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RESEARCH ARTICLE

Cow–calf efficiency of beef cows grazing different herbage allowances of rangelands: hepatic mechanisms related to energy efficiency

Alberto Casal https://orcid.org/0000-0002-0418-7410 A * , Mercedes Garcia-Roche B C , Adriana Cassina C , Pablo Soca A and Mariana Carriquiry B
+ Author Affiliations
- Author Affiliations

A Departamento de Producción Animal y Pasturas, Facultad de Agronomía, Universidad de la República, Ruta 3 km 363, 60000 Paysandú, Uruguay.

B Departamento de Producción Animal y Pasturas, Facultad de Agronomía, Universidad de la República, Montevideo, Uruguay.

C Center for Free Radical and Biomedical Research (CEINBIO) and Departamento de Bioquímica, Facultad de Medicina, Universidad de la República, Montevideo, Uruguay.

* Correspondence to: alcas@adinet.com.uy

Handling Editor: Luis Felipe Silva

Animal Production Science 62(6) 529-538 https://doi.org/10.1071/AN20410
Submitted: 6 August 2020  Accepted: 4 January 2022   Published: 22 February 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Improvement in efficiency of energy utilisation of cow–calf systems could benefit beef production profitability and sustainability. Energy efficiency has been associated with mitochondrial function; therefore, hepatic mitochondrial function and oxidative stress could play a key role in energy efficiency of beef cows.

Aim: We evaluated the effect of two herbage allowances from rangelands (Campos biome) on cow–calf energy efficiency, hepatic mitochondrial density and function, and oxidative stress of purebred (Hereford and Aberdeen Angus) and reciprocal F1 crossbred beef cows.

Methods: Mature cows (n = 32) were used in a complete randomised block design with a factorial arrangement of herbage allowance (2.5 vs 4 kg dry matter/day; low vs high) and cow genotype (pure vs crossbred) over 3 years. At the end of the third year, cows were slaughtered at 190 ± 10 days postpartum. Liver was dissected and weighed, and samples were collected and snap-frozen pending analysis of mitochondrial density and oxidative stress markers. Estimated cow–calf energy efficiency was calculated by using total cow estimated metabolisable energy intake as input and calf energy retained at weaning as output.

Key results: Cow–calf energy efficiency was greater (P ≤ 0.07) for high than low herbage allowance and for crossbred than purebred cows. Mitochondrial density biomarkers (hepatic citrate synthase enzyme activity, citrate synthase mRNA, and mitochondrial:nuclear DNA ratio) were greater (P ≤ 0.03) for high than low herbage allowance. Plasma pro-oxidants and plasma antioxidant capacity were greater (P ≤ 0.07) for crossbred than purebred cows. Plasma oxidative stress index and expression of hepatic 4-hydroxynonenal protein adducts were affected (P ≤ 0.06) by herbage allowance × cow genotype interaction.

Conclusion: Greater cow–calf energy efficiency was associated with greater hepatic mitochondrial density without differences in mitochondrial function. Contrary to expectation, greater efficiency of crossbred than purebred cows was associated with increased hepatic oxidative damage, which probably reflects greater liver metabolic activity in crossbreds.

Implications: Herbage allowance and cow genotype affect cow–calf efficiency, hepatic mitochondrial function and oxidative stress markers. Greater efficiency of crossbred cows seems associated with increased hepatic oxidative damage.

Keywords: antioxidants, cow–calf system, crossbred cows, gene expression, hepatic metabolism, mitochondrial density biomarkers, mitochondrial function, oxidative stress, proteins.


References

Abuelo A, Hernández J, Benedito JL, Castillo C (2013) Oxidative stress index (OSi) as a new tool to assess redox status in dairy cattle during the transition period. Animal 7, 1374–1378.
Oxidative stress index (OSi) as a new tool to assess redox status in dairy cattle during the transition period.Crossref | GoogleScholarGoogle Scholar | 23510791PubMed |

Abuelo A, Hernández J, Benedito JL, Castillo C (2015) The importance of the oxidative status of dairy cattle in the periparturient period: revisiting antioxidant supplementation. Journal of Animal Physiology and Animal Nutrition 99, 1003–1016.
The importance of the oxidative status of dairy cattle in the periparturient period: revisiting antioxidant supplementation.Crossref | GoogleScholarGoogle Scholar | 25475653PubMed |

AOAC (2000) ‘Official methods of analysis of the association of official analytical chemists.’ (AOAC International: Gaithersburg, MD, USA)

Argüelles S, García S, Maldonado M, Machado A, Ayala A (2004) Do the serum oxidative stress biomarkers provide a reasonable index of the general oxidative stress status? Biochimica et Biophysica Acta – General Subjects 1674, 251–259.
Do the serum oxidative stress biomarkers provide a reasonable index of the general oxidative stress status?Crossref | GoogleScholarGoogle Scholar |

Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine and Cellular Longevity 2014, 360438
Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal.Crossref | GoogleScholarGoogle Scholar | 24999379PubMed |

Baldwin RL, McLeod KR, Capuco AV (2004) Visceral tissue growth and proliferation during the bovine lactation cycle. Journal of Dairy Science 87, 2977–2986.
Visceral tissue growth and proliferation during the bovine lactation cycle.Crossref | GoogleScholarGoogle Scholar | 15375059PubMed |

Berretta E, Risso D, Montossi F, Pigurina G (2000) Campos in Uruguay. In ‘Grassland ecophysiology and grazing ecology’. (Eds G Lemaire, J Hogdson, A de Moraes, C Nabinger, PC Carvalho) pp. 377–394. (CAB International: Curitiba, PR, Brazil)

Bottje WG, Carstens GE (2009) Association of mitochondrial function and feed efficiency in poultry and livestock species. Journal of Animal Science 87, E48–E63.
Association of mitochondrial function and feed efficiency in poultry and livestock species.Crossref | GoogleScholarGoogle Scholar | 19028862PubMed |

Brouwer E (1965) Report of sub-committee on constants and factors. In ‘Energy metabolism. Proceedings 3rd symposium European Association of Animal Production’. (Ed. KL Blaxter) pp. 441–443. Publication No. 11. (Academic Press: London, UK)

Casal A, Veyga M, Astessiano AL, Espasandin AC, Trujillo AI, Soca P, Carriquiry M (2014) Visceral organ mass, cellularity indexes and expression of genes encoding for mitochondrial respiratory chain proteins in pure and crossbred mature beef cows grazing different forage allowances of native pastures. Livestock Science 167, 195–205.
Visceral organ mass, cellularity indexes and expression of genes encoding for mitochondrial respiratory chain proteins in pure and crossbred mature beef cows grazing different forage allowances of native pastures.Crossref | GoogleScholarGoogle Scholar |

Casal A, Astessiano AL, Espasandin AC, Trujillo AI, Soca P, Carriquiry M (2017) Changes in body composition during the winter gestation period in mature beef cows grazing different herbage allowances of native grasslands. Animal Production Science 57, 520–529.
Changes in body composition during the winter gestation period in mature beef cows grazing different herbage allowances of native grasslands.Crossref | GoogleScholarGoogle Scholar |

Casal A, Garcia-Roche M, Navajas EA, Cassina A, Carriquiry M (2018) Hepatic mitochondrial function in Hereford steers with divergent residual feed intake phenotypes. Journal of Animal Science 96, 4431–4443.
Hepatic mitochondrial function in Hereford steers with divergent residual feed intake phenotypes.Crossref | GoogleScholarGoogle Scholar | 30032298PubMed |

Casal A, Garcia-Roche M, Navajas EA, Cassina A, Carriquiry M (2020) Differential hepatic oxidative status in steers with divergent residual feed intake phenotype. Animal 14, 78–85.
Differential hepatic oxidative status in steers with divergent residual feed intake phenotype.Crossref | GoogleScholarGoogle Scholar | 31218981PubMed |

Celi P (2011) Biomarkers of oxidative stress in ruminant medicine. Immunopharmacology and Immunotoxicology 33, 233–240.
Biomarkers of oxidative stress in ruminant medicine.Crossref | GoogleScholarGoogle Scholar | 20849293PubMed |

Chen K-L, Wang H-L, Jiang L-Z, Yong Q, Cai-Xia Y, Wei-Wei C, Ji-Feng Z, Guang-Dong X (2020) Heat stress induces apoptosis through disruption of dynamic mitochondrial networks in dairy cow mammary epithelial cells. In Vitro Cellular & Developmental Biology – Animal 56, 322–331.
Heat stress induces apoptosis through disruption of dynamic mitochondrial networks in dairy cow mammary epithelial cells.Crossref | GoogleScholarGoogle Scholar |

Chirase NK, Greene LW, Purdy CW, Loan RW, Auvermann BW, Parker DB, Walborg EF Chirase NK, Greene LW, Purdy CW, Loan RW, Auvermann BW, Parker DB, Walborg EF (2004) Effect of transport stress on respiratory disease, serum antioxidant status, and serum concentrations of lipid peroxidation biomarkers in beef cattle. American Journal of Veterinary Research 65, 860–864.
Effect of transport stress on respiratory disease, serum antioxidant status, and serum concentrations of lipid peroxidation biomarkers in beef cattle.Crossref | GoogleScholarGoogle Scholar | 15198229PubMed |

Connor EE, Kahl S, Elsasser TH, Parker JS, Li RW, Van Tassell CP, Baldwin RL, Barao SM (2010) Enhanced mitochondrial complex gene function and reduced liver size may mediate improved feed efficiency of beef cattle during compensatory growth. Functional & Integrative Genomics 10, 39–51.
Enhanced mitochondrial complex gene function and reduced liver size may mediate improved feed efficiency of beef cattle during compensatory growth.Crossref | GoogleScholarGoogle Scholar |

Cundiff LV (2004) Implication of breed type evaluations. In ‘Management issues and industry challenges in defining time’. (Animal Science, University of Florida: Gainesville, FL, USA) Available at http://animal.ifas.ufl.edu/beef_extension/bcsc/2004/pdf/cundiff.pdf [Accessed 30 May 2014]

Do Carmo M, Claramunt M, Carriquiry M, Soca P (2016) Animal energetics in extensive grazing systems: rationality and results of research models to improve energy efficiency of beef Cow–calf grazing Campos systems. Journal of Animal Science 94, 84–92.
Animal energetics in extensive grazing systems: rationality and results of research models to improve energy efficiency of beef Cow–calf grazing Campos systems.Crossref | GoogleScholarGoogle Scholar |

Do Carmo M, Sollenberger LE, Carriquiry M, Soca P (2018) Controlling herbage allowance and selection of cow genotype improve cow–calf productivity in Campos grasslands. The Professional Animal Scientist 34, 32–41.
Controlling herbage allowance and selection of cow genotype improve cow–calf productivity in Campos grasslands.Crossref | GoogleScholarGoogle Scholar |

Ferrell CL, Garrett WN, Hinman N (1976) Growth, development, and composition of the udder and gravid uterus of beef heifers during pregnancy. Journal of Animal Science 42, 1477–1489.
Growth, development, and composition of the udder and gravid uterus of beef heifers during pregnancy.Crossref | GoogleScholarGoogle Scholar | 931823PubMed |

Guo W, Jiang L, Bhasin S, Khan SM, Swerdlow RH (2009) DNA extraction procedures meaningfully influence qPCR-based mtDNA copy number determination. Mitochondrion 9, 261–265.
DNA extraction procedures meaningfully influence qPCR-based mtDNA copy number determination.Crossref | GoogleScholarGoogle Scholar | 19324101PubMed |

Gutiérrez V, Espasandin AC, Astessiano AL, Casal A, López-Mazz C, Carriquiry M (2013) Calf foetal and early life nutrition on grazing conditions: metabolic and endocrine profiles and body composition during the growing phase. Journal of Animal Physiology and Animal Nutrition 97, 720–731.
Calf foetal and early life nutrition on grazing conditions: metabolic and endocrine profiles and body composition during the growing phase.Crossref | GoogleScholarGoogle Scholar | 22712599PubMed |

Hancock CR, Han D-H, Higashida K, Kim SH, Holloszy JO (2011) Does calorie restriction induce mitochondrial biogenesis? A reevaluation. The FASEB Journal 25, 785–791.
Does calorie restriction induce mitochondrial biogenesis? A reevaluation.Crossref | GoogleScholarGoogle Scholar | 21048043PubMed |

Haydock KP, Shaw NH (1975) Correction – The comparative yield method for estimating dry matter yield of pasture. Australian Journal of Experimental Agriculture and Animal Husbandry 15, 663–670.
Correction – The comparative yield method for estimating dry matter yield of pasture.Crossref | GoogleScholarGoogle Scholar |

Herd RM, Arthur PF (2009) Physiological basis for residual feed intake. Journal of Animal Science 87, E64–E71.
Physiological basis for residual feed intake.Crossref | GoogleScholarGoogle Scholar | 19028857PubMed |

Jenkins TG, Ferrell CL (1994) Productivity through weaning of nine breeds of cattle under varying feed availabilities: I. Initial evaluation. Journal of Animal Science 72, 2787–2797.
Productivity through weaning of nine breeds of cattle under varying feed availabilities: I. Initial evaluation.Crossref | GoogleScholarGoogle Scholar | 7730170PubMed |

Koch RM, Swiger LA, Chambers D, Gregory KE (1963) Efficiency of feed use in beef cattle. Journal of Animal Science 22, 486–494.
Efficiency of feed use in beef cattle.Crossref | GoogleScholarGoogle Scholar |

Lancaster PA, Carstens GE, Michal JJ, Brennan KM, Johnson KA, Davis ME (2014) Relationships between residual feed intake and hepatic mitochondrial function in growing beef cattle. Journal of Animal Science 92, 3134–3141.
Relationships between residual feed intake and hepatic mitochondrial function in growing beef cattle.Crossref | GoogleScholarGoogle Scholar | 24894006PubMed |

Laporta J, Rosa GJM, Naya H, Carriquiry M (2014) Liver functional genomics in beef cows on grazing systems: novel genes and pathways revealed. Physiological Genomics 46, 138–147.
Liver functional genomics in beef cows on grazing systems: novel genes and pathways revealed.Crossref | GoogleScholarGoogle Scholar | 24326346PubMed |

Larsen S, Nielsen J, Hansen CN, Nielsen LB, Wibrand F, Stride N, Schroder HD, Boushel R, Helge JW, Dela F, Hey-Mogensen M (2012) Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. Journal of Physiology 590, 3349–3360.
Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects.Crossref | GoogleScholarGoogle Scholar |

Lee H-C, Wei Y-H (2005) Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. International Journal of Biochemistry and Cell Biology 37, 822–834.
Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress.Crossref | GoogleScholarGoogle Scholar | 15694841PubMed |

Lobley GE, Milne V, Lovie JM, Reeds PJ, Pennie K (1980) Whole body and tissue protein synthesis in cattle. British Journal of Nutrition 43, 491–502.
Whole body and tissue protein synthesis in cattle.Crossref | GoogleScholarGoogle Scholar |

Macoon B, Sollenberger LE, Moore JE, Staples CR, Fike JH, Portier KM (2003) Comparison of three techniques for estimating the forage intake of lactating dairy cows on pasture. Journal of Animal Science 81, 2357–2366.
Comparison of three techniques for estimating the forage intake of lactating dairy cows on pasture.Crossref | GoogleScholarGoogle Scholar | 12968712PubMed |

Montaño-Bermudez M, Nielsen MK, Deutscher GH (1990) Energy requirements for maintenance of crossbred beef cattle with different genetic potential for milk. Journal of Animal Science 68, 2279–2288.
Energy requirements for maintenance of crossbred beef cattle with different genetic potential for milk.Crossref | GoogleScholarGoogle Scholar | 2401650PubMed |

Morris CA, Baker RL, Johnson DL, Carter AH, Hunter JC (1987) Reciprocal crossbreeding of Angus and Hereford cattle. 3. Cow weight, reproduction, maternal performance, and lifetime production. New Zealand Journal of Agricultural Research 30, 453–467.
Reciprocal crossbreeding of Angus and Hereford cattle. 3. Cow weight, reproduction, maternal performance, and lifetime production.Crossref | GoogleScholarGoogle Scholar |

Mott GO (1960) Grazing pressure and the measurement of pasture production. In ‘Proceedings of 8th International Grasslands Congress’, 11–21 July 1960. pp. 606–611. Reading, UK. (International Grasslands Congress)

National Academies of Sciences, Engineering, and Medicine (2016) ‘Nutrient requirements of beef cattle’, 8th rev. edn. (The National Academies Press: Washington, DC)
| Crossref |

National Research Council (2000) ‘Nutrient requirements of beef cattle: update 2000’, 7th rev. edn. (The National Academies Press: Washington, DC)
| Crossref |

Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, Carruba MO (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science 310, 314–317.
Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS.Crossref | GoogleScholarGoogle Scholar | 16224023PubMed |

Parnell PF, Herd RM, Perry D, Bootle B (1994) The Trangie experiment – response in growth rate, size, maternal ability, reproductive performance, carcase composition, feed requirements and herd profitability. In ‘Proceedings of the Australian Society of Animal Production’. Perth, WA, Australia. Vol. 20, pp. 17–26. (Australian Society of Animal Production)

Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45
A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 11328886PubMed |

Radi R (2018) Oxygen radicals, nitric oxide, and peroxynitrite: redox pathways in molecular medicine. Proceedings of the National Academy of Sciences of the United States of America 115, 5839–5848.
Oxygen radicals, nitric oxide, and peroxynitrite: redox pathways in molecular medicine.Crossref | GoogleScholarGoogle Scholar | 29802228PubMed |

Ramos MH, Kerley MS (2013) Mitochondrial complex I protein differs among residual feed intake phenotype in beef cattle. Journal of Animal Science 91, 3299–3304.
Mitochondrial complex I protein differs among residual feed intake phenotype in beef cattle.Crossref | GoogleScholarGoogle Scholar | 23798519PubMed |

Reid CR, Bailey CM, Judkins MB (1991) Metabolizable energy for maintenance of beef-type Bos taurus and Bos indicus × Bos taurus cows in a dry, temperate climate. Journal of Animal Science 69, 2779–2786.
Metabolizable energy for maintenance of beef-type Bos taurus and Bos indicus × Bos taurus cows in a dry, temperate climate.Crossref | GoogleScholarGoogle Scholar | 1885390PubMed |

Rolfe DFS, Brand MD (1997) The physiological significance of mitochondrial proton leak in animal cells and tissues. Bioscience Reports 17, 9–16.
The physiological significance of mitochondrial proton leak in animal cells and tissues.Crossref | GoogleScholarGoogle Scholar |

Scarlato S, Faber A, Do Carmo M, Soca P (2011) Foraging behaviour of beef cows grazing native pasture: I. Effect of breed and herbage allowance on grazing and ruminating time. In ‘Proceedings of the 9th International Rangeland Congress’. (Eds SR Feldman, GE Oliva, MB Sacido) p. 657. (International Rangeland Congress: Rosario, Argentina)

Schägger H, Noack H, Halangk W, Brandt U, von Jagow G (1995) Cytochrome-c oxidase in developing rat heart enzymic properties and amino-terminal sequences suggest identity of the fetal heart and the adult liver isoform. European Journal of Biochemistry 230, 235–241.

Scholljegerdes EJ, Summers AF (2016) How do we identify energetically efficient grazing animals? Journal of Animal Science 94, 103–109.
How do we identify energetically efficient grazing animals?Crossref | GoogleScholarGoogle Scholar |

Smit HJ, Taweel HZ, Tas BM, Tamminga S, Elgersma A (2005) Comparison of techniques for estimating herbage intake of grazing dairy cows. Journal of Dairy Science 88, 1827–1836.
Comparison of techniques for estimating herbage intake of grazing dairy cows.Crossref | GoogleScholarGoogle Scholar | 15829676PubMed |

Sollenberger LE, Moore JE, Allen VG, Pedreira CGS (2005) Reporting forage allowance in grazing experiments. Crop Science 45, 896–900.
Reporting forage allowance in grazing experiments.Crossref | GoogleScholarGoogle Scholar |

Trotti R, Carratelli M, Barbieri M, Micieli G, Bosone D, Rondanelli M, Bo P (2001) Oxidative stress and a thrombophilic condition in alcoholics without severe liver disease. Haematologica 86, 85–91.

Turrens JF (2003) Mitochondrial formation of reactive oxygen species. The Journal of Physiology 552, 335–344.
Mitochondrial formation of reactive oxygen species.Crossref | GoogleScholarGoogle Scholar | 14561818PubMed |

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 | 1660498PubMed |

Wang H, Oster G (1998) Energy transduction in the F1 motor of ATP synthase. Nature 396, 279–282.
Energy transduction in the F1 motor of ATP synthase.Crossref | GoogleScholarGoogle Scholar | 9834036PubMed |

Weikard R, Kühn C (2016) 1089 Mitochondrial biogenesis and DNA content in metabolically tissues of lactating cows with divergent milk production. Journal of Animal Science 94, 522–523.
1089 Mitochondrial biogenesis and DNA content in metabolically tissues of lactating cows with divergent milk production.Crossref | GoogleScholarGoogle Scholar |