Next Article in Journal
Molecular Identification of the “Facciuta Della Valnerina” Local Goat Population Reared in the Umbria Region, Italy
Next Article in Special Issue
Fermentative Quality and Animal Acceptability of Ensiled Persimmon Skin with Absorbents for Practical Use in Ruminant Feed
Previous Article in Journal
Experimental Evidence Reveals Both Cross-Infection and Cross-Contamination Risk of Embryo Storage in Liquid Nitrogen Biobanks
Previous Article in Special Issue
Effect of Feeding Hazelnut Skin on Animal Performance, Milk Quality, and Rumen Fatty Acids in Lactating Ewes
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Feeding Agroindustrial Byproducts to Light Lambs: Influence on Growth Performance, Diet Digestibility, Nitrogen Balance, Ruminal Fermentation, and Plasma Metabolites

by
Trinidad de Evan
1,
Almudena Cabezas
2,
Jesús de la Fuente
2 and
María Dolores Carro
1,*
1
Departamento de Producción Agraria, ETSIAAB, Universidad Politécnica de Madrid, Ciudad Universitaria, 28040 Madrid, Spain
2
Departamento de Producción Animal, Facultad de Veterinaria, Universidad Complutense de Madrid, 28040 Madrid, Spain
*
Author to whom correspondence should be addressed.
Animals 2020, 10(4), 600; https://doi.org/10.3390/ani10040600
Submission received: 15 March 2020 / Revised: 29 March 2020 / Accepted: 30 March 2020 / Published: 1 April 2020
(This article belongs to the Special Issue Waste and/or By-Products Use in the “Circular Economy” Idea)

Abstract

:

Simple Summary

Feeding agroindustrial byproducts to ruminants can have multiple benefits, such as lowering feeding costs, reducing competition with human food, decreasing environmental impact associated with byproducts disposal, and improving the quality of animal products. In order to use these byproducts in practical feeding, their effects on animal performance and health should be assessed. In this study, we evaluated the effect of replacing 44% of conventional feeds in a high-cereal concentrate for light lambs with three byproducts: Corn distiller’s dried grains with solubles (18%), dried citrus pulp (18%), and exhausted olive cake (8%), all of which are highly produced in the Mediterranean area. We observed that the inclusion of these byproducts did not affect feed intake, growth performance, ruminal fermentation (with exception of NH3-N concentrations), or plasma metabolites in growing lambs. Compared with the high-cereal concentrate, feeding the concentrate including the byproducts resulted in a reduction of potentially human-edible ingredients from 64.4% to 38.7%. In conclusion, 44% of cereal grains and protein feeds in the concentrate for light lambs can be replaced with a mixture of corn distiller’s dried grains with solubles, dried citrus pulp, and exhausted olive cake without negatively affecting growing performance and animal health.

Abstract

The objective of this study was to evaluate the effect of replacing cereals and protein concentrates in a high-cereal concentrate (control) for light lambs with corn distiller’s dried grains with solubles (DDGS; 18%), dried citrus pulp (DCP; 18%), and exhausted olive cake (EOC; 8%) in a byproduct (BYP) concentrate on growth performance, digestibility, ruminal fermentation, and plasma metabolites. Two homogeneous groups of Lacaune lambs (13.8 kg ± 0.25 kg) were fed one of each concentrates and barley straw ad libitum until reaching about 26 kg body weight. There were no differences between groups on feed intake, average daily gain, or feed conversion ratio, but the control diet had greater (p < 0.001) dry matter digestibility. Diet had no effect on post-mortem ruminal pH and total volatile fatty acid concentrations and profile, but NH3-N concentrations were lower (p = 0.003) for the BYP-fed group compared with the control one. However, plasma concentrations of amino acids, total proteins, urea, and hepatic enzymes were not affected by the diet. In conclusion, 44% of feed ingredients in the concentrate for light lambs can be replaced with a mixture of corn DDGS, DCP, and EOC without negatively affecting growing performance and animal health.

1. Introduction

Agroindustrial byproducts have been traditionally used for small ruminant feeding in low-input systems, but their use is continuously increasing worldwide. Although either the shortage or the high cost of conventional feeds has been the main reason for feeding byproducts to livestock, other reasons are equally or even more important to support their current use. Some byproducts are highly contaminant, and their use in animal feeding can help to reduce the environmental problems caused by their accumulation and to lower the carbon footprint of animal products when locally produced byproducts are used [1]. Most byproducts are not potentially edible by humans, and they therefore do not compete directly with human food [2]. Additionally, some byproducts contain bioactive compounds that can improve animal health and the quality of animal products [3,4] while contributing to farm sustainability.
Three byproducts originated in the olive oil, citrus, and ethanol industries, all highly produced in the Mediterranean area, were used in this study. Olive oil production has tripled in the last 60 years with an estimated production of 3.1 × 106 t for the 2019/20 crop year [5] and is concentrated in the Mediterranean area, with Spain being the first world producer and exporter [6]. The two-phase system used to obtain olive oil generates a high-moisture byproduct named “alperujo,” which can be partially destoned, dried, and subjected to a chemical extraction to obtain pomace olive oil in a process that generates “exhausted olive cake” (EOC) as a waste [7]. Citrus fruits are produced worldwide, and about 70% of total production is grown in the Northern Hemisphere (mainly in the USA and countries in the Mediterranean area), although Brazil is the largest producer [8]. The main byproduct of citrus industry is citrus pulp, a high-moisture product that can be dried (DCP) and used in ruminant feeding as energy source [9]. Both EOC and DCP are rich in polyphenols [7,9,10], and they may therefore modify ruminal fermentation and improve animal health. Dried distillers grains with solubles (DDGS) are byproducts of the ethanol industry. Whereas there is a lot of information available on the effects of DDGS in dairy cows feeding, their influence on lamb growth has been much less studied. The objective of this study was therefore to assess the effects of replacing conventional feed ingredients in a concentrate with a mixture of EOC, DCP, and DDGS on feed intake, growth performance, nutrient digestibility, nitrogen (N) balance, ruminal fermentation, and plasma metabolites in light lambs.

2. Materials and Methods

The lambs used in this trial were cared for and handled in accordance with the Spanish guidelines for experimental animal protection, and experimental procedures were approved by the General Direction of Livestock and Agriculture of the Community of Madrid (Approval number PROEX 035/17).

2.1. Animals and Experimental Diets

Twenty four Lacaune male lambs, with an initial body weight (BW) of 13.8 ± 0.25 kg, were homogeneously distributed in two groups according to their BW. Lambs were penned individually in 1-m x 1-m pens with slatted floor, which were placed 1 m above the floor and equipped with two feeders and an automatic drinker. Each group of lambs was randomly assigned to one of the two dietary treatments: A high-cereal concentrate (control) and a byproduct containing concentrate (BYP), in which 44% of conventional feed ingredients (corn, barley, soybean meal, palm meal, and wheat bran) were replaced with corn DDGS, DCP, and EOC (18%, 18%, and 8% of concentrate, respectively, as-fed basis). The ingredients and chemical composition of both concentrates is shown in Table 1. Corn DDGS and DCP were commercially available and EOC was obtained from an extraction plant located in the south of Spain (Puente Genil, Córdoba). Concentrate ingredients were ground and pelleted (4-mm size). The concentrates were formulated to meet the nutritive requirements of light lambs [11]. Both concentrates were formulated to have similar crude protein (CP) and neutral-detergent fiber (NDF) content. Lambs were fed ad libitum concentrate and barley straw and had free access to fresh water over the trial. The barley straw contained (as-fed basis) 92.3%, 7.25%, 2.90%, 1.60%, 71.9%, and 38.0% of dry matter (DM), ashes, CP, ether extract (EE), NDF, and acid-detergent fiber (ADF), respectively. According to INRA [11], 1 kg of barley straw has 0.30 forage units for meat production (UFV).

2.2. Experimental Procedure and Measurements

The experiment lasted for six weeks and included seven days for diet adaptation. Concentrate and straw intakes were measured twice per week, whereas BW of all lambs was determined weekly. Samples of offered concentrate and straw were taken weekly for analysis of chemical composition. On days 0, 21, and the slaughter day, blood samples were taken from each lamb by jugular venipuncture into tubes containing EDTA immediately before feeding. Samples were centrifuged (5000× g, 10 min, 4 °C), and the plasma was immediately frozen (−20 °C) until determination of concentrations of amino acids, albumin, globulins, total proteins, urea, and cholesterol, the activities of the enzymes lactate dehydrogenase (LDH), alkaline phosphatase (ALP), creatine phosphokinase (CPK), glutamic oxaloacetic transaminase (GOT), glutamic pyruvic transaminase (GPT), and gamma-glutamyl transpeptidase (GGT).
In the fourth week of the trial, the digestibility of the diets and the nitrogen balance were measured in nine lambs per treatment. Trays were placed under the slated floor of each pen for feces and urine collection. The trays had holes for urine collection, which was collected in a bucket containing a solution of H2SO4 (10%, vol/vol) to keep the pH below 3.0 [12]. The feces and urine voided by each lamb in 24 h were quantitatively collected for six days and aliquots (10%) were sampled daily for digestibility and N balance determination, respectively. Daily samples were pooled to form a composite sample for feces and urine for each lamb, which was frozen until analysis.
In the last week of the trial, lambs were slaughtered at a commercial slaughterhouse located 20 km away from the experimental farm on two different days. The six lambs of each treatment with the greatest body weight were slaughtered the first day, and the rest of lambs the second day. Lambs had free access to feed and water until about 2 h before slaughter, and were slaughtered according to commercial practices involving head electrical stunning and severing the carotid arteries and jugular veins. After slaughter and dressing, the full gastrointestinal tract was removed and samples from rumen contents were immediately taken. The ruminal content was homogenized, a sample of about 300 g was filtered through four layers of gauze, and the pH of the fluid was immediately measured using a Crisson Basic 20 pH-meter (Crisson Instruments, Barcelona, Spain). Then, 2 mL of fluid were mixed with 2 mL of 0.5 N HCl and samples were frozen (−20°C) until analyses of volatile fatty acids (VFA) and NH3-N concentrations. In addition, the color of the rumen epithelium was evaluated as described by Haro [13]. Briefly, a sample (10 × 10 cm) of the rumen wall was collected from the ventral area of the rumen after empting the rumen content. Samples were washed with saline solution, displayed on a white surface under an intense and homogeneous light, and the color was evaluated using a scale from 1 to 5. The lightest epithelium received a score of 1 and the darkest one received a score of 5, whereas the rest of the samples were assigned scores according to their color intensity. The evaluation was performed by four trained persons (blind to treatment allocation), and the average score was used for statistical analysis.

2.3. Chemical Analyses

The procedures of the Association of Official Analytical Chemists [14] were used to analyze the DM (method 934.01), ash (method 942.05), and EE (method 920.39) content in samples of diet ingredients and feces. The N content of diet ingredients, feces, and urine was determined according to the Dumas method using a TruSpec CN equipment (Leco Corp. St. Joseph, MI, USA). Analysis of NDF in feed ingredients and feces was carried out according to Van Soest et al. [15] and that of ADF and lignin according to Robertson and Van Soest [16]. All fiber analyses were carried out using an Ankom 220 Fiber Analyzer unit (Ankom Technology Corp., Macedon, NY, USA), and results were expressed exclusive of residual ash. Concentrations of VFA in ruminal fluid were analyzed by gas chromatography using a Shimadzu GC 2010 chromatography (Shimazdu Europa GmbH, Duisburg, Germany) provided with a TR-FFAP column (30 m × 0.53 mm × 1 µm; Supelco, Madrid, Spain) according to the procedure described by García-Martinez [17], whereas NH3-N concentrations were determined by the phenol-hypochlorite method of Wheatherburn [18].
Plasma concentrations of amino acids were determined by high-performance liquid chromatography (HPLC) as described by Frank and Powers [19], whereas those of albumin, globulins, total proteins, urea, cholesterol, and the enzymes LDH, ALP, CPK, GOT, GPT, and GCT were determined using an automatic biochemistry analyzer (Hitachi 7020; Hitachi High Technologies, Inc., Ibaraki, Japan).

2.4. Statistical Analyses

Data on feed intake, growth performance, ruminal fermentation, meat composition, digestibility, and N balance were analyzed with one-way analysis of variance using the GLM PROC of the SAS [20]. Data on plasma concentrations of amino acids and metabolites were analyzed as a mixed model with repeated measures over time using the PROC MIXED of SAS [20]. The model included the diet, time, and their interaction as fixed effects, and the lamb as random effects. The level of statistical significance was set at p < 0.05, and p values between 0.05 and 0.10 were considered trends.

3. Results and Discussion

The proportion of each byproduct in the diet was selected from the results of in vitro studies by our group [21] and published in vivo studies [9,10]. The DCP contained (as-fed basis) 6.25%, 4.86%, 17.9%, and 3.28% of ashes, CP, NDF, and EE, respectively, whereas these values were 5.32%, 26.4%, 37.1%, and 9.81% for corn DDGS, and 14.0%, 7.48%, 46.4%, and 2.91% for EOC. The chemical composition of the used byproducts was within the range of values reported in the literature [7,11]. The two concentrates were formulated to have similar CP and NDF contents, but the BYP concentrate resulted in slightly greater CP amount than expected. The proportion of potentially human-edible ingredients in each concentrate was calculated as proposed by Wilkinson [22], and it was decreased from 64.4% in the control concentrate to 38.7% in the BYP concentrate, showing that feeding BYP to lambs resulted in lower competition with human nutrition.

3.1. Feed Intake, Growht Performance, Diet Digestibility, and Nitrogen Balance

As shown in Table 2, there were no differences between the two experimental groups in either concentrate or straw intake, indicating that BYP palatability was not negatively affected by the inclusion of byproducts. Barley straw intake was low in both groups, averaging 4.64% and 5.29% of the total DM intake for the control and BYP-fed lambs, respectively, which is in agreement with the low straw intake observed in previous studies by our group in light lambs under similar feeding conditions [12,13]. Both concentrates had similar NDF content (Table 1), but the fiber of DDGS and DCP is rapidly degraded in the rumen [23] and it might therefore be less effective at stimulating rumination. However, the lambs fed the BYP concentrate did not augment their intake of straw to increase their intake of physically effective fiber.
There were no differences between groups in final BW, average daily gain (ADG), and feed conversion rate. In agreement with these results, feeding the BYP concentrate did not affect carcass weights (p ≥ 0.704) or carcass yield compared with control concentrate. Values for these parameters were in the range previously reported by others for light lambs fed high-cereal concentrates and slaughtered at about 25–26 kg BW [12,13,24,25]. The lack of differences between the groups in growth performance is consistent with their similar energy intake, which averaged 0.840 and 0.834 daily forage units for meat production (UFV) for the control and BYP groups, respectively.
The digestibility of both DM and organic matter (OM) was greater (p < 0.001) for control than for BYP concentrate (Table 3), but there were no differences (p ≥ 0.120) between concentrates in the digestibility of CP, NDF, and ADF. The lower DM and OM digestibility of the BYP concentrate may have been partly due to its lower content in non-structural carbohydrates (35.2% vs. 45.7% for BYP and control concentrates, respectively), which is a highly digestible fraction, and its greater lignin content (1.79% vs. 2.80%). Values of diet digestibility were in the range reported by others for lambs fed high-cereal diets [12,13,26,27] and diets including olive cake [28] or dehydrated citrus pulp [29].
The greater (p = 0.024) N intake of the BYP-fed lambs was due to the greater CP content of BYP compared with the control concentrate, as there was no differences between groups in concentrate intake (Table 3). The daily fecal N excretion of BYP group was also greater (p = 0.012) than that for control group, but differences disappeared when fecal N excretion was expressed as proportion of the ingested N, which is consistent with the lack of differences in CP digestibility. There were no differences between groups in the amount of urinary and retained N, either expressed as g/d or as a proportion of the ingested N. Values of N retention were in the range of those previously reported for young growing lambs fed diets with similar CP levels [12,30].

3.2. Ruminal Fermentation and Plasma Metabolites

There was no effect (p ≥ 0.247) of the type of concentrate on post-mortem ruminal pH, total VFA concentrations, molar proportions of individual VFA, or acetate/propionate ratio (Table 4). The pH values and acetate/propionate ratios were similar to those reported for lambs fed high-cereal concentrates and straw [13,26,31,32]. The lower (p = 0.003) NH3-N concentrations in the rumen of BYP-fed lambs compared with control-fed lambs might indicate lower CP degradability in the BYP-concentrate. In fact, DDGS protein has lower ruminal degradability than other concentrate feeds, such as soybean and palm meal [23,33], which were replaced in the BYP-concentrate. In addition, 50.8% of the CP in the EOC was bound to the ADF, indicating low N availability [23]. Concentrations of NH3-N in the rumen of control-fed lambs were adequate for microbial growth [34], but those in BYP-fed lambs might have been limiting. However, the lack of differences in any of the ruminal parameters measured precludes this hypothesis.
The reasons for the trend (p = 0.092) to darker color of the ruminal epithelium in the lambs fed the BYP-concentrate are unclear. A darker color of ruminal epithelium is usually associated to keratinized tissue [35], but the lack of differences between the two groups of lambs in both growth performance and most ruminal parameters indicate that ruminal absorption was not negatively affected in the BYP-fed lambs.
There were no effects (p ≥ 0.109) of the diet on plasma concentrations of any amino acid, and no diet x sampling day interactions (p ≥ 0.151) were detected (Table 5). These results are consistent with the lack of differences between groups in growth rates and CP digestibility, and indicate no amino acid limitation in the BYP group compared with the control one. Changes in plasma amino acids due to dietary modifications were the consequence of modifications in the flow of total amino acids into the duodenum, including amino acids from both dietary and microbial origin. The lack of differences between groups in plasma amino acids concentrations supports the hypothesis that microbial protein synthesis was not limited in BYP-fed lambs, despite the low ruminal NH3-N concentrations. In agreement with previous studies [36], the concentrations of most amino acids increased or tended (p ≤ 0.065) to increase as lambs grew older, with the exception of glutamic acid, histidine, glycine, arginine, alanine, and cysteine, which did not change over the trial. The increased amino acids concentrations at the end of the trial are in accordance with the greater growth rate of the lambs at this time, as amino acids are used for protein synthesis and tissue formation [37].
No diet x time interactions (p ≥ 0.223) were detected in any of the metabolites measured in the blood of lambs (Table 6). The lack of differences between diets in plasma concentrations of urea (p = 0.585) is in accordance with the similar concentrations of amino acids observed in both groups of lambs. Plasma urea concentrations reflect the amount of urea produced in the liver from amino acid catabolism [38], although they were also highly affected by the amount of NH3-N absorbed from the rumen. The similar (p ≥ 0.276) levels of albumin, globulins, and total proteins in the plasma of both groups agree well with the lack of differences in plasma concentrations of amino acids and urea. Plasma concentrations of these metabolites, excluding globulins, increased with time. The normal [39,40,41] and similar levels of cholesterol and enzymes activities (LDH, ALP, CPK, GOT, GPT, and CGT) observed in both groups over the trial indicate that feeding the BYP diet did not negatively affect liver function.
Finally, it is worth mentioning that under the conditions of our study, the cost of the control and BYP concentrates were 0.270 €/kg and 0.262 €/kg, respectively, resulting in a calculated cost of concentrate per kg of gain was 0.787 € and 0.777 € per control and BYP concentrate, respectively. However, these results may vary, as feed prices are highly volatile.

4. Conclusions

Our results indicate that a mixture of corn DDGS, DCP and EOC can replace 44% of cereal grains and protein feeds in the concentrate for light lambs without negatively affecting the feed intake, growth performance, or health of lambs. The use of these byproducts reduced the potentially human-edible ingredients in the concentrate from 64.4% to 38.7% and slightly decreased the feeding costs. In situations of high prices of cereals and protein feeds, the use of byproducts by lamb farmers can be more economically profitable than in the present study.

Author Contributions

M.D.C. and J.d.l.F. obtained the funding and conceived the experiments; T.d.E., A.C., J.d.l.F., and M.D.C. performed the lambs trial; T.d.E. and A.C. analyzed the samples; T.d.E. did data calculations, conducted statistical analysis, and wrote the draft; M.D.C. and J.F. provided advice and critically reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Spanish State Research Agency (AEI) and the European Regional Development Fund (Project AGL2016-75322-C2-1-R).

Acknowledgments

Thanks are given to SACYR Industrial for providing free the exhausted olive cake used in this study. The authors are thankful to Chistian Jiménez and Carlos Chasipanta for their help in animal feeding and data collection.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Gerber, P.J.; Uwizeye, A.; Schulte, R.P.O.; Opio, C.I.; de Boer, I.J.M. Nutrient use efficiency: A valuable approach to benchmark the sustainability of nutrient use in global livestock production? Curr. Opin. Environ. Sustain. 2014, 9, 122–1309. [Google Scholar] [CrossRef]
  2. Bakshi, M.P.S.; Wadhwa, M.; Makkar, H. Waste to worth: Vegetable wastes as animal feed. Cab. Rev. 2016, 11, 1–26. [Google Scholar] [CrossRef]
  3. Vasta, V.; Nudda, A.; Cannas, A.; Lanza, M.; Priolo, A. Alternative feed resources and their effects on the quality of meat and milk from small ruminants. Anim. Feed Sci. Technol. 2008, 147, 223–246. [Google Scholar] [CrossRef]
  4. Correddu, F.; Lunesu, M.F.; Buffa, G.; Atzori, A.S.; Nudda, A.; Battacone, G.; Pulina, G. Can Agro-Industrial By-Products Rich in Polyphenols be Advantageously Used in the Feeding and Nutrition of Dairy Small Ruminants? Animals 2020, 10, 131. [Google Scholar] [CrossRef] [Green Version]
  5. International Olive Oil Organization. Olive Oil Estimates 2019/20 Crop Year. Available online: https://www.internationaloliveoil.org/olive-oil-estimates-2019-20-crop-year/ (accessed on 10 January 2020).
  6. MAPA 2020. Ministerio de Agricultura, Pesca y Alimentación. Available online: http://www.mapa.gob.es/ (accessed on 10 January 2020).
  7. Marcos, C.N.; García-Rebollar, P.; de Blas, C.; Carro, M.D. Variability in the Chemical Composition and In Vitro Ruminal Fermentation of Olive Cake By-Products. Animals 2019, 9, 109. [Google Scholar] [CrossRef] [Green Version]
  8. UNCTD. United Nations Conference on Trade and Development. 2020. Available online: https://unctad.org/SearchCenter/Pages/results.aspx?k=citrus%20production (accessed on 10 January 2020).
  9. Bampidis, V.A.; Robinson, P.H. Citrus by-products as ruminant feeds: A review. Anim. Feed Sci. Technol. 2006, 128, 175–217. [Google Scholar] [CrossRef]
  10. Molina-Alcaide, E.; Yáñez-Ruíz, D.R. Potential use of olive by-products in ruminant feeding: A review. Anim. Feed Sci. Technol. 2008, 147, 247–264. [Google Scholar] [CrossRef]
  11. Sauvant, D.; Delaby, L.; Noziere, P. INRA Feeding System for Ruminants; Noziere, P., Sauvant, D., Delaby, L., Eds.; Wageningen Academic Publishers: Wageningen, The Netherlands, 2017. [Google Scholar]
  12. Carro, M.D.; Ranilla, M.J.; Giráldez, F.J.; Mantecón, A.R. Effects of malate supplementation on feed intake, digestibility, microbial protein synthesis and plasma metabolites in lambs fed a high-concentrate diet. J. Anim. Sci. 2006, 84, 405–410. [Google Scholar] [CrossRef] [Green Version]
  13. Haro, A.N.; González, J.; de Evan, T.; de la Fuente, J.; Carro, M.D. Effects of feeding rumen-protected sunflower seed and meal protein on feed intake, diet digestibility, ruminal and cecal fermentation, and growth performance of lambs. Animals 2019, 9, 415. [Google Scholar] [CrossRef] [Green Version]
  14. Association of Official Analytical Chemists (AOAC). Official Methods of Analysis, 18th ed.; AOAC International: Gaithersburg, MD, USA, 2005. [Google Scholar]
  15. Van Soest, P.J.; Robertson, J.B.; Lewis, B.A. Methods for dietary fiber, neutral detergent fiber and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 1991, 74, 3583–3597. [Google Scholar] [CrossRef]
  16. Robertson, J.B.; Van Soest, P.J. The detergent system of analysis and its application to human foods. In The Analysis of Dietary Fiber in Food; James, W.P.T., Theander, O., Eds.; Marcel Dekker Inc.: New York, NY, USA, 1981; pp. 123–142. [Google Scholar]
  17. García-Martínez, R.; Ranilla, M.J.; Tejido, M.L.; Carro, M.D. Effects of disodium fumarate on in vitro rumen microbial growth, methane production and fermentation of diets differing in their forage concentrate ratio. Br. J. Nutr. 2005, 94, 71–77. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Weatherburn, M.W. Phenol-hypochlorite reaction for determination of ammonia. Anal. Chem. 1967, 39, 971–974. [Google Scholar] [CrossRef]
  19. Frank, M.P.; Powers, R.W. Simple and rapid quantitative high-performance liquid chromatographic analysis of plasma amino acids. J. Chromatogr. B. Analyt. Technol. Biomed. Life Sci. 2007, 852, 646–649. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. SAS Institute. SAS/STAT® Users Guide, Version 9.3; SAS Inst. Inc.: Cary, NC, USA, 2017. [Google Scholar]
  21. Jiménez, C. Use of Agroindustrial by-Products (Olive Cake, Tomato Pulp and Wine Lees) in Diets for Fattening Lambs: In Vitro Evaluation. Master’s Thesis, Technical University of Madrid, Madrid, Spanish, 2018. [Google Scholar]
  22. Wilkinson, J.M. Re-defining efficiency of feed use by livestock. Animal 2011, 5, 1014–1022. [Google Scholar] [CrossRef] [Green Version]
  23. NRC (National Research Council). Nutrient Requirements of Dairy Cattle, 7th ed.; National Academy of Sciences: Washington, DC, USA, 2001. [Google Scholar]
  24. Manso, T.; Mantecón, A.R.; Giráldez, F.J.; Lavín, P.; Castro, T. Animal performance and chemical body composition of lambs fed diets with different protein supplements. Small Rum. Res. 1998, 29, 185–191. [Google Scholar] [CrossRef]
  25. Carrasco, S.; Ripoll, G.; Sanz, A.; Álvarez-Rodríguez, J.; Panea, B.; Revilla, R.; Joy, M. Effect of feeding system on growth and carcass characteristics of Churra Tensina light lambs. Livest. Sci. 2009, 121, 56–63. [Google Scholar] [CrossRef]
  26. Blanco, C.; Giráldez, F.J.; Prieto, N.; Morán, L.; Andrés, S.; Benavides, J.; Tejido, M.L.; Bodas, R. Effects of dietary inclusion of sunflower soap stocks on nutrient digestibility, growth performance, and ruminal and blood metabolites of light fattening lambs. J. Anim. Sci. 2014, 92, 4086–4094. [Google Scholar] [CrossRef] [Green Version]
  27. Blanco, C.; Bodas, R.; Prieto, N.; Andrés, S.; López, S.; Giráldez, F.J. Concentrate plus ground barley straw pellets can replace conventional feeding systems for light fattening lambs. Small Rum. Res. 2014, 116, 137–143. [Google Scholar] [CrossRef] [Green Version]
  28. Owaimer, A.; Kraidees, M.; Al-saiady, M.; Zahran, S.; Abouheif, M. Effect of Feeding Olive Cake in Complete Diet on Performance and Nutrient Utilization of Lambs. Asian-Australas J. Anim. Sci. 2004, 17, 491–496. [Google Scholar] [CrossRef]
  29. Sharif, M.; Ashraf, M.S.; Mushtaq, N.; Nawaz, H.; Mustafa, M.I.; Ahmad, F.; Younas, M.; Javaid, A. Influence of varying levels of dried citrus pulp on nutrient intake, growth performance and economic efficiency in lambs. J. Appl. Anim. Res. 2018, 46, 264–268. [Google Scholar] [CrossRef] [Green Version]
  30. Awawdeh, M.S.; Dager, H.K.; Obeidat, B.S. Effects of alternative feedstuffs on growth performance, carcass characteristics, and meat quality of growing Awassi lambs. Ital. J. Anim. Sci. 2019, 18, 777–785. [Google Scholar] [CrossRef] [Green Version]
  31. Rodríguez, R.B.; de Frutos Fernández, P.; García, F.J.G.; Angulo, G.H.; Puente, S.L. Effect of sodium bicarbonate supplementation on feed intake, digestibility, digesta kinetics, nitrogen balance and ruminal fermentation in young fattening lambs. Span. J. Agric. Res. 2009, 2, 330–341. [Google Scholar]
  32. Andrés, S.; Jaramillo, E.; Bodas, R.; Blanco, C.; Benavides, J.; Fernández, P.; González, E.P.; Frutos, J.; Belenguer, A.; Lopéz, S.; et al. Grain grinding size of cereals in complete pelleted diets for growing lambs: Effects on ruminal microbiota and fermentation. Small Rum. Res. 2018, 159, 38–44. [Google Scholar] [CrossRef]
  33. Benchaar, C.; Hassanat, F.; Gervais, R.; Chouinard, P.Y.; Julien, C.; Petit, V.; Massé, D.I. Effects of increasing amounts of corn dried distillers grains with solubles in dairy cow diets on methane production, ruminal fermentation, digestion, N balance, and milk production. J. Dairy Sci. 2013, 96, 1–15. [Google Scholar] [CrossRef] [PubMed]
  34. Firkins, J.L.; Yu, Z.; Morrison, M. Ruminal nitrogen metabolism: Perspectives for integration of microbiology and nutrition for dairy cows. J. Dairy Sci. 2007, 90, E1–E16. [Google Scholar] [CrossRef] [PubMed]
  35. Carrasco, C.; Carro, M.D.; Fuentaja, A.; Medel, P. Performance, carcass and ruminal fermentation characteristics of heifers fed concentrates differing in energy level and cereal type (corn vs. wheat). Span. J. Agric. Res. 2017, 15, 13. [Google Scholar] [CrossRef] [Green Version]
  36. Bergen, W.G.; Henneman, H.A.; Magee, W.T. Effect of dietary protein level and protein source on plasma and tissue free amino acids in growing sheep. J. Nutr. 1973, 103, 575–585. [Google Scholar] [CrossRef] [Green Version]
  37. Bergen, W.G. Free amino acids in blood of ruminants-physiological and nutritional regulation. J. Anim. Sci. 1979, 49, 1577–1589. [Google Scholar] [CrossRef]
  38. Calsamiglia, A.; Ferret, A.; Reynolds, C.K.; Kristensen, N.B.; Van Vuuren, A.M. Strategies for optimizing nitrogen use by ruminants. Animal 2010, 4, 1184–1196. [Google Scholar] [CrossRef]
  39. Lestingi, A.; Toteda, F.; Vicenti, A.; de De Marzo, D.; Facciolongo, A.M. The Use of Faba Bean and Sweet Lupin Seeds Alone or in Combination for Growing Lambs. 1. Effects on Growth Performance, Carcass Traits, and Blood Parameters. Pakistan J. Zool. 2015, 47, 989–996. [Google Scholar]
  40. Lobón, S.; Joy, M.; Casasús, I.; Rufino-Moya, P.J.; Blanco, M. Field Pea can be Included in Fattening Concentrate without Deleterious Effects on the Digestibility and Performance of Lambs. Animals 2020, 10, 243. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  41. Xu, Y.; Li, Z.; Moraes, L.E.; Shen, J.; Yu, Z.; Zhu, W. Effects of Incremental Urea Supplementation on Rumen Fermentation, Nutrient Digestion, Plasma Metabolites, and Growth Performance in Fattening Lambs. Animals. 2019, 9, 652. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Table 1. Ingredient and chemical composition of experimental concentrates.
Table 1. Ingredient and chemical composition of experimental concentrates.
ItemControlBYP
Ingredients (% as fed)
Corn33.026.8
Barley20.0-
Wheat10.010.0
Soybean meal 47%12.210.2
Palm meal8.8-
Colza meal2.52.5
Wheat bran10.03.0
Dry citrus pulp-18.0
Corn DDGS-18.0
Olive cake-8.0
Others 13.53.5
Chemical composition (%, as-fed basis)
Dry matter (DM)89.788.6
Ashes4.825.97
Crude protein (CP)16.217.5
Ether extract (EE)3.756.44
Neutral detergent fiber (NDF)19.219.5
Acid detergent fiber (ADF)7.479.31
Acid detergent lignin1.792.80
Non-structural carbohydrates (NSC) 245.735.2
Forage units for meat production (UFV) 31.000.96
1 For both concentrates: 1.2% Calcium soap; 1.0% calcium carbonate; 0.8% sodium bicarbonate; 0.3% NaCl, and 0.2% vitamin-mineral premix; 2 Calculated as DM − (ashes + CP + EE + NDF); 3 Calculated according to INRA [11].
Table 2. Initial and final body weight, feed intake, average daily gain, feed conversion rate, carcass weights, and carcass yield of light lambs fed either a high-cereal concentrate (control) or a concentrate including byproducts (BYP) 1.
Table 2. Initial and final body weight, feed intake, average daily gain, feed conversion rate, carcass weights, and carcass yield of light lambs fed either a high-cereal concentrate (control) or a concentrate including byproducts (BYP) 1.
ItemControl (n = 12)BYP (n = 12)SEM 2p-Value
Initial body weight (kg)13.613.90.950.595
Feed intake (g/d)
Concentrate82885477.90.568
Straw40.347.713.400.341
Total86990277.90.463
Final body weight (kg)26.226.41.250.744
Average daily gain (g/d)28428832.90.844
Feed conversion rate (g concentrate/g)2.922.970.3200.747
Carcass traits
Hot carcass weight (kg)14.414.20.760.704
Cold carcass weight (kg)13.613.60.900.987
Cold carcass yield (%)51.951.52.150.765
1 BYP concentrate contained 18% corn DDGS, 18% dried citrus pulp and 8% exhausted olive cake (as-fed basis); 2 Standard error of the mean.
Table 3. Diet digestibility and nitrogen balance in light lambs fed either a high-cereal concentrate (control) or a concentrate including byproducts (BYP) 1.
Table 3. Diet digestibility and nitrogen balance in light lambs fed either a high-cereal concentrate (control) or a concentrate including byproducts (BYP) 1.
ItemControl (n = 9)BYP (n = 9)SEM 2p-Value
Digestibility (%)
Dry matter79.174.40.74< 0.001
Organic matter81.476.70.69< 0.001
Crude protein75.273.10.970.141
Neutral detergent fiber53.354.81.800.570
Acid detergent fiber47.652.01.910.120
Nitrogen (N) balance
N intake (g/d)21.824.10.660.024
Fecal N
g/d5.406.490.2730.012
% of ingested N24.826.90.9690.141
Urinary N
g/d4.735.170.5980.616
% of ingested N21.421.42.280.988
Retained N
g/d11.712.50.550.312
% of ingested N53.851.72.210.519
1 BYP concentrate contained 18% corn DDGS, 18% dried citrus pulp and 8% exhausted olive cake (as-fed basis); 2 Standard error of the mean.
Table 4. Ruminal parameters measured post-mortem and rumen wall color in light lambs fed either a high-cereal concentrate (control) or a concentrate including byproducts (BYP) 1.
Table 4. Ruminal parameters measured post-mortem and rumen wall color in light lambs fed either a high-cereal concentrate (control) or a concentrate including byproducts (BYP) 1.
ItemControl (n = 12)BYP (n = 12)SEM 2p-Value
pH5.405.620.1260.263
NH3-N (mg/l)69.245.72.170.003
Total volatile fatty acids (VFA; mM)14013015.10.643
Molar proportions (mol/100 mol)
Acetate52.852.81.710.987
Propionate33.233.62.170.900
Butyrate9.268.180.9390.424
Isobutyrate0.580.450.0900.332
Isovalerate0.670.540.1040.388
Valerate3.013.800.2970.073
Caproate0.560.680.1310.516
Acetate/propionate ratio (mol/mol)1.771.640.1750.593
Rumen wall colour 32.193.190.4020.092
1 BYP concentrate contained 18% corn DDS, 18% dried citrus pulp and 8% exhausted olive cake (as-fed basis); 2 Standard error of the mean; 3 Scored from 1 (pale) to 5 (dark).
Table 5. Plasma concentrations of amino acids in light lambs fed either control concentrate (CON; n = 12) or a concentrate including byproducts (BYP; n = 12) at the beginning (day 0) and end (day 42) of the trial 1.
Table 5. Plasma concentrations of amino acids in light lambs fed either control concentrate (CON; n = 12) or a concentrate including byproducts (BYP; n = 12) at the beginning (day 0) and end (day 42) of the trial 1.
ItemDietDayp-Value
042SEM 2DietDayDiet × Day
Amino acid (µmol/L)
Aspartic acidCON34.739.01.230.909<0.0010.156
BYP33.141.4
Glutamic acidCON17720522.80.6080.1620.767
BYP186227
AsparagineCON41.146.64.570.7420.0650.439
BYP35.748.8
SerineCON57.475.66.970.5470.0620.597
BYP65.776.2
GlutamineCON57.569.66.860.9020.0530.721
BYP55.873.2
HistidineCON35.438.72.360.2380.1320.841
BYP31.535.8
GlycineCON27429532.50.3120.8710.433
BYP336303
ThreonineCON77.815414.080.826<0.0010.631
BYP88.5150
ArginineCON11213913.50.3680.3430.340
BYP112112
AlanineCON63.367.06.510.7600.6540.926
BYP66.769.2
TyrosineCON58.572.26.620.9710.0100.403
BYP53.478.8
CysteineCON20319918.80.8240.7860.914
BYP213205
ValineCON10315516.50.280<0.0010.267
BYP102194
MethionineCON32.541.82.420.859<0.0010.223
BYP29.745.5
TryptophanCON28.035.21.670.294<0.0010.387
BYP25.431.8
PhenylalanineCON47.053.84.120.7410.0230.385
BYP45.259.6
IsoleucineCON57.570.47.670.4830.0210.375
BYP56.083.4
LeucineCON63.899.111.240.109<0.0010.151
BYP66.7137
LysineCON93.911810.210.9530.0050.406
BYP83.9127
Essential AACON53976663.70.531<0.0010.422
BYP528865
Total AACON17522134189.30.6540.0640.934
BYP18332249
1 BYP concentrate contained 18% corn DDGS, 18% dried citrus pulp and 8% exhausted olive cake (as-fed basis); 2 Standard error of the mean.
Table 6. Plasma concentrations of metabolites in light lambs fed either a high-cereal concentrate (CON; n = 12) or a concentrate including byproducts (BYP; n = 12) over the trial 1.
Table 6. Plasma concentrations of metabolites in light lambs fed either a high-cereal concentrate (CON; n = 12) or a concentrate including byproducts (BYP; n = 12) over the trial 1.
Item 2DietDay p-Value
02142SEMd 3SEMsd 3DietDayDiet × Day
Urea
(mg/100 mL)
CON22.9 ab20.3 a25.4 b0.710.860.5850.0040.889
BYP23.1 ab22.0 a25.8 b
Albumine
(mg/100 mL)
CON2.12 a2.30 a2.53 b0.0400.0490.276<0.0010.571
BYP2.28 a2.32 a2.59 b
Globulins
(g/100 mL)
CON3.183.323.550.0970.1180.5560.3160.742
BYP3.163.273.30
Total proteins
(g/100 mL)
CON5.30 a5.62 ab6.00 b0.0950.1170.6920.0030.483
BYP5.44 ab5.38 a5.88 b
Cholesterol
(mg/100 mL)
CON54.3 b38.8 a40.1 a1.942.380.876<0.0010.952
BYP53.8 b37.3 a40.6 a
LDH (Units/L)CON502 a670 b653 b12.815.70.638<0.0010.538
BYP495 a706 b673 b
ALP (Units/L)CON2.15 a1.45 a5.08 b0.2930.3590.592<0.0010.922
BYP2.18 a1.70 a5.30 b
CPK (Units/L)CON102 a201 b123 a9.912.10.780<0.0010.954
BYP96.6 a203 b114 a
GOT (Units/L)CON45.2 a70.8 b72.5 b2.182.6750.522<0.0010.889
BYP45.6 a72.5 b76.6 b
GPT (Units/L)CON5.62 a13.1 c9.54 b0.4360.5340.755<0.0010.738
BYP6.09 a12.6 c8.92 b
GGT (Units/L)CON10198.11063.434.200.1140.2150.223
BYP102122117
a,b,c Within a row, means with different superscript differ (p < 0.05); 1 BYP concentrate contained 18% corn DDGS, 18% dried citrus pulp and 8% exhausted olive cake (as-fed basis); 2 LDH: Lactate dehydrogenase, ALP: Alkaline phosphatase, CPK: creatine phosphokinase, GOT: Glutamic oxaloacetic transaminase, GPT: Glutamic pyruvic transaminase, GCT: Gamma-glutamyl transpeptidase; 3 SEMd and SEMsd: Standard error of the mean for diet and sampling day effects, respectively.

Share and Cite

MDPI and ACS Style

de Evan, T.; Cabezas, A.; de la Fuente, J.; Carro, M.D. Feeding Agroindustrial Byproducts to Light Lambs: Influence on Growth Performance, Diet Digestibility, Nitrogen Balance, Ruminal Fermentation, and Plasma Metabolites. Animals 2020, 10, 600. https://doi.org/10.3390/ani10040600

AMA Style

de Evan T, Cabezas A, de la Fuente J, Carro MD. Feeding Agroindustrial Byproducts to Light Lambs: Influence on Growth Performance, Diet Digestibility, Nitrogen Balance, Ruminal Fermentation, and Plasma Metabolites. Animals. 2020; 10(4):600. https://doi.org/10.3390/ani10040600

Chicago/Turabian Style

de Evan, Trinidad, Almudena Cabezas, Jesús de la Fuente, and María Dolores Carro. 2020. "Feeding Agroindustrial Byproducts to Light Lambs: Influence on Growth Performance, Diet Digestibility, Nitrogen Balance, Ruminal Fermentation, and Plasma Metabolites" Animals 10, no. 4: 600. https://doi.org/10.3390/ani10040600

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop