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Understanding oral stereotypies in calves: alternative strategies, hypothalamic–pituitary–adrenal axis (re)activity and gene by environment interactions

Published online by Cambridge University Press:  08 November 2016

L. E Webb*
Affiliation:
Animal Production Systems Group, Wageningen University, PO Box 338, 6708 WD Wageningen, The Netherlands
C. G van Reenen
Affiliation:
Animal Production Systems Group, Wageningen University, PO Box 338, 6708 WD Wageningen, The Netherlands Livestock Research, Wageningen University and Research, PO Box 338, 6708 WD Wageningen, The Netherlands
B Engel
Affiliation:
Biometris, Wageningen University, PO Box 16, 6700 AA Wageningen, The Netherlands
H Berends
Affiliation:
Trouw Nutrition R&D, PO Box 220, 5830 AE Boxmeer, The Netherlands
W. J. J Gerrits
Affiliation:
Animal Nutrition Group, Wageningen University, PO Box 338, 6708 WD Wageningen, The Netherlands
E. A. M Bokkers
Affiliation:
Animal Production Systems Group, Wageningen University, PO Box 338, 6708 WD Wageningen, The Netherlands
*
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Abstract

Stereotypies are used as indicators of poor animal welfare and it is, therefore, important to understand underlying factors mediating their development. In calves, two oral stereotypies, that is, tongue playing and object manipulation, result mostly from insufficient structure in the diet. Three hypotheses were studied: (1) oral stereotypies in calves are one of two alternative strategies, the alternative being hypo-activity; (2) stereotyping and non-stereotyping calves differ in terms of cortisol secretion; (3) oral stereotypy development in calves rests on a gene by environment interaction. Eight-week-old bull calves (n=48) were assigned to one of four solid feed allowances (0, 9, 18 or 27 g dry matter/kg metabolic weight per day) with the following composition: 50% concentrate, 25% maize silage and 25% straw on dry matter basis. The calves received milk replacer in buckets, the provision of which was adjusted to achieve equal growth rates. At 14 to 18 weeks of age, calves were exposed to a challenge, that is, tethering inside cages. Oral stereotypies and inactivity were recorded in the home pens in the 4 weeks before the challenge using instantaneous scan sampling. Salivary cortisol levels were measured at −120, +40, +80, +120 min and +48 h relative to the challenge. Individual differences in behaviour were recorded in the first 30 min after challenge implementation using focal animal sampling and continuous recording, and these elements were entered into a principal component (PC) analysis to extract PCs. Regression analyses were performed to find relationships between stereotypies and inactivity, stereotypies and cortisol, and stereotypies and PCs (individual differences, genes) and solid feed (environment). Relationships between PCs and cortisol were also investigated to help with the interpretation of PCs. Hypotheses 1 and 2 were rejected. Hypothesis 3, however, was supported: calves with a zero solid feed allowance, that is, in the most barren environment, showed links between stereotypies and two of the PCs. Calves that displayed high levels of idle and rapid locomotion and low levels of oral contact with the cage during the challenge also displayed high levels of object manipulation in the home pens. Calves that displayed low levels of stepping and turning attempts during the challenge also displayed high levels of tongue playing in the home pens. This study corroborates the gene by environment interaction on the development of oral stereotypies in calves.

Type
Research Article
Copyright
© The Animal Consortium 2016 

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References

Andersen, IL, Boe, KE, Foerevik, G, Janczak, AM and Bakken, M 2000. Behavioural evaluation of methods for assessing fear responses in weaned pigs. Applied Animal Behaviour Science 69, 227240.Google Scholar
Berends, H, van den Borne, JJGC, Alferink, SJJ, van Reenen, CG, Bokkers, EAM and Gerrits, WJJ 2012. Low-protein solid feed improves the utilization of milk replacer for protein gain in veal calves. Journal of Dairy Science 95, 66546664.Google Scholar
Bergeron, R, Badnell-Waters, AJ, Lambton, S and Mason, G 2006. Stereotypic oral behaviour in captive ungulates: foraging, diet and gastrointestinal function. In Stereotypic animal behaviour. Fundamentals and applications to welfare (ed. G Mason and J Rushen), pp. 1957. CAB International, Wallingford, UK.Google Scholar
Cabib, S 2006. The neurobiology of stereotypy II: the role of stress. In Stereotypic animal behaviour. Fundamentals and applications to welfare (ed. G Mason and J Rushen), pp. 227255. CAB International, Wallingford, UK.Google Scholar
Cronin, GM 1985. The development and significance of abnormal stereotyped behaviours in tethered sows. Agricultural University of Wageningen, Wageningen, The Netherlands.Google Scholar
Freymond, SB, Bardou, D, Briefer, EF, Bruckmaier, R, Fouche, N, Fleury, J, Maigrot, AL, Ramseyer, A, Zuberbuhler, K and Bachmann, I 2015. The physiological consequences of crib-biting in horses in response to an ACTH challenge test. Physiology & Behavior 151, 121128.Google Scholar
Friend, TH, Dellmeier, GR and Gbur, EE 1985. Comparison of four methods of calf confinement. 1. Physiology. Journal of Animal Science 60, 10951101.Google Scholar
Fureix, C, Walker, M, Harper, L, Reynolds, K, Saldivia-Woo, A and Mason, G 2016. Stereotypic behaviour in standard non-enriched cages is an alternative to depression-like responses in C57BL/6 mice. Behavioural Brain Research 305, 186190.Google Scholar
Gabriels, RL, Agnew, JA, Pan, ZX, Holt, KD, Reynolds, A and Laudenslager, ML 2013. Elevated repetitive behaviors are associated with lower diurnal salivary cortisol levels in autism spectrum disorder. Biological Psychology 93, 262268.Google Scholar
Gottlieb, DH, Capitanio, JP and McCowan, B 2013. Risk factors for stereotypic behavior and self-biting in rhesus macaques (Macaca mulatta): animal’s history, current environment, and personality. American Journal of Primatology 75, 9951008.Google Scholar
Ijichi, CL, Collins, LM and Elwood, RW 2013. Evidence for the role of personality in stereotypy predisposition. Animal Behaviour 85, 11451151.Google Scholar
Jensen, KH, Pedersen, LJ, Nielsen, EK, Heller, KE, Ladewig, J and Jorgensen, E 1996. Intermittent stress in pigs: effects on behavior, pituitary-adrenocortical axis, growth, and gastric ulceration. Physiology & Behavior 59, 741748.Google Scholar
Kenward, MG and Roger, JH 1997. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53, 983997.Google Scholar
Mason, GJ 1991. Stereotypies and suffering. Behavioural Processes 25, 103115.Google Scholar
Mason, GJ and Latham, NR 2004. Can’t stop, won’t stop: is stereotypy a reliable animal welfare indicator? Animal Welfare 13, S57S69.Google Scholar
McBride, SD and Cuddeford, D 2001. The putative welfare-reducing effects of preventing equine stereotypic behaviour. Animal Welfare 10, 173189.Google Scholar
Meagher, RK, Campbell, DL, Dallaire, JA, Díez-León, M, Palme, R and Mason, GJ 2013. Sleeping tight or hiding in fright? The welfare implications of different subtypes of inactivity in mink. Applied Animal Behaviour Science 144, 138146.CrossRefGoogle Scholar
Miller, GE, Chen, E and Zhou, ES 2007. If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. Psychological Bulletin 133, 2545.Google Scholar
Morisse, JP, Cotte, JP, Huonnic, D and Martrenchar, A 1999. Influence of dry feed supplements on different parameters of welfare in veal calves. Animal Welfare 8, 4352.Google Scholar
Mormède, P, Andanson, S, Auperin, B, Beerda, B, Guemene, D, Malmkvist, J, Manteca, X, Manteuffel, G, Prunet, P, van Reenen, CG, Richard, S and Veissier, I 2007. Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiology & Behavior 92, 317339.Google Scholar
Nagy, K, Bodo, G, Bardos, G, Banszky, N and Kabai, P 2010. Differences in temperament traits between crib-biting and control horses. Applied Animal Behaviour Science 122, 4147.Google Scholar
Negrâo, JA, Porcinato, MA, De Passillé, AM and Rushen, J 2004. Cortisol in saliva and plasma of cattle after ACTH administration and milking. Journal of Dairy Science 87, 17131718.Google Scholar
Redbo, I 1998. Relations between oral stereotypies, open-field behavior, and pituitary-adrenal system in growing dairy cattle. Physiology & Behavior 64, 273278.Google Scholar
Reimert, I, Bolhuis, JE, Kemp, B and Rodenburg, TB 2013. Indicators of positive and negative emotions and emotional contagion in pigs. Physiology & Behavior 109, 4250.Google Scholar
Schouten, WGP and Wiepkema, PR 1991. Coping styles of tethered sows. Behavioural Processes 25, 125132.Google Scholar
Ursin, H and Eriksen, HR 2004. The cognitive activation theory of stress. Psychoneuroendocrinology 29, 567592.Google Scholar
van Reenen, CG, Engel, B and Ruis-Heutinck, LFM 2004. Behavioural reactivity of heifer calves in potentially alarming test situations: a multivariate and correlational analysis. Applied Animal Behaviour Science 85, 1130.Google Scholar
Webb, LE, Bokkers, EAM, Engel, B, Berends, H, Gerrits, WJJ and van Reenen, CG 2012. Behaviour and welfare of veal calves fed different amounts of solid feed supplemented to a milk replacer ration adjusted for similar growth. Applied Animal Behaviour Science 136, 108116.Google Scholar
Webb, LE, van Reenen, CG, Berends, H, Engel, B, de Boer, IJM, Gerrits, WJJ and Bokkers, EAM 2015. The role of solid feed amount and composition and of milk replacer supply in veal calf welfare. Journal of Dairy Science 98, 54675481.Google Scholar
Wiepkema, PR 1987. Developmental aspects of motivated behavior in domestic animals. Journal of Animal Science 65, 12201227.Google Scholar
Würbel, H, Bergeron, R and Cabib, S 2006. The coping hypothesis of stereotypic behaviour. In Stereotypic animal behaviour. Fundamentals and applications to welfare (ed. G Mason and J Rushen), pp. 1415. CAB International, Wallingford, UK.Google Scholar