Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

The effects of barley replacement by dehydrated citrus pulp on feed intake, performance, feeding behaviour and serum metabolic indicators in lambs

M. N. N. E. Gobindram A , M. Bognanno B , G. Luciano C , M. Avondo C , G. Piccione D and L. Biondi C E
+ Author Affiliations
- Author Affiliations

A Agricultural Transformation by Innovation (AgTraIn) – Erasmus Mundus Joint Doctorate Program; Di3A, Animal Production Division, University of Catania, Via Valdisavoia 5, 95123, Catania, Italy.

B Department AGRARIA, University of Reggio Calabria, località Feo di Vito snc, 89122, Reggio Calabria, Italy.

C Di3A, Animal Production Division, University of Catania, Via Valdisavoia 5, 95123, Catania, Italy.

D Department of Veterinary Sciences, Polo Universitario Annunziata, University of Messina, 98168, Messina, Italy.

E Corresponding author. Email: lubiondi@unict.it

Animal Production Science 57(1) 133-140 https://doi.org/10.1071/AN141010
Submitted: 18 December 2014  Accepted: 30 July 2015   Published: 20 October 2015

Abstract

The citrus industry produces a wide amount of citrus pulp which can represent an alternative feed resource for feeding ruminants. However, citrus pulp also contains chemicals such as polyphenols, which can cause toxicity, limiting its use. We investigated the potential of replacing barley by dehydrated citrus pulp (DCP), at two levels of inclusion (24% and 35% on an as-fed basis), in a lamb fattening diet and monitored the performance, feeding pattern and serum parameters of the experimental lambs. The consumption of a diet containing up to 35% of DCP resulted in equivalent performance, feed efficiency and carcass weight and yield as compared with animals ingesting a cereal-based diet (control). The daily feed consumption pattern was slightly affected by the inclusion of citrus pulp in the diet. In terms of serum haematochemical profile, DCP ingesting animals had similar levels to control lambs. Pertaining to the serum protein profile, DCP addition had minor effects. A significant increase in the albumin content and in the albumin to globulin ratio was observed in the animals ingesting 35% DCP compared with the control-fed ones; but the values were not at a level to cause metabolic distress. The use of high levels of DCP in small ruminant fattening can ensure equivalent animal performances and metabolic welfare while providing a value addition to a local by-product.

Additional keywords: dehydrated citrus pulp, polyphenols, serum metabolites, serum protein profile.


References

Ahooei GR, Foroughi AR, Tahmasbi AM, Shahdadi AR, Vakili R (2011) Effects of different levels of dried citrus pulp and urea on performance of fattening male calves. Journal of Animal and Veterinary Advances 10, 1811–1816.
Effects of different levels of dried citrus pulp and urea on performance of fattening male calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktVKmsr4%3D&md5=7f3ae7e1efed67839e256f3a606e69a2CAS |

Alberghina D, Casella S, Vazzana I, Ferrantelli V, Giannetto C, Piccione G (2010) Analysis of serum proteins in clinically healthy goats (Capra hircus) using agarose gel electrophoresis. Veterinary Clinical Pathology 39, 317–321.
Analysis of serum proteins in clinically healthy goats (Capra hircus) using agarose gel electrophoresis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbltV2ntg%3D%3D&md5=177440b8450b3b7e84f36d981bbc8f41CAS | 20412548PubMed |

Amparo C, Martinez-Monzo J, Chafer T, Fito P (1998) Limonene from citrus. In Mazza, Giuseppe, ed. Functional foods: biochemical and processing aspects. Vol. 1. CRC Press, 1998.

AOAC (1995) ‘Official methods of analysis.’ 16th edn. (Association of Official Analytical Chemists: Arlington, WA)

Arthington JD, Kunkle WE, Martin AM (2002) Citrus pulp for cattle. In ‘The veterinary clinics of North America-food animal practice’. (Eds G Rogers, M Poore) pp. 317–328. (W.B. Saunders Company: Philadelphia, PA)

Balasundram N, Sundram K, Samman S (2006) Phenolic compounds in plants and agri-industrial by-products: antioxidant activity, occurrence, and potential uses. Food Chemistry 99, 191–203.
Phenolic compounds in plants and agri-industrial by-products: antioxidant activity, occurrence, and potential uses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjslygsLc%3D&md5=5e0a52e6cb9e36bdcbf93b52400cb40bCAS |

Bampidis VA, Robinson PH (2006) Citrus by-products as ruminant feeds: a review. Animal Feed Science and Technology 128, 175–217.
Citrus by-products as ruminant feeds: a review.Crossref | GoogleScholarGoogle Scholar |

Battacharya AN, Harb M (1973) Dried citrus pulp as grain replacement for Awasi lambs. Journal of Animal Science 36, 1175–1180.

Belibasakis NG, Tsirgogianni D (1996) Effects of dried citrus pulp on milk yield, milk composition and blood components of dairy cows. Animal Feed Science and Technology 60, 87–92.
Effects of dried citrus pulp on milk yield, milk composition and blood components of dairy cows.Crossref | GoogleScholarGoogle Scholar |

Ben-Ghedalia D, Yosef E, Miron J, And Est Y (1989) The effects of starch and pectin-rich diets on quantitative aspects of digestion in sheep. Animal Feed Science and Technology 24, 289–298.
The effects of starch and pectin-rich diets on quantitative aspects of digestion in sheep.Crossref | GoogleScholarGoogle Scholar |

Broom DM (1991) Animal welfare: concepts and measurement. Journal of Animal Science 69, 4167–4175.

Bueno MS, Ferrari E, Bianchini D, Leinz FF, Rodrigues CFC (2002) Effect of replacing corn with dehydrated citrus pulp in diets of growing kids. Small Ruminant Research 46, 179–185.
Effect of replacing corn with dehydrated citrus pulp in diets of growing kids.Crossref | GoogleScholarGoogle Scholar |

Callaway T, Carroll JA, Arthington JD, Edrington TS, Anderson RC, Ricke SC, Crandall P, Collier C, Nisbet DJ (2011a) Citrus products and their use against bacteria: potential health and cost benefits. In: ‘Nutrients, dietary supplements, and nutriceuticals: cost analysis versus clinical benefits’. (Eds RR Watson, JK Gerald, VR Preedy) pp. 277–286. (Springer Sciences – Business Media LLC: New York, NY)

Callaway TR, Carroll J, Arthington JD, Edrington TS, Anderson RC, Rossman ML, Carr MA, Genovese KJ, Ricke SC, Crandall P, Nisbet DJ (2011b) Orange peel products can reduce Salmonella populations in ruminants. Foodborne Pathogens and Disease 8, 1071–1075.
Orange peel products can reduce Salmonella populations in ruminants.Crossref | GoogleScholarGoogle Scholar | 21651339PubMed |

Callaway TR, Carroll J, Arthington JD, Edrington TS, Rossman ML, Carr MA, Krueger NA, Ricke SC, Crandall P, Nisbet DJ (2011c) Research Note: Escherichia coli O157:H7 populations in ruminants can be reduced by orange peel product feeding. Journal of Food Protection 74, 1917–1921.
Research Note: Escherichia coli O157:H7 populations in ruminants can be reduced by orange peel product feeding.Crossref | GoogleScholarGoogle Scholar | 22054194PubMed |

Ceciliani F, Ceron JJ, Eckersall PD, Sauerwein H (2012) Acute phase proteins in ruminants. Journal of Proteomics 75, 4207–4231.
Acute phase proteins in ruminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmvFChtLs%3D&md5=1ab176771372ab8c3bf1b425bd73bdd4CAS | 22521269PubMed |

Durmic Z, Blache D (2012) Bioactive plant and plant products: effects on animal function, health and welfare. Animal Feed Science and Technology 176, 150–162.
Bioactive plant and plant products: effects on animal function, health and welfare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVyksLbK&md5=5ed690a2337d7edd8d02b145bc9e9212CAS |

Eckersall PD (2008) Proteins, proteomics, and the dysproteinemias. Clinical Biochemistry of Domestic Animals 6, 114–155.

Farver TB (1997) Concepts of normality in clinical biochemistry. II. Reference interval determination and use. In ‘Clinical biochemistry of domestic animals’. 5th edn. (Eds J Kaneko, J Harvey, M Bruss) pp. 2–9. (Academic Press: San Diego, CA)

Fattouch S, Caboni P, Coroneo V, Tuberoso C, Angioni A, Dessi S, Marzouki N, Cabras P (2007) Antimicrobial activity of Tunisian quince (Cydonia oblonga Miller) pulp and peel polyphenolic extracts. Journal of Agricultural and Food Chemistry 55, 963–969.
Antimicrobial activity of Tunisian quince (Cydonia oblonga Miller) pulp and peel polyphenolic extracts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtVegtA%3D%3D&md5=84a3422bf97ad3b4d4a3a1af9871de30CAS | 17263500PubMed |

Frutos P, Hervás G, Giráldez FJ, Mantecón AR (2004) Review: tannins and ruminant nutrition. Spanish Journal of Agricultural Research 2, 191–202.
Review: tannins and ruminant nutrition.Crossref | GoogleScholarGoogle Scholar |

Gilaverte S, Susin I, Pires AV, Ferreira EM, Mendes CQ, Gentil RS, Biehl MV, Rodrigues GH (2011) Diet digestibility, ruminal parameters and performance of Santa Ines sheep fed dried citrus pulp and wet brewer grain. Revista Brasileira de Zootecnia 40, 639–647.
Diet digestibility, ruminal parameters and performance of Santa Ines sheep fed dried citrus pulp and wet brewer grain.Crossref | GoogleScholarGoogle Scholar |

Gill W (2004) Applied sheep behavior. Agricultural Extension Service, 1–24. Available at http://animalscience.ag.utk.edu/sheep/pdf/appliedsheepbehavior-wwg-2-04.pdf [Verified 1 July 2014]

Gobindram NEM, Bognanno M, Luciano G, Lanza M, Biondi L (2014) Carob pulp inclusion in lambs’ diet: effect on intake, performance, feeding behaviour and blood metabolites. Animal Production Science
Carob pulp inclusion in lambs’ diet: effect on intake, performance, feeding behaviour and blood metabolites.Crossref | GoogleScholarGoogle Scholar |

Gravador RS, Jongberg S, Andersen ML, Luciano G, Priolo A, Lund MN (2014) Dietary citrus pulp improves protein stability in lamb meat stored under aerobic conditions. Meat Science 97, 231–236.
Dietary citrus pulp improves protein stability in lamb meat stored under aerobic conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXltFeqsbw%3D&md5=45355e2edb953cef2559d026d45958e1CAS | 24583333PubMed |

Inserra L, Priolo A, Biondi L, Lanza M, Bognanno M, Gravador RN, Luciano G (2014) Dietary citrus pulp reduces lipid oxidation in lamb meat. Meat Science 96, 1489–1493.
Dietary citrus pulp reduces lipid oxidation in lamb meat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXislOitL4%3D&md5=0b0d63f70f9fb67542a60dd5cccbbdf9CAS | 24440744PubMed |

ISTAT (2015) Data warehouse ‘Censimento Agricoltura 2010’. Available at http://dati.istat.it/Index.aspx?lang=en&SubSessionId=a9921983-14c4-4a08-842e-50323c892151&themetreeid=101 [Verified 22 June 2015]

Kale PN, Adsule PG (1995) Citrus. In ‘Handbook of fruit science and technology: production, composition, storage and processing’. (Eds DK Salunkhe, SS Kadam) pp. 39–65. (Marcel Dekker, Inc.: New York, NY)

Kim SC, Adesogan AT, Arthington JD (2007) Optimising nitrogen utilization in growing steers fed forage diets supplemented with dried citrus pulp. Journal of Animal Science 85, 2548–2555.
Optimising nitrogen utilization in growing steers fed forage diets supplemented with dried citrus pulp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFSjtrjN&md5=8fd53c829ada8f87d3ceebc73325d774CAS | 17526670PubMed |

Lanza M, Scerra M, Bognanno M, Buccioni A, Cilione C, Biondi L, Priolo A, Luciano G (2015) Fatty acid metabolism in lambs fed citrus pulp. Journal of Animal Science
Fatty acid metabolism in lambs fed citrus pulp.Crossref | GoogleScholarGoogle Scholar | 26115304PubMed |

Madrid J, Hernández F, Pulgar MA, Cid JM (1997) Urea and citrus by-product of straw-based diets for goats: effect on barley straw digestibility. Small Ruminant Research 24, 149–155.
Urea and citrus by-product of straw-based diets for goats: effect on barley straw digestibility.Crossref | GoogleScholarGoogle Scholar |

Makkar HPS, Blümmel M, Borowy NK, Becker K (1993) Gravimetric determination of tannins and their correlations with chemical and protein precipitation methods. Journal of the Science of Food and Agriculture 61, 161–165.

Mathur A, Verma SK, Purohit R, Gupta V, Dua VK, Prasad GBKS, Mathur D, Singh S (2011) Evaluation of in vitro antimicrobial and antioxidant activities of peel and pulp of some citrus fruits. Journal of Biotechnology and Biotherapeutics 1, 1–17.

Middleton E, Kandaswami C (1994) Potential health-promoting properties of citrus flavonoids. Food Technology 48, 115–119.

Miron J, Yosef E, Ben-Ghedalia D, Chase LE, Bauman DE, Solomon R (2002) Digestibility by dairy cows of monosaccharide e constituents in total mixed rations containing citrus pulp. Journal of Dairy Science 85, 89–94.
Digestibility by dairy cows of monosaccharide e constituents in total mixed rations containing citrus pulp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFGhtLY%3D&md5=45de5b2483ee31765f697f2e3f4694b5CAS | 11860125PubMed |

Morales H, Stuart JR, González J, Gutiérrez E, Bernal H, Colin J (2010) Productive performance and dynamics of blood metabolites in Pelibuey lambs, fed cereals, dehydrated citrus pulp and urea. Cuban Journal of Agricultural Science 44, 129–133.

Moss AR (1994) Methane production by ruminants-literature review of I dietary manipulation to reduce methane production and II Laboratory procedures for estimating methane potential of diets. Nutrition Abstracts and Reviews (Ser. B) 64, 785–806.

Ndlovu T, Chimonyo M, Okoh AI, Muchenje V, Dzama K, Dube S, Raats JG (2009) A comparison of nutritionally-related blood metabolites among Nguni, Bonsmara and Angus steers raised on sweet-veld. Veterinary Journal (London, England) 179, 273–281.
A comparison of nutritionally-related blood metabolites among Nguni, Bonsmara and Angus steers raised on sweet-veld.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFemu7c%3D&md5=e3746321652f60fa4902df572791fb76CAS |

Nordi ECP, Costa RLD, David CMG, Parren GAE, Freitas ACB, Lameirinha LP, Katiki LM, Buenoa MS, Quirino CR, Gamac PE, Bizzo HR, Chagas ACS (2014) Supplementation of moist and dehydrated citrus pulp in the diets of sheep artificially and naturally infected with gastrointestinal nematodes on the parasitological parameters and performance. Veterinary Parasitology 205, 532–539.
Supplementation of moist and dehydrated citrus pulp in the diets of sheep artificially and naturally infected with gastrointestinal nematodes on the parasitological parameters and performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1Ors7fL&md5=f15e33cb59d6379a44f493cfd534ed3aCAS |

Ohl F, Van der Staay FJ (2012) Animal welfare: at the interface between science and society. Veterinary Journal (London, England) 192, 13–19.
Animal welfare: at the interface between science and society.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38zks1elsw%3D%3D&md5=6e56aaf006b8660607400b9c08d77d09CAS |

Piccione G, Messina V, Giannetto C, Casella S, Assenza A, Fazio F (2011) Seasonal variations of the serum proteins in sheep and goats. Archiv Tierzucht 54, 399–405.

Provenza FD, Villalba JJ, Dziba LE, Atwood SB, Banner RE (2003) Linking herbivore experience, varied diets, and plant biochemical diversity. Small Ruminant Research 49, 257–274.
Linking herbivore experience, varied diets, and plant biochemical diversity.Crossref | GoogleScholarGoogle Scholar |

Rihani N (1991) Valeur alimentaire et utilisation des sous-produits des agrumes en alimentation animale. Options Méditerranéennes-Série Séminaires 16, 113–117.

Saunders GK, Blodgett DJ, Hutchins TA, Prater RM, Robertson JL, Friday PA, Scarratt WK (2000) Suspected citrus pulp toxicosis in dairy cattle. Journal of Veterinary Diagnostic Investigation 12, 269–271.
Suspected citrus pulp toxicosis in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvlsVOlsQ%3D%3D&md5=69013f3cf2df3f029b80ea7651475acfCAS | 10826844PubMed |

Tao NG, Liu YJ, Tang YF, Zhang JH, Zhang ML, Zeng HY (2009) Essential oil composition and antimicrobial activity of Citrus reticulate. Chemistry of Natural Compounds 32, 1–2.

Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.
Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2FnvVCltA%3D%3D&md5=e5c1ebe000070887297cc2a8c330cfc1CAS | 1660498PubMed |

Villalba JJ, Bach A, Ipharraguerre IR (2011) Feeding behavior and performance of lambs are influenced by flavor diversity. Journal of Animal Science 89, 2571–2581.
Feeding behavior and performance of lambs are influenced by flavor diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXps12jt70%3D&md5=807e110cab4409ec28ae1e87f6a3f000CAS | 21454862PubMed |

Wadhwa M, Bakshi MPS (2013) Utilization of fruit and vegetable wastes as livestock feed and as substrates for generation of other value-added products. FAO RAP Publication, 2013/04. (Ed. HPS Makkar) Available at http://www.fao.org/docrep/018/i3273e/i3273e.pdf [Verified 2 September 2015]

Waziri MA, Ribadu AY, Sivachelvan N (2010) Changes in the serum proteins, hematological and some serum biochemical profiles in the gestation period in the Sahel goats. Veterinary Archives 80, 215–224.

Welch JG, Smith AM (1971) Effect of beet pulp and citrus pulp on rumination activity. Journal of Animal Science 33, 472–475.