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RESEARCH ARTICLE

Melatonin treatment during late gestation of undernourished ewes: lamb body temperature and mother–young behaviours after birth

A. Freitas-de-Melo https://orcid.org/0000-0003-1418-0148 A , F. Sales B , R. Ungerfeld https://orcid.org/0000-0003-4685-2105 A and V. H. Parraguez https://orcid.org/0000-0002-3621-2705 C D *
+ Author Affiliations
- Author Affiliations

A Departamento de Biociencias Veterinarias, Facultad de Veterinaria, Universidad de la República, Montevideo, Uruguay.

B INIA Kampenaike, Punta Arenas 6212707, Chile.

C Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Santa Rosa 11735, Santiago 8820808, Chile.

D Facultad de Ciencias Agronómicas, Universidad de Chile, Santa Rosa 11315, Santiago 8820808, Chile.

* Correspondence to: vparragu@uchile.cl

Handling Editor: Alan Tilbrook

Animal Production Science 62(2) 131-136 https://doi.org/10.1071/AN21016
Submitted: 16 January 2021  Accepted: 13 September 2021   Published: 22 October 2021

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

Abstract

Context: In extensive grazing sheep systems, pregnant ewes undergo periods of undernutrition because gestation coincides with winter when natural pasture is of lowest quantity and poorest quality. The lamb’s weight and thermoregulatory capacity, and the ewe–lamb bond at birth, may be compromised. Maternal melatonin treatment during gestation may reverse these effects.

Aim: The aim was to determine the effects of melatonin treatment of single-lambing, undernourished ewes during the last third of gestation on lamb birthweights and body temperatures, and on ewe–lamb interactive behaviour after birth.

Methods: At Day 100 of gestation, 39 single-bearing ewes received a subcutaneous melatonin implant, and 54 ewes served as controls with no implant. Throughout gestation, the ewes remained under extensive conditions grazing on natural pasture. Measurements were made of lamb birthweight, body temperatures (surface temperature by infrared thermography and rectal temperature), and ewe–lamb behaviours during a handling test at 6–17 h after lambing.

Key results: There was no effect of melatonin treatment on lamb birthweight or rectal temperature, or on ewe–lamb interaction behaviours. Hip minimum surface temperature was greater in lambs from melatonin-treated ewes than lambs from control ewes (21.2°C ± 0.9°C vs 18.8°C ± 0.8°C; P = 0.05), and there was a similar trend for hip mean surface temperature (24.6°C ± 0.9°C vs 22.3°C ± 0.7°C; P = 0.06). Rump surface temperatures were greater in male than female lambs: maximum (27.9°C ± 1.2°C vs 22.9°C ± 1.2°C; P = 0.01), minimum (22.2°C ± 1.5°C vs 16.7°C ± 1.5°C; P = 0.02) and mean (25.4°C ± 1.3°C vs 20.5°C ± 1.3°C; P = 0.02).

Conclusion: Melatonin treatment during the last third of ewe pregnancy slightly enhanced the surface temperature of lambs at birth but did not influence ewe–lamb interaction behaviour after birth (i.e. after establishment of the ewe–lamb bond).

Implications: Further study in more depth is warranted into the possible effects of maternal supplementation with commercial melatonin implants on lamb development, thermoregulatory capacity, behaviour and survival rates in extensive grazing systems, including the effect on ewe–lamb behaviours immediately after birth for both singletons and twins.

Keywords: bond, filial attachment, lamb behaviour, maternal behaviour, sheep, survival, undernutrition, welfare.


References

Abecia JA, Forcada F, Vázquez MI, Muiño-Blanco T, Cebrián-Pérez JA, Pérez-Pe R, Casao A (2019) Role of melatonin on embryo viability in sheep. Reproduction, Fertility and Development 31, 82–92.
Role of melatonin on embryo viability in sheep.Crossref | GoogleScholarGoogle Scholar |

Abud MJ, Bielli A, Ithurralde J, Álvarez-Oxiley A, Freitas-de-Melo A, López Pérez A, Ungerfeld R, Pérez-Clariget R (2020) Effect of two forage allowances offered to pregnant ewes until middle and late gestation on foetus development. South African Journal of Animal Science 50, 471–480.
Effect of two forage allowances offered to pregnant ewes until middle and late gestation on foetus development.Crossref | GoogleScholarGoogle Scholar |

Budge H, Bispham J, Dandrea J, Evans E, Heasman L, Ingleton PM, Sullivan C, Wilson V, Stephenson T, Symonds ME (2000) Effect of maternal nutrition on brown adipose tissue and its prolactin receptor status in the fetal lamb. Pediatric Research 47, 781–786.
Effect of maternal nutrition on brown adipose tissue and its prolactin receptor status in the fetal lamb.Crossref | GoogleScholarGoogle Scholar | 10832738PubMed |

Cloete SWP (1993) Observations on neonatal progress of Dormer and South African Mutton Merino lambs. South African Journal of Animal Science 23, 38–42.

Coubrough CA, Castell MC (1998) Fetal sex determination by ultrasonically locating the genital tubercle in ewes. Theriogenology 50, 263–267.
Fetal sex determination by ultrasonically locating the genital tubercle in ewes.Crossref | GoogleScholarGoogle Scholar | 10734494PubMed |

Dwyer CM (2008) Genetic and physiological determinants of maternal behavior and lamb survival: implications for low-input sheep management. Journal of Animal Science 86, E246–E258.
Genetic and physiological determinants of maternal behavior and lamb survival: implications for low-input sheep management.Crossref | GoogleScholarGoogle Scholar | 17709772PubMed |

Dwyer CM, Lawrence AB, Bishop SC, Lewis M (2003) Ewe–lamb bonding behaviours at birth are affected by maternal undernutrition in pregnancy. British Journal of Nutrition 89, 123–136.
Ewe–lamb bonding behaviours at birth are affected by maternal undernutrition in pregnancy.Crossref | GoogleScholarGoogle Scholar |

Everett-Hincks JM, Blair HT, Stafford KJ, Lopez-Villalobos N, Kenyon PR, Morris ST (2005) The effect of pasture allowance fed to twin- and triplet-bearing ewes in late pregnancy on ewe and lamb behaviour and performance to weaning. Livestock Production Science 97, 253–266.
The effect of pasture allowance fed to twin- and triplet-bearing ewes in late pregnancy on ewe and lamb behaviour and performance to weaning.Crossref | GoogleScholarGoogle Scholar |

Freitas-de-Melo A, Ungerfeld R, Hötzel MJ, Abud MJ, Alvarez-Oxiley A, Orihuela A, Damián JP, Pérez-Clariget R (2015) Mother–young behaviours at lambing in grazing ewes: effects of lamb sex and food restriction in pregnancy. Applied Animal Behaviour Science 168, 31–36.
Mother–young behaviours at lambing in grazing ewes: effects of lamb sex and food restriction in pregnancy.Crossref | GoogleScholarGoogle Scholar |

Freitas-de-Melo A, Terrazas A, Ungerfeld R, Orihuela A, Hötzel M, Pérez-Clariget R (2018) Influence of low pasture allowance during pregnancy on the attachment between ewes and their lambs at birth and during lactation. Applied Animal Behaviour Science 199, 9–16.
Influence of low pasture allowance during pregnancy on the attachment between ewes and their lambs at birth and during lactation.Crossref | GoogleScholarGoogle Scholar |

Flinn T, Kleemann DO, Swinbourne AM, Kelly JM, Weaver AC, Walker SK, Gatford KL, Kind KL, van Wettere WHEJ (2020a) Neonatal lamb mortality: major risk factors and the potential ameliorative role of melatonin. Journal of Animal Science and Biotechnology 11, 1–11.
Neonatal lamb mortality: major risk factors and the potential ameliorative role of melatonin.Crossref | GoogleScholarGoogle Scholar |

Flinn T, Gunn JR, Kind K L, Swinbourne AM, Weaver AC, Kelly JM, Walker SK, Gatford KL, van Wettere WHEJ, Kleemann DO (2020b) Maternal melatonin implants improve twin Merino lamb survival. Journal of Animal Science 98, skaa344
Maternal melatonin implants improve twin Merino lamb survival.Crossref | GoogleScholarGoogle Scholar | 33091925PubMed |

Flinn T, McCarthy NL, Swinbourne AM, Gatford KL, Weaver AC, McGrice HA, Kelly JM, Walker SK, Kind KL, Kleemann DO, van Wettere WHEJ (2020c) Supplementing Merino ewes with melatonin during the last half of pregnancy improves tolerance of prolonged parturition and survival of second-born twin lambs. Journal of Animal Science 98, skaa372
Supplementing Merino ewes with melatonin during the last half of pregnancy improves tolerance of prolonged parturition and survival of second-born twin lambs.Crossref | GoogleScholarGoogle Scholar | 33205209PubMed |

Guesdon V, Malpaux B, Delagrange P, Spedding M, Cornilleau F, Chesneau D, Haller J, Chaillou E (2013) Rapid effects of melatonin on hormonal and behavioral stressful responses in ewes. Psychoneuroendocrinology 38, 1426–1434.
Rapid effects of melatonin on hormonal and behavioral stressful responses in ewes.Crossref | GoogleScholarGoogle Scholar | 23337408PubMed |

Jones AK, Reed SA (2017) Benefits of ultrasound scanning during gestation in the small ruminant. Small Ruminant Research 149, 163–171.
Benefits of ultrasound scanning during gestation in the small ruminant.Crossref | GoogleScholarGoogle Scholar |

Labeur L, Villiers G, Small AH, Hinch GN, Schmoelzl S (2017) Infrared thermal imaging as a method to evaluate heat loss in newborn lambs. Research in Veterinary Science 115, 517–522.
Infrared thermal imaging as a method to evaluate heat loss in newborn lambs.Crossref | GoogleScholarGoogle Scholar | 28968573PubMed |

Lemley CO, Meyer AM, Camacho LE, Neville TL, Shukla P, O’Rourke ST, Caton JS, Vonnahme KA (2011) Umbilical cord blood flow following melatonin supplementation in adequately fed or nutrient restricted ewes. Biology of Reproduction 85, 458
Umbilical cord blood flow following melatonin supplementation in adequately fed or nutrient restricted ewes.Crossref | GoogleScholarGoogle Scholar |

Lemley CO, Meyer AM, Camacho LE, Neville TL, Newman DJ, Caton JS, Vonnahme KA (2012) Melatonin supplementation alters uteroplacental hemodynamics and fetal development in an ovine model of intrauterine growth restriction. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 302, R454–R467.
Melatonin supplementation alters uteroplacental hemodynamics and fetal development in an ovine model of intrauterine growth restriction.Crossref | GoogleScholarGoogle Scholar | 22129617PubMed |

Lira R (2012) Suplementación estratégica. In ‘Bases para la producción ovina en Magallanes’. (Eds O Strauch, R Lira) pp. 92–103. (INIA Kampenaike: Punta Arenas, Chile)

Malpaux B, Tricoire H, Mailliet F, Daveau A, Migaud M, Skinner DC, Pelletier J, Chemineau P (2002) Melatonin and seasonal reproduction: understanding the neuroendocrine mechanisms using the sheep as a model. Reproduction 59, 167–179.

Mellor DJ, Stafford KJ (2004) Animal welfare implications of neonatal mortality and morbidity in farm animals. The Veterinary Journal 168, 118–133.
Animal welfare implications of neonatal mortality and morbidity in farm animals.Crossref | GoogleScholarGoogle Scholar | 15301760PubMed |

Menant O, Ungerfeld R, Pérez-Clariget R, Freitas-de-Melo A (2020) Is body surface temperature measured on the single ‘lambs’ back a reliable indicator of the ewe–lamb bond around birth? Journal of Thermal Biology 93, 102699
Is body surface temperature measured on the single ‘lambs’ back a reliable indicator of the ewe–lamb bond around birth?Crossref | GoogleScholarGoogle Scholar | 33077120PubMed |

Miller DR, Blache D, Jackson RB, Downie EF, Roche JR (2010) Metabolic maturity at birth and neonate lamb survival: association among maternal factors, litter size, lamb birth weight, and plasma metabolic and endocrine factors on survival and behavior. Journal of Animal Science 88, 581–592.
Metabolic maturity at birth and neonate lamb survival: association among maternal factors, litter size, lamb birth weight, and plasma metabolic and endocrine factors on survival and behavior.Crossref | GoogleScholarGoogle Scholar | 19897628PubMed |

Morris ST (2017) Overview of sheep production systems. In ‘Advances in sheep welfare’. (Eds DM Ferguson, C Lee, A Fisher) pp. 19–35. (Woodhead Publishing: Sawston, UK)

Russel AJF, Doney JM, Gunn RG (1969) Subjective assessment of body fat in live sheep. The Journal of Agricultural Science 72, 451–454.
Subjective assessment of body fat in live sheep.Crossref | GoogleScholarGoogle Scholar |

Sales F, Peralta OA, Narbona E, McCoard S, González-Bulnes A, Parraguez VH (2019) Rapid communication: maternal melatonin implants improve fetal oxygen supply and body weight at term in sheep pregnancies. Journal of Animal Science 97, 839–845.
Rapid communication: maternal melatonin implants improve fetal oxygen supply and body weight at term in sheep pregnancies.Crossref | GoogleScholarGoogle Scholar | 30452689PubMed |

Sales F, Parraguez VH, Freitas-de-Melo A, Ungerfeld R (2020) Maternal nutrition and antioxidant supplementation: effects on mother–young behaviors in a Patagonian sheep extensive grazing system. Applied Animal Behaviour Science 228, 105010
Maternal nutrition and antioxidant supplementation: effects on mother–young behaviors in a Patagonian sheep extensive grazing system.Crossref | GoogleScholarGoogle Scholar |

Seron-Ferre M, Reynolds H, Mendez NA, Mondaca M, Valenzuela F, Ebensperger E, Guillermo J, Valenzuela GJ, Herrera EA, Llanos AJ, Torres-Farfan C (2015) Impact of maternal melatonin suppression on amount and functionality of brown adipose tissue (BAT) in the newborn sheep. Frontiers in Endocrinology 5, 232
Impact of maternal melatonin suppression on amount and functionality of brown adipose tissue (BAT) in the newborn sheep.Crossref | GoogleScholarGoogle Scholar | 25610428PubMed |

Valle A, Catala-Niell A, Colom B, Garcia-Palmer FJ, Oliver J, Roca P (2005) Sex-related differences in energy balance in response to caloric restriction. American Journal of Physiology-Endocrinology and Metabolism 289, E15–E22.
Sex-related differences in energy balance in response to caloric restriction.Crossref | GoogleScholarGoogle Scholar | 15701677PubMed |