Temporary sensory separation of ewes from lambs effects stress-related behaviours and hormones of Small-tailed Han ewes
Chengquan Han
A # , Yueshang Wang A B # , Min Li A , Fukuan Li A , Zhennan Wang A , Yan Yang C , Hui Wang A * and Shenjin Lv A *
A
B
C
Handling Editor: Alan Tilbrook
Abstract
Different individuals within a group can form strong links through auditory, visual, and tactile senses. Temporarily separating sheep into subflocks, although not involving complete social isolation of individuals, can be stressful, especially when ewes are separated from lambs.
This study aimed to explore the effects of 1-h temporary ewe–lamb sensory separations on stress-related behaviours during separation, as well as its effect on stress-related hormones of ewes.
Small-tailed Han ewes were randomly assigned to the following four groups (six each): the auditory + visual + tactile separation (A + V + T group), visual + tactile separation (V + T group), tactile separation (T group), and the control (C group). Then, the ewes were separated from their lambs for 1 h on Postnatal Days 14, 21, 28, 35 and 42. Ewe behaviours during the separations were observed using focal animal-sampling methods.
Results showed that the separated ewes (A + V + T, V + T, and T groups) spent more time looking and exploring and less time lying (P < 0.05). Ewes showed more exploring behaviour in T group (P < 0.05). Ewes that gave birth to two lambs showed more urinating behaviour (P < 0.05). There was no significant difference in the level of stress-related hormones in ewes among the four different separation-method groups (A + V + T, V + T, T, and C groups).
One hour ewe-lamb sensory separation affected the stress related behaviours of Small-tailed Han ewes during separation, but it did not cause differences in stress-related hormones in ewes after the separation. Ewes showed increased exploring or urinating behaviour when they were separated through lack of tactile contact only with lambs, or when ewes give birth to two lambs.
Ewes temporarily separated from their lambs are less stressed if they are unable to hear or see the lambs, thereby improving ewe welfare. These effects appear more pronounced in ewes with multiple lambs and provides new perspectives for further studies on the effect of litter size on ewe-lamb bonding.
Keywords: ewe–lamb bonding, ewes, hormone, lack of tactile contact, small-tailed Han sheep, stress-related behaviour, temporary sensory separation, welfare.
References
Alexander G (1977) Role of auditory and visual cues in mutual recognition between ewes and lambs in Merino sheep. Applied Animal Ethology 3(1), 65-81.
| Crossref | Google Scholar |
Atkinson AC, Riani M, Corbellini A (2021) The box–cox transformation: review and extensions. Statistical Science 36(2), 239-255.
| Crossref | Google Scholar |
Averós X, Marchewka J, Beltrán de Heredia I, Zanella AJ, Ruiz R, Estevez I (2015) Space allowance during gestation and early maternal separation: effects on the fear response and social motivation of lambs. Applied Animal Behaviour Science 163, 98-109.
| Crossref | Google Scholar |
Barnard S, Matthews LR, Messori S, Podaliri Vulpiani M, Ferri N (2015) Behavioural reactivity of ewes and lambs during partial and total social isolation. Applied Animal Behaviour Science 163, 89-97.
| Crossref | Google Scholar |
Carr JA (2002) Stress, neuropeptides, and feeding behavior: a comparative perspective. Integrative and Comparative Biology 42(3), 582-590.
| Crossref | Google Scholar | PubMed |
Cockram MS, Ranson M, Imlah P, Goddard PJ, Burrells C, Harkiss GD (1994) The behavioural, endocrine and immune responses of sheep to isolation. Animal Science 58, 389-399.
| Crossref | Google Scholar |
Damián JP, de Soto L, Espindola D, Gil J, van Lier E (2021) Intranasal oxytocin affects the stress response to social isolation in sheep. Physiology & Behavior 230, 113282.
| Crossref | Google Scholar | PubMed |
Degabriele R, Fell LR (2001) Changes in behaviour, cortisol and lymphocyte types during isolation and group confinement of sheep. Immunology & Cell Biology 79(6), 583-589.
| Crossref | Google Scholar | PubMed |
Ferrer LM, Lacasta D, Ortin A, Ramos JJ, Tejedor MT, Borobia M, Perez M, Castells E, Ruiz de Arcaute M, Ruiz H, Windsor PA (2020) Impact of a topical anaesthesia wound management formulation on pain, inflammation and reduction of secondary infections after tail docking in lambs. Animals 10(8), 1255.
| Crossref | Google Scholar |
Forster R, Falder N (2024) Managing weaning issues in lambs and ewes. Part 2: management of ewes following weaning. In Practice 46(4), 188-196.
| Crossref | Google Scholar |
Kent JE, Molony V, Graham MJ (1998) Comparison of methods for the reduction of acute pain produced by rubber ring castration or tail docking of week-old lambs. The Veterinary Journal 155(1), 39-51.
| Crossref | Google Scholar | PubMed |
Kleinhenz MD, Weeder M, Montgomery S, Martin M, Curtis A, Magnin G, Lin Z, Griffin J, Coetzee JF (2022) Short term feeding of industrial hemp with a high cannabidiolic acid (CBDA) content increases lying behavior and reduces biomarkers of stress and inflammation in Holstein steers. Scientific Reports 12(1), 3683.
| Crossref | Google Scholar | PubMed |
Kry J, Cordeira J (2018) Binge-eating behavior in socially-isolated female mice. Journal of Young Investigators 35, 7-11.
| Crossref | Google Scholar |
Lévy F, Gervais R, Kindermann U, Litterio M, Poindron P, Porter R (1991) Effects of early post-partum separation on maintenance of maternal responsiveness and selectivity in parturient ewes. Applied Animal Behaviour Science 31(1-2), 101-110.
| Crossref | Google Scholar |
Li FK, Yang Y, Jenna K, Xia CH, Lv SJ, Wei WH (2018) Effect of heat stress on the behavioral and physiological patterns of Small-tail Han sheep housed indoors. Tropical Animal Health and Production 50(8), 1893-1901.
| Crossref | Google Scholar | PubMed |
Lin C-H, Tsai I-L, Su C-H, Tseng D-Y, Hwang P-P (2011) Reverse effect of mammalian hypocalcemic cortisol in fish: cortisol stimulates Ca2+ uptake via glucocorticoid receptor-mediated vitamin D3 metabolism. PLoS ONE 6(8), e23689.
| Crossref | Google Scholar | PubMed |
Loberg JM, Hernandez CE, Thierfelder T, Jensen MB, Berg C, Lidfors L (2008) Weaning and separation in two steps – a way to decrease stress in dairy calves suckled by foster cows. Applied Animal Behaviour Science 111(3-4), 222-234.
| Crossref | Google Scholar |
Lyons DM, Price EO, Moberg GP (1993) Social grouping tendencies and separation-induced distress in juvenile sheep and goats. Developmental Psychobiology 26(5), 251-259.
| Crossref | Google Scholar | PubMed |
McKusick BC, Thomas DL, Berger YM (2001) Effect of weaning system on commercial milk production and lamb growth of east Friesian dairy sheep. Journal of Dairy Science 84(7), 1660-1668.
| Crossref | Google Scholar | PubMed |
Mellor DJ, Stafford KJ (2000) Acute castration and/or tailing distress and its alleviation in lambs. New Zealand Veterinary Journal 48(2), 33-43.
| Crossref | Google Scholar | PubMed |
Merkies K, DuBois C, Marshall K, Parois S, Graham L, Haley D (2016) A two-stage method to approach weaning stress in horses using a physical barrier to prevent nursing. Applied Animal Behaviour Science 183, 68-76.
| Crossref | Google Scholar |
Minton JE, Blecha F (1990) Effect of acute stressors on endocrinological and immunological functions in lambs1. Journal of Animal Science 68(10), 3145-3151.
| Crossref | Google Scholar | PubMed |
Mora P, Mota D, Arch-Tirado E, Roldán P, Vázquez-Cruz C, Terrazas AM, Rosas M, Orihuela A (2017) Behavior of lambs at different ages during brief periods of increased sensorial isolation from their mothers. Journal of Veterinary Behavior 22, 29-34.
| Crossref | Google Scholar |
Mora-Medina P, Mota-Rojas D, Arch-Tirado E, Orozco-Gregorio H (2015) Animal welfare in lambs: ewe–lamb separation. Large Animal Review 21(1), 39-44.
| Google Scholar |
Mora-Medina P, Orihuela-Trujillo A, Roldan-Santiago P, Arch-Tirado E, Vázquez-Cruz C, Mota-Rojas D (2018) Metabolic changes during brief periods of ewe–lamb separation at different ages. Animal Production Science 58(7), 1297-1306.
| Crossref | Google Scholar |
Nakhate KT, Kokare DM, Singru PS, Subhedar NK (2011) Central regulation of feeding behavior during social isolation of rat: evidence for the role of endogenous CART system. International Journal of Obesity 35, 773-784.
| Crossref | Google Scholar | PubMed |
Napolitano F, De Rosa G, Sevi A (2008) Welfare implications of artificial rearing and early weaning in sheep. Applied Animal Behaviour Science 110(1-2), 58-72.
| Crossref | Google Scholar |
Newberry RC, Swanson JC (2008) Implications of breaking mother–young social bonds. Applied Animal Behaviour Science 110(1-2), 3-23.
| Crossref | Google Scholar |
Nowak R, Porter RH, Levy F, Orgeur P, Schaal B (2000) Role of mother–young interactions in the survival of offspring in domestic mammals. Reviews of Reproduction 5(3), 153-163.
| Crossref | Google Scholar | PubMed |
Nowak R, Keller M, Val-Laillet D, Lévy F (2007) Perinatal visceral events and brain mechanisms involved in the development of mother–young bonding in sheep. Hormones and Behavior 52(1), 92-98.
| Crossref | Google Scholar | PubMed |
Nowak R, Keller M, Lévy F (2011) Mother-young relationships in sheep: a model for a multidisciplinary approach of the study of attachment in mammals. Journal of Neuroendocrinology 23(11), 1042-1053.
| Crossref | Google Scholar | PubMed |
Orgeur P, Mavric N, Yvore P, Bernard S, Nowak R, Schaal B, Levy F (1998) Artificial weaning in sheep: consequences on behavioural, hormonal and immuno-pathological indicators of welfare. Applied Animal Behaviour Science 58, 87-103.
| Google Scholar |
Osborne J (2010) Improving your data transformations: applying the Box-Cox transformation. Practical Assessment, Research and Evaluation 15(1), 12.
| Crossref | Google Scholar |
Pan L, Zheng L, Wu X, Zhu Z, Wang S, Lu Y, He Y, Yang Q, Ma X, Wang X, Yang H, Zhan L, Luo Y, Li X, Zhou Y, Wang X, Luo J, Wang L, Duan S, Wang H (2022) A short period of early life oxytocin treatment rescues social behavior dysfunction via suppression of hippocampal hyperactivity in male mice. Molecular Psychiatry 27(10), 4157-4171.
| Crossref | Google Scholar | PubMed |
Panksepp J (2005) Affective consciousness: core emotional feelings in animals and humans. Consciousness and Cognition 14(1), 30-80.
| Crossref | Google Scholar | PubMed |
Pérez-León I, Orihuela A, Lidfors L, Aguirre V (2006) Reducing mother–young separation distress by inducing ewes into oestrus at the day of weaning. Animal Welfare 15(4), 383-389.
| Crossref | Google Scholar |
Poindron P, Caba M, Arrati PG, Krehbiel D, Beyer C (1994) Responses of maternal and non-maternal ewes to social and mother–young separation. Behavioural Processes 31(1), 97-110.
| Crossref | Google Scholar | PubMed |
Searby A, Jouventin P (2003) Mother–lamb acoustic recognition in sheep: a frequency coding. Proceedings of the Royal Society of London. Series B: Biological Sciences 270(1526), 1765-1771.
| Crossref | Google Scholar |
Sèbe F, Aubin T, Boué A, Poindron P (2008) Mother–young vocal communication and acoustic recognition promote preferential nursing in sheep. Journal of Experimental Biology 211(22), 3554-3562.
| Google Scholar | PubMed |
Simitzis P, Petrou M, Demiris N, Deligeorgis S (2012) Effect of pre-weaning temporary isolation within different age periods on the early post-weaning behaviour of juvenile lambs. Applied Animal Behaviour Science 141(1-2), 43-48.
| Crossref | Google Scholar |
Soto R, Terrazas A, Poindron P, Gonzalez-Mariscal G (2021) Regulation of maternal behavior, social isolation responses, and postpartum estrus by steroid hormones and vaginocervical stimulation in sheep. Hormones and Behavior 136, 105061.
| Crossref | Google Scholar | PubMed |
Thompson RKR, Foltin RW, Boylan RJ, Sweet A, Graves CA, Lowitz CE (1981) Tonic immobility in Japanese quail can reduce the probability of sustained attack by cats. Animal Learning & Behavior 9(1), 145-149.
| Crossref | Google Scholar |
van Adrichem PWM, Vogt JE (1993) The effect of isolation and separation on the metabolism of sheep. Livestock Production Science 33, 151-159.
| Crossref | Google Scholar |
Vandenheede M, Bouissou MF, Picard M (1998) Interpretation of behavioural reactions of sheep towards fear-eliciting situations. Applied Animal Behaviour Science 58(3-4), 293-310.
| Crossref | Google Scholar |
Vierin M, Bouissou M-F (2003) Responses of weaned lambs to fear-eliciting situations: origin of individual differences. Developmental Psychobiology 42(2), 131-147.
| Crossref | Google Scholar | PubMed |
Walser ES, Alexander G (1980) Mutual recognition between ewes and lambs. Reproduction Nutrition Development 20(3B), 807-816.
| Crossref | Google Scholar | PubMed |
Wenker ML, van Reenen CG, Bokkers EAM, McCrea K, de Oliveira D, Sørheim K, Cao Y, Bruckmaier RM, Gross JJ, Gort G, Verwer CM (2022) Comparing gradual debonding strategies after prolonged cow-calf contact: stress responses, performance, and health of dairy cow and calf. Applied Animal Behaviour Science 253, 105694.
| Crossref | Google Scholar |
Yayou K-I, Nakamura M, Ito S (2009) Effects of AVP V1a and CRH receptor antagonist on psychological stress responses to frustrating condition in sheep. Journal of Veterinary Medical Science 71(4), 431-439.
| Crossref | Google Scholar | PubMed |
