., et al., Productive and metabolic parameters in lambs fed diets with castor seed meal. Livestock Science (2015), http://dx.doi.org/10.1016/j.livsci.2015.09.015i

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6

Table 8 Performance of lambs fed diets containing castor seed meal in substitution of soybean meal. Item

TWG ADG FC

Castor seed meal (%)

SEM

0

25

50

75

100

12.01 0.17 6.97

11.20 0.16 7.95

11.42 0.16 8.44

10.01 0.14 8.88

10.52 0.15 7.01

0.50 0.00 0.45

P-valuen L

Q

0.2546 0.2546 0.7296

0.8296 0.8296 0.1425

TWG¼ total weight gain (kg);ADG¼ average daily gain (g/day);FC ¼feed conversion (kg DMintake/kg LW gain);SEM ¼standard error of the mean; L¼ significance for linear effect; Q¼ significance for quadratic effect; P-value n

¼significant probability at 5%.

CP, EE, and NFC, as previously discussed. The EE digestibility showed a quadratic response, with maximum value of 81.41% at the level of 81.14% CSM (Table 4).It is possible that, as the fiber intake increased, the passage rate of the feed in the rumen decreased, and hence the fat degradation. The reduced digestibility of DM and OM is associated with reduction in NFC intake and increase inNDFap and iNDF intakes, which are caused by the increased NDFap and iNDF with inclusion of CSM in the diets. The reduction (Po 0.05) in digestibility of NDFap was due to the higher iNDF contents in the diets with CSM. The impact of iNDF on the digestibility and passage rate of the fiber was demonstrated by Sampaio et al. (2010), who found that high iNDF in diets may have its action weakened by a balanced use of nitrogen, because in this way it is possible to elevate the microbial efficiency and increase the escape speed of this fraction. Besides, lignin, iNDFis also composed of cellulose and indigestible hemicellulose; therefore, iNDF may influence not only the fiber digestibility, but also the digestibility of other fractions like DM, OM, and the high concentration of TDN in the diet. Non-fibrous carbohydrates (NFC) are usually completely degraded in the rumen or digested throughout the intestinal tract of ruminants (Kozloski et al., 2006). The reduced digestibility of NFC is linked to the low participation of this component in diets and the reduced NFC intake caused by the substitution of soybean meal for CSM. According to Detmann et al. (2006), the acid detergent insoluble nitrogen (ADIN) content of a feed is only an indicative and it cannot predict potential digestibility of the total nitrogen compounds, which explains why ADIN values in the soybean and castor-seed meals of 3.82% and 5.25% of the total nitrogen (TN), respectively, did not influence the CP digestibility. Miranda et al. (2008) evaluated the protein and amino-acid composition of tropical forage plants and observed that although protein sources are similar in CP content, they differ in soluble protein as well as the amount of total amino acids in the crude protein. The soy protein has 71.75% trully digestible (Pires et al., 2006), and soybean meal has 72.50% effective degradability at the passage rate of 5%/h (Fortaleza et al., 2009), whereas the CSM is a protein source with lower effective degradability (62% at the passage rate of 5%) as compared with soybean meal (Moreira et al., 2003). However, these factors did not promote differences in the digestibility of CP among the tested diets, probably because the intestinal digestion of CP offset the reduction of rumen degradation. The reduction of TDN was possibly caused by the reduced digestibility of NDFap and NFC, which are nutrients included in the calculation of TDN and that directly affect the observed values. The TDN intake required for lambs with 30 kg body weight and an average daily gain of 200 g/day is 0.56 kg/day (NRC, 2007), and despite the reduction in the TDN intake and digestibility values among the tested diets, these values were sufficient to meet the

animals’ requirements. The consumed nitrogen decreased by 2.94 g/day with every 25% substituted. According to the NRC (2007), the daily nitrogen intake values for lambs in the same weight range and with daily gains of 200 g/day is 19.7 g; thus, it can be noted that N requirements were met, because the average was 31.48 g/day. Nitrogen intake above the requirements may result in larger losses of fecal and urinary N, (Van Soest, 1994), which may cause metabolic losses. The nitrogen content in feces (Fecal N) and urine (Urine N) averaged 6.98 and 2.44 g, respectively. In spite of higher N intake, there was no increase in fecal N excretion, which was lower than the 6 to 8% of fecal losses from the consumed protein described by Van Soest (1994); given that for the average CP intake of 184 g/day obtained in the present study the estimated nitrogen excretion in the feces (Fecal N) is 11.06 g/day. The values obtained in the current study were similar to the 8.73 and 2.14found by Silva et al. (2010) for fecal and urine nitrogen, respectively, in a study evaluating metabolism of nitrogen compounds in sheep fed diets containing four levels (0%, 33%, 66% and 100%) of CSM. The decrease in the absorbed nitrogen content, which reduced by 2.80 g at every 25% of soybean meal substituted for CSM, is related to the reduced intake and digestibility of total carbohydrates and TDN as the CSM levels in the diets were increased (Tables 3 and 4), because the nitrogen flow in the rumen is influenced by intake level and diet composition. According to Santos (2011), the ruminal bacteria synthesize amino acids from ammonia, and this process requires energy and α-keto-acids in addition to other nutrients, and the more rumen-degradable the carbohydrate is, the more energy will be available for bacterial growth. Thus, the reduced use of the consumed nitrogen did not influence the amount of nitrogen in the feces, which is represented by the indigestible protein of the feed plus the nitrogen from bacterial cells that multiply in the large intestine utilizing endogenous urea, including secretions and desquamation. The ratio between retained and absorbed nitrogen did not show differences, likely because the biological value of the rumendegradable protein was the same among the diets and because microbial-crude-protein amino acids were constantly produced. The decreased nitrogen balance possibly resulted from the reduced absorption of nitrogen. The highest value for nitrogen balance was obtained with the control diet (without CSM), in which the highest CP intake was also observed (Table 3). The ammonia that is not incorporated into the microbial nitrogen compounds is largely absorbed through the ruminal epithelium and enters the portal circulation or exits as digesta, and is absorbed in intestines. The absorbed ammonia is converted to urea in liver, and returns partially to the gastrointestinal tract via saliva or transepithelial transport (Kozloski, 2011) and part of it is excreted via urine. The observed values prove that the nitrogen balance was positive and thus suggests balance between the dietary protein and digestible energy. The serum ALT and AST levels were 16.70 and 175.91 IU/L, respectively. The observed ALT values were lower than the 22–28 IU/ L considered normal for lambs, whereas the results obtained for AST are within the standard 60 to 280 IU/L for lambs according to Radostits et al. (2002). These results agree with those reported by Oliveira et al. (2010), who studied the effects of CSM treated or untreated with calcium hydroxide in the feeding of sheep and did not observe negative effects of the ALT and AST levels on the hepatic function of the animals. The results obtained in this study also agree with those observed by Menezes et al. (2012), who did not detect alterations in these enzymes when partially replacing (0%, 15%, 30% and 45%) soybean meal with CSM in sheep diets. The gamma-glutamyltransferaseis an enzyme present in the serum, and, when changed, it indicates the occurrence of liver

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disease and disorder (González and Scheffer, 2003). The average 60.93 found for GGT is higher than the 20–52 IU/L described as normal by Kaneko et al. (2008) and than the 49.79 IU/L obtained by Batista et al. (2009); this fact cannot be characterized as an effect of CSM, because the diet with 0% CSM also showed values above those considered normal. It is possible that the Santa Inês breed displays higher values for this enzyme (Peneluc et al., 2009; Nunes et al., 2010), in addition to other factors such as age, sex, or even the animals'adaptability to the environment or rearing system, such as environmental and climatic conditions, the rearing management and feeding (Meira et al., 2009). Thus, it was found that the hepatic cells were not degenerated with intakes of up to 27% CSM in the total diet, and we confirm that detoxification with calcium hydroxide was effective in eliminating ricin. The average total protein, albumin and globulin values of 6.52, 3.43 and 3.17 g/dL, respectively, are within the normality standards, which range from 6.0 to 7.9 g/dL for total proteins (Kaneko et al., 2008), 2.4 to 3.9 g/dL for albumin (Kaneko et al., 1997) and from 3.1 to 5.1 g/dL for globulin (Hearly and Falk, 1974). These values also corroborate the 6.95, 3.04 and 4.02 g/dL found by Batista et al. (2009) for total proteins, albumin and globulin, respectively, in 371 sheep from Northeast Brazil. The nutritional status of the animal, especially the protein levels and the hepatic function has a direct influence on the blood protein synthesis rate, since this production occurs mainly in the liver (González and Scheffer, 2003). The protein intake and the blood urea level have a positive correlation, just as the dietary energy, which is used by the ruminal microorganisms to transform the ammonia nitrogen into bacterial protein (González et al., 2000). Hence, high urea values may indicate both an excess of nitrogen compounds and a deficit of energy (González and Scheffer, 2003). The average urea value among the tested diets was 63.65 mg/mL, which is close to the 24– 60 mg/dL considered the normality range (González et al., 2000); this may indicate balance between the energy and protein from the experimental diets, with efficient use of the ammonia in the rumen. In spite of the reductions observed in the intake and digestibility of some nutritional components with the increase in the CSM levels and the low ADG (below the recommended 0.2 kg (average0.16 kg)), the nutrient intake was satisfactory, given that gains were similar (P 40.05) among the diets. The average DM intake among the tested CSM levels was 1.11 kg/day, and, according to the values described in the NRC (2007) and used in the calculation of experimental diets, results close to 1.05 kg/day were expected. It is possible that the elevated initial body weight would be the main reason why the lambs did not reach the expected average daily gain, because in addition to appropriate DM intake, the metabolic and hepatic profiles proved that there was no problem in the animals’ health. The positive and similar weight gains among the diets with CSM indicates that there was no metabolic loss and that the diets provided intake and absorption of nutrients and adequate conversion into animal protein, which was also true in the values obtained with the total substitution, which corresponded to 27% of the CSM in the diet with 100%. The performance results obtained in this study diverge from those found by Pompeu et al. (2012), who evaluated four levels (0%, 33%, 66% and 100%) of detoxified castor seed cake in diets for Morada Nova lambs and observed a linear decrease in average daily gain. The likely explanation for such differences between the animal performance in our study and that reported by Pompeu et al. (2012) is the lower EE content of CSM, which thus has no detrimental effect on the fiber digestibility.

7

5. Conclusion Replacing up to 50% of soybean meal castor seed meal, corresponding to 13.5% of the total diet, reduces intake and digestibility of the nutritional components but does not alter blood parameters, hepatic function or productive performance of feedlotfinished Santa Inês lambs.

Conflict of interest statement The authors declare that there is no conflict of interest.

Acknowledgments The authors thank Fapesb (Fundação de Amparo à Pesquisa do Estado da Bahia) for the financial support.

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