Edited by: Anusorn Cherdthong, Khon Kaen University, Thailand
Reviewed by: Wuttigrai Boonkum, Khon Kaen University, Thailand; Adham Al-Sagheer, Zagazig University, Egypt
This article was submitted to Animal Nutrition and Metabolism, a section of the journal Frontiers in Veterinary Science
†These authors have contributed equally to this work and share first authorship
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Heat stress has become a widespread concern in the world, which is one of the major environmental stressors and causes substantial economic loss in the rabbit industry. Heat stress leads to multiple damages to the health of rabbits, such as organ damage, oxidative stress, disordered endocrine regulation, suppressed immune function and reproductive disorders, ultimately, induces the decreased production performance and increased mortality. Nutritional approaches, including feeding strategies, adjusting feed formula, and supplementing vitamins, minerals, electrolytes, Chinese herbal medicines, and functional active substances to the feed, were reported to mitigate the detrimental effects of heat stress in rabbits. Therefore, elucidating the damage of heat stress to rabbits; proper management and nutritional approaches should be considered to solve the heat stress issue in rabbits. This review highlights the scientific evidence regarding the effects of heat stress on rabbit's immune function, endocrine, blood biochemical changes, antioxidant capacity and production performance, and the potential mitigation strategies of nutritional intervention to alleviate heat stress in rabbits; which could contribute to develop nutritional strategies in relieving heat stress of rabbits.
During recent years, the rabbit meat production is growing in China and European countries to meet the increasing demands of diverse meat product, which has become a highly specialized industry (
Heat stress is a condition where rabbits are unable to maintain a balance between heat production and emission. High ambient temperature in summer is easy to cause heat stress in rabbits, which brings a series of adverse effects to rabbit production (
Challenges and opportunities for the rabbit industry in the context of global warming-induced heat stress.
The immune dysfunction in rabbits caused by heat stress through the regulation of brain, sympathetic nerve and adrenal cortical hormone (
Under high ambient temperature, the synthesis of hypothalamic thyroid stimulating hormone (TSH) is highly reduced, resulting in a decrease of TSH in the anterior lobe of the pituitary gland and a reduction of thyroid hormone in rabbits; the decreased thyroid hormone could lower the metabolic rate and heat production of rabbits (
The blood biochemical index plays a crucial role in reflecting the metabolic changes and organ damage in rabbits under heat stress situation. The concentrations of total protein, blood glucose and triglyceride are decreased, whereas cholesterol concentrations are markedly increased during heat stress in rabbits (
The produced free radicals are removed to maintain a dynamic balance in the body during thermoneutral temperature. As summarized in
Effects of heat stress on antioxidant capacity and related signaling pathway of rabbits.
The reproductive performance of rabbits is an important trait that affecting the economic benefits of rabbit production. The high reproductive performance leads to short generation interval in rabbit which provide the needed animal protein with low capital outlay and time (
The growth of embryos, pregnancy rate, litter size, litter weight and milk yield of female rabbits are affected by heat stress (
Male rabbits are more sensitive to high temperatures than female rabbits. The synthesis and secretion of hypothalamic gonadotropin-releasing hormone (GnRH) are inhibited under high temperature, which significantly affects the function of testis and decreases the semen quality in male rabbits (
As summarized in
Summarize the impacts of heat stress on rabbits.
Carcass and meat quality traits of rabbits, such as tenderness and color, are crucial to consumer acceptance (
Compared with morning and evening, the appetite of rabbits is decreased in the summer noon. Therefore, the feeding strategy of rabbits needs to be combined with its physiological status to adjust the feeding time and amount. The specific strategies are to appropriately increase the feeding in the morning and evening, less fed or feeding of the green and juicy feeds are used at noon (
The beneficial effects of nutritional strategies in heat-stressed rabbit.
Green and juicy food | – | Decrease heat stress and relieve thirst and diuresis, prevent rabbit coccidiosis and enteritis | ( |
Ice water | – | The body weight ↑, feed intake and feed conversion rate ↑ | ( |
Fat | 3,050 Kcal DE kg−1 of diet | Production performance (e.g., body weight, daily weight gain, litter size and weight, reduce pre-weaning mortality)↑ | ( |
– | Improve the palatability of feed, the appetite ↑, feed intake and growth rate ↑ | ( |
|
Amino acid | 50–100 mg kg−1 of diet | Haemato-biochemical and reproductive indicators in male rabbits↑ | ( |
Vitamin C | 500 mg kg−1 of diet | (1) T3, T4 ↑cortisol and glucose levels, body temperature↓ | ( |
200 mg kg−1 of diet | (2) Corticosterone and MDA in blood ↓ | ( |
|
200 mg kg−1 of diet | (3) Reverse the liver and kidney dysfunction | ( |
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200 mg kg−1 of BW | (4) mRNA and protein expression of HSP70 in liver and kidney tissues ↑ cortisol and leptin ↓, satiety signal ↑ | ( |
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1g L−1 in DW | (5) Productive and reproductive performance, oocyte maturation rate↑ | ( |
|
Vitamin E | 40 mg kg−1 of diet | (1) Semen quality; T3, T4 hormonal levels↑, body temperature and respiration rate↓. | ( |
320–640 mg kg−1 of diet | (2) T-AOC ↑ | ( |
|
150 mg kg−1 of diet | (3) Semen quality, plasma glucose, high-density lipoprotein↑ plasma cholesterol and triglyceride ↓ | ( |
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100 mg kg−1 of diet | (4) Pregnancy rate, litter size, lipid metabolism, antioxidant capacity ↑ | ( |
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Vitamin A | 750 IU of diet | (1) Antioxidant enzyme activity ↑, lipid peroxidation ↓ | ( |
1.2–1.5 times higher than NRC (1977) | (2) Skin temperature, rectal temperature and pulse ↓ | ( |
|
NaHCO3 | 300 mg kg−1 of BW | (1) Dissolving mucus, invigorating the stomach, inhibiting acid and increasing appetite | ( |
– | (2) Sodium↑ and respiratory alkali poisoning ↓ | ( |
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0.1–0.2% in DW | (3) Invigorate the stomach and regulate blood acid-base balance | ( |
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KCl | – | (1) Maintains intracellular osmotic pressure and acid-base balance | ( |
0.3–0.5% in DW | (2) Relieve heat stress, replenish potassium loss, and maintain blood potassium concentration. | ( |
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KHCO3 | – | (1) Maintain the blood potassium concentration and improve the HCO3- concentration | ( |
2.5% in diet | (2) Production performance and blood biochemical indexes ↑ | ( |
|
NH4Cl | 2% in DW | Recover the high blood pH value, regulate acid-base balance and prevent respiratory alkali poisoning | ( |
Zinc | 1.5 times higher than NRC (1977) | (1) Anti-heat stress agent, trace elements in milk ↑, litter size and weight ↑ | ( |
1 mg subcutaneous injection | (2) The lipid metabolism function ↑ | ( |
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Chromium | 0.8–1.0 mg kg−1 of diet | (1) Alleviate the damage on testicular spermatogenic function testosterone, LH and FSH in serum ↑ | ( |
0.4 mg kg−1 of diet | (2) Daily gain and feed intake ↑, cellular immunity function ↑ | ( |
|
Selenium | 0.3 mg kg−1 of diet | (1) Rectal temperature ↓, serum total protein content, albumin content and GSH-Px activity ↑. The total protein, albumin, ALT, fructose and total antioxidant capacity ↑, MDA ↓ | ( |
25–50 mg kg−1 of diet | (2) Body weight and average daily gain ↑, GSH and CAT activities ↑and reduce MDA ↑ | ( |
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Chinese herbal medicines | – | (1) Immunologic enhancement and antivirus action | ( |
20 mg injection | (2) Lymphocyte proliferation and antibody titer ↑ | ( |
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1–3% in diet | (3) Production performance, reproductive performance and antioxidant level ↑ | ( |
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1% in diet | (4) Mortality ↓ | ( |
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5% in diet | (5) Intestinal mucosa structure ↑ | ( |
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4.4 g in diet | (6) Sperm yield and survival rate ↑, sperm malformation rate ↓ | ( |
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L-Carnitine | 50 mg kg−1 of diet | (1) Rectal temperature, heart rate, and respiration rate ↓, growth indices, feed conversion ratio, blood hemoglobin, white blood cell counts, total protein, glucose, and red blood cell counts ↑ | ( |
100 mg kg−1 of diet | (2) Sperm motility, serum antioxidative status ↑ | ( |
|
Algae | 100 mg kg−1 of diet | (1) Production performance, antioxidants indices ↑, inflammatory responses and intestinal pathogens ↓ | ( |
300 mg kg−1 of diet | (2) Conception rate, kindling rate, litter size, embryo quality and the ovulatory response ↑ | ( |
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Essential oils | 300 mg kg−1 of diet | Plasma testosterone concentration and GSH activity, sperm output, sperm cell counts, intact acrosome, sperm normality ↑, sperm cells with abnormal tail and plasma MDA contents ↓ | ( |
100–150 mg kg−1 of diet | Haemato-biochemicals constitutes, immunologic status, antioxidant capacity, and fertility traits ↑, lipid peroxidation ↓ | ( |
|
Plant extract | 100–300 mg kg−1 of diet | (1) Growth performance, carcass traits and antioxidant status ↑ | ( |
5–10 g kg−1 of diet | (2) Body weight, feed intake, SOD, T-AOC and GSH-Px ↑, MDA and cortisol content ↓ | ( |
|
50 mg kg−1 of BW | (3) Heat tolerance, oxidative status and semen quality ↑ | ( |
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1,000 mg kg−1 of diet | (4) Hematological and antioxidative indicators ↑ | ( |
|
10 mg kg−1 of BW | (5) Redox status, hormonal balance, total litter size, kindling rate, litter size at birth and litter weight at birth ↑ | ( |
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Tannins | 10 g·kg−1 of diet | Body weight, feed intake, SOD, T-AOC and GSH-Px activities ↑, MDA and cortisol levels ↓ | ( |
5 or 10 g·kg−1 of diet | Growth performance, carcass and meat quality traits ↑, lipid peroxidation of meat ↓ | ( |
The feed intake of rabbits is significantly decreased during heat stress, resulting in insufficient nutrients and energy intake (
During protein digestion, heat is produced in the metabolic process due to the serious heat increment, and the heat dissipation is greatly decreased during heat stress (
In addition to adjusting the energy and protein concentrations in the feed formula, it has been found that the pellet feed has high nutrient density and ideal palatability, which can also improve the production performance of heat-stressed rabbits (
Vitamin C, known as ascorbic acid, provides anti-stress and antioxidant function (
Vitamin E is an intracellular antioxidant, and its lipid solubility makes it a suitable membrane antioxidant against oxidative damage, maintaining the function of the cell membrane system and reducing the release of creatine kinase in muscle cells during stress, thereby preventing excessive calcium influx and interfering with normal cell metabolism (
Vitamin A is associated with innate immunity, T cell proliferation and antibody production (
Because of the dense hair and absence of sweat glands, rabbits use their ears and respite to decrease the body temperature during heat stress (
The activity of more than 300 enzymes (e.g., oxidoreductases, transferases, hydrolases, lyases, isomerases, and ligases) requires zinc as substrates (
Chromium is an essential mineral, which is an integral component of chromodulin and also necessary for insulin functioning (
Selenium is involved in many key physiological processes, such as reproduction, immunity and growth, and is an essential trace element for mammals (
Chinese herbal medicines and their ingredients equip immunologic enhancement and antivirus action, which can be used as immunopotentiator or anti-infection drugs (
At present, the functional active substances, including L-carnitine, algae, essential oils, plant extract, tannins etc., which have been got growing attentions and were also used to improve the health and production in rabbit during heat stress.
L-carnitine (LC) is a functional additive which work as an important role in fatty acid metabolism and energy production (
Algae have been exhausted for several years as nourishment for people and animals owing to the outstanding nutritious profile and great carotenoid substance (
The essential oils have been widely used as effective feed additives for promoting the growth performance in animals, and they appear many beneficial aspects such antimicrobial and antioxidant functions (
Plant extract has also been used to decrease the heat stress in recent year. Grape seed extract contains a lot of polyphenols, which are powerful free radical scavengers and antioxidants to decrease the oxidative stress and DNA damage (
Tannins are a group of polyphenolic compounds, which consist of aromatic rings with one or more hydroxyl groups, which can combine with free radicals to form resonance-stabilized phenoxyl radicals, this structure indicate the strong antioxidant properties of tannins (
The role of functional active substances in relieving heat stress of rabbits is due to the biological activities, such as antioxidant, anti-inflammatory, antibacterial functions, therefore, the bioactive substances have broad application prospects in rabbits under heat stress situation. However, existing reports mainly researched the protective effects of active substances on growth rate, carcass traits, meat quality, reproductive performance, redox status, and immune response of heat-stressed rabbits, the study of molecular mechanism is lacking. In future studies, it is necessary to elucidate the underlying mechanisms of the beneficial effects of active substances in rabbits under heat stress. Meanwhile, it is also worthwhile to study the mitigation effect of active substances on heat stress-induced impairment of intestinal barrier function in rabbits.
In summary, heat stress has been a severe challenge for modern rabbit industry, especially in the tropical and subtropical regions. Heat stress results from several factors (e.g., high environmental temperature and humidity, high stocking density), which causes a series of unfavorable changes in immune function, endocrine, blood biochemical indexes and antioxidant capacity, thus negatively affecting the production performance (e.g., growth rate, carcass and meat quality, reproductive performance) in rabbits. Therefore, researchers need to further study the physiological change caused by neuroendocrine under heat stress and figure out a holistic approach to attenuate the detrimental effect of heat stress on rabbits. The potential use of feeding strategies and nutritional regulation could be beneficial to ameliorate heat stress. Further studies should be attempted on the combination of several approaches for relieving heat stress and evaluating the efficiency and economic benefit in rabbit production.
BB and W-CL: conceptualization and writing—review and editing. Z-LL, SP, and FC: selection and collection of bibliographies, and the data curation. Z-LL and FC: writing—original draft preparation. W-CL: supervision, project administration, and funding acquisition. All authors have read and agreed to the published version of the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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