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Journal of Integrative Agriculture  2023, Vol. 22 Issue (3): 844-852    DOI: 10.1016/j.jia.2022.08.073
Animal Science · Veterinary Medicine Advanced Online Publication | Current Issue | Archive | Adv Search |
Effect of group size and regrouping on physiological stress and behavior of dairy calves

LYU Jing1*, WANG Chao1*, ZHAO Xun-wu2, MIAO Er-yu1, WANG Zhi-peng1, XU Yuan1, BAI Xiu-juan1#, BAO Jun1#

1 College of Animal Science and Technology, Northeast Agricultural University, Harbin 150030, P.R.China

2 College of Wildlife and Protected Area, Northeast Forestry University, Harbin 150040, P.R.China

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一般在断奶后,牧场为便于生产管理,将来自不同群体大小的犊牛进行混群或重新分组,这种常规操作对犊牛的福利存在负面影响。混群前的社交经验可能会缓解混群应激,但仍需要更多研究验证这一假设,因此本文通过出生后单栏饲养或群养犊牛在混群后的生理和行为指标的变化,探究早期社会环境对犊牛抗应激能力的影响。将132头初生犊牛随机分为单栏饲养、3头群养、6头群养、12头群养,共4个处理组SG3G6G12组,每组6个重复)。60日龄时,将每个处理组(SG3G6G12)2重复引入较大的围栏中,形成44头犊牛规模的新群体。分别记录重组前后生理参数,包括心率(HR)、唾液皮质醇(S-CORT)、唾液分泌免疫球蛋白A(SIgA)、白介素-2IL-2)、白介素-6IL-6)、肿瘤坏死因子-α(TNF-α)水平和行为反应。重组后,无论是单栏饲养还是群养组犊牛HRS-CORT立即升高(P<0.05),但与群养犊牛相比,单栏饲养犊牛差异更显著(P<0.05)。单栏饲养犊牛的SIgAIL-2水平下降(P<0.05),且IL-2在所有组中最低(P<0.05)。此外,犊牛混群后具有不同的行为表现,包括活动时间和休息时间的变化,与新环境应激引发的负面情绪有关。群居犊牛的互相修饰、玩耍、探索行为和趴卧时间较多(P<0.05),而单栏饲养犊牛的自我梳理、攻击行为、站立和行走时间则显著增加(P < 0.05)。研究表明,单栏饲养犊牛可能比群养犊牛更易产生混群应激,从而对行为和神经生理产生影响,而出生后的群居经验则可能帮助犊牛缓解这种应激。


Mixing or regrouping of calves from different pens is a common animal management practice on the farm, which frequently occurs after weaning and has a negative effect on calve welfare.  Social integration before regrouping may relieve stresses, but more evidences are needed to verify this hypothesis.  The present study aimed to investigate acute physiological and behavioral variations of individually- or group-housed calves after being introduced into a mixed group.  A total of 132 postnatal calves were randomly divided into groups of 1, 3, 6 and 12 animals (S, G3, G6, and G12; 6 replicates in each group) until 59 days of age.  At 60 days of age, every two replicates from different groups (S, G3, G6 and G12) were introduced in a larger pen which containing 44 of the aboved experimental calves.  Before and after regrouping, physiological parameters of stress, including heart rate (HR), saliva cortisol (S-CORT), saliva secretory immunoglobulin A (SIgA), interleukin-2 (IL-2), interleukin-6 (IL-6), tumor necrosis factor-α (TNF-α) levels, and behavioral responses were recorded.  After regrouping, HR and S-CORT increased immediately (P<0.05), and higher (P<0.05) levels of such molecules were found in S calves compared to those in group-housed calves.  Levels of SIgA and IL-2 were decreased (P<0.05), and the lowest (P<0.05) IL-2 values were found in S calves compared to those in group-housed calves.  In addition, the introduced calves displayed a distinct behavior, including altered active and rest time, which was associated with negative emotions triggered by the novel surroundings.  Allogrooming, play, exploration behaviors and lying time were increased significantly (P<0.05) in group-housed calves than those in S calves.  Conversely, self-grooming, aggressive behaviors, standing and walking time were increased (P<0.05) in S calves than those in group-housed calves.  These findings suggest that individually-housed calves may be more susceptible to stressors arising from regrouping than group-housed calves, which consequently negatively affected behavioral and neuroendocrine responses.  Furthermore, moving calves with previous social experience may help mitigate regrouping stress.

Keywords:  calf       regrouping       group size       behavior       stress       welfa  
Received: 01 November 2021   Accepted: 06 May 2022
Fund: The study was supported by the National Natural Science Foundation of China (2012BAD12B00).
About author:  LYU Jing, E-mail:; WANG Chao, E-mail:; #Correspondence BAO Jun, E-mail:; BAI Xiu-juan, E-mail: * These authors contributed equally to this study.

Cite this article: 

LYU Jing, WANG Chao, ZHAO Xun-wu, MIAO Er-yu, WANG Zhi-peng, XU Yuan, BAI Xiu-juan, BAO Jun. 2023. Effect of group size and regrouping on physiological stress and behavior of dairy calves. Journal of Integrative Agriculture, 22(3): 844-852.

Abdelfattah E M, Schutz M M, Lay D C, Marchant-Forde J N, Eicher S D. 2013. Effect of group size on behavior, health, production, and welfare of veal calves. Journal of Animal Science, 91, 5455–5465.
Berk M, Williams L J, Jacka F N, O’Neil A, Maes M. 2013. So depression is an inflammatory disease, but where does the inflammation come from? BMC Medicine, 11, 200.
Bøe K E, Færevik G. 2003. Grouping and social preferences in calves, heifers and cows. Applied Animal Behaviour Science, 80, 175–190.
Bouissou M F, Boissy A, Le Neindre P, Veissier I. 2001. The social behaviour of cattle. In: Keeling L, Gonyou H, eds., Social Behaviour of Farm Animals. Commonwealth Agricultural Bureaux International, Wallingford, UK. pp. 113–145. 
Broom D M, Kirkden R D. 2004. Welfare, stress, behaviour and pathophysiology. In: Dunlop R H, Malbert C H, eds., Veterinary Pathophysiology. Blackwell, Ames, IA. pp. 337–369.
Chacón Pérez G, García-Belenguer Laita S, Illera del Portal J C, Palacio Liesa J, del Portal J C I. 2004. Validation of an EIA technique for the determination of salivary cortisol in cattle. Spanish Journal of Agricultural Research, 2, 45–51.
Cobb C J, Obeidat B S, Sellers M D, Pepper-Yowell A R, Hanson D L. 2014. Improved performance and heightened neutrophil responses during the neonatal and weaning periods among outdoor group-housed Holstein calves. Journal of Dairy Science, 97, 930–939.
Costa J, Keyserlingk M A G V, Weary D M. 2016. Invited review: Effects of group housing of dairy calves on behavior, cognition, performance, and health. Journal of Dairy Science, 99, 2453–2467.
Dantzer R. 2001. Cytokine, sickness behavior, and depression. Immunology & Allergy Clinics of North America, 15, 7–24.
Duve L R, Jensen M B. 2011. The level of social contact affects social behaviour in pre-weaned dairy calves. Applied Animal Behaviour Science, 135, 34–43.
Duve L R, Jensen M B. 2012. Social behavior of young dairy calves housed with limited or full social contact with a peer 1. Journal of Dairy Science, 95, 5936–5945.
Færevik G, Andersen I L, Jensen M B, Bøe K E. 2007. Increased group size reduces conflicts and strengthens the preference for familiar group mates after regrouping of weaned dairy calves (Bos taurus). Applied Animal Behaviour Science, 108, 215–228.
Færevik G, Jensen M B, Bøe K E. 2006. Dairy calves social preferences and the significance of a companion animal during separation from the group. Applied Animal Behaviour Science, 99, 205–221.
Gaillard C, Meagher R K, von Keyserlingk M A G, Weary D M. 2014. Social housing improves dairy calves’ performance in two cognitive tests. PLoS ONE, 9, e90205. 
Gary P M, Valeria A W. 1982. Effect of differential rearing on the behavioral and adrenocortical response of lambs to a novel environment. Applied Animal Ethology, 8, 269–279.
Gourkow N, Hamon S C, Phillips C. 2014. Effect of gentle stroking and vocalization on behaviour, mucosal immunity and upper respiratory disease in anxious shelter cats. Preventive Veterinary Medicine, 117, 266–275.
Grignard L, Boissy A, Boivin X, Garel J P, Neindre P L. 2000. The social environment influences the behavioural responses of beef cattle to handling. Applied Animal Behaviour Science, 68, 1–11.
Guhad F A, Hau J. 1996. Salivary IgA as a marker of social stress in rats. Neuroscience Letters, 216, 137–140.
Gygax M J, Roulet-Perez E, Meagher-Villemure K, Jakobs C, Salomons G S, Boulat O, Superti-Furga A, Ballhausen D, Bonafé L. 2009. Sudden unexpected death in an infant with L-2-hydroxyglutaric aciduria. European Journal of Pediatrics, 168, 957–962.
Hasegawa N, Nishiwaki A, Sugawara K, Ito I. 1997. The effects of social exchange between two groups of lactating primiparous heifers on milk production, dominance order, behavior and adrenocortical response. Applied Animal Behaviour Science, 51, 15–27.
Hennessy M B. 1997. Hypothalamic-pituitary-adrenal responses to brief social separation. Neuroscience and Biobehavioral Reviews, 21, 11–29.
Jensen M B, Budde M. 2006. The effects of milk feeding method and group size on feeding behavior and cross-sucking in group-housed dairy calves. Journal of Dairy Science, 89, 4778–4783.
Jensen M B, Larsen L E. 2014. Effects of level of social contact on dairy calf behavior and health. Journal of Dairy Science, 97, 5035–5044.
Jensen M B, Vestergaard K S, Krohn C C, Munksgaard L. 1997. Effect of single versus group housing and space allowance on responses of calves during open-field tests. Applied Animal Behaviour Science, 54, 109–121.
Kerr S, Wood-Gush D. 1987. The development of behaviour patterns and temperament in dairy heifers. Behavioural Processes, 15, 1–16.
Kikkawa A, Uchida Y, Naka De T, Taguchi K. 2003. Salivary secretory IgA concentrations in beagle dogs. Journal of Veterinary Medical Science, 65, 689–693.
Louise H, Margit B J, Leif L J. 2002. Calves’ motivation for access to two different types of social contact measured by operant conditioning. Applied Animal Behaviour Science, 79, 175–194.
Lv J, Li J H, Chao W, Wang Z P, Bi Y J, Zhang X, Yi R, Li X, Bao J. 2018. Positive or negative emotion induced by feeding success or failure can affect behaviors, heart rate and immunity of suckling calves. Physiology & Behavior, 196, 185–189.
Lv J, Zhao X W, Su H, Wang Z P, Bao J. 2021. Effects of group size on the behaviour, heart rate, immunity, and growth of Holstein dairy calves. Applied Animal Behaviour Science, 241, 105378.
Mattiello S, Battini M, Rosa G D, Napolitano F, Dwyer C. 2019. How can we assess positive welfare in Ruminants? Animals, 9, 758.
Millson G C, Kimberlin R H, Manning E J, Collis S C. 1979. Early distribution of radioactive liposomes and scrapie infectivity in mouse tissues following administration by different routes. Veterinary Microbiology, 4, 89–99.
Mittwoch-Jaffe T, Shalit F, Srendi B, Yehuda S. 1995. Modification of cytokine secretion following mild emotional stimuli. Neuroreport, 6, 789–792.
Napolitano F, Braghieri A, Cifuni G F, Pacelli C, Girolami A. 2002. Behaviour and meat production of organically farmed unweaned lambs. Small Ruminant Research, 43, 179–184.
Napolitano F, Rosa G D, Sevi A. 2008. Welfare implications of artificial rearing and early weaning in sheep. Applied Animal Behaviour Science, 110, 58–72.
Neisen G, Wechsler B, Gygax L. 2009. Effects of the introduction of single heifers or pairs of heifers into dairy-cow herds on the temporal and spatial associations of heifers and cows. Applied Animal Behaviour Science, 119, 127–136.
Oostindjer M, Brand H, Kemp B, Bolhuis J E. 2011a. Effects of environmental enrichment and loose housing of lactating sows on piglet behaviour before and after weaning. Applied Animal Behaviour Science, 134, 31–41.
Oostindjer M, Munoz J M, Van d B H, Kemp B, Bolhuis J E. 2011b. Maternal presence and environmental enrichment affect food neophobia of piglets. Biology Letters, 7, 19–22. 
de Paula V A, Keyserlingk M, Weary D M. 2010. Effects of pair versus single housing on performance and behavior of dairy calves before and after weaning from milk. Journal of Dairy Science, 93, 3079–3085.
de Paula V A, de Passille A M, Weary D M. 2012. Effects of the early social environment on behavioral responses of dairy calves to novel events. Journal of Dairy Science, 95, 5149–5155.
Rault J L. 2012. Friends with benefits: Social support and its relevance for farm animal welfare. Applied Animal Behaviour Science, 136, 1–14.
Raussi S, Boissy A, Delval E, Pradel P, Kaihilahti J, Veissier I. 2005. Does repeated regrouping alter the social behaviour of heifers? Applied Animal Behaviour Science, 93, 1–12. 
Schirmann K, Chapinal N, Weary D M, Heuwieser W, Keyserlingk M. 2011. Short-term effects of regrouping on behavior of prepartum dairy cows. Journal of Dairy Science, 94, 2312–2319.
Segerstrom S C, Miller G E. 2004. Psychological stress and the human immune system: A meta-analytic study of 30 years of inquiry. Psychological Bulletin, 130, 601–630.
Silva P, Moraes J, Mendonca L G D, Scanavez A A, Nakagawa G, Ballou M A, Walcheck B, Haines D, Endres M I, Chebel R C. 2013. Effects of weekly regrouping of prepartum dairy cows on innate immune response and antibody concentration. Journal of Dairy Science, 96, 7649–7657.
Stull C, Reynolds J. 2008. Calf welfare. Veterinary Clinics of North America Food Animal Practice, 24, 191–203.
Takeda K, Sato S, Sugawara K. 2003. Familiarity and group size affect emotional stress in Japanese Black heifers. Applied Animal Behaviour Science, 82, 1–11.
Veissier I, Chazal P, Pradel P, Le Neindre P. 1997. Providing social contacts and objects for nibbling moderates reactivity and oral behaviors in veal calves. Journal of Animal Science, 72, 356–365.
Watanuki S, Kim Y K. 2005. Physiological responses induced by pleasant stimuli. Journal of Physiological Anthropology and Applied Human Science, 24, 135–138.

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