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PERSPECTIVES ON ANIMAL BIOSCIENCES (Open Access)

Importance of circadian rhythms in dairy nutrition

Kevin J. Harvatine https://orcid.org/0000-0001-6422-2647 A *
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A Department of Animal Science, Penn State University, University Park, PA, USA.

* Correspondence to: kjh182@psu.edu

Handling Editor: David Masters

Animal Production Science 63(18) 1827-1836 https://doi.org/10.1071/AN23085
Submitted: 28 February 2023  Accepted: 26 June 2023  Published: 18 July 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Biological rhythms are repeating patterns that are driven by time-keeping mechanisms within the animal and are adaptive as they coordinate physiology and metabolism with the external environment. The dairy cow has a well recognised natural daily pattern of feed intake and milk synthesis, but regulation of these rhythms has not been well described in the literature or well considered in current dairy management. Recent discoveries have clearly described circadian time-keeping mechanisms in peripheral tissues that are responsive to the timing of food availability. Some management strategies on dairy farms may desynchronise the interactions between central and mammary circadian timekeepers, resulting in reduced milk yield and efficiency. Feeding a total mixed ration is commonly assumed to create constant ruminal conditions, but the large variation in the rate of feed intake across the day causes large fluctuations in rumen fermentation and absorbed nutrients. Milk composition also differs across the day due to both dynamics in nutrient absorption and biological regulation attempting to match milk yield and composition with calf requirements across the day. Recent work has shown that milk synthesis varies over the day and is modified by the timing of feed intake and nutrient absorption. These rhythms have also been shown to be affected by the timing of feed delivery. We expect that maximal milk yield and efficiency are achieved when we have more consistent rumen fermentation and match the timing of nutrient absorption and mammary capacity for milk synthesis. Managing feeding times provides the opportunity to modify feed intake across the day, but behavioural responses are complex. Appreciating the impact of circadian rhythms provides the foundation to develop nutrition and management strategies considering circadian dynamics of intake and milk synthesis and provides opportunities for new gains in cow efficiency, welfare, and health.

Keywords: chrononutrition, daily pattern, diurnal, feeding behaviour, rumen fermentation, rumination, synchrony.

References

Adamovich Y, Rousso-Noori L, Zwighaft Z, Neufeld-Cohen A, Golik M, Kraut-Cohen J, Wang M, Han X, Asher G (2014) Circadian clocks and feeding time regulate the oscillations and levels of hepatic triglycerides. Cell Metabolism 19, 319-330.
| Crossref | Google Scholar | PubMed |

Albright JL (1993) Feeding behavior of dairy cattle. Journal of Dairy Science 76, 485-498.
| Crossref | Google Scholar |

Allen MS, Bradford BJ, Harvatine KJ (2005) The cow as a model to study food intake regulation. Annual Review of Nutrition 25, 523-547.
| Crossref | Google Scholar | PubMed |

Asher G, Schibler U (2011) Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metabolism 13, 125-137.
| Crossref | Google Scholar | PubMed |

Bass J, Takahashi JS (2010) Circadian integration of metabolism and energetics. Science 330, 1349-1354.
| Crossref | Google Scholar | PubMed |

Bauman DE, McCutcheon SN, Steinhour WD, Eppard PJ, Sechen SJ (1985) Sources of variation and prospects for improvement of productive efficiency in the dairy cow: a review. Journal of Animal Science 60, 583-592.
| Crossref | Google Scholar | PubMed |

Boehning D, Snyder SH (2002) Carbon monoxide and clocks. Science 298, 2339-2340.
| Crossref | Google Scholar | PubMed |

Casey TM, Plaut K (2012) Lactation Biology Symposium: circadian clocks as mediators of the homeorhetic response to lactation. Journal of Animal Science 90, 744-754.
| Crossref | Google Scholar | PubMed |

Casey TM, Plaut K (2022) Circadian clocks and their integration with metabolic and reproductive systems: our current understanding and its application to the management of dairy cows. Journal of Animal Science 100, skac233.
| Crossref | Google Scholar |

Casey T, Crodian J, Suárez-Trujillo A, Erickson E, Weldon B, Crow K, Cummings S, Chen Y, Shamay A, Mabjeesh SJ, Plaut K (2016) CLOCK regulates mammary epithelial cell growth and differentiation. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 311, R1125-R1134.
| Crossref | Google Scholar | PubMed |

Casey T, Suarez-Trujillo A, Cummings S, Huff K, Crodian J, Bhide K, Aduwari C, Teeple K, Shamay A, Mabjeesh SJ, San Miguel P, Thimmapuram J, Plaut K (2021) Core circadian clock transcription factor BMAL1 regulates mammary epithelial cell growth, differentiation, and milk component synthesis. PLoS ONE 16, e0248199.
| Crossref | Google Scholar | PubMed |

Cermakian N, Lange T, Golombek D, Sarkar D, Nakao A, Shibata S, Mazzoccoli G (2013) Crosstalk between the circadian clock circuitry and the immune system. Chronobiology International 30, 870-888.
| Crossref | Google Scholar | PubMed |

Chamorro R, Jouffe C, Oster H, Uhlenhaut NH, Meyhöfer SM (2023) When should I eat: a circadian view on food intake and metabolic regulation. Acta Physiologica 237, e13936.
| Crossref | Google Scholar |

DeVries TJ, von Keyserlingk MAG, Beauchemin KA (2005) Frequency of feed delivery affects the behavior of lactating dairy cows. Journal of Dairy Science 88, 3553-3562.
| Crossref | Google Scholar | PubMed |

DeVries TJ, Beauchemin KA, von Keyserlingk MAG (2007) Dietary forage concentration affects the feed sorting behavior of lactating dairy cows. Journal of Dairy Science 90, 5572-5579.
| Crossref | Google Scholar | PubMed |

Dibner C, Schibler U, Albrecht U (2010) The mammalian circadian timing system: organization and coordination of central and peripheral clocks. Annual Review of Physiology 72, 517-549.
| Crossref | Google Scholar | PubMed |

Doherty CJ, Kay SA (2010) Circadian control of global gene expression patterns. Annual Review of Genetics 44, 419-444.
| Crossref | Google Scholar | PubMed |

Escobar C, Cailotto C, Angeles-Castellanos M, Delgado RS, Buijs RM (2009) Peripheral oscillators: the driving force for food-anticipatory activity. European Journal of Neuroscience 30, 1665-1675.
| Crossref | Google Scholar | PubMed |

Evans JA, Davidson AJ (2013) Health consequences of circadian disruption in humans and animal models. Progress in Molecular Biology and Translational Science 119, 283-323.
| Crossref | Google Scholar | PubMed |

Finger A-M, Kramer A (2021) Peripheral clocks tick independently of their master. Genes & Development 35, 304-306.
| Crossref | Google Scholar | PubMed |

Giannetto C, Piccione G (2009) Daily rhythms of 25 physiological variables in Bos taurus maintained under natural conditions. Journal of Applied Biomedicine 7, 55-61.
| Crossref | Google Scholar |

Golombek DA, Casiraghi LP, Agostino PV, Paladino N, Duhart JM, Plano SA, Chiesa JJ (2013) The times they’re a-changing: effects of circadian desynchronization on physiology and disease. Journal of Physiology–Paris 107, 310-322.
| Crossref | Google Scholar | PubMed |

Hall MB, Huntington GB (2008) Nutrient synchrony: sound in theory, elusive in practice. Journal of Animal Science 86, E287-E292.
| Crossref | Google Scholar | PubMed |

Hansen J (2017) Night shift work and risk of breast cancer. Current Environmental Health Reports 4, 325-339.
| Crossref | Google Scholar | PubMed |

Hara R, Wan K, Wakamatsu H, Aida R, Moriya T, Akiyama M, Shibata S (2001) Restricted feeding entrains liver clock without participation of the suprachiasmatic nucleus. Genes to Cells 6, 269-278.
| Crossref | Google Scholar | PubMed |

Harvatine KJ (2012) Circadian patterns of feed intake and milk composition variability. In ‘Proceedings of the 21st tri-state dairy nutrition conference’, Fort Wayne, IN, USA. (Ohio State University)

Hosseinkhani A, Devries TJ, Proudfoot KL, Valizadeh R, Veira DM, von Keyserlingk MAG (2008) The effects of feed bunk competition on the feed sorting behavior of close-up dry cows. Journal of Dairy Science 91, 1115-1121.
| Crossref | Google Scholar | PubMed |

Isobe Y, Hida H, Nishino H (2011) Circadian rhythm of enolase in suprachiasmatic nucleus depends on mitochondrial function. Journal of Neuroscience Research 89, 936-944.
| Crossref | Google Scholar | PubMed |

Jin Y, Hur T-Y, Hong Y (2017) Circadian rhythm disruption and subsequent neurological disorders in night-shift workers. Journal of Lifestyle Medicine 7, 45-50.
| Crossref | Google Scholar | PubMed |

Lefcourt AM, Huntington JB, Akers RM, Wood DL, Bitman J (1999) Circadian and ultradian rhythms of body temperature and peripheral concentrations of insulin and nitrogen in lactating dairy cows. Domestic Animal Endocrinology 16, 41-55.
| Crossref | Google Scholar | PubMed |

Li H, Li K, Zhang K, Li Y, Gu H, Liu H, Yang Z, Cai D (2021) The circadian physiology: implications in livestock health. International Journal of Molecular Sciences 22, 2111.
| Crossref | Google Scholar |

Litichevskiy L, Thaiss CA (2022) The oscillating gut microbiome and its effects on host circadian biology. Annual Review of Nutrition 42, 145-164.
| Crossref | Google Scholar | PubMed |

Matamoros C, Cai J, Patterson AD, Harvatine KJ (2021) Comparison of the effects of short-term feeding of sodium acetate and sodium bicarbonate on milk fat production. Journal of Dairy Science 104, 7572-7582.
| Crossref | Google Scholar | PubMed |

Matamoros C, Salfer IJ, Bartell PA, Harvatine KJ (2022) Effect of the timing of sodium acetate infusion on the daily rhythms of milk synthesis and plasma metabolites and hormones in Holstein cows. Journal of Dairy Science 105, 7432-7445.
| Crossref | Google Scholar | PubMed |

Maulfair DD, Fustini M, Heinrichs AJ (2011) Effect of varying total mixed ration particle size on rumen digesta and fecal particle size and digestibility in lactating dairy cows. Journal of Dairy Science 94, 3527-3536.
| Crossref | Google Scholar | PubMed |

McCabe CJ, Suarez-Trujillo A, Teeple KA, Casey TM, Boerman JP (2021) Chronic prepartum light-dark phase shifts in cattle disrupt circadian clocks, decrease insulin sensitivity and mammary development, and are associated with lower milk yield through 60 days postpartum. Journal of Dairy Science 104, 2422-2437.
| Crossref | Google Scholar | PubMed |

Mohawk JA, Green CB, Takahashi JS (2012) Central and peripheral circadian clocks in mammals. Annual Review of Neuroscience 35, 445-462.
| Crossref | Google Scholar | PubMed |

Nakahata Y, Sahar S, Astarita G, Kaluzova M, Sassone-Corsi P (2009) Circadian control of the NAD+ salvage pathway by CLOCK-SIRT1. Science 324, 654-657.
| Crossref | Google Scholar | PubMed |

Nikkhah A, Furedi CJ, Kennedy AD, Crow GH, Plaizier JC (2008) Effects of feed delivery time on feed intake, milk production, and blood metabolites of dairy cows. Journal of Dairy Science 91, 4249-4260.
| Crossref | Google Scholar | PubMed |

Niu M, Harvatine KJ (2018a) Short communication: the effects of morning compared with evening feed delivery in lactating dairy cows during the summer. Journal of Dairy Science 101, 396-400.
| Crossref | Google Scholar | PubMed |

Niu M, Harvatine KJ (2018b) The effects of feeding a partial mixed ration plus a top-dress before feeding on milk production and the daily rhythm of feed intake and plasma hormones and metabolites in dairy cows. Journal of Dairy Science 101, 164-171.
| Crossref | Google Scholar | PubMed |

Niu M, Ying Y, Bartell PA, Harvatine KJ (2014) The effects of feeding time on milk production, total-tract digestibility, and daily rhythms of feeding behavior and plasma metabolites and hormones in dairy cows. Journal of Dairy Science 97, 7764-7776.
| Crossref | Google Scholar | PubMed |

Niu M, Ying Y, Bartell PA, Harvatine KJ (2017) The effects of feeding rations that differ in fiber and fermentable starch within a day on milk production and the daily rhythm of feed intake and plasma hormones and metabolites in dairy cows. Journal of Dairy Science 100, 187-198.
| Crossref | Google Scholar | PubMed |

Plaut K, Casey T (2012) Does the circadian system regulate lactation? Animal: an International Journal of Animal Bioscience 6, 394-402.
| Crossref | Google Scholar |

Quist MA, LeBlanc SJ, Hand KJ, Lazenby D, Miglior F, Kelton DF (2008) Milking-to-milking variability for milk yield, fat and protein percentage, and somatic cell count. Journal of Dairy Science 91, 3412-3423.
| Crossref | Google Scholar | PubMed |

Raffrenato E, Badenhorst MJ, Harvatine KJ, Shipandeni MNT, du Plessis L, Esposito G, van Zyl WH (2022) The diurnal patterns of ruminal enzymatic activity and in vitro digestibility of starch, neutral detergent fiber, and protein. Journal of Dairy Science 105, 4961-4970.
| Crossref | Google Scholar | PubMed |

Ramsey KM, Yoshino J, Brace CS, Abrassart D, Kobayashi Y, Marcheva B, Hong H-K, Chong JL, Buhr ED, Lee C, Takahashi JS, Imai S-I, Bass J (2009) Circadian clock feedback cycle through NAMPT-mediated NAD+ biosynthesis. Science 324, 651-654.
| Crossref | Google Scholar | PubMed |

Robinson PH, Gill M, Kennelly JJ (1997) Influence of time of feeding a protein meal on ruminal fermentation and forestomach digestion in dairy cows. Journal of Dairy Science 80, 1366-1373.
| Crossref | Google Scholar | PubMed |

Rottman LW, Ying Y, Zhou K, Bartell PA, Harvatine KJ (2014) The daily rhythm of milk synthesis is dependent on the timing of feed intake in dairy cows. Physiological Reports 2, e12049.
| Crossref | Google Scholar | PubMed |

Rottman LW, Ying Y, Zhou K, Bartell PA, Harvatine KJ (2015) The effects of feeding rations that differ in neutral detergent fiber and starch concentration within a day on production, feeding behavior, total-tract digestibility, and plasma metabolites and hormones in dairy cows. Journal of Dairy Science 98, 4673-4684.
| Crossref | Google Scholar | PubMed |

Rutter GA (2001) Nutrient-secretion coupling in the pancreatic islet β-cell: recent advances. Molecular Aspects of Medicine 22, 247-284.
| Crossref | Google Scholar | PubMed |

Rutter J, Reick M, McKnight SL (2002) Metabolism and the control of circadian rhythms. Annual Review of Biochemistry 71, 307-331.
| Crossref | Google Scholar | PubMed |

Salfer IJ, Harvatine KJ (2018) The effect of night restricted feeding on the molecular circadian clock of the mammary gland. Journal of Dairy Science 101(Suppl. 1), 405.
| Google Scholar |

Salfer IJ, Harvatine KJ (2020) Night-restricted feeding of dairy cows modifies daily rhythms of feed intake, milk synthesis and plasma metabolites compared with day-restricted feeding. British Journal of Nutrition 123, 849-858.
| Crossref | Google Scholar |

Salfer IJ, Morelli MC, Ying Y, Allen MS, Harvatine KJ (2018) The effects of source and concentration of dietary fiber, starch, and fatty acids on the daily patterns of feed intake, rumination, and rumen pH in dairy cows. Journal of Dairy Science 101, 10911-10921.
| Crossref | Google Scholar | PubMed |

Salfer IJ, Crawford CE, Rottman LW, Harvatine KJ (2021) The effects of feeding rations that differ in neutral detergent fiber and starch within a day on the daily pattern of key rumen microbial populations. JDS Communications 2, 334-339.
| Crossref | Google Scholar | PubMed |

Salfer IJ, Matamoros CI, Bartell PA, Harvatine KJ (2023) Effects of the timing of protein infusion on the daily rhythms of milk synthesis and plasma hormones and metabolites in dairy cows. Journal of Dairy Science 106, Accepted.
| Crossref | Google Scholar |

Schingoethe DJ (2017) A 100-year review: total mixed ration feeding of dairy cows. Journal of Dairy Science 100, 10143-10150.
| Crossref | Google Scholar | PubMed |

Sinturel F, Spaleniak W, Dibner C (2022) Circadian rhythm of lipid metabolism. Biochemical Society Transactions 50, 1191-1204.
| Crossref | Google Scholar | PubMed |

Stokkan K-A, Yamazaki S, Tei H, Sakaki Y, Menaker M (2001) Entrainment of the circadian clock in the liver by feeding. Science 291, 490-493.
| Crossref | Google Scholar | PubMed |

Strohmaier S, Devore EE, Zhang Y, Schernhammer ES (2018) A review of data of findings on night shift work and the development of DM and CVD events: a synthesis of the proposed molecular mechanisms. Current Diabetes Reports 18, 132.
| Crossref | Google Scholar | PubMed |

Suárez-Trujillo A, Casey TM (2016) Serotoninergic and circadian systems: driving mammary gland development and function. Frontiers in Physiology 7, 301.
| Crossref | Google Scholar | PubMed |

Suarez-Trujillo A, Wernert G, Sun H, Steckler TS, Huff K, Cummings S, Franco J, Klopp RN, Townsend JR, Grott M, Johnson JS, Plaut K, Boerman JP, Casey TM (2020) Exposure to chronic light-dark phase shifts during the prepartum nonlactating period attenuates circadian rhythms, decreases blood glucose, and increases milk yield in the subsequent lactation. Journal of Dairy Science 103, 2784-2799.
| Crossref | Google Scholar | PubMed |

Suarez-Trujillo A, Hoang N, Robinson L, McCabe CJ, Conklin D, Minor RC, Townsend J, Plaut K, George UZ, Boerman J, Casey TM (2022) Effect of circadian system disruption on the concentration and daily oscillations of cortisol, progesterone, melatonin, serotonin, growth hormone, and core body temperature in periparturient dairy cattle. Journal of Dairy Science 105, 2651-2668.
| Crossref | Google Scholar | PubMed |

Takahashi JS, Hong H-K, Ko CH, McDearmon EL (2008) The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nature Reviews Genetics 9, 764-775.
| Crossref | Google Scholar | PubMed |

Taleb Z, Karpowicz P (2022) Circadian regulation of digestive and metabolic tissues. American Journal of Physiology: Cell Physiology 323, C306-C321.
| Crossref | Google Scholar | PubMed |

Urrutia NL, Harvatine KJ (2017) Acetate dose-dependently stimulates milk fat synthesis in lactating dairy cows. The Journal of Nutrition 147, 763-769.
| Crossref | Google Scholar | PubMed |

Verwoerd W, Wellby M, Barrell G (2006) Absence of a causal relationship between environmental and body temperature in dairy cows (Bos taurus) under moderate climatic conditions. Journal of Thermal Biology 31, 533-540.
| Crossref | Google Scholar |

von Keyserlingk MAG, Weary DM (2010) Review: feeding behaviour of dairy cattle: measures and applications. Canadian Journal of Animal Science 90, 303-309.
| Crossref | Google Scholar |

Walker WH, II, Walton JC, DeVries AC, Nelson RJ (2020) Circadian rhythm disruption and mental health. Translational Psychiatry 10, 28.
| Crossref | Google Scholar | PubMed |

Yang WZ, Beauchemin KA (2006) Effects of physically effective fiber on chewing activity and ruminal pH of dairy cows fed diets based on barley silage. Journal of Dairy Science 89, 217-228.
| Crossref | Google Scholar | PubMed |

Ying Y, Rottman LW, Crawford C, Bartell PA, Harvatine KJ (2015) The effects of feeding rations that differ in neutral detergent fiber and starch concentration within a day on rumen digesta nutrient concentration, pH, and fermentation products in dairy cows. Journal of Dairy Science 98, 4685-4697.
| Crossref | Google Scholar | PubMed |