Acute stress assessment using infrared thermography in fattening rabbits reacting to handling under winter and summer conditions

  • Juan A. Jaén-Téllez Universidad de Sevilla, Escuela Técnica Superior de Ingeniería Agronómica, Dept. Ciencias Agroforestales, 41013 Sevilla
  • María J. Sánchez-Guerrero Universidad de Sevilla, Escuela Técnica Superior de Ingeniería Agronómica, Dept. Ciencias Agroforestales, 41013 Sevilla http://orcid.org/0000-0003-4357-9908
  • José I. López-Campos Universidad de Sevilla, Escuela Técnica Superior de Ingeniería Agronómica, Dept. Ciencias Agroforestales, 41013 Sevilla
  • Mercedes Valera Universidad de Sevilla, Escuela Técnica Superior de Ingeniería Agronómica, Dept. Ciencias Agroforestales, 41013 Sevilla http://orcid.org/0000-0003-1742-550X
  • Pedro González-Redondo Universidad de Sevilla, Escuela Técnica Superior de Ingeniería Agronómica, Dept. Ciencias Agroforestales, 41013 Sevilla http://orcid.org/0000-0002-3324-2861
Keywords: temperature, welfare, thermoregulation

Abstract

Aim of study: This study assesses acute stress by measuring, through infrared thermography in summer and winter, the temperature of the eye, outer ear, inner ear and nose in 40 fattening rabbits before and after handling.

Area of study: Seville (Spain).

Material and methods: Body thermographic temperatures were recorded during a 38-day fattening period twice weekly and twice a day, before and after the handler held the rabbits in their arms for one minute. Ambient temperature and relative humidity were also recorded, and their influence on body temperatures was assessed. For each anatomical part, the variation of the temperature between the handled and undisturbed rabbit, and the differential temperature between the anatomical part in the undisturbed rabbit and the ambient temperature were calculated.

Main results: The variation in temperatures between handled and undisturbed rabbits ranged from 0.25±0.041 ºC for eye to 3.09±0.221 ºC for outer ear in summer and -0.41±0.182 ºC for nose to 2.09±0.178 ºC for outer ear in winter. The day of the fattening period influenced all the temperature traits during summer and winter, except for the inner ear in winter. In summer, unlike winter, the temperature variation at the end of fattening period between handled and undisturbed rabbits was lower than at weaning (-0.04 to 1.94 ºC vs. 0.54 to 5.52 ºC, respectively). The temperatures in undisturbed rabbits were correlated with ambient temperature.

Research highlights: Measuring body temperature with infrared thermography is a useful tool to evaluate acute stress in handled rabbits, with the inner ear and eye the most reliable body parts for measuring it.

Downloads

Download data is not yet available.

References

Ardiaca M, Brotóns NJ, Montesinos A, 2010. Aproximación a las urgencias y cuidados intensivos en conejos, psitácidas y reptiles. Clínica Veterinaria de Pequeños Animales 30 (1): 5-14.

Bartolomé E, Sánchez MJ, Molina A, Schaefer AL, Cervantes I, Valera M, 2013. Using eye temperature and heart rate for stress assessment in young horses competing in jumping competitions and its possible influence on sport performance. Animal 7 (12): 2044-2053. https://doi.org/10.1017/S1751731113001626

Benato L, Rooney NJ, Murrell JC, 2019. Pain and analgesia in pet rabbits within the veterinary environment: a review. Vet Anaesth Analg 46 (2): 151-162. https://doi.org/10.1016/j.vaa.2018.10.007

Bilkó Á, Altbäcker V, 2000. Regular handing early in the nursing period eliminates fear responses toward human beings in wild and domestic rabbits. Dev Psychobiol 36 (1): 78-87. https://doi.org/10.1002/(SICI)1098-2302(200001)36:1<78::AID-DEV8>3.0.CO;2-5

BOE, 2013. Real Decreto 53/2013, de 1 de febrero, por el que se establecen las normas básicas aplicables para la protección de los animales utilizados en experimentación y otros fines científicos, incluyendo la docencia. Ministerio de la Presidencia, Gobierno de España. Boletín Oficial del Estado 34: 11370-11421.

Bowler K, Manning R, 1994. Membranes as the critical targets in cellular heat injury and resistance adaptation. In: Temperature adaptation of biological membranes; Cossins AR (ed.). Section 15, pp: 185-204. Portland Press, London. ISBN: 9781855780620.

Broom DM, 2011. Animal welfare: concepts, study methods and indicators. Rev Colomb Cienc Pec 24 (3): 306-321.

Cabezas S, Blas J, Marchant TA, Moreno S, 2007. Physiological stress levels predict survival probabilities in wild rabbits. Horm Behav 51 (3): 313-320. https://doi.org/10.1016/j.yhbeh.2006.11.004

Cañón J, (Ed). 2015. Historia, caracterización y situación del conejo Antiguo Pardo Español. ASEMUCE-Servicio de Genética UCM. https://www.ucm.es/data/cont/docs/345-2016-12-07-Raza_Conejos_Antiguo_Pardo_Español.pdf

Cervera C, Fernández-Carmona J, 1998. Nutrition and the climatic environment. In: The nutrition of the rabbit; De Blas C, Wiseman J (eds.). pp: 267-284. CAB Int, Wallingford, UK. ISBN: 978-0851992792. https://doi.org/10.1079/9781845936693.0267

Collier RJ, Baumgard LH, Zimbelman RB, Xiao Y, 2019. Heat stress: physiology of acclimation and adaptation. Anim Front 9 (1): 12-19. https://doi.org/10.1093/af/vfy031

Coureaud G. Rödel HG, Le Normand B, Fortun-Lamothe L, Bignon L, 2015. Habitat e comportement. In: Le lapin. De la biologie à l'élevage; Gidenne T (ed.). pp: 107-136. Éditions Quae, Versailles, France. ISBN: 9782759224166.

Csatádi K, Kustos K, Eiben C, Bilkó Á, Altbäcker V, 2005. Even minimal human contact linked to nursing reduces fear responses toward humans in rabbits. Appl Anim Behav Sci 95 (1-2): 123-128. https://doi.org/10.1016/j.applanim.2005.05.002

Daader AH, Al-Sagheer AA, Gabr HA, Abd El-Moniem EA, 2018. Alleviation of heat-stress-related physiological perturbations in growing rabbits using natural antioxidants. Span J Agric Res 16 (3): e0610. https://doi.org/10.5424/sjar/2018163-13184

Dalmau A, Catanese B, Rafel O, Rodriguez P, Fuentes C, Llonch P, Mainau E, Velarde A, Ramón J, Taberner E, López-Béjar M, Piles M, 2015. Effect of high temperatures on breeding rabbit behaviour. Anim Prod Sci 55 (9): 1207-1214. https://doi.org/10.1071/AN13440

De Lima V, Piles M, Rafel O, López-Béjar M, Ramón J, Velarde A, Dalmau A, 2013. Use of infrared thermography to assess the influence of high environmental temperature on rabbits. Res Vet Sci 95 (2): 802-810. https://doi.org/10.1016/j.rvsc.2013.04.012

Dickens MJ, Romero LM, 2013. A consensus endocrine profile for chronically stressed wild animals does not exist. Gen Comp Endocr 191: 177-189. https://doi.org/10.1016/j.ygcen.2013.06.014

Duval F, González F, Rabia H, 2010. Neurobiología del estrés. Revista Chilena de Neuro-Psiquiatría 48 (4): 307-318. https://doi.org/10.4067/S0717-92272010000500006

Emam AM, Afonso S, Azoz AAA, González-Redondo P, Mehaisen GMK, Ahmed NA, Ferrand N, 2016a. Microsatellite polymorphism in some Egyptian and Spanish common rabbit breeds. Proc. 11th World Rabbit Congress, Qingdao (China), Jun 15-18. pp: 31-34.

Emam AM, Afonso S, Azoz AAA, González-Redondo P, Mehaisen GMK, Ahmed NA, Ferrand N, 2016b. Origin of Egyptian and Spanish common rabbits: evidence from mitochondrial DNA cytochrome b sequence analysis. Proc. 11th World Rabbit Congress, Qingdao (China), Jun 15-18. pp: 35-38.

FAOSTAT, 2019. Statistics Database. Food and Agriculture Organization of the United Nations. Rome (Italy). http://www.fao.org/faostat/en/#data

Fayez I, Marai M, Alnaimy A, Habeeb M, 1994. Thermoregulation in rabbits. In: Rabbit production in hot climates; Baselga M, Marai IFM (eds.), CIHEAM, Zaragoza. Cahiers Opt Méditerr 8: 33-41.

Ferré JS, Rosell JM 2000. Alojamiento y patología. In: Enfermedades del conejo; Rosell JM (ed.). Vol. II, pp: 167-210. Mundi-Prensa, Madrid. ISBN: 9788471149077.

Ferreira C, Castro F, Piorno V, Catalán I, Delibes-Mateos M, Rouco C, Mínguez LE, Aparicio F, Blanco-Aguiar JA, Ramírez E, et al., 2015. Biometrical analysis reveals major differences between the two subspecies of the European rabbit. Biol J Linn Soc 116 (1): 106-116. https://doi.org/10.1111/bij.12556

Gascón FM, Verde M, 1987. Efecto estresante de la manipulación en el conejo. Proc. XII Simp. de Cunicultura de ASESCU, Guadalajara (Spain), May 20-22. pp: 125-132.

Glaser R, Kiecolt-Glaser JK, 2005. Stress-induced immune dysfunction: implications for health. Nat Rev Immunol 5 (3): 243-251. https://doi.org/10.1038/nri1571

Gonzalez RR, Kluger MJ, Hardy JD, 1971. Partitional calorimetry of the New Zealand White rabbit at temperatures 5-35 ºC. J Appl Physiol 31 (5): 728-734. https://doi.org/10.1152/jappl.1971.31.5.728

González-Redondo P, 2016. Resultados preliminares de rendimiento reproductivo y de engorde de un núcleo de cría de conejos de tipo Común Doméstico Español. Proc. XLI Simp. de Cunicultura de ASESCU, Hondarribia (Spain), May 12-13. pp: 180-185.

Greco D, Stabenfeldt GH, 1997. Endocrine glands and their function, In: Textbook of veterinary physiology; Cunningham JG (ed.). 2nd ed, pp: 404-439. WB Saunders Company St. Louis, USA. ISBN: 9780721664248.

Grissom N, Bhatnagar S, 2009. Habituation to repeated stress: get used to it. Neurobiol Learn Mem 92 (2): 215-224. https://doi.org/10.1016/j.nlm.2008.07.001

Kataoka N, Hioki H, Kaneko T, Nakamura K, 2014. Psychological stress activates a dorsomedial hypothalamus-medullary raphe circuit driving brown adipose tissue thermogenesis and hyperthermia. Cell Metab 20 (2): 346-358. https://doi.org/10.1016/j.cmet.2014.05.018

Kuchel O, 1991. Stress and catecholamines. Methods Achiev Exp Pathol 14: 80-103.

Lattin CR, Romero LM, 2014. Chronic stress alters concentration of corticosterone receptors in a tissue-specific manner in wild house sparrows (Passer domesticus). J Exp Biol 217 (14): 2601-2608. https://doi.org/10.1242/jeb.103788

Lebas F, Coudert P, de Rochambeau H, Thébault RG, 1997. The rabbit - Husbandry, health and production. FAO, Rome. ISBN: 9789251034415.

Long NC, Vander AJ, Kluger MJ, 1990. Stress-induced rise of body temperature in rats is the same in warm and cool environments. Physiol Behav 47 (4): 773-775. https://doi.org/10.1016/0031-9384(90)90093-J

Ludwig N, Gargano M, Luzi F, Carenzi C, Verga M, 2007. Technical note: applicability of infrared thermography as a non invasive measurement of stress in rabbit. World Rabbit Sci 15 (4): 199-206. https://doi.org/10.4995/wrs.2007.588

Luzi F, Ludwig N, Monzani M, Gargano M, Ricci C, Redaelli V, Verga M, 2007. Procedures for analyses of sequence of thermal images in welfare study of rabbit. Proc. 4th Int. Workshop on the Assessment of Animal Welfare at Farm and Group Level (WAFL), Ghent (Belgium), Sep 10-13. p. 85.

Manteca X, 1998. Neurophysiology and assessment of welfare. Meat Sci 49 (Suppl 1): S205-S218. https://doi.org/10.1016/S0309-1740(98)90049-3

Minton JE, 1994. Function of the hypothalamic-pituitary-adrenal axis and the sympathetic nervous system in models of acute stress in domestic farm animals. J Anim Sci 72 (7): 1891-1898. https://doi.org/10.2527/1994.7271891x

Monclús R, Rödel HG, Palme R, von Holst D, De Miguel J, 2006. Non-invasive measurement of the physiological stress response of wild rabbits to the odour of a predator. Chemoecology 16 (1): 25-29. https://doi.org/10.1007/s00049-005-0324-6

Möstl E, Palme R, 2002. Hormones as indicators of stress. Domest Anim Endocrin 23 (1-2): 67-74. https://doi.org/10.1016/S0739-7240(02)00146-7

Nelson RJ, 2000. An introduction to behavioral endocrinology, 2nd edition. Sinauer Ass. Inc. Pub., MA, USA. ISBN: 0-87893-616-5

OJ, 2010. Directive 2010/63/EU of 22 September 2010 on the protection of animals used for scientific purposes. European Parliament and Council. Official J European Union, L276: 33-79.

Okab AB, El-Banna SG, Koriem AA, 2008. Influence of environmental temperatures on some physiological and biochemical parameters of New-Zealand rabbit males. Slovak J Anim Sci 41 (1): 12-19.

Olivas I, Villagrá A, 2013. Technical Note: Effect of handling on stress-induced hyperthermia in adult rabbits. World Rabbit Sci 21 (1): 41-44. https://doi.org/10.4995/wrs.2013.1178

Peaston RT, Weinkove C, 2004. Measurement of catecholamines and their metabolites. Ann Clin Biochem 41 (1): 17-38. https://doi.org/10.1258/000456304322664663

Podberscek AL, Blackshaw JK, Beattie AW, 1991. The behaviour of group penned and individually caged laboratory rabbits. Appl Anim Behav Sci 28 (4): 353-363. https://doi.org/10.1016/0168-1591(91)90167-V

Price EO, 2002. Animal domestication and behavior. CAB Int, Wallingford, UK. ISBN: 9780851995977. https://doi.org/10.1079/9780851995977.0000

Samoggia G, 1987. Esigenze fisioclimatiche dei conigli nell'allevamento intensivo. Rivista di Coniglicoltura 24 (5): 16-20.

Sánchez MJ, Bartolomé E, Valera M, 2016. Genetic study of stress assessed with infrared thermography during dressage competitions in the Pura Raza Español horse. Appl Anim Behav Sci 174: 58-65. https://doi.org/10.1016/j.applanim.2015.11.006

Sanmiguel RA, Díaz V, 2011. Mecanismos fisiológicos de la termorregulación en animales de producción. Rev Colomb Cienc Anim 4 (1): 88-94.

Silva S, Mourão JL, Ribeiro L, Gonçalves C, Pinheiro V, 2014. Utilização de imagens termográficas por infravermelhos para avaliar a temperatura de láparos em ninhos com diferente material. Proc. XXXIX Simp. de Cunicultura de ASESCU, Tudela (Spain), May 29-30. pp: 67-70.

Silva SR, Mourão JL, Guedes C, Monteiro D, Pinheiro V, 2015. Utilización de imágenes video y termográficas para estimar el peso vivo de conejos en cebo. Proc. XL Simp. de Cunicultura de ASESCU, Santiago de Compostela (Spain), May 28-29. pp: 115-117.

Soleimani AF, Kasim A, Alimon AR, Zulkifli I, 2008. Durability of induced heat tolerance by short term heat challenge at broilers marketing age. Pak J Biol Sci 11 (17): 2163-2166. https://doi.org/10.3923/pjbs.2008.2163.2166

Stewart M, Webster JR, Schaefer AL, Cook NJ, Scott SL, 2005. Infrared thermography as a non-invasive tool to study animal welfare. Anim Welfare 14 (4): 319-325.

Stewart M, Webster JR, Verkerk GA, Schaefer AL, Colyn JJ, Stafford KJ, 2007. Non-invasive measurement of stress in dairy cows using infrared thermography. Physiol Behav 92 (3): 520-525. https://doi.org/10.1016/j.physbeh.2007.04.034

Temple D, Mainau E, Manteca X, 2014. Practical note - Fear caused by poor human-animal relationship. Farm Animal Welfare Education Centre. https://www.fawec.org/media/com_lazypdf/pdf/Nota-n-2-fear-en.pdf

Touma C, Sachser N, Möstl E, Palme R, 2003. Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen Comp Endocrinol 130 (3): 267-278. https://doi.org/10.1016/S0016-6480(02)00620-2

Travain T, Colombo ES, Heinzl E, Bellucci D, Previde EP, Valsecchi P, 2015. Hot dogs: Thermography in the assessment of stress in dogs (Canis familiaris)-A pilot study. J Vet Behav 10 (1): 17-23. https://doi.org/10.1016/j.jveb.2014.11.003

Trocino A, Xiccato G, 2006. Animal welfare in reared rabbits: a review with emphasis on housing systems. World Rabbit Sci 14 (2): 77-93. https://doi.org/10.4995/wrs.2006.553

Valera M, Bartolomé E, Sánchez MJ, Molina A, Cook N, Schaefer AL, 2012. Changes in eye temperature and stress assessment in horses during show jumping competitions. J Equine Vet Sci 32 (12): 827-830. https://doi.org/10.1016/j.jevs.2012.03.005

Veissier I, Boissy A, 2007. Stress and welfare: Two complementary concepts that are intrinsically related to the animal's point of view. Physiol Behav 92 (3): 429-433. https://doi.org/10.1016/j.physbeh.2006.11.008

Warriss PD, Pope SJ, Brown SN, Wilkins LJ, Knowles TG, 2006. Estimating the body temperature of groups of pigs by thermal imaging. Vet Rec 158 (10): 331-334. https://doi.org/10.1136/vr.158.10.331

Wingfield JC, Hunt K, Breuner C, Dunlap K, Fowler GS, Freed L, Lepson J, 1997. Environmental stress, field endocrinology, and conservation biology. In: Behavioral approaches to conservation in the wild; Buchholz JR, Clemmons R (eds.). pp: 95-131. Cambridge University Press, Cambridge, UK. ISBN: 9780521589604.

Xu HT, 1996. The behaviour of the rabbit. Proc. 6th World Rabbit Congress. Toulouse (France), Jul 09-12. pp: 437-440.

Yamasaki-Maza A, Yamasaki-Maza L, Ruiz-Rojas JL, 2017. Temperatura ambiente y humedad relativa y su relación con el bienestar en conejos (Oryctolagus cuniculus) en engorda en el trópico seco. Proc. Congr. Mesoam. de Invest. UNACH. Digital Magazine 4: 1366-1371.

Zeferino CP, Moura ASAMT, Fernandes S, Kanayama JS, Scapinello C, Sartori JR, 2011. Genetic group × ambient temperature interaction effects on physiological responses and growth performance of rabbits. Livest Sci 140 (1-3): 177-183. https://doi.org/10.1016/j.livsci.2011.03.027

Zucca D, Redaelli V, Marelli SP, Bonazza V, Heinzl E, Verga M, Luzi F, 2012. Effect of handling in pre-weaning rabbits. World Rabbit Sci 20 (2): 97-101. https://doi.org/10.4995/wrs.2012.1083

Published
2020-09-22
How to Cite
Jaén-TéllezJ. A., Sánchez-GuerreroM. J., López-CamposJ. I., ValeraM., & González-RedondoP. (2020). Acute stress assessment using infrared thermography in fattening rabbits reacting to handling under winter and summer conditions. Spanish Journal of Agricultural Research, 18(2), e0502. https://doi.org/10.5424/sjar/2020182-15706
Section
Animal health and welfare