Effect of gestational and lactational exposure to heat stress on performance in rabbits


  • F. Marco-Jiménez Universitat Politècnica de València
  • F.J. García-Diego Universitat Politècnica de València
  • J.S. Vicente Universitat Politècnica de València




heat stress, growth performance, gestation, lactation, rabbit


Reproductive performance is greatly affected by environmental factors such as temperature. Heat stress (HS) during pregnancy and lactation can influence not only foetal growth but also postnatal development of kits. The aim of this study was to test the effect of HS during gestation and lactation on postnatal growth till Spanish commercial liveweight. To investigate this, 32 primiparous non lactating rabbit does were exposed to 1 of 2 environmental treatments: high temperature (between 25 and 36°C, HS group; n=16) or thermoneutral conditions (between 14 and 20°C, TN group; n=16). Does were allowed to acclimate 30 d before the artificial insemination. At birth, kits were allocated into 4 groups: HS was only applied during gestation (G group; n=54); HS was applied during gestation and lactation period (GL group; n=85); HS was only applied during lactation period (L group; n=60); and TN was applied during gestation and lactation period (C group; n=77). All litters were kept under each experimental environment until weaning at day 30. Then, litters were moved to TN temperatures until slaughter at day 63. Compared with TN does, the HS does presented lower litter size (9.7 and 11.4; P<0.05), litter weight (503.0 vs. 630.5 g; P<0.05) and kit weight at birth (56.6 vs. 61.4 g; P<0.05), as well as a higher stillborn rate (25.4 vs. 9.9%; P<0.05). The kits from does subjected to HS during gestation (G group) had similar postnatal growth compared to offspring from does gestated in TN conditions (C group), whereas kits from does that experienced HS during gestation and lactation (GL group) and during their lactation (L group) presented decreased postnatal growth. Together, these results demonstrate that kits from does that underwent HS during gestation did not alter postnatal growth until Spanish commercial liveweight, whereas HS during lactation resulted in decreased postnatal growth.


Download data is not yet available.

Author Biographies

F. Marco-Jiménez, Universitat Politècnica de València

Institute of Science and Animal Technology, Laboratorio de Biotecnología de la Reproducción

F.J. García-Diego, Universitat Politècnica de València

Department of Applied Physics (U.D. Agrónomos)

J.S. Vicente, Universitat Politècnica de València

Institute of Science and Animal Technology, Laboratorio de Biotecnología de la Reproducción


Barker D.J.P. 1995. Fetal origins of coronary heart disease. Brit. Med. J., 311: 171-174. doi:10.1136/bmj.311.6998.171

Barker D.J.P., Godfrey K.M., Gluckman P.D., Harding J.E., Owens J.A., Robinson J.S. 1993. Fetal nutrition and cardiovascular disease in adult life. Lancet, 341: 938-941. doi:10.1016/0140-6736(93)91224-A

Baumgard L.H., Rhoads R.P. Jr. 2013. Effects of heat stress on postabsorptive metabolism and energetics. Ann. Rev. Anim. Biosci., 1: 311-337.


Bloemhof S., Van der Waaij E.H., Merks J.W., Knol E.F. 2008. Sow line differences in heat stress tolerance expressed in reproductive performance traits. J. Anim. Sci., 86: 3330-3337. doi:10.2527/jas.2008-0862

Boddicker R.L., Seibert J.T., Johnson J.S., Pearce S.C., Selsby J.T., Gabler N.K., Lucy M.C., Safranski T.J., Rhoads R.P., Baumgard L.H., Ross J.W. 2014. Gestational heat stress alters postnatal offspring body composition indices and metabolic parameters in pigs. PLoS One, 9: e110859. doi:10.1371/journal.pone.0110859

Chen X., Fahy A.L., Green A.S., Anderson M.J., Rhoads R.P., Limesand S.W. 2010. β2-Adrenergic receptor desensitization in perirenal adipose tissue in fetuses and lambs with placental insufficiency-induced intrauterine growth restriction. J. Physiol., 588: 3539-3549. doi:10.1113/jphysiol.2010.192310

Dalle Zotte A., Remignon H., Ouhayoun J. 2005. Effect of feed rationing during post-weaning growth on meat quality, muscle energy metabolism and fibre properties of Biceps femoris muscle in the rabbits. Meat Sci., 70: 301-306. doi:10.1016/j.meatsci.2005.01.016

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: 802-810. doi:10.1016/j.rvsc.2013.04.012

El Saidy N.R., El-Sayed Allam F., Balabel T.M., El-Midany S.A.A. 2016. Evaluation of using honey, cool water and levamisole against heat stress on different traits of rabbits under egyptian summer conditions. World Vet. J., 6: 10-18.

Estany J., Baselga M., Blasco A., Camacho J. 1989. Mixed model methodology for the estimation of genetic response to selection in litter size of rabbits. Livest. Prod. Sci., 21: 67-75. doi:10.1016/0301-6226(89)90021-3

FAOSTAT (Food and Agriculture Organization of the United Nations, authors). 2009. Available online: http://faostat.fao.org/default.aspx. Accessed September 2009.

FAOSTAT (Food and Agriculture Organization of the United Nations, authors). 2012. Available online: http://faostat.fao.org/site/569/DesktopDefault.aspx?

PageID=569#ancor Accessed September 2012.

Fernández-Carmona J., Alqedra I., Cervera C., Moya J., Pascual J.J. 2003. Effect of lucerne-based diets on performance of reproductive rabbit does at two temperatures. Anim. Sci., 76: 283-295. doi:10.1017/S1357729800053534

Fernández-Carmona J., Cervera C., Sabater C., Blas E. 1995. Effect of diet composition on the production of rabbit breeding does housed in a traditional building and at 30°C. Anim. Feed Sci. Tech., 52: 289-297. doi:10.1016/0377-8401(94)00715-L

Foxcroft G.R., Dixon W.T., Dyck M.K., Novak S., Harding J.C., Almeida F.C. 2009. Prenatal programming of postnatal development in the pig. Soc. Reprod. Fertil. suppl., 66: 213-231.

Foxcroft G.R., Dixon W.T., Novak S., Putman C.T., Town S.C., Vinsky M.D. 2006. The biological basis for prenatal programming of postnatal performance in pigs. J. Anim. Sci., 84: 105-112. doi:10.2527/2006.8413_supplE105x

García-Diego F.J., Pascual J.J., Marco-Jiménez F. 2011. Technical Note: Design of a large variable temperature chamber for heat stress studies in rabbits. World Rabbit Sci., 19: 225-231. doi:10.4995/wrs.2011.938

Gidenne T., Combes S., Feugier A., Jehl N., Arveux P., Boisot P., Briens C., Corrent E., Fortune H., Montessuy S., Verdelhan S. 2009. Feed restriction strategy in the growing rabbit. 2. Impact on digestive health, growth and carcass characteristics. Animal, 3: 509-515. doi:10.1017/S1751731108003790

Guilloteau P., Waterland R.A. 2005. Does nutrition during infancy and early childhood contribute to later obesity via metabolic imprinting of epigenetic gene regulatory mechanisms? Nestlé Nutrition Institute Workshop Series: Pediatric Program, 56: 157-171. doi:10.1159/000086298

Hamid H.Y., Abu Bakar Zakaria M.Z., Yong Meng G., Haron A.W., Mohamed Mustapha N. 2012. Effects of elevated ambient temperature on reproductive outcomes and offspring growth depend on exposure time. Sci. World J., 359134. doi:10.1100/2012/359134

Hansen P.J. 2009. Effects of heat stress on mammalian reproduction. Philos. T. Roy. Soc. B, 364: 3341-3350. doi:10.1098/rstb.2009.0131

Johnson J.S., Abuajamieh M., Sanz Fernandez M.V., Seibert J.T., Stoakes S.K., Keating A.F., Ross J.W., Selsby J.T., Rhoads R.P., Baumgard L.H. 2015. The impact of in utero heat stress and nutrient restriction on progeny body composition. J. Therm. Biol., 53: 143-150. doi:10.1016/j.jtherbio.2015.10.002

Langley-Evans S.C., Bellinger L., McMullen S. 2005. Animal models of programming: early life influences on appetite and feeding behaviour. Matern. Child Nutr., 1: 142-148. doi:10.1111/j.1740-8709.2005.00015.x

Lau C., Rogers J.M. 2004. Embryonic and fetal programming of physiological disorders in adulthood. Birth Defects Res C., 72: 300-312. doi:10.1002/bdrc.20029

Lebas F., Coudert P., Rouvier R., Rochambeau H. 1986. The rabbit; husbandry, health and production. FAO Animal Production and Health Series 21.

Ledin I. 1984. Effect of restricted feeding and realimentation on compensatory growth, carcass composition and organ growth in rabbit. Ann. Zootech., 33: 33-50. doi:10.1051/animres:19840103

LPHSI. 1990. Livestock and Poultry Heat Stress Indices Agriculture Engineering Technology Guide. Clemson, SC, USA: Clemson University., 29634.

Luber G., McGeehin M. 2008. Climate change and extreme heat events. Am. J. Prev. Med., 35: 429-435. doi:10.1016/j.amepre.2008.08.021

Maertens L., De Groote G. 1990. Comparison of feed intake and milk yield of does under normal and high ambient temperature. J. Appl. Rabbit Res., 13: 159-162.

Maertens L., Lebas F., Szendrő Zs. 2006. Rabbit milk: A review of quantity, quality and non-dietary affecting factors. World Rabbit Sci., 14: 205-230. doi:10.4995/wrs.2006.565

Makarevich A.V., Olexiková L., Chrenek P., Kubovicová E., Fréharová K., Pivko J. 2007. The effect of hyperthermia in vitro on vitality of rabbit preimplantation embryos. Physiol. Res., 56: 789-96.

Marai I.F.M., Habeeb A.A.M. 1998. Adaptability of Bos taurus cattle under hot climate conditions. Ann. Arid Zone, 37: 253-281.

Marai I.F.M., Habeeb A.A.M., Gad AE. 2002. Rabbits’ productive, reproductive and physiological performance traits as affected by heat stress: a review. Livest. Prod. Sci., 78: 71-90. doi:10.1016/S0301-6226(02)00091-X

Marco-Jiménez F., Naturil-Alfonso C., Peñaranda D.S., Jiménez-Trigos E., García-Diego F.J., Vicente J.S. 2013. Maternal exposure to high temperatures disrupts OCT4 mRNA expression of rabbit pre-implantation embryos and endometrial tissue. Reprod. Domest. Anim., 48: 429-434. doi:10.1111/rda.12092

Marco-Jiménez F., Naturil-Alfonso C., Peñaranda D.S., Jiménez-Trigos E., García-Diego F.J., Vicente J.S. 2014. Effect

of exposure to heatwave during blastocyst formation on reproductive performance of female rabbits. Reprod. Dom. Anim., 49: 629-635. doi:10.1111/rda.12338

Maya-Soriano M.J., Taberner E., Sabés-Alsina M., Ramon J., Rafel O., Tusell L., Piles M., López-Béjar M. 2015. Daily exposure to summer temperatures affects the motile subpopulation structure of epididymal sperm cells but not male fertility in an in vivo rabbit model. Theriogenology, 84: 384-389. doi:10.1016/j.theriogenology.2015.03.033

McMillen I.C., Muhlhausler B.S., Duffield J.A., Yuen B.S.J. 2004. Prenatal programming of postnatal obesity: fetal nutrition and the regulation of leptin synthesis and secretion before birth. Proc. Nutr. Soc., 63: 405-412. doi:10.1079/PNS2004370

Méndez J., de Blas C., Fraga M.J. 1986. The effects of diet and remating interval after parturition on the reproductive performance of the commercial doe rabbit. J. Anim. Sci., 62: 1624-1634. doi:10.2527/jas1986.6261624x

Pascual J.J., Cervera C., Blas E., Fernández-Carmona J. 1999. Effect of high fat diets on the performance, milk yield and milk composition of multiparous rabbit does. Anim. Sci., 68: 151- 162. doi:10.1017/S1357729800050177

Petracci M., Bianchi M., Cavani C. 2009. Development of Rabbit Meat Products Fortified With n-3 Polyunsaturated Fatty Acids. Nutrients, 1: 111-118. doi:10.3390/nu1020111

Pinney S.E., Simmons R.A. 2010. Epigenetic mechanisms in the development of type 2 diabetes. Trends Endocrin. Met., 21:223-229. doi:10.1016/j.tem.2009.10.002

Pluess M., Belsky J. 2011. Prenatal programming of postnatal plasticity? Dev. Psychopathol., 23: 29-38. doi:10.1017/S0954579410000623

Poigner J., Szendrő Z.S., Lévai A., Radnai I., Biró-Németh E. 2000. Effect of birth weight and litter size on growth and mortality in rabbits. World Rabbit Sci., 8: 17-22. doi:10.4995/wrs.2000.413

Rakes J.M., Heird C.E., Harris G.C., Wittorff E.K., Johnson Z.B. 1988. Effects of heat stress, nutrition and gonadotrophins on reproduction of New Zealand rabbit proceeding of 11th International Congress on Animal Reproduction and Artificial Insemination. University College, Dublin, Ireland, Vol. 3, Breef Communication.

Renaudeau D., Collin A., Yahav S., de Basilio V., Gourdine J.L., Collier R.J. 2012. Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal, 6: 707-


Rhind S.M., Rae M.T., Brooks A.N. 2001. Effects of nutrition and environmental factors on the fetal programming of the reproductive axis. Reproduction, 122: 205-214. doi:10.1530/rep.0.1220205

Roseboom T., de Rooij S., Painter R. 2006. The Dutch famine and its long-term consequences for adult health. Early Hum. Dev., 82: 485-491. doi:10.1016/j.earlhumdev.2006.07.001

Shiota K., Kayamura T. 1989. Effects of prenatal heat stress on postnatal growth, behavior and learning capacity in mice. Biol. Neonate, 56: 6-14. doi:10.1159/000242981

SPSS. 2002. SPSS 21.0 software package; SPSS Inc., Chicago, Illinois, USA, 2002

Symeon G.K., Goliomytis M., Bizelis I., Papadomichelakis G., Pagonopoulou O., Abas Z., Deligeorgis S.G., Chadio S.E. 2015. Effects of gestational maternal undernutrition on growth, carcass composition and meat quality of rabbit offspring. PLoS One, 10: e0118259. doi:10.1371/journal.pone.0118259

Szendrő Zs., Papp Z., Kustos K. 1998. Effect of environmental temperature and restricted feeding on production of rabbit does. 2nd International Conférence on Rabbit production in hot climate, Adana Sept. 1998, Cahier Options Méditéranéennes Vol. 41: 11-17.

Tusell L., David I., Bodin L., Legarra A., Rafel O., López-Bejar M., Piles M. 2011. Using the product threshold model for estimating separately the effect of temperature on male and female fertility. J. Anim. Sci., 89: 3983-3995. doi:10.2527/jas.2011-3924

Verga M., Luzi F., Carenzi C. 2007. Effects of husbandry and management systems on physiology and behaviour of farmed and laboratory rabbits. Horm. Behav., 52: 122-129. doi:10.1016/j.yhbeh.2007.03.024

Zeferino C.P., Komiyama C.M., Fernandes S., Sartori J.R., Teixeira P.S., Moura A.S. 2013. Carcass and meat quality traits of rabbits under heat stress. Animal, 7: 518-523. doi:10.1017/S1751731112001838

Zeferino C.P., Moura A.S.A.M.T., Fernandes S., Kanayama J.S., Scapinello C., Sartori J.R. 2011. Genetic group × ambient temperature interaction effects on physiological responses and growth performance of rabbits. Livest. Sci., 140: 177-183. doi:10.1016/j.livsci.2011.03.027