Oral stereotypic behaviors in farm animals and their causes

Abstract

High stocking density and suboptimal conditions limit animal behaviors in modern livestock farming. This is particularly evident in captive animals, in which the motivation for foraging behavior is often thwarted. Oral stereotypic behaviors are common in farm animals. Ruminants (e.g., cattle and sheep) show oral stereotypic behaviors such as tongue-rolling, self-sucking, and inter-sucking. Captive pigs exhibit oral stereotypic behaviors such as bar-biting, sham-chewing, and ear-biting. Chickens peck at drinkers, feeders, and pens. Stereotypic behavior in livestock can be reduced by selecting a specific diet composition that prolongs their eating time and increases their satiety. Furthermore, reducing stocking density and enriching the farming environment encourage livestock to explore and reduce stereotypic behavior. It is important to note that stereotypic behavior is also influenced by organismal physiology. Stereotypic behavior was considered an indicator of poor animal welfare. However, recent research has revealed that animals engage in stereotypic behavior as a response to external stimuli, aiming to alleviate the negative impact of these stimuli on their well-being. Animals that frequently show stereotypic behavior may have higher levels of stress. Certain stress indicators also affect the expression of stereotypic behavior, such as 5-hydroxytryptamine and dopamine. Consequently, further investigation is necessary to understand how stereotypic behaviors affect the physiological state and metabolic processes of animals. This paper discusses the research progress on the oral stereotypic behaviors of farm animals. The objective is to establish a foundation for enhancing livestock feeding conditions and optimizing feeding practices, ultimately reducing stereotypic behaviors.

Keywords

animal behavior / animal diets / animal welfare / farming management / oral stereotypic behavior

References

[1] Dantzer, R. (1991). Stress, stereotypies and welfare. Behavioural Processes, 25(2–3), 95–102.

[2] Webb, L. E., van Reenen, C. G., Engel, B., Berends, H., Gerrits, W. J. J., & Bokkers, E. A. M. (2017). Understanding oral stereotypies in calves: Alternative strategies, hypothalamic–pituitary–adrenal axis (re)activity and gene by environment interactions. Animal, 11(6), 1054–1062.

[3] Ridge, E. E., Foster, M. J., & Daigle, C. L. (2020). Effect of diet on non-nutritive oral behavior performance in cattle: A systematic review. Livestock Science, 238, 104063.

[4] Pan, L., Nian, H., Zhang, R., Liu, H., Li, C., Wei, H., Yi, R., Li, J., Li, X., & Bao, J. (2022). Stereotypic behaviors are associated with physiology and immunity differences in long-term confined sows. Physiology & Behavior, 249, 113776.

[5] Ahola, M. K., Vapalahti, K., & Lohi, H. (2017). Early weaning increases aggression and stereotypic behaviour in cats. Scientific Reports, 7(1), 10412.

[6] Novak, J., Bailoo, J. D., Melotti, L., Rommen, J., & Würbel, H. (2015). An exploration based cognitive bias test for mice: Effects of handling method and stereotypic Behaviour. PLoS One, 10(7), e0130718.

[7] Kelly, K. R., Harrison, M. L., Size, D. D., & MacDonald, S. E. (2015). Individual effects of seasonal changes, visitor density, and concurrent bear behavior on stereotypical behaviors in captive polar bears (Ursus maritimus). Journal of Applied Animal Welfare Science, 18(1), 17–31.

[8] Mason, G., Clubb, R., Latham, N., & Vickery, S. (2007). Why and how should we use environmental enrichment to tackle stereotypic behaviour? Applied Animal Behaviour Science, 102(3–4), 163–188.

[9] Miller, L. J., Kuczaj, S., & Herzing, D. (2011). Stereotypic behavior in wild marine carnivores? Zoo Biology, 30(4), 365–370.

[10] Peça, J., Feliciano, C., Ting, J. T., Wang, W., Wells, M. F., Venkatraman, T. N., Lascola, C. D., Fu, Z., & Feng, G. (2011). Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature, 472(7344), 437–442.

[11] Boddicker, N., Gabler, N. K., Spurlock, M. E., Nettleton, D., & Dekkers, J. C. M. (2011). Effects of ad libitum and restricted feed intake on growth performance and body composition of Yorkshire pigs selected for reduced residual feed intake. Journal of Animal Science, 89(1), 40–51.

[12] Jarvis, S., Van der Vegt, B. J., Lawrence, A. B., McLean, K. A., Deans, L. A., Chirnside, J., & Calvert, S. K. (2001). The effect of parity and environmental restriction on behavioural and physiological responses of pre-parturient pigs. Applied Animal Behaviour Science, 71(3), 203–216.

[13] Mellor, D. (2016). Moving beyond the “five freedoms” by updating the “five provisions” and introducing aligned “animal welfare aims”. Animals, 6(10), 59.

[14] Mason, G., & Latham, N. (2004). Can’t stop, won’t stop: Is stereotypy a reliable animal welfare indicator? Animal Welfare, 13(S1), S57–S69.

[15] Hughes, B. O., & Duncan, I. J. H. (1988). The notion of ethological ‘need’ models of motivation and animal welfare. Animal Behaviour, 36(6), 1696–1707.

[16] Jensen, P., & Toates, F. M. (1993). Who needs ‘behavioural needs’? Motivational aspects of the needs of animals. Applied Animal Behaviour Science, 37(2), 161–181.

[17] Hemsworth, P. H. (2018). Key determinants of pig welfare: Implications of animal management and housing design on livestock welfare. Animal Production Science, 58(8), 1375.

[18] Mason, G. J. (1991). Stereotypies: A critical review. Animal Behaviour, 41(6), 1015–1037.

[19] Roche, J. R., Friggens, N. C., Kay, J. K., Fisher, M. W., Stafford, K. J., & Berry, D. P. (2009). Invited review: Body condition score and its association with dairy cow productivity, health, and welfare. Journal of Dairy Science, 92(12), 5769–5801.

[20] Fureix, C., Benhajali, H., Henry, S., Bruchet, A., Prunier, A., Ezzaouia, M., Coste, C., Hausberger, M., Palme, R., & Jego, P. (2013). Plasma cortisol and faecal cortisol metabolites concentrations in stereotypic and non-stereotypic horses: Do stereotypic horses cope better with poor environmental conditions? BMC Veterinary Research, 9(1), 3.

[21] Jones, M. A., Van Lierop, M., Mason, G., & Pillay, N. (2010). Increased reproductive output in stereotypic captive Rhabdomys females: Potential implications for captive breeding. Applied Animal Behaviour Science, 123(1–2), 63–69.

[22] Sun, F., Zhao, Q., Chen, X., Zhao, G., & Gu, X. (2022). Physiological indicators and production performance of dairy cows with tongue rolling stereotyped behavior. Frontiers in Veterinary Science, 9, 840726.

[23] Downey, B. C., & Tucker, C. B. (2023). Early life access to hay does not affect later life oral behavior in feed-restricted heifers. Journal of Dairy Science, 106(8), 5672–5686.

[24] Robbins, J. A., McCandless, K., Weary, D. M., & Paros, M. (2023). Breed, parity, and days in milk affect risk of tongue rolling in dairy cows. JDS Communications, 4(3), S2666910223000170.

[25] Binev, R. (2022). Tongue rolling stereotypy in cattle – Etiological, epidemiological and clinical investigations. BJVM, 25(1), 80–88.

[26] Sun, F., Zhao, Q., Chen, X., Zhao, G., & Gu, X. (2022). Feed tossing behaviour of Holstein cows: evaluation of physiological stress state and rumen fermentation function. BMC Veterinary Research, 18(1), 371.

[27] Seabra, J. C., Dittrich, J. R., & do Vale, M. M. (2021). Factors associated with the development and prevalence of abnormal behaviors in horses: Systematic review with meta-analysis. Journal of Equine Veterinary Science, 106, 103750.

[28] McGreevy, P. D., Cripps, P. J., French, N. P., Green, L. E., & Nicol, C. J. (1995). Management factors associated with stereotypic and redirected behaviour in the thoroughbred horse. Equine Veterinary Journal, 27(2), 86–91.

[29] Luescher, U. A., McKeown, D. B., & Dean, H. (1998). A cross-sectional study on compulsive behaviour (stable vices) in horses. Equine Veterinary Journal, 30(27), 14–18.

[30] Albright, J. D., Mohammed, H. O., Heleski, C. R., Wickens, C. L., & Houpt, K. A. (2009). Crib-biting in US horses: Breed predispositions and owner perceptions of aetiology. Equine Veterinary Journal, 41(5), 455–458.

[31] Appleby, M. C., & Lawrence, A. B. (1987). Food restriction as a cause of stereotypic behaviour in tethered gilts. Animal Science, 45(1), 103–110.

[32] Demba, S., & Rose, S. (2023). Changes in amount and length of periods of stereotypic behavior in Jersey cows with and without access to pasture. Frontiers in Animal Science, 4, 1148523.

[33] Redbo, I. (1990). Changes in duration and frequency of stereotypies and their adjoining behaviours in heifers, before, during and after the grazing period. Applied Animal Behaviour Science, 26(1-2), 57-67.

[34] Marinath, L., Vaz, J., Kumar, D., Thiyagesan, K., & Baskaran, N. (2019). Drivers of stereotypic behaviour and physiological stress among captive jungle cat (Felis chaus Schreber, 1777) in India. Physiology & Behavior, 210, 112651.

[35] Lawrence, A. B., & Illius, A. W. (1989). Methodology for measuring hunger and food needs using operant conditioning in the pig. Applied Animal Behaviour Science, 24(4), 273–285.

[36] Redbo, I., Emanuelson, M., Lundberg, K., & Oredsson, N. (1996). Feeding level and oral stereotypies in dairy cows. Animal Science, 62(2), 199–206.

[37] Santoso, U. (2001). Effects of early feed restriction on growth, fat accumulation and meat composition in unsexed broiler chickens. Asian-Australasian Journal of Animal Sciences, 14(11), 1585–1591.

[38] Seo, T., Sato, S., Kosaka, K., Sakamoto, N., Tokumoto, K., & Katoh, K. (1998). Development of tongue-playing in artificially reared calves: Effects of offering a dummy-teat, feeding of short cut hay and housing system. Applied Animal Behaviour Science, 56(1), 1–12.

[39] Zhou, X., Lv, Q., Qin, Y., Yuan, N., Li, Y., Zhou, M., & Meng, X. (2023). Effects of social stress on the welfare of captive male Alpine musk deer: Stereotypic behavior, fecal cortisol, and musk secretion. Applied Animal Behaviour Science, 258, 105828.

[40] Nicolaisen, T., Risch, B., Lühken, E., van Meegen, C., Fels, M., & Kemper, N. (2019). Comparison of three different farrowing systems: Skin lesions and behaviour of sows with special regard to nursing behaviour in a group housing system for lactating sows. Animal, 13(11), 2612–2620.

[41] Munari, C., Ponzio, P., Macchi, E., Elkhawagah, A. R., Tarantola, M., Ponti, G., & Mugnai, C. (2020). A multifactorial evaluation of different reproductive rhythms and housing systems for improving welfare in rabbit does. Applied Animal Behaviour Science, 230, 105047.

[42] Wells, D. L. (2005). A note on the influence of visitors on the behaviour and welfare of zoo-housed gorillas. Applied Animal Behaviour Science, 93(1–2), 13–17.

[43] Sekar, M., Rajagopal, T., & Archunan, G. (2008). Influence of zoo visitor presence on the behavior of captive Indian gaur (Bos gaurus gaurus) in a zoological park. Journal of Applied Animal Welfare Science, 11(4), 352–357.

[44] Quirke, T., O’Riordan, R. M., & Zuur, A. (2012). Factors influencing the prevalence of stereotypical behaviour in captive cheetahs (Acinonyx jubatus). Applied Animal Behaviour Science, 142(3–4), 189–197.

[45] Kirmizigul A. H., Ozcelik M., Ogun M., Erkilic E. E., Paksoy N., Merhan O., & Uzlu E. (2019). Dil Oynatma Hastalığı Olan Sığırlarda Serum Cu, M., Zn Seviyeleri ve Oksidatif Stres. Kafkas Univ Vet Fak Derg [Internet].

[46] Redbo, I. (1992). The influence of restraint on the occurrence of oral stereotypies in dairy cows. Applied Animal Behaviour Science, 35(2), 115–123.

[47] Redbo, I. (1998). Relations between oral stereotypies, open-field behavior, and pituitary–adrenal system in growing dairy cattle. Physiology & Behavior, 64(3), 273–278.

[48] Krause, K. M., Combs, D. K., & Beauchemin, K. A. (2002). Effects of forage particle size and grain fermentability in midlactation cows. II. Ruminal pH and chewing activity. Journal of Dairy Science, 85(8), 1947–1957.

[49] Welch, J. G., & Smith, A. M. (1970). Forage quality and rumination time in cattle. Journal of Dairy Science, 53(6), 797–800.

[50] Yang, W. Z., & Beauchemin, K. A. (2006). Physically effective fiber: Method of determination and effects on chewing, ruminal acidosis, and digestion by dairy cows. Journal of Dairy Science, 89(7), 2618–2633.

[51] Giger-Reverdin, S., Rigalma, K., Desnoyers, M., Sauvant, D., & Duvaux-Ponter, C. (2014). Effect of concentrate level on feeding behavior and rumen and blood parameters in dairy goats: Relationships between behavioral and physiological parameters and effect of between-animal variability. Journal of Dairy Science, 97(7), 4367–4378.

[52] Oba, M., & Allen, M. S. (2000). Effects of brown midrib 3 mutation in corn silage on productivity of dairy cows fed two concentrations of dietary neutral detergent fiber: 2. Chewing activities. Journal of Dairy Science, 83(6), 1342–1349.

[53] Allen, M. S. (2000). Effects of diet on short-term regulation of feed intake by lactating dairy cattle. Journal of Dairy Science, 83(7), 1598–1624.

[54] Beauchemin, K. A., Yang, W. Z., & Rode, L. M. (2003). Effects of particle size of Alfalfa-based dairy cow diets on chewing activity, ruminal fermentation, and milk production. Journal of Dairy Science, 86(2), 630–643.

[55] Hajratwala, B. R. (1982). Particle size reduction by a Hammer Mill I: Effect of output screen size, feed particle size, and mill speed. Journal of Pharmaceutical Sciences, 71(2), 188–190.

[56] Cooper, J., & Jackson, R. (1996). A comparison of the feeding behaviour of sheep in straw yards and on slats. Applied Animal Behaviour Science, 49(1), 99.

[57] Vasseur, S., Paull, D. R., Atkinson, S. J., Colditz, I. G., & Fisher, A. D. (2006). Effects of dietary fibre and feeding frequency on wool biting and aggressive behaviours in housed Merino sheep. Australian Journal of Experimental Agriculture, 46(7), 777.

[58] Wiepkema, P. R., Van Hellemond, K. K., Roessingh, P., & Romberg, H. (1987). Behaviour and abomasal damage in individual veal calves. Applied Animal Behaviour Science, 18(3–4), 257–268.

[59] Soberon, F., Raffrenato, E., Everett, R. W., & Van Amburgh, M. E. (2012). Preweaning milk replacer intake and effects on long-term productivity of dairy calves. Journal of Dairy Science, 95(2), 783–793.

[60] de Passillé A. M. (2001). Sucking motivation and related problems in calves. Applied Animal Behaviour Science, 72(3), 175–187.

[61] Veissier, I., de Passillé A. M., Després, G., Rushen, J., Charpentier, I., Ramirez de la Fe, A. R., & Pradel, P. (2002). Does nutritive and non-nutritive sucking reduce other oral behaviors and stimulate rest in calves? Journal of Animal Science, 80(10), 2574–2587.

[62] Salter, R. S., Reuscher, K. J., & Van Os, J. M. C. (2021). Milk- and starter-feeding strategies to reduce cross sucking in pair-housed calves in outdoor hutches. Journal of Dairy Science, 104(5), 6096–6112.

[63] Ahmed, I. A., Helal, M. A., Ramadan, S. G., Mahboub, H. D., Byomi, A. M., & Reddy, P. G. (2014). Risk factors associated with galactophagia and its impacts on some productive and reproductive traits in dairy cows and buffaloes. Research & Reviews: Journal of Dairy Science and Technology, 4(2), 1–7.

[64] Lidfors, L., & Isberg, L. (2003). Intersucking in dairy cattle—Review and questionnaire. Applied Animal Behaviour Science, 80(3), 207–231.

[65] Martínez-de la Puente, J., Moreno-Indias, I., Morales-Delanuez, A., Ruiz-Díaz, M. D., Hernández-Castellano, L. E., Castro, N., & Argüello, A. (2011). Effects of feeding management and time of day on the occurrence of self-sucking in dairy goats. The Veterinary Record, 168(14), 378.

[66] Salman, Y., Semieka, M., Karmi, M., & Al-lethie, A. A. (2022). A novel surgical technique for prevention of self-sucking in cattle and buffaloes: Tongue piercing. BMC Veterinary Research, 18(1), 192.

[67] El-Sherif, M. W. (2018). Tongue reshaping: A new surgical method to prevent self-sucking in dairy cows. Open Veterinary Journal, 8(2), 140.

[68] Larson, G., Dobney, K., Albarella, U., Fang, M., Matisoo-Smith, E., Robins, J., Lowden, S., Finlayson, H., Brand, T., Willerslev, E., Rowley-Conwy, P., Andersson, L., & Cooper, A. (2005). Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science, 307(5715), 1618–1621.

[69] Stolba, A., & Wood-Gush, D. G. M. (1989). The behaviour of pigs in a semi-natural environment. Animal Science, 48(2), 419–425.

[70] Bergeron, R., Bolduc, J., Ramonet, Y., Meunier-Salaün, M. C., & Robert, S. (2000). Feeding motivation and stereotypies in pregnant sows fed increasing levels of fibre and/or food. Applied Animal Behaviour Science, 70(1), 27–40.

[71] de Leeuw, J. A., Bolhuis, J. E., Bosch, G., & Gerrits, W. J. J. (2008). Effects of dietary fibre on behaviour and satiety in pigs. Proceedings of the Nutrition Society, 67(4), 334–342.

[72] Hetherington, M. M., & Regan, M. F. (2011). Effects of chewing gum on short-term appetite regulation in moderately restrained eaters. Appetite, 57(2), 475–482.

[73] Steingoetter, A., Buetikofer, S., Curcic, J., Menne, D., Rehfeld, J. F., Fried, M., Schwizer, W., & Wooster, T. J. (2017). The dynamics of gastric emptying and self-reported feelings of satiation are better predictors than gastrointestinal hormones of the effects of lipid emulsion structure on fat digestion in healthy adults—A Bayesian Inference Approach. The Journal of Nutrition, 147(4), 706–714.

[74] Oelke, C. A., Bernardi, M. L., Nunes, P. R., Weber, N. C., Veit, F. C., & Leal Ribeiro, A. M. (2018). Physiological and behavioral response of sows fed with different levels of dietary fiber during gestation. Journal of Veterinary Behavior, 28, 54–57.

[75] Raubenheimer, D., & Simpson, S. J. (2019). Protein leverage: Theoretical foundations and ten points of clarification. Obesity, 27(8), 1225–1238.

[76] Studnitz, M., Jensen, M. B., & Pedersen, L. J. (2007). Why do pigs root and in what will they root? Applied Animal Behaviour Science, 107(3–4), 183–197.

[77] Ettle, T., & Roth, F. X. (2004). Specific dietary selection for tryptophan by the piglet. Journal of Animal Science, 82(4), 1115–1121.

[78] Ettle, T., & Roth, F. X. (2005). Dietary preferences for feeds varying in threonine concentration by the piglet. Physiology & Behavior, 85(3), 289–295.

[79] Ursinus, W. W., Van Reenen, C. G., Reimert, I., & Bolhuis, J. E. (2014). Tail biting in pigs: Blood serotonin and fearfulness as pieces of the Puzzle? PLoS One, 9(9), e107040.

[80] Meer, Y. V. D., Gerrits, W. J. J., Jansman, A. J. M., Kemp, B., & Bolhuis, J. E. (2017). A link between damaging behaviour in pigs, sanitary conditions, and dietary protein and amino acid supply. PLoS One, 12(5), e0174688.

[81] Terlouw, E. M. C., Wiersma, A., Lawrence, A. B., & Macleod, H. A. (1993). Ingestion of food facilitates the performance of stereotypies in sows. Animal Behaviour, 46(5), 939–950.

[82] Van Der Peet-Schwering, C. M. C., Spoolder, H. A. M., Kemp, B., Binnendijk, G. P., Den Hartog, L. A., & Verstegen, M. W. A. (2003). Development of stereotypic behaviour in sows fed a starch diet or a non-starch polysaccharide diet during gestation and lactation over two parities. Applied Animal Behaviour Science, 83(2), 81–97.

[83] Lawrence, A. B., & Terlouw, E. M. C. (1993). A review of behavioral factors involved in the development and continued performance of stereotypic behaviors in pigs. Journal of Animal Science, 71(10), 2815–2825.

[84] Aguayo-Ulloa, L. A., Villarroel, M., Pascual-Alonso, M., Miranda-de la Lama, G. C., & María, G. A. (2014). Finishing feedlot lambs in enriched pens using feeder ramps and straw and its influence on behavior and physiological welfare indicators. Journal of Veterinary Behavior, 9(6), 347–356.

[85] Zhang, J., Yu, L., & Yin, G. (2022). Evaluation of behavior and affective state of different-parity sows with strong/weak pupil light reflex. Animals, 12(9), 1184.

[86] Salak-Johnson, J. L., DeDecker, A. E., Horsman, M. J., & Rodriguez-Zas, S. L. (2012). Space allowance for gestating sows in pens: Behavior and immunity. Journal of Animal Science, 90(9), 3232–3242.

[87] Liu, H., Huang, X., Xu, J., Mao, H., Li, Y., Ren, K., Ma, G., Xue, Q., Tao, H., Wu, S., & Wang, W. (2021). Dissection of the relationship between anxiety and stereotyped self-grooming using the Shank3B mutant autistic model, acute stress model and chronic pain model. Neurobiology of Stress, 15, 100417.

[88] Liu, X., Song, P., Yan, H., Zhang, L., Wang, L., Zhao, F., Gao, H., Hou, X., Shi, L., Li, B., & Wang, L. (2021). A comparison of behavior, physiology, and offspring resilience of gestating sows when raised in a group housing system and individual stalls. Animals, 11(1), 2076.

[89] Riber, A. B., Tahamtani, F. M., & Steenfeldt, S. (2021). Effects of qualitative feed restriction in broiler breeder pullets on behaviour in the home environment. Applied Animal Behaviour Science, 235, 105225.

[90] Nielsen, B. L., Thodberg, K., Malmkvist, J., & Steenfeldt, S. (2011). Proportion of insoluble fibre in the diet affects behaviour and hunger in broiler breeders growing at similar rates. Animal, 5(8), 1247–1258.

[91] van Emous, R. A., Kwakkel, R., van Krimpen, M., & Hendriks, W. (2015). Effects of different dietary protein levels during rearing and different dietary energy levels during lay on behaviour and feather cover in broiler breeder females. Applied Animal Behaviour Science, 168, 45–55.

[92] de Jong, I. C., Enting, H., van Voorst, A., & Blokhuis, H. J. (2005). Do low-density diets improve broiler breeder welfare during rearing and laying? Poultry Science, 84(2), 194–203.

[93] van Emous, R. A., & Mens, A. J. W. (2021). Effects of twice a day feeding and split feeding during lay on broiler breeder production performance, eggshell quality, incubation traits, and behavior. Poultry Science, 100(11), 101419.

[94] McAuley, M., Buijs, S., Muns, R., Gordon, A., Palmer, M., Meek, K., & O’Connell, N. (2022). Effect of reduced dietary protein level on finishing pigs’ harmful social behaviour before and after an abrupt dietary change. Applied Animal Behaviour Science, 256, 105762.

[95] Taylor, N. R., Main, D. C. J., Mendl, M., & Edwards, S. A. (2010). Tail-biting: A new perspective. The Veterinary Journal, 186(2), 137–147.

[96] Asensio, X., Abdelli, N., Piedrafita, J., Soler, M. D., & Barroeta, A. C. (2020). Effect of fibrous diet and vitamin C inclusion on uniformity, carcass traits, skeletal strength, and behavior of broiler breeder pullets. Poultry Science, 99(5), 2633–2644.

[97] Zuidhof, M. J., Robinson, F. E., Feddes, J. J. R., Hardin, R. T., Wilson, J. L., Mckay, R. I., & Newcombe, M. (1995). The effects of nutrient dilution on the well-being and performance of female broiler breeders. Poultry Science, 74(3), 441–456.

[98] Hanis, F., Chung, E. L. T., Kamalludin, M. H., & Idrus, Z. (2020). Discovering the relationship between dietary nutrients and cortisol and ghrelin hormones in horses exhibiting oral stereotypic behaviors: A review. Journal of Veterinary Behavior, 39, 90–98.

[99] Leme, D. P., Parsekian, A. B. H., Kanaan, V., & Hötzel, M. J. (2014). Management, health, and abnormal behaviors of horses: A survey in small equestrian centers in Brazil. Journal of Veterinary Behavior, 9(3), 114–118.

[100] Hothersall, B., & Nicol, C. (2009). Role of diet and feeding in normal and stereotypic behaviors in horses. Veterinary Clinics of North America: Equine Practice, 25(1), 167–181.

[101] Whisher, L., Raum, M., Pina, L., Pérez, L., Erb, H., Houpt, C., & Houpt, K. (2011). Effects of environmental factors on cribbing activity by horses. Applied Animal Behaviour Science, 135(1-2), 63-69.

[102] Gillham, S. B., Dodman, N. H., Shuster, L., Kream, R., & Rand, W. (1994). The effect of diet on cribbing behavior and plasma β-endorphin in horses. Applied Animal Behaviour Science, 41(3-4), 147-153.

[103] Albright, J., Sun, X., & Houpt, K. (2017). Does cribbing behavior in horses vary with dietary taste or direct gastric stimuli? Applied Animal Behaviour Science, 189, 36–40.

[104] Hemmann, K., Ahonen, S., Raekallio, M., Vainio, O., & Lohi, H. (2014). Exploration of known stereotypic behaviour-related candidate genes in equine cirb-biting. Animal, 8(3), 347–353.

[105] Prebble, J. L., Langford, F. M., Shaw, D. J., & Meredith, A. L. (2015). The effect of four different feeding regimes on rabbit behaviour. Applied Animal Behaviour Science, 169, 86-92.

[106] Mulder, A., Nieuwenkamp, A. E., van der Palen, J. G., van Rooijen, G. H., & Beynen, A. C. (1992). Supplementary hay reduces fur chewing in rabbits. Tijdschrift voor Diergeneeskunde, 117(22), 655–658.

[107] Surridge, A. K., Bell, D. J., & Hewitt, G. M. (1999). From population structure to individual behaviour: Genetic analysis of social structure in the European wild rabbit (Oryctolagus cuniculus). Biological Journal of the Linnean Society, 68(1–2), 57–71.

[108] Verga, M., Luzi, F., & Carenzi, C. (2007). Effects of husbandry and management systems on physiology and behaviour of farmed and laboratory rabbits. Hormones and Behavior, 52(1), 122–129.

[109] Koolhaas, J. M., Bartolomucci, A., Buwalda, B., de Boer, S. F., Flügge, G., Korte, S. M., Meerlo, P., Murison, R., Olivier, B., Palanza, P., Richter-Levin, G., Sgoifo, A., Steimer, T., Stiedl, O., van Dijk, G., Wöhr, M., & Fuchs, E. (2011). Stress revisited: A critical evaluation of the stress concept. Neuroscience & Biobehavioral Reviews, 35(5), 1291–1301.

[110] Ijichi, C. L., Collins, L. M., & Elwood, R. W. (2013). Evidence for the role of personality in stereotypy predisposition. Animal Behaviour, 85(6), 1145–1151.

[111] Briefer Freymond, S., Bardou, D., Briefer, E. F., Bruckmaier, R., Fouché N., Fleury, J., Maigrot, A.-L., Ramseyer, A., Zuberbühler, K., & Bachmann, I. (2015). The physiological consequences of crib-biting in horses in response to an ACTH challenge test. Physiology & Behavior, 151, 121–128.

[112] Pell, S. M., & McGreevy, P. D. (1999). A study of cortisol and beta-endorphin levels in stereotypic and normal thoroughbreds. Applied Animal Behaviour Science, 64(2), 81–90.

[113] Clegg, H. A., Buckley, P., Friend, M. A., & McGreevy, P. D. (2008). The ethological and physiological characteristics of cribbing and weaving horses. Applied Animal Behaviour Science, 109(1), 68–76.

[114] Irvine, C. H., & Alexander, S. L. (1994). Factors affecting the circadian rhythm in plasma cortisol concentrations in the horse. Domestic Animal Endocrinology, 11(2), 227–238.

[115] McBride, S. D., & Cuddeford, D. (2001). The putative welfare-reducing effects of preventing equine stereotypic behaviour. Animal Welfare, 10(2), 173–189.

[116] Bachmann, I., Bernasconi, P., Herrmann, R., Weishaupt, M. A., & Stauffacher, M. (2003). Behavioural and physiological responses to an acute stressor in crib-biting and control horses. Applied Animal Behaviour Science, 82(4), 297–311.

[117] Anisman, H., & Matheson, K. (2005). Stress, depression, and anhedonia: Caveats concerning animal models. Neuroscience & Biobehavioral Reviews, 29(4-5), 525-546.

[118] Ruis, M. A. W., te Brake, J. H. A., van de Burgwal, J. A., de Jong, I. C., Blokhuis, H. J., & Koolhaas, J. M. (2000). Personalities in female domesticated pigs: Behavioural and physiological indications. Applied Animal Behaviour Science, 66(1–2), 31–47.

[119] Cooper, S. J., & Dourish, C. T. (1991). The neurobiology of stereotyped behaviour. International Clinical Psychopharmacology, 6(2), 128.

[120] Abdallah, L., Bonasera, S. J., Hopf, F. W., O’Dell, L., Giorgetti, M., Jongsma, M., Carra, S., Pierucci, M., Di Giovanni, G., Esposito, E., Parsons, L. H., Bonci, A., & Tecott, L. H. (2009). Impact of serotonin 2C receptor null mutation on physiology and behavior associated with nigrostriatal dopamine pathway function. Journal of Neuroscience, 29(25), 8156–8165.

[121] Giorgi, O., Piras, G., & Corda, M. G. (2007). The psychogenetically selected Roman high- and low-avoidance rat lines: A model to study the individual vulnerability to drug addiction. Neuroscience & Biobehavioral Reviews, 31(1), 148–163.

[122] Caramaschi, D., de Boer, S. F., & Koolhaas, J. M. (2007). Differential role of the 5-HT1A receptor in aggressive and non-aggressive mice: An across-strain comparison. Physiology & Behavior, 90(4), 590–601.

[123] Baribeau, D. A., Vigod, S., Pullenayegum, E., Kerns, C. M., Mirenda, P., Smith, I. M., Vaillancourt, T., Volden, J., Waddell, C., Zwaigenbaum, L., Bennett, T., Duku, E., Elsabbagh, M., Georgiades, S., Ungar, W. J., Zaidman-Zait, A., & Szatmari, P. (2020). Repetitive behavior Severity as an early indicator of risk for elevated anxiety symptoms in autism spectrum disorder. Journal of the American Academy of Child & Adolescent Psychiatry, 59(7), 890–899.e3.

[124] Baribeau, D. A., Vigod, S., Pullenayegum, E., Kerns, C. M., Mirenda, P., Smith, I. M., Vaillancourt, T., Volden, J., Waddell, C., Zwaigenbaum, L., Bennett, T., Duku, E., Elsabbagh, M., Georgiades, S., Ungar, W. J., Zaidman Zait, A., & Szatmari, P. (2021). Co-occurring trajectories of anxiety and insistence on sameness behaviour in autism spectrum disorder. British Journal of Psychiatry, 218(1), 20–27.

[125] Bolhuis, J. E., Schouten, W. G. P., Schrama, J. W., & Wiegant, V. M. (2006). Effects of rearing and housing environment on behaviour and performance of pigs with different coping characteristics. Applied Animal Behaviour Science, 101(1-2), 68-85.

[126] Farmer, A. L., & Lewis, M. H. (2023). Reduction of restricted repetitive behavior by environmental enrichment: Potential neurobiological mechanisms. Neuroscience & Biobehavioral Reviews, 152, 105291.

[127] Lewis, M. H., Lindenmaier, Z., Boswell, K., Edington, G., King, M. A., & Muehlmann, A. M. (2018). Subthalamic nucleus pathology contributes to repetitive behavior expression and is reversed by environmental enrichment. Genes, Brain and Behavior, 17(8), e12468.

[128] Bechard, A. R., Cacodcar, N., King, M. A., & Lewis, M. H. (2016). How does environmental enrichment reduce repetitive motor behaviors? Neuronal activation and dendritic morphology in the indirect basal ganglia pathway of a mouse model. Behavioural Brain Research, 299, 122–131.

[129] Bechard, A. R., Bliznyuk, N., & Lewis, M. H. (2017). The development of repetitive motor behaviors in deer mice: Effects of environmental enrichment, repeated testing, and differential mediation by indirect basal ganglia pathway activation. Developmental Psychobiology, 59(3), 390–399.

[130] Tanimura, Y., Vaziri, S., & Lewis, M. H. (2010). Indirect basal ganglia pathway mediation of repetitive behavior: Attenuation by adenosine receptor agonists. Behavioural Brain Research, 210(1), 116–122.

[131] Turner, C. A., Yang, M. C., & Lewis, M. H. (2002). Environmental enrichment: Effects on stereotyped behavior and regional neuronal metabolic activity. Brain Research, 938(1–2), 15–21.

[132] Turner, C. A., & Lewis, M. H. (2003). Environmental enrichment: Effects on stereotyped behavior and neurotrophin levels. Physiology & Behavior, 80(2–3), 259–266.

[133] Bernardino, T., Tatemoto, P., de Moraes, J. E., Morrone, B., & Zanella, A. J. (2021). High fiber diet reduces stereotypic behavior of gilts but does not affect offspring performance. Applied Animal Behaviour Science, 243, 105433.

[134] Bergeron, R., Badnell-Waters, A. J., Lambton, S., & Mason, G. (2006). Stereotypic oral behaviour in captive ungulates: Foraging, diet and gastrointestinal function. In G. Mason & J. Rushen (Eds.), Stereotypic animal behaviour: Fundamentals and applications to welfare [Internet] (2nd ed., pp. 19–57). CABI.

[135] Girard, M. T. E., Zuidhof, M. J., & Bench, C. J. (2017). Feeding, foraging, and feather pecking behaviours in precision-fed and skip-a-day-fed broiler breeder pullets. Applied Animal Behaviour Science, 188, 42–49.

[136] Horvath, K. C., & Miller-Cushon, E. K. (2017). The effect of milk-feeding method and hay provision on the development of feeding behavior and non-nutritive oral behavior of dairy calves. Journal of Dairy Science, 100(5), 3949–3957.

[137] Mirzaei, M., Khorvash, M., Ghorbani, G. R., Kazemi-Bonchenari, M., & Ghaffari, M. H. (2017). Growth performance, feeding behavior, and selected blood metabolites of Holstein dairy calves fed restricted amounts of milk: No interactions between sources of finely ground grain and forage provision. Journal of Dairy Science, 100(2), 1086–1094.

[138] Devant, M., Penner, G. B., Marti, S., Quintana, B., Fábregas, F., Bach, A., & Arís, A. (2016). Behavior and inflammation of the rumen and cecum in Holstein bulls fed high-concentrate diets with different concentrate presentation forms with or without straw supplementation. Journal of Animal Science, 94(9), 3902–3917.

[139] Montoro, C., Miller-Cushon, E. K., DeVries, T. J., & Bach, A. (2013). Effect of physical form of forage on performance, feeding behavior, and digestibility of Holstein calves. Journal of Dairy Science, 96(2), 1117–1124.

[140] Castells, L., Bach, A., Araujo, G., Montoro, C., & Terré M. (2012). Effect of different forage sources on performance and feeding behavior of Holstein calves. Journal of Dairy Science, 95(1), 286–293.

[141] Jiang, X., Lu, N., Xue, Y., Liu, S., Lei, H., Tu, W., Lu, Y., & Xia, D. (2019). Crude fiber modulates the fecal microbiome and steroid hormones in pregnant Meishan sows. General and Comparative Endocrinology, 277, 141–147.

[142] Souza da Silva, C., Bolhuis, J. E., Gerrits, W. J. J., Kemp, B., & van den Borne, J. J. G. C. (2013). Effects of dietary fibers with different fermentation characteristics on feeding motivation in adult female pigs. Physiology & Behavior, 110(111), 148–157.

RIGHTS & PERMISSIONS

2024 The Authors. Animal Research and One Health published by John Wiley & Sons Australia, Ltd on behalf of Institute of Animal Science, Chinese Academy of Agricultural Sciences.