Neurological modulation of facial expressions in pigs and implications for production

Daniel Mota-Rojas; Agustín Orihuela; Julio Martínez-Burnes; Jocelyn Gómez; Patricia Mora-Medina; Belen Alavez; Luisa Ramírez; Miguel González-Lozano

doi:10.31893/jabb.20031

Keywords:

Abstract

The facial expressions of animals constitute a means of manifesting emotions, fulfilling functions related to social interactions in several species. Interest has come to use facial expressions as a tool for predicting intentions; in the case of aggression, for example, impeding attacks between individuals prevents negative economic and emotional impacts. Recent research has sought to associate facial expressions with painful events as tail-cropping and castration on the assumption that objective evaluations of the presence or absence of grimaces in pigs’ snouts may allow us to determine the intensity of the pain they perceive. Furthermore, to continue developing scales that will complement the existing piglet grimace scale (PGS), which is not yet fully-validated in terms of reliability. Another area of research is interpreting expressions of fear during traumatic events like pre-slaughter handling. Also, the phenomenon of emotional contagion in groups of animals suggests the need to focus on their emotions, since recognizing them could allow us to prevent alterations of meat quality. These approaches reveal the need for a detailed compilation of the facial expressions of pigs based on current scientific literature regarding emotions, alimentation, and pain-related behavioral responses in pigs.
References
1. Becerril-Herrera M, Alonso-Spilsbury M, Lemus-Flores C, Guerrero-Legarreta I, Olmos-Hernández A, Ramírez-Necoechea R, Mota-Rojas D (2009) CO2 stunning may compromise pigs welfare compared with electrical stunning. Meat Science 81:233-237.
2. Bennett V, Gourkow N, Mills DS (2017) Facial correlates of emotional behaviour in the domestic cat (Felis catus). Behavioural Processes 141:342-350.
3. Boissy A, Manteuffel G, Jensen M, Oppermann R, Spruijt B, Keeling L, Aubert A (2007) Assessment of positive emotions in animals to improve their welfare. Physiology and Behavior 92:375-397.
4. Boumans I, Bokkers E, Hofstede G, & De Boer I. (2015) Understanding feeding patterns in growing pigs by modelling growth and motivation. Applied Animal Behaviour Science 171:69-80.
5. Boumans I, De Boer I, Hofstede G, & Bokkers E (2018) How social factors and behavioural strategies affect feeding and social interaction patterns in pigs. Physiology and Behavior 194:23-40.
6. Brown S, Knowles T, Wilkins L, Chadd S, Warriss P (2005) The response of pigs to being loaded or unloaded onto commercial animal transporters using three systems. The Veterinary Journal 170:91-100.
7. Brown S, Klaffenbock M, Macleod I, Burnett A (2015) Evidence for litter differences in play behaviour in pre-weaned pigs. Applied Animal Behaviour Science 172: 17-25.
8. Bruce LL, Neary T J (1995) The limbic system of tetrapodes: a comparative analysis of cortical and amygdala populations. Brain, Behavior and Evolution 46:224-34.
9. Brudzynski SM (2010) Communication of Emotions in Animals. Encyclopedia of Behavioral 1:302-307.
10. Caeiro CC, Burrows AM, Waller BM (2017) Development and application of CatFACS: are human cat adopters influenced by cat facial expressions?. Applied Animal Behaviour Science 189:66-78.
11. Camerlink I, Coulange E, Farish M, Baxter EM, Turner SP (2018) Facial expression as a potential measure of both intent and emotion. Scientific Reports 8:1-9.
12. Carcò G, Dalla M, Carraro L, Latorre M, Fondevila M, Gallo L, Schiavon S (2018) Influence of mild feed restriction and mild reduction in dietary amino acid content on feeding behaviour of group-housed growing pigs. Applied Animal Behaviour Science 198: 27-35.
13. Dalla-Costa E, Minero M, Lebelt D, Stucke D, Canali E, Leach MC (2014) Development of the horse grimace scale (HGS) as a pain assessment tool in horses undergoing routine castration. PLOS ONE 9:e92281.
14. Darwin C (1872) The expression of the emotions in man and animals (1st ed). London, John Murray, Albemarle street 1872.
15. Descovich K, Wathan J, Leach M, Buchanan-Smith H, Flecknell P, Farningham D, Vick, SJ (2017) Facial expression: An under-utilized tool for the assessment of welfare in mammals. ALTEX 34:409-29.
16. Di Giminiani P, Brierley VL, Scollo A, Gottardo F, Malcolm EM, Edwards SA, Leach MC (2016) The Assessment of facial expressions in piglets undergoing tail docking and castration: toward the development of the piglet grimace scale Frontiers in Veterinary Science 3:100.
17. Dyce KM, Sack WO, Wensing CJG (2010) Anatomia Veterinaria. México, McGraw-Hill.
18. Edgar J, Lowe J, Paul E, Nicol C, (2011) Respuesta materna aviar a la angustia de los pollitos. Proceedings of the Royal Society B. Biological Science 278:3129-3134.
19. Farb CR, LeDoux JE (1998) NMDA and AMPA receptors in the lateral nucleus of the amygdala are postsynaptic to auditory thalamic afferents. Synapse 27:106-21.
20. Ekman P, Friesen W (1978) Facial Action Coding System: a Technique for the Measurement of Facial Movement. CA: Consulting Psychologists Press, Palo Alto.
21. Figueroa J, Solá-Oriol D, Manteca X, Pérez J, Dwyer D (2015) Anhedonia in pigs? Effects of social stress and restraint stress on sucrose preference. Physiology and Behavior 151:509-515.
22. Finka LR, Luna SP, Brondani JT, Tzimiropoulos Y, McDonagh J, Farnworth MJ, Mills DS (2019) Geometric morphometrics for the study of facial expressions in non-human animals, using the domestic cat as an exemplar. Scientific Reports 9:9883.
23. Flecknell P, Leach M, Bateson M (2011) Affective state and quality of life in mice. Pain 152:963-964.
24. Flores-Peinado S, Mota-Rojas D, Guerrero-Legarreta I, Mora-Medina P, Cruz-Monterrosa R, Gómez J, Hernández MA, Cruz-Playas J, Martínez-Burnes J (2020) Pre-slaughter stress in pigs, infrared thermography assessment and meat quality. International Journal of Animal Science and Medicine 8:(Accepted).
25. Forkman B, Boissy A, Meunier-Salaün M, Canali E, Jones R (2007) A critical review of fear tests used on cattle, pigs, sheep, poultry and horses. Physiology and Behavior 92:340-374.
26. Frías D 2015 Evaluación de métodos utilizados para medir la palatabilidad en cerdos de recría. MV Thesis, Universidad de Chile, Chile.
27. Fridlund AJ (1994) Human facial expression: An evolutionary view. USA, Academic Press.
28. Friel M, Kunc, HP, Griffin K, Asher L, Collins LM (2019) Positive and negative contexts predict duration of pig vocalisations. Scientific Reports 9:2062.
29. Gleerup KB, Forkman B, Lindegaard C, Andersen PH (2015) An equine pain face. Veterinary Anaesthesia and Analgesia 42:103-114.
30. González-Lozano M, Mota-Rojas D, Orihuela A, Martínez-Burnes J, Di Francia, Braghieri A, Berdugo GJ, Mora MP, Ramírez NR, Napolitano F (2020) Behavioral, physiological and reproductive performance in buffaloes during eutocic and dystocic parturitions. Applied Animal Science 36:407–422.
31. Gray JA (1991) The Neuropsychology of Temperament. In Strelau, J., & Angleitner, A., (Eds.). Explorations in Temperament. Perspectives on Individual Differences (pp. 105-128). Boston: Springer.
32. Häger C, Biernot S, Buettner M, Glage S, Keubler LM, Held N, Bleich EM, Otto K, Müller CW, Decker S, Talbot SR, Bleich A (2017) The Sheep Grimace Scale as an indicator of post-operative distress and pain in laboratory sheep. Plos One
33. Herskin MS, Di Giminiani P (2018) Pain in pigs: characterisation, mechanisms and indicators. Advances in Pig Welfare 325-355.
34. Holden E, Calvo G, Collins M, Bell A, Reid J, Scott EM, Nolan AM (2014) Evaluation of facial expression in acute pain in cats. Journal of Small Animal Practice 55:615-21.
35. Hernández-Avalos I, Mota-Rojas D, Mora-Medina P, Martínez-Burnes J, Casas-Alvarado A, Verduzco-Mendoza A, Lezama-García K, Olmos-Hernández A (2019) Review of different methods used for clinical recognition and assessment of pain in dogs and cats. International Journal of Veterinary Science and Medicine 7:43-54.
36. Horstmann G (2003) What do facial expressions convey: Feeling states, behavioral intentions, or actions requests? Emotion 3:150-166.
37. Iglesias S, Del Castillo A, Muñoz J (2016) Reconocimiento facial de expresión emocional: diferencias por licenciaturas. Acta de Investigación Psicológica 6:2494-2499.
38. Julle-Danière É, Micheletta J, Whitehouse J, Joly M, Gass C, Burrows AM, Waller BM (2015) MaqFACS (Macaque Facial Action Coding System) can be used to document facial movements in Barbary macaques (Macaca sylvanus). PeerJ 3:e1248.
39. Keating SCJ, Thomas AA, Flecknell PA, Leach MC (2012) Evaluation of EMLA Cream for Preventing Pain during Tattooing of Rabbits: Changes in Physiological, Behavioural and Facial Expression Responses. PLOS ONE 7:e44437.
40. Krugmann K, Warken F, Krieter J, Cyzcholl I (2019) Are behavioral test capable of measuring positive affective states in growing pigs? Animals 9:274.
41. Lane S. M, Briffa, M (2017) The price of attack: rethinking damage costs in animal contests. Animal Behaviour 126:23-29.
42. Langford DJ, Bailey AL, Chanda ML, Clarke SE, Drummond TE, Echols S, Glick S, Ingrao J, Klassen-Ross T, LaCroix-Fralish ML, Matsumiya L, Sorge RE, Sotocinal SG, Tabaka JM, Wong DM, van den Maagdenberg AMJ, Ferrari MD, Craig KD, Mogil JS (2010) Coding of facial expressions of pain in the laboratory mouse. Nature Methods 7:447-449.
43. Leliveld L, Pupjan S, Tuchdcherer A, Puppe B (2016) Behaviural and physiological measures indicate subtle variations in the emotional valence of young pigs. Physiology andBehavior 157:116-124. htt
44. Lezama-García K, Orihuela A, Olmos-Hernández A, Reyes-Long S, Mota-Rojas D (2019a) Invited review: Facial expressions and emotions in domestic animals. CAB Reviews 14:1-12.
45. Lezama-García K, Maiti Ch, Mota-Rojas D, Martínez-Burnes J., Barrios-García H, Gazzano A (2019b) Maternal behaviour in domestic dogs. International Journal of Veterinary Science and Medicine 7:20–30.
46. Manteca X, Temple D, Mainau E, Llonch P (2017) Assessment of pain in sheep. The Farm Animal Welfare Fact Sheet. FAWEC-Farm Animal Welfare Education Centre. 17.
47. Marcet-Rius M, Pageat P, Bienboire-Frosini C, Teruel E, Monneret P, Leclercq J, Lafont-Lecuelle C, Cozzi A (2018) Tail and ear movements as possible indicators of emotions in pigs. Applied Animal Behaviour Science 205:14-18.
48. Marcet-Rius M, Fábrega E, Cozzi A, Bienboire-Frosini C, Descout E, Velarde A, Pageat P (2019a) Are tail and ear movements indicators of emotions in tail-docked pigs in response to environment enrichment? Animals 9:449.
49. Marcet-Rius M, Kalonji G, Cozzi A, Bienboire-Frosini C, Monneret P, Kowalczyk I, Teruel E, Codecasa E. Pageat P (2019b) Effects of straw provision, as environment enrichment, on behavioural indicators of welfare and emotions in pig reared in an experimental system. Livestock Science 21:89-94.
50. Maselyne J, Saeys W, Van Nuffel A (2015) Review: Quantifying animal feeding behaviour with a focus on pigs. Physiology and Behavior 138:37-51.
51. McLennan K (2018) Why pain is still a welfare issue for farm animals, and how facial expression could be the answer. Agriculture 8:127.
52. McLennan KM, Miller AL, Dalla Costa E, Stucke D, Corke MJ, Broom DM, Leach MC (2019) Conceptual and methodological issues relating to pain assessment in mammals: The development and utilisation of pain facial expression scales. Applied Animal Behaviour Science 217:1-15.
53. Merskey H, Bogduk N (1994) Classification of chronic pain: descriptions of chronic pain syndromes and definitions of pain terms (2nd ed.). Seattle, IASP Press.
54. Mellor DJ (2012) Animal emotions, behaviour and the promotion of positive welfare states. New Zealand and Veterinary Journal 60:1-8.
55. Mellor D, Beausoleil N (2015) Extending the ‘Five Domains’ model for animal welfare assessment to incorporate positive welfare states. Animal Welfare 24:241–53.
56. Molero A, 2007 Aprendizaje aversivo gustativo: Características, paradigma y mecanismos cerebrales. Anales de Psicología-Spain 23:57-64.
57. Mota-Rojas D, Becerril M, Lemus C, Sanchez P, Gonzalez M, Olmos SA, Ramirez R, Alonso-Spilsbury M (2006) Effects of mid-summer transport duration on pre- and post-slaughter performance and pork quality in Mexico. Meat Science 73:404-412.
58. Mota-Rojas D, Becerril-Herrera M, Alonso-Spilsbury M, Flores-Peinado S, Ramírez-Necoechea R, Ramírez JA, Mora-Medina, Soní E, Trujillo-Ortega ME (2012) Effects of long distance transport and CO2 stunning on critical blood values in pigs. Meat Science 90:893-898.
59. Mota-Rojas D, Velarde A, Maris-Huertas S, Cajiao PMN (2016). Editors. In: Animal welfare, a global vision in Ibero-America. [Bienestar Animal una visión global en Iberoamérica]. 3rd ed. Barcelona, Spain. Elsevier; p. 516.
60. Mota-Rojas D, López A, Martínez-Burnes J, Muns R, Villanueva-García D, Mora-Medina P, Gonzalez-Lozano M, Olmos HA, and Ramírez NR (2018a). Invited review: Is vitality assessment important in neonatal animals? CAB Reviews 13(036):1–13.
61. Mota-Rojas D, Orihuela A, Strappini-Asteggiano A, Cajiao PMN, Aguera-Buendia E, Ghezzi M, Alonso, SML (2018b) Teaching animal welfare in veterinary schools in Latin America. International Journal of Animal Science and Medicine 6:131–40.
62. Mota-Rojas D, Lezama GK, Alavez VB, Flores PK, González LC, Morales FL, Nava AJ, Mora-Medina P (2018c). The language of animals: importance of the tail and ears. Agro Meat, Buenos Aires, Argentina. Dic, 2018. p.1-10.
63. Mota-Rojas D, Martínez-Burnes J, Napolitano F, Domínguez MM, Guerrero LI, Mora-Medina P, Ramírez NR, Lezama GK, González-Lozano M (2020a) Invited review: Dystocia: Factors affecting parturition in domestic animals. CAB Rev. 15:1–14.
64. Mota-Rojas D, Broom DM, Orihuela A, Velarde A, Napolitano F, Alonso-Spilsbury M (2020b) Effects of human-animal relationship on animal productivity and welfare. Journal of Animal Behaviour and Biometeorology 8:196-205.
65. Müller BR, Souza SV, Biscarra-Bellio JC, Maiolino-Molento CF (2019) Facial expression of pain in Nellore and Crossbred beef cattle. Journal of Veterinary Behavior 34:60-65.
66. Murphy E, Nordquist R, Van der Staay F (2014) A review of behavioural methods to study emotion and mood in pigs, Sus scrofa. Applied Animal Behaviour Science 159:9-28.
67. Nalon E, Maes D, Piepers S, Taylor P, Van Riet MMJ, Janssens GPJ, Tuyttens FAM (2015) Factors affecting mechanical nociceptive thresholds in healthy sows. Veterinary Anaesthesia and Analgesia
68. Núñez V 2015 Estudio de palatabilidad en cerdos de recría en base a soluciones de glutamato monosódico. MV Thesis, Universidad de Chile, Chile.
69. Orihuela A, Mota-Rojas D, Velarde A, Strappini-Asteggiano A, Thielo de la Vega L, Borderas-Tordesillas F, Alonso-Spilsbury M (2018) Invited review: environmental enrichment to improve behaviour in farm animals. CAB Reviews 13:1–25.
70. Parr L, Waller B, Burrows A, Gothard K, Vick S (2010) MaqFACS: a muscle-based facial movement coding system for the Rhesus macaque. American Journal of Physical Anthropology 143:625-630.
71. Parr LA, Waller BM, Vick SJ, Bard KA (2007) Classifying chimpanzee facial expressions using muscle action. Emotion 7:172.
72. Paul E, Harding E, Mendl M (2005) Measuring emotional processes in animals: the utility of a cognitive approach. Neuroscience Biobehavioral Reviews 29:469-491.
73. Paul E, Mendl M (2018) Animal emotion: Descriptive and prescriptive definitions and their implications for a comparative perspective. Applied Animal Behaviour Science 205:202-209.
74. Reimert I, Bolhuis E, Rodenburg B (2013) Indicators of positive and negative emotions and emotional contagion in pigs. Physiology Behaviour 109:42-50.
75. Rolls T (2000) The Brain Emotion. Trends in Cognitive Sciences, Cambridge University Press, 3:281- 282.
76. Rutherford KMD (2002) Assessing pain in animals. Animal Welfare 11:31-53.
77. Sneddon LU, Elwood RW, Adamo SA, Leach MC (2014) Defining and assessing animal pain. Animal Behaviour 97:201-212.
78. Sotocinal SG, Sorge RE, Zaloum A, Tuttle AH, Martin LJ, Wieskopf JS, Mapplebeck JCS, Wei P, Zhan S, Zhang S, McDougall JJ, King OD, Mogil JS (2011) The Rat Grimace Scale: A Partially Automated Method for Quantifying Pain in the Laboratory Rat via Facial Expressions. Molecular Pain 7:55.
79. Rutherford KMD, Donald RD, Lawrence AB, Wemelsfelder F (2012) Qualitative Behavioural Assessment of emotionality in pigs. Applied Animal Behaviour Science 139:218-224.
80. Temple D, Manteca X, Velarde A, Dalmau A (2011) Assessment of animal welfare through behavioural parameters in Iberian pigs in intensive and extensive conditions. Applied Animal Behaviour Science 131:29-39.
81. Tuttle AH, Molinaro MJ, Jethwa JF, Sotocinal SG, Prieto JC, Styner MA, Mogil JS, Zylka MJ (2018) A deep neural network to assess spontaneous pain from mouse facial expressions. Molecular Pain 14:1-19.
82. Van de Perre V, Permentier L, De Bie S, Verbeke G, Geers G (2010) Effect of unloading, lairage, pig handling, stunning and season on pH of pork. Meat Science 86:931-937.
83. Vermeulen L, Van de Perre V, Permentier L, De Bie S, Verbeke G, Geers R (2015) Pre-slaughter handling and pork quality. Meat Science 100:118-123.
84. Viscardi AV, Hunniford M, Lawlis P, Leach M, Turner PV (2017) Development of a piglet grimace scale to evaluate piglet pain using facial expressions following castration and tail docking: a pilot study. Frontiers in Veterinary Science 4:51.
85. Viscardi AV, Turner PV (2018) Efficacy of buprenorphine for management of surgical castration pain in piglets. BMC Veterinary Research 14:318.
86. Waller BM, Whitehouse J, Micheletta J (2017) Rethinking primate facial expression: A predictive framework. Neuroscience Biobehavioral Reviews 82:13-21.
87. Waller BM, Julle-Daniere E, Micheletta J (2020) Measuring the evolution of facial ‘expression’ using multi-species FACS. Neuroscience Biobehavioral Reviews 113:1-11.
88. Wathan J, Burrows AM, Waller BM, McComb K (2015) EquiFACS: the equine facial action coding system. Plos One 10:e0137818.
89. Whittaker AL, Howarth GS (2014) Use of spontaneous behaviour measures to assess pain in laboratory rats and mice: How are we progressing? Applied Animal Behaviour Science 151:1–12.
90. Whittaker AL, Marsh LE (2019) The role of behavioural assessment in determining ‘positive’ affective states in animals. CAB Reviews 14:1-13.

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How to cite

Mota-Rojas, D., Orihuela, A., Martínez-Burnes, J., Gómez, J., Mora-Medina, P., Alavez, B., Ramírez, L., & González-Lozano, M. (2020). Neurological modulation of facial expressions in pigs and implications for production. Journal of Animal Behaviour and Biometeorology, 8(4), 232–243. https://doi.org/10.31893/jabb.20031

[1] Becerril-Herrera M, Alonso-Spilsbury M, Lemus-Flores C, Guerrero-Legarreta I, Olmos-Hernández A, Ramírez-Necoechea R, Mota-Rojas D (2009) CO2 stunning may compromise pigs welfare compared with electrical stunning. Meat Science 81:233-237.

[2] Bennett V, Gourkow N, Mills DS (2017) Facial correlates of emotional behaviour in the domestic cat (Felis catus). Behavioural Processes 141:342-350.

[3] Boissy A, Manteuffel G, Jensen M, Oppermann R, Spruijt B, Keeling L, Aubert A (2007) Assessment of positive emotions in animals to improve their welfare. Physiology and Behavior 92:375-397.

[4] Boumans I, Bokkers E, Hofstede G, & De Boer I. (2015) Understanding feeding patterns in growing pigs by modelling growth and motivation. Applied Animal Behaviour Science 171:69-80.

[5] Boumans I, De Boer I, Hofstede G, & Bokkers E (2018) How social factors and behavioural strategies affect feeding and social interaction patterns in pigs. Physiology and Behavior 194:23-40.

[6] Brown S, Knowles T, Wilkins L, Chadd S, Warriss P (2005) The response of pigs to being loaded or unloaded onto commercial animal transporters using three systems. The Veterinary Journal 170:91-100.

[7] Brown S, Klaffenbock M, Macleod I, Burnett A (2015) Evidence for litter differences in play behaviour in pre-weaned pigs. Applied Animal Behaviour Science 172: 17-25.

[8] Bruce LL, Neary T J (1995) The limbic system of tetrapodes: a comparative analysis of cortical and amygdala populations. Brain, Behavior and Evolution 46:224-34.

[9] Brudzynski SM (2010) Communication of Emotions in Animals. Encyclopedia of Behavioral 1:302-307.

[10] Caeiro CC, Burrows AM, Waller BM (2017) Development and application of CatFACS: are human cat adopters influenced by cat facial expressions?. Applied Animal Behaviour Science 189:66-78.

[11] Camerlink I, Coulange E, Farish M, Baxter EM, Turner SP (2018) Facial expression as a potential measure of both intent and emotion. Scientific Reports 8:1-9.

[12] Carcò G, Dalla M, Carraro L, Latorre M, Fondevila M, Gallo L, Schiavon S (2018) Influence of mild feed restriction and mild reduction in dietary amino acid content on feeding behaviour of group-housed growing pigs. Applied Animal Behaviour Science 198: 27-35.

[13] Dalla-Costa E, Minero M, Lebelt D, Stucke D, Canali E, Leach MC (2014) Development of the horse grimace scale (HGS) as a pain assessment tool in horses undergoing routine castration. PLOS ONE 9:e92281.

[14] Darwin C (1872) The expression of the emotions in man and animals (1st ed). London, John Murray, Albemarle street 1872.

[15] Descovich K, Wathan J, Leach M, Buchanan-Smith H, Flecknell P, Farningham D, Vick, SJ (2017) Facial expression: An under-utilized tool for the assessment of welfare in mammals. ALTEX 34:409-29.

[16] Di Giminiani P, Brierley VL, Scollo A, Gottardo F, Malcolm EM, Edwards SA, Leach MC (2016) The Assessment of facial expressions in piglets undergoing tail docking and castration: toward the development of the piglet grimace scale Frontiers in Veterinary Science 3:100.

[17] Dyce KM, Sack WO, Wensing CJG (2010) Anatomia Veterinaria. México, McGraw-Hill.

[18] Edgar J, Lowe J, Paul E, Nicol C, (2011) Respuesta materna aviar a la angustia de los pollitos. Proceedings of the Royal Society B. Biological Science 278:3129-3134.

[19] Farb CR, LeDoux JE (1998) NMDA and AMPA receptors in the lateral nucleus of the amygdala are postsynaptic to auditory thalamic afferents. Synapse 27:106-21.

[20] Ekman P, Friesen W (1978) Facial Action Coding System: a Technique for the Measurement of Facial Movement. CA: Consulting Psychologists Press, Palo Alto.

[21] Figueroa J, Solá-Oriol D, Manteca X, Pérez J, Dwyer D (2015) Anhedonia in pigs? Effects of social stress and restraint stress on sucrose preference. Physiology and Behavior 151:509-515.

[22] Finka LR, Luna SP, Brondani JT, Tzimiropoulos Y, McDonagh J, Farnworth MJ, Mills DS (2019) Geometric morphometrics for the study of facial expressions in non-human animals, using the domestic cat as an exemplar. Scientific Reports 9:9883.

[23] Flecknell P, Leach M, Bateson M (2011) Affective state and quality of life in mice. Pain 152:963-964.

[24] Flores-Peinado S, Mota-Rojas D, Guerrero-Legarreta I, Mora-Medina P, Cruz-Monterrosa R, Gómez J, Hernández MA, Cruz-Playas J, Martínez-Burnes J (2020) Pre-slaughter stress in pigs, infrared thermography assessment and meat quality. International Journal of Animal Science and Medicine 8:(Accepted).

[25] Forkman B, Boissy A, Meunier-Salaün M, Canali E, Jones R (2007) A critical review of fear tests used on cattle, pigs, sheep, poultry and horses. Physiology and Behavior 92:340-374.

[26] Frías D 2015 Evaluación de métodos utilizados para medir la palatabilidad en cerdos de recría. MV Thesis, Universidad de Chile, Chile.

[27] Fridlund AJ (1994) Human facial expression: An evolutionary view. USA, Academic Press.

[28] Friel M, Kunc, HP, Griffin K, Asher L, Collins LM (2019) Positive and negative contexts predict duration of pig vocalisations. Scientific Reports 9:2062.

[29] Gleerup KB, Forkman B, Lindegaard C, Andersen PH (2015) An equine pain face. Veterinary Anaesthesia and Analgesia 42:103-114.

[30] González-Lozano M, Mota-Rojas D, Orihuela A, Martínez-Burnes J, Di Francia, Braghieri A, Berdugo GJ, Mora MP, Ramírez NR, Napolitano F (2020) Behavioral, physiological and reproductive performance in buffaloes during eutocic and dystocic parturitions. Applied Animal Science 36:407–422.

[31] Gray JA (1991) The Neuropsychology of Temperament. In Strelau, J., & Angleitner, A., (Eds.). Explorations in Temperament. Perspectives on Individual Differences (pp. 105-128). Boston: Springer.

[32] Häger C, Biernot S, Buettner M, Glage S, Keubler LM, Held N, Bleich EM, Otto K, Müller CW, Decker S, Talbot SR, Bleich A (2017) The Sheep Grimace Scale as an indicator of post-operative distress and pain in laboratory sheep. Plos One

[33] Herskin MS, Di Giminiani P (2018) Pain in pigs: characterisation, mechanisms and indicators. Advances in Pig Welfare 325-355.

[34] Holden E, Calvo G, Collins M, Bell A, Reid J, Scott EM, Nolan AM (2014) Evaluation of facial expression in acute pain in cats. Journal of Small Animal Practice 55:615-21.

[35] Hernández-Avalos I, Mota-Rojas D, Mora-Medina P, Martínez-Burnes J, Casas-Alvarado A, Verduzco-Mendoza A, Lezama-García K, Olmos-Hernández A (2019) Review of different methods used for clinical recognition and assessment of pain in dogs and cats. International Journal of Veterinary Science and Medicine 7:43-54.

[36] Horstmann G (2003) What do facial expressions convey: Feeling states, behavioral intentions, or actions requests? Emotion 3:150-166.

[37] Iglesias S, Del Castillo A, Muñoz J (2016) Reconocimiento facial de expresión emocional: diferencias por licenciaturas. Acta de Investigación Psicológica 6:2494-2499.

[38] Julle-Danière É, Micheletta J, Whitehouse J, Joly M, Gass C, Burrows AM, Waller BM (2015) MaqFACS (Macaque Facial Action Coding System) can be used to document facial movements in Barbary macaques (Macaca sylvanus). PeerJ 3:e1248.

[39] Keating SCJ, Thomas AA, Flecknell PA, Leach MC (2012) Evaluation of EMLA Cream for Preventing Pain during Tattooing of Rabbits: Changes in Physiological, Behavioural and Facial Expression Responses. PLOS ONE 7:e44437.

[40] Krugmann K, Warken F, Krieter J, Cyzcholl I (2019) Are behavioral test capable of measuring positive affective states in growing pigs? Animals 9:274.

[41] Lane S. M, Briffa, M (2017) The price of attack: rethinking damage costs in animal contests. Animal Behaviour 126:23-29.

[42] Langford DJ, Bailey AL, Chanda ML, Clarke SE, Drummond TE, Echols S, Glick S, Ingrao J, Klassen-Ross T, LaCroix-Fralish ML, Matsumiya L, Sorge RE, Sotocinal SG, Tabaka JM, Wong DM, van den Maagdenberg AMJ, Ferrari MD, Craig KD, Mogil JS (2010) Coding of facial expressions of pain in the laboratory mouse. Nature Methods 7:447-449.

[43] Leliveld L, Pupjan S, Tuchdcherer A, Puppe B (2016) Behaviural and physiological measures indicate subtle variations in the emotional valence of young pigs. Physiology andBehavior 157:116-124. htt

[44] Lezama-García K, Orihuela A, Olmos-Hernández A, Reyes-Long S, Mota-Rojas D (2019a) Invited review: Facial expressions and emotions in domestic animals. CAB Reviews 14:1-12.

[45] Lezama-García K, Maiti Ch, Mota-Rojas D, Martínez-Burnes J., Barrios-García H, Gazzano A (2019b) Maternal behaviour in domestic dogs. International Journal of Veterinary Science and Medicine 7:20–30.

[46] Manteca X, Temple D, Mainau E, Llonch P (2017) Assessment of pain in sheep. The Farm Animal Welfare Fact Sheet. FAWEC-Farm Animal Welfare Education Centre. 17.

[47] Marcet-Rius M, Pageat P, Bienboire-Frosini C, Teruel E, Monneret P, Leclercq J, Lafont-Lecuelle C, Cozzi A (2018) Tail and ear movements as possible indicators of emotions in pigs. Applied Animal Behaviour Science 205:14-18.

[48] Marcet-Rius M, Fábrega E, Cozzi A, Bienboire-Frosini C, Descout E, Velarde A, Pageat P (2019a) Are tail and ear movements indicators of emotions in tail-docked pigs in response to environment enrichment? Animals 9:449.

[49] Marcet-Rius M, Kalonji G, Cozzi A, Bienboire-Frosini C, Monneret P, Kowalczyk I, Teruel E, Codecasa E. Pageat P (2019b) Effects of straw provision, as environment enrichment, on behavioural indicators of welfare and emotions in pig reared in an experimental system. Livestock Science 21:89-94.

[50] Maselyne J, Saeys W, Van Nuffel A (2015) Review: Quantifying animal feeding behaviour with a focus on pigs. Physiology and Behavior 138:37-51.

[51] McLennan K (2018) Why pain is still a welfare issue for farm animals, and how facial expression could be the answer. Agriculture 8:127.

[52] McLennan KM, Miller AL, Dalla Costa E, Stucke D, Corke MJ, Broom DM, Leach MC (2019) Conceptual and methodological issues relating to pain assessment in mammals: The development and utilisation of pain facial expression scales. Applied Animal Behaviour Science 217:1-15.

[53] Merskey H, Bogduk N (1994) Classification of chronic pain: descriptions of chronic pain syndromes and definitions of pain terms (2nd ed.). Seattle, IASP Press.

[54] Mellor DJ (2012) Animal emotions, behaviour and the promotion of positive welfare states. New Zealand and Veterinary Journal 60:1-8.

[55] Mellor D, Beausoleil N (2015) Extending the ‘Five Domains’ model for animal welfare assessment to incorporate positive welfare states. Animal Welfare 24:241–53.

[56] Molero A, 2007 Aprendizaje aversivo gustativo: Características, paradigma y mecanismos cerebrales. Anales de Psicología-Spain 23:57-64.

[57] Mota-Rojas D, Becerril M, Lemus C, Sanchez P, Gonzalez M, Olmos SA, Ramirez R, Alonso-Spilsbury M (2006) Effects of mid-summer transport duration on pre- and post-slaughter performance and pork quality in Mexico. Meat Science 73:404-412.

[58] Mota-Rojas D, Becerril-Herrera M, Alonso-Spilsbury M, Flores-Peinado S, Ramírez-Necoechea R, Ramírez JA, Mora-Medina, Soní E, Trujillo-Ortega ME (2012) Effects of long distance transport and CO2 stunning on critical blood values in pigs. Meat Science 90:893-898.

[59] Mota-Rojas D, Velarde A, Maris-Huertas S, Cajiao PMN (2016). Editors. In: Animal welfare, a global vision in Ibero-America. [Bienestar Animal una visión global en Iberoamérica]. 3rd ed. Barcelona, Spain. Elsevier; p. 516.

[60] Mota-Rojas D, López A, Martínez-Burnes J, Muns R, Villanueva-García D, Mora-Medina P, Gonzalez-Lozano M, Olmos HA, and Ramírez NR (2018a). Invited review: Is vitality assessment important in neonatal animals? CAB Reviews 13(036):1–13.

[61] Mota-Rojas D, Orihuela A, Strappini-Asteggiano A, Cajiao PMN, Aguera-Buendia E, Ghezzi M, Alonso, SML (2018b) Teaching animal welfare in veterinary schools in Latin America. International Journal of Animal Science and Medicine 6:131–40.

[62] Mota-Rojas D, Lezama GK, Alavez VB, Flores PK, González LC, Morales FL, Nava AJ, Mora-Medina P (2018c). The language of animals: importance of the tail and ears. Agro Meat, Buenos Aires, Argentina. Dic, 2018. p.1-10.

[63] Mota-Rojas D, Martínez-Burnes J, Napolitano F, Domínguez MM, Guerrero LI, Mora-Medina P, Ramírez NR, Lezama GK, González-Lozano M (2020a) Invited review: Dystocia: Factors affecting parturition in domestic animals. CAB Rev. 15:1–14.

[64] Mota-Rojas D, Broom DM, Orihuela A, Velarde A, Napolitano F, Alonso-Spilsbury M (2020b) Effects of human-animal relationship on animal productivity and welfare. Journal of Animal Behaviour and Biometeorology 8:196-205.

[65] Müller BR, Souza SV, Biscarra-Bellio JC, Maiolino-Molento CF (2019) Facial expression of pain in Nellore and Crossbred beef cattle. Journal of Veterinary Behavior 34:60-65.

[66] Murphy E, Nordquist R, Van der Staay F (2014) A review of behavioural methods to study emotion and mood in pigs, Sus scrofa. Applied Animal Behaviour Science 159:9-28.

[67] Nalon E, Maes D, Piepers S, Taylor P, Van Riet MMJ, Janssens GPJ, Tuyttens FAM (2015) Factors affecting mechanical nociceptive thresholds in healthy sows. Veterinary Anaesthesia and Analgesia

[68] Núñez V 2015 Estudio de palatabilidad en cerdos de recría en base a soluciones de glutamato monosódico. MV Thesis, Universidad de Chile, Chile.

[69] Orihuela A, Mota-Rojas D, Velarde A, Strappini-Asteggiano A, Thielo de la Vega L, Borderas-Tordesillas F, Alonso-Spilsbury M (2018) Invited review: environmental enrichment to improve behaviour in farm animals. CAB Reviews 13:1–25.

[70] Parr L, Waller B, Burrows A, Gothard K, Vick S (2010) MaqFACS: a muscle-based facial movement coding system for the Rhesus macaque. American Journal of Physical Anthropology 143:625-630.

[71] Parr LA, Waller BM, Vick SJ, Bard KA (2007) Classifying chimpanzee facial expressions using muscle action. Emotion 7:172.

[72] Paul E, Harding E, Mendl M (2005) Measuring emotional processes in animals: the utility of a cognitive approach. Neuroscience Biobehavioral Reviews 29:469-491.

[73] Paul E, Mendl M (2018) Animal emotion: Descriptive and prescriptive definitions and their implications for a comparative perspective. Applied Animal Behaviour Science 205:202-209.

[74] Reimert I, Bolhuis E, Rodenburg B (2013) Indicators of positive and negative emotions and emotional contagion in pigs. Physiology Behaviour 109:42-50.

[75] Rolls T (2000) The Brain Emotion. Trends in Cognitive Sciences, Cambridge University Press, 3:281- 282.

[76] Rutherford KMD (2002) Assessing pain in animals. Animal Welfare 11:31-53.

[77] Sneddon LU, Elwood RW, Adamo SA, Leach MC (2014) Defining and assessing animal pain. Animal Behaviour 97:201-212.

[78] Sotocinal SG, Sorge RE, Zaloum A, Tuttle AH, Martin LJ, Wieskopf JS, Mapplebeck JCS, Wei P, Zhan S, Zhang S, McDougall JJ, King OD, Mogil JS (2011) The Rat Grimace Scale: A Partially Automated Method for Quantifying Pain in the Laboratory Rat via Facial Expressions. Molecular Pain 7:55.

[79] Rutherford KMD, Donald RD, Lawrence AB, Wemelsfelder F (2012) Qualitative Behavioural Assessment of emotionality in pigs. Applied Animal Behaviour Science 139:218-224.

[80] Temple D, Manteca X, Velarde A, Dalmau A (2011) Assessment of animal welfare through behavioural parameters in Iberian pigs in intensive and extensive conditions. Applied Animal Behaviour Science 131:29-39.

[81] Tuttle AH, Molinaro MJ, Jethwa JF, Sotocinal SG, Prieto JC, Styner MA, Mogil JS, Zylka MJ (2018) A deep neural network to assess spontaneous pain from mouse facial expressions. Molecular Pain 14:1-19.

[82] Van de Perre V, Permentier L, De Bie S, Verbeke G, Geers G (2010) Effect of unloading, lairage, pig handling, stunning and season on pH of pork. Meat Science 86:931-937.

[83] Vermeulen L, Van de Perre V, Permentier L, De Bie S, Verbeke G, Geers R (2015) Pre-slaughter handling and pork quality. Meat Science 100:118-123.

[84] Viscardi AV, Hunniford M, Lawlis P, Leach M, Turner PV (2017) Development of a piglet grimace scale to evaluate piglet pain using facial expressions following castration and tail docking: a pilot study. Frontiers in Veterinary Science 4:51.

[85] Viscardi AV, Turner PV (2018) Efficacy of buprenorphine for management of surgical castration pain in piglets. BMC Veterinary Research 14:318.

[86] Waller BM, Whitehouse J, Micheletta J (2017) Rethinking primate facial expression: A predictive framework. Neuroscience Biobehavioral Reviews 82:13-21.

[87] Waller BM, Julle-Daniere E, Micheletta J (2020) Measuring the evolution of facial ‘expression’ using multi-species FACS. Neuroscience Biobehavioral Reviews 113:1-11.

[88] Wathan J, Burrows AM, Waller BM, McComb K (2015) EquiFACS: the equine facial action coding system. Plos One 10:e0137818.

[89] Whittaker AL, Howarth GS (2014) Use of spontaneous behaviour measures to assess pain in laboratory rats and mice: How are we progressing? Applied Animal Behaviour Science 151:1–12.

[90] Whittaker AL, Marsh LE (2019) The role of behavioural assessment in determining ‘positive’ affective states in animals. CAB Reviews 14:1-13.

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