Abstract
Profitable production of rabbit meat requires comfortable environment for expression of good quality traits embedded in the genetic components of rabbits. One of the major problems facing rabbit production is heat stress, especially in hot regions of the world. This is further aggravated by global warming being experienced as a result of climate change. Rabbits have no or few sweat glands, complicating the problem of heat dissipation, thereby predisposing the animals to heat stress (HS). Heat stress adversely affect welfare and adaptation, feed consumption and utilization, immunity and health status, growth, reproduction, and milk production in rabbits. Rabbits are homoeothermic animals. They should be capable of body temperature regulation within a narrow range. Thermoregulation is extremely poor in rabbits because of lack of sweat glands. Rabbits are highly sensitive to high ambient temperature. The presence of thick insulator fur on the skin further impedes heat loss in rabbits. This review summarizes data available literatures in the last two decades (2000–2020). Short compilation on management techniques adopted in rearing rabbits under hot conditions is included.
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References
Abdal-Rahman SAH, Baqey DAA (2016) Effect of the thermal changes on physiological, biochemical and histological traits in pregnant and embryo of New Zealand white rabbits. Int J Advan Biol Res 6:313–327
Abd El-Aziz AH, Mahrose KM, El-Kasrawy NI, Alsenosy AA (2021) Yeast as growth promoter in two breeds of growing rabbits with special reference to its economic implications. An Acad Bras Cienc 93:e20190274. https://doi.org/10.1590/0001-3765202120190274
Abdel-Monem UM, Khalil BA, Mahrose KM (2007) Effects of feeding times on performance of New Zealand White rabbit does. The 5th International Congress of Rabbit Production under hot climates, December 4–7, Hurghada, Egypt
Abdel-Monem UM, Mahrose KM, Khalil BA (2009a) Effects of increasing dietary energy level on performance of adult New Zealand White and Flander rabbits under summer conditions of Egypt. Zag Vet J 37:105–114
Abdel-Monem UM, Mahrose KM, Khalil BA (2009b) Effects of cage density and climatic conditions on the performance of growing rabbits. Zag Vet J 37:198–208
Abdelnour SA, El-Saadony MT, Saghir SAM, Abd El- Hack ME, Al-shargi OYA, Al-Gabri N, Salama A (2020) Mitigating negative impacts of heat stress in growing rabbits via dietary prodigiosin supplementation. Livest Sci 240:104220
Agea I, García ML, Argente MJ (2021) Preliminary study of body temperature emissivity in rabbits selected for litter size residual variability. Agric 11:604. https://doi.org/10.3390/agriculture11070604
Ajasin FO, Omole AJ, Oluokun JA, Obi OO, Owosibo A (2004) Performance characteristics of weaned rabbits fed plantain peel as replacement for maize. World J Zool 1:30–32
Aldemir M, Okulu E, Kosemehmetoglu K, Ener K, Topal F, Evirgen O, Gurleyik E, Avcı A (2014) Evaluation of the protective effect of quercetin against cisplatin-induced renal and testis tissue damage and sperm parameters in rats. Andrologia 46:1089–1097. https://doi.org/10.1111/and.12197
Al-Sagheer AA, Daader AH, Gabr HA, Abd El-Moniem EA (2017) Palliative effects of extra virgin olive oil, gallic acid, and lemongrass oil dietary supplementation on growth performance, digestibility, carcass traits, and antioxidant status of heat-stressed growing New Zealand White rabbits. Environ Sci Pollut Res 24:6807–6818. https://doi.org/10.1007/s11356-017-8396-8
Al-Zafry SR, Medan MS (2012) Effects of vitamin E and selenium complex on heat stressed rabbits. Suez Canal Vet Med J 22:129–138
Anoh KU, Barje PP, Iyeghe-Erakpotobor GT, Akpa GN (2017) Growth performance of heat stressed rabbits fed diets supplemented with synthetic and organic antioxidants. Nig J Anim Prod 44:177–180
Anoh KU, Olayinka OI, Abdulahi I, Atte PO (2018) Ameliorative effects of Bi-carbonate buffer, vitamin C and baobab fruit pulp meal on progesterone and testosterone secretion in heat stressed rabbits. Nig J Anim Sci 20:459–465
Asemota OD, Aduba P, Bello-Onaghise G, Orheruata AM (2017) Effect of temperature-humidity index (THI) on the performance of rabbits (Oryctolagus cuniculus) in the humid tropics. Archiv De Zootec 66:257–261
Askar AA, Ismail EII (2012) Impact of heat stress exposure on some reproductive and physiological traits of rabbit does. Egypt J Anim Prod 49:151–159
Badr AM (2015) Effect of feeding time and vitamin C levels on performance of rabbit does during the mild and hot seasons in Egypt. Nature and Sci 13:25–29
Bharti S, Misro MM, Rai U (2014) Quercetin supplementation restores testicular function and augments germ cell survival in the estrogenized rats. Mol Cell Endocrinol 383:10–20
Bloch V, Barchilon N, Halachmi I, Druyan S (2020) Automatic broiler temperature measuring by thermal camera. Biosys Eng 199:127–134
Bouwknecht JA, Olivier B, Paylor RE (2007) The stress-induced hyperthermia paradigm as a physiological animal model for anxiety: a review of pharmacological and genetic studies in the mouse. Neurosci Biobehav Rev 31:41–59. https://doi.org/10.1016/j.neubiorev.2006.02.002
Chipo MM, Mango L, Kugedera AT, Lovemore M (2019) Challenges and opportunities to rabbit (Oryctolagus cuniculus) production and marketing. Int J Agric Agribus 5:37–44
Collier RJ, Gebremedhin KG (2015) Thermal biology of domestic animals. Ann Rev Anim Biosci 3:10–20
Corino C, Modina S, Di Giancamillo A, Chiapparini S, Rossi R (2019) Seaweeds in pig nutrition. Animals 9:1126. https://doi.org/10.3390/ani9121126
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. Spanish J Agric Res 16:e0610. https://doi.org/10.5424/sjar/2018163-13184
Daader AH, Yousef MK, Abdel-Samee AM, Abd El-Nour SA (2016) Recent trends in rabbit does reproductive management: special reference to hot regions (Invited paper). Proceedings 11th World Rabbit Congress – June 15–18, 2016 - Qingdao - China, 149–166
Dalle Zotte A (2014) Rabbit farming for meat purposes. Anim Front 4:62–67
EFSA (2005) The impact of the current housing and husbandry systems on health and welfare of farmed domestic rabbits. Europ Food Safe Auth EFSA J 267:1–31
El-Bayoumi KM, Abdel-Hamid TM, El-Tarabany MS, Sherief WR (2018) Influence of stocking density on growth performance traits, blood chemistry and the expression of HSP70 and IGF-I genes in New Zealand White rabbits. Slov Vet Res 55:201–210
El-Hanoun AM, Elkomy AE, Fares WA, Shahien EH (2014) Impact of royal jelly to improve reproductive performance of male rabbits under hot summer conditions. World Rabbit Sci 22:241–248. https://doi.org/10.4995/wrs.2014.1677
El-Medany SA, El-Reffaei WHM (2015) Evaluation canola meal on growing rabbits; nutritionally and on their nutritional meat quality. J Food Nut Res 3:220–234
El-Raffa AM (2004) Rabbit production in hot climates. Proceedings - 8th World Rabbit Congress, September 7–10, 2004, Puebla, Mexico (Invited Paper)
El-Ratel I, Gabr AA (2019) Effect of spirulina and vitamin E on reproduction and in vitro embryo production in heat-stressed rabbits. Pak J Biol Sci 22:545–553
El-Ratel I, Attia KAH, El-Raghi AA, Fouda SF (2021) Relief of the negative effects of heat stress on semen quality, reproductive efficiency and oxidative capacity of rabbit bucks using different natural antioxidants. Anim Biosci 34:844–854
FAO (1997) The rabbit: husbandry, health and production. In: Lebas F., Coudert P., de Rochambeau H., Thebault R.G. (eds.). FAO Animal Production and Health 21. Food and Agriculture Organization of United Nations, Rome 250pp
Farghly MFA, Mahrose KM, Farghaly MM (2017) Changing feeding time to avoid the harmful effects of hot summer on performance of growing New Zealand White rabbits. Egypt J Rabbit Sci 27:447–461
Farghly MFA, Mahrose KM, Mahmoud GB, Ali RM, Daghash W, Metwally KA, Abougaba MS (2020) Lighting programs as an appliance to improve growing New Zealand white rabbit’s performance. Inter J Biometeorol 64:1295–1303. https://doi.org/10.1007/s00484-020-01906-z
Farghly MFA, Mahrose KM, Peris SI, Abou-Kassem DE, Metwally KA, Abougabal MS, Abd El-Aziz A (2021) Effects of lighting source as an environmental strategy for heat stress amelioration in growing Californian rabbits during summer season. Anim Biotechnol. https://doi.org/10.1080/10495398.2021.1895186
Fouad MA (2005) Some management practices to improve reproductive performance of New Zealand rabbit does in hot climate. J Egypt Med Ass 65:317–329
Frangiadaki E, Golidi E, Menegatos I, Luzi F (2003) Comparison of does’ performances under high and moderate temperature in a Greek commercial farm. World Rabbit Sci 11:137–143
Garcia ML, Argente MJ (2017) Exposure to high ambient temperatures alters embryology in rabbits. Int J Biometeorol 61:1555–1560
Gumus R, Gelen SU, Koseoglu S, Ozkanlar S, Ceylan ZG, Imik H (2018) The effects of fucoxanthin dietary inclusion on the growth performance, antioxidant metabolism and meat quality of broilers. Braz J Poultry Sci 20:487–496
Hahn GL, Gaughan JB, Mader TL, Eigenberg RA (2009) Thermal indices and their applications and thermal environmental managements. ASABE EP 113–130.
Haque A, Rahman M, Bora J (2016) Effect of breed, weaning age and feeding regime on chemical composition of rabbit meat. Int J Vet Sci Anim Husb 1:12–13
Harvell CD, Mitchell CE, Ward JR, Altimer S, Dobson AP, Ostfeld S, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Sci 296:2158–2162
Hassan F, Mahrose KM, Basyony MM (2016) Effects of grape seed extract as a natural antioxidant on growth performance, carcass characteristics and antioxidant status of rabbits during heat stress. Arch Anim Nutr 70:141–154
Hassan F, Mobarez S, Mohamed M, Attia Y, Mekawy A, Mahrose K (2021) Zinc and/ or selenium enriched spirulina as antioxidants in growing rabbit diets to alleviate the deleterious impacts of heat stress during summer season. Animals 11, accepted for publication.
Hernández P, Dalle Zotte A (2010) Influence of diet on rabbit meat quality. In: de Blas C, Wiseman J (eds) The nutrition of the rabbit. CABI-Publishing, Oxon, UK, pp 163–178
Hosny SH, Hashem NM, Morsy AS, Abo-elezz ZR (2020) Effects of organic selenium on the physiological response, blood metabolites, redox status, semen quality, and fertility of rabbit bucks kept under natural heat stress conditions. Frontier in Vet Sci 7:1–14
Hurst P, Termine P, Karl M (2005) Agricultural workers and their contribution to sustainable agriculture and rural development. FAO, Rome
Igono MO, Jotvedt G, Sanford-Crane HT (1992) Environmental profile and critical temperature effects on milk production of Holstein cows in desert climate. Int Biometerol 36:77–87
Jaén-Téllez JA, Sánchez-Guerrero MJ, López-Campos JI, Valera M, González-Redondo P (2020) Acute stress assessment using infrared thermography in fattening rabbits reacting to handling under winter and summer conditions. Spanish J Agric Res 18:e0502. https://doi.org/10.5424/sjar/2020182-15706
Jimoh OA, Ayedun ES, Oyelade WA, Oloruntola OD, Daramola OT, Ayodele SO, Omoniyi IS (2018) Protective effect of soursop (Annona muricata linn.) juice on oxidative stress in heat stressed rabbits. J Anim Sci Technol 60:28. https://doi.org/10.1186/s40781-018-0186-4
Jimoh OA, Ewuola EO (2016) Thermoregulatory response of exotic rabbit breeds during peak temperature-humidity index of Ibadan. Trop Anim Prod Invest 19:41–47
Jimoh OA, Ewuola EO (2018) Thermophysiological traits in four exotic breeds of rabbit at least temperature-humidity index in humid tropics. The J Basic Appl Zool 79:18–23
Jimoh OA, Ewuola EO, Balogun AS (2017) Oxidative stress markers in exotic breeds of rabbit during peak of heat stress in Ibadan. Nig J Adv Biol Biotechn 12:1–9
Kang S, Da-hye KİM, Lee S, Lee T, Kyung-woo L, Hong-hee C, Moon B, Ayasan T, Choi, YH (2020) An acute, rather than progressive, increase in temperature-humidity index has severe effects on mortality in laying hens. Frontiers. SCI. https://doi.org/10.3389/fvets.2020.568093
Kunc P, Knizkova I (2012) The use of infrared thermography in livestock production and veterinary field. In: Infrared Thermography Recent Advances and Future Trends (editor; Meola C.), Bentham Science Publishers, United Arab Emirates, pp. 85–101. https://doi.org/10.2174/97816080514341120101
Lamarca DSF, Pereira DF, Magalhães MM, Salgado DD (2018) Climate change in layer poultry farming: impact of heat waves in region of Bastos, Brazil. Braz J Poultry Sci 20:657–664
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
Lukefahr SD, Ruiz-Feria CA (2003) Rabbit growth performance in a subtropical and semi-tropical arid environment, effects of hair clipping, ear length and body temperature. Livest Res Rural Dev 15:1–9
Mady EA, Karousa MM, El-laithy SM, Souad AA (2018) Effect of season on New Zealand White (NZW) rabbits’ behavior and reproductive and productive performance. Benha Vet Med J 35:274–284
Maertens L, Gidenne T (2016) Feed efficiency in rabbit production: nutritional, technico-economical and environmental aspects. In: Proceeding of. 11th World Rabbit Congress - Abstracts, 15–18 June, 2016, Quingdao, China, 131–151.
Maertens L, Lebas F, Szendrö Z (2006) Rabbit milk: a review of quantity, quality and non-dietary affecting factors. World Rabbit Sci 14:205–230
Mahrose KM (2000) Environmental studies on growth and reproduction traits in rabbits. Thesis, Faculty of Agriculture, Zagazig University, Egypt, M.Sc
Mahrose KM, Abd El-Monem UM, Peris SI (2010) Effects of photoperiod and mating or semen collection times on the performance of does and bucks of New Zealand White rabbits under hot climatic conditions of Egypt. In The 6th International Conference on Rabbit Production in Hot Climates, pp. 503–520, February 1–4, Assuit, Egypt
Marai IFM, Ayyat MS, Abd El-Monem UM (2001) Growth performance and reproductive traits at first parity of New Zealand White female rabbits as affected by heat stress and its alleviation under Egyptian conditions. Trop Anim Health Prod 33:1–12
Marai IFM, Habeeb AAM, Gad AE (2002) Rabbit´s productive, reproductive and physiological performance traits as affected by heat stress: a review. Livest Prod Sci 78:71–90
Marco-Jiménez F, García-Diego FJ, Vicente JS (2017) Effect of gestational and lactational exposure to heat stress on performance in rabbits. World Rabbit Sci 25:17–25
Maya-Soriano MJ, Taberner E, Sabés-Alsina M, Ramon J, Rafel O, Tusell L, Piles M, Lopez-Bejar 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
Michalak I, Chojnacka K (2015) Algae as production systems of bioactive compounds. Eng Life Sci 15:160–176. https://doi.org/10.1002/elsc.201400191
Michalak I, Mahrose KM (2020) Seaweeds, intact and processed, as a valuable component of poultry feed. J Marine Sci Eng 8:620. https://doi.org/10.3390/jmse8080620
Mousa-Balabel TM, El-Sheikh RA, Moustafa EH (2017) New strategies for controlling heat stress in New Zealand White (NZW) Rabbits in Egypt. Life Sci J 14:64–70
Mousa-Balabel TM (2004) Effect of heat stress on New Zealand White rabbits’ behavior and performance. Minufiya Vet J 3:125–134
Naseer Z, Ahmad E, Epikmen ET, Uçan U, Boyacioğlu M, Ipek E, Akosy M (2017) Quercetin supplemented diet improves follicular development, oocyte quality, and reduces ovarian apoptosis in rabbits during summer heat stress. Theriogen 96:136–141
Okab AB, El-Banna SG (2003) Physiological and biochemical parameters in New-Zealand white male rabbits during spring and summer seasons. Egypt J Basic Appl Physiol 2:289–300
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 41:12–19
Ondruska L, Rafay J, Okab AB, Ayoub MA, Al-Haidary AA, Samara EM, Parkanyi V, Chrastinova L, Jurcik R, Massanyi P, Lukac N, Supuka P (2011) Influence of elevated ambient temperature upon some physiological measurements of New Zealand White rabbits. Vet Med 56:180–186
Oseni SO, Lukefahr SD (2014) Rabbit production in low-input systems in Africa; situation, knowledge and perspective – a review. J World Rabbit Sci Assoc 22:147–160
Øverland M, Mydland LT, Skrede A (2018) Marine macroalgae as sources of protein and bioactive compounds in feed for monogastric animals. J Sci Food Agric 99:13–24. https://doi.org/10.1002/jsfa.9143
Panesar R, Kaur S, Panesar PS (2015) Production of microbial pigments utilizing agroindustrial waste: a review. Curr Opin Food Sci 1:70–76
Pascual JJ, Fonfria MJ, Alqedra I, Cervera C, Fernández–Carmona J (2000) Use of lucerne-based diets on reproductive rabbit does. Proceeding pof 7th World Rabbit Congress, Valencia, Spain, C 379–384
Pei Y, Wu Y, Cao J, Qin Y (2012) Effects of chronic heat stress on the reproductive capacity of male Rex rabbits. Livest Sci 146:13–21
Perenlei G, Tojo H, Okada T, Kubota M, Kadowaki M, Fujimura S (2014) Effect of dietary astaxanthin rich yeast, Phaffia rhodozyma, on meat quality of broiler chickens. Anim Sci J 85:895–903
Sabatakou AO, Xylouri ME, Sotirakoglou AK, Fragkiadakis GM, Noikokyris NP (2007) Histochemical and biochemical characteristics of weaning rabbit intestine. World Rabbit Sci 15:173–178
Sabés-Alsina M, Tallo-Parra O, Mogas MT, Morrell JM, Lopez-Bejar M (2016) Heat stress has an effect on motility and metabolic activity of rabbit spermatozoa. Anim Reprod Sci 173:18–23
Sakr OG, Mousa BH, Emam KRS, Morsy AS, Ahmed NA (2019) Effect of early heat shock exposure on physiological responses and reproduction of rabbits under hot desert conditions. World Vet J 9:90–101
Saracila M, Panaite T, Tabuc C, Soica C, untea A, Ayasan T, Criste RD, (2020) Dietary ascorbic acid and chromium supplementation for broilers reared under thermoneutral conditions vs. high heat stress. Sci Paper-Anim Sci Series: Lucrări Ştiinţifice - Seria Zootehnie 73:41–47
Sharaf AK, El-Darawany AA, Nasr AS, Habeeb AAM (2019) Recent techniques for amelioration the effect of heat stress conditions on male rabbits. Zag J Agric Res 46:501–514
Sharaf AK, El-Darawany AA, Nasr AS, Habeeb AAM (2021) Alleviation the negative effects of summer heat stress by adding selenium with vitamin E or AD3E vitamins mixture in drinking water of female rabbits. Biol Rhythm Res 52:535–548. https://doi.org/10.1080/09291016.2019.1613796
Shebl HM, Ayoub MA, Kishik WH, Khalil HA, Khalifa RM (2008) Effect of thermal stresses on the physiological and productive performance of pregnant doe rabbits. Agric Res J 8:15–24
Shehu BM, Buba W, Yusuf M (2018) Probiotic supplemented-diet mitigated the effects of hot-dry season on growth performance and welfare of rabbits in Zaria, Kaduna State. Nig J Anim Sci 20:55–60
Sheiha AM, Abdelnour SA, Abd El-Hack ME, Khafaga AF, Metwally KA, Ajarem JS, Maodaa SN, Allam AA, El-Saadony MT (2020) Effects of dietary biological or chemical-synthesized nano-selenium supplementation on growing rabbits exposed to thermal stress. Animals 10:430
Stott PG, Jennings N, Harris S (2010) Is the large size of the pinna of the ear of the European hare (Lepus europaeus) due to its role in thermoregulation or in anterior capital shock absorption? J Morphol 271:674–681
Szendrő Z, Papp Z, Kustos K (2018) Effect of ambient temperature and restricted feeding on the production of rabbit does and their kits. Acta Agraria Kaposvariensis 22:1–17
Thornton PK, van de Steeg J, Notenbaert A, Herrero M (2009) The impacts of climate change on livestock and livestock systems in developing countries: a review of what we know and what we need to know. Agric Syst 101:113–127
Turner TT, Lysiak JJ (2008) Oxidative stress: a common factor in testicular dysfunction. J Androl 29:488–498
Ume SI, Ezeano CI, Onwujiariri EB (2018) Effect of climate change on rabbit production and choice of adaptation coping strategies by smallholder farmers in Anambra State, Nigeria. Int J Innovations Agric Sci 2:161–173
UNO (2015) Population 2030: Demographic challenges and opportunities for sustainable development planning (ST/ESA/SER.A/389). United Nations Organisation, Department of Economic and Social Affairs, Population Division.
Villalobos O, Guillen O, Garcia J (2008) Effect of cage density on growth and carcass performance of fattening rabbits under tropical heat stress conditions. World Rabbit Sci 16:89–97
Virmani M, Neelam SK, Kapoor PK, Malik RK, GERA S, (2019) Amelioration of heat stress in rabbits through supplementation of Emblica officinalis. Haryana Vet 58:127–129
Yaeram J, Setchell BP, Maddocks S (2006) Effect of heat stress on the fertility of male mice in vivo and in vitro. Reprod Fert Dev 18:647–653
Yagci A, Zik B, Uguz C, Altunbas K (2006) Histology and morphometry of White New Zealand rabbit skin. Ind Vet J 83:876–880
Yassein SA, Mahmoud KGM, Maghraby N, Ezzo OH (2008) Hot climate effects and their amelioration on some productive and reproductive traits in rabbit does. World Rabbit Sci 16:173–181
Zeferino CP, Komiyama CM, Fernandes S, Sartori JR, Teixeira PSS, Moura ASAMT (2013) Carcass and meat quality traits of rabbits under heat stress. Anim 7:518–523
Zeweil HS, Mandour MA, Mahmoud SAS, El-Gendy YM (2009) Effect of ascorbic acid supplementation on does of rabbits exposed to different ambient temperatures. J Appl Sci Res 5:2448–2460
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The authors acknowledge the encouragement and support of Prof. Olusegun Ayodeji Osinowo of the Department of Animal Physiology, Federal University of Agriculture, Abeokuta, Nigeria.
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Oladimeji, A.M., Johnson, T.G., Metwally, K. et al. Environmental heat stress in rabbits: implications and ameliorations. Int J Biometeorol 66, 1–11 (2022). https://doi.org/10.1007/s00484-021-02191-0
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DOI: https://doi.org/10.1007/s00484-021-02191-0