Table 1.

Summary of the functional roles of taurine, L-theanine, L-citrulline and betaine in poultry species

Animal model	Dosage and administration	Stress model/study design	Major findings	Reference
Taurine
One-day-old Ross broilers	0.1% taurine was added to drinking water from 2 weeks of age	The treatments consisted of control birds which were reared at 24 °C and HS group at 34 °C, 60% RH from 3 to 5 weeks of age	Taurine lowered the gene and protein expressions of heat shock proteins in the liver and muscle tissues of HS broilers	[68]
Julia layer chicks (6 days old)	Taurine was dissolved in 0.85% saline containing 0.1% Evans blue for intracerebroventricular (ICV) injection	Chicks were ICV injected with either saline or 5 μmol taurine and exposed to either 35 ± 1 °C or 30 ± 1 °C for 60 mins in temperature controlled chambers	Central taurine induced dose-dependent hypothermia and inhibited food intake under control temperature. During heat stress, central taurine altered the plasma metabolites suggesting that brain taurine may supply energy and protect against oxidative stress during high temperature in chicks.	[69]
Male Arbor Acres broilers	Basal diet was supplemented with 5 g/kg taurine	Broilers were raised at thermoneutrality, 22 °C or under consistent HS at 32 °C, 55 ± 5% RH from 28 days of age	Taurine had no positive effects on the growth performance of HS birds but it alleviated the adverse impacts of HS on the jejunal morphology, increased duodenal somatostatin and peptide YY hormones, and upregulated the intestinal expression of appetite related genes in HS broilers	[70]
Male Arbor Acres broiler chicks	Broilers were fed the basal diet supplemented with 5.00 g/kg taurine	At 28 days old, broilers were subjected to thermoneutral (22 °C), consistent HS, (32 °C), or HS + Taurine (consistent 32 °C, basal diet + 5.00 g/kg taurine) and 55 ± 5% RH for a 14-day trial	Taurine decreased reactive oxygen species and malonaldehyde but increased nuclear factor erythroid 2-related factor 2 (Nrf2), NAD(P) H quinone dehydrogenase 1 and heme oxygenase 1 expression in HS broilers. Taurine also alleviated mitochondrial damage and improved the breast meat quality in chronic HS broilers	[71]
Male Arbor Acres broilers	Broilers were fed basal diet supplemented with 5.00 g/kg taurine from 28 days old	Broilers were randomly distributed to positive control (22 °C, basal diet), HS, (constant 32 °C, basal diet), or heat stress + taurine, 55 ± 5% RH for 14 d.	Taurine supplementation did not alleviate the high cloacal temperature in chronic HS broilers. Taurine improved the carcass by facilitating lipolysis for energy, enhancing protein synthesis, and suppressing protein degradation in the breast muscles in HS broilers	[72]
Male Arbor Acres broilers	Experimental diet was supplemented with 5 g/kg taurine	Broilers were grouped as control group (22 °C), HS group (32 °C) and HS + taurine fed group	Taurine supplementation attenuated breast muscle loss induced by chronic HS via reversing endoplasmic reticulum stress induced apoptosis and suppressing protein catabolism. Taurine moderated the decreases in breast muscle mass and yield in chronic HS broilers.	[73]
Laying Japanese quails (Coturnix coturnix japonica) at 5 weeks of age	Taurine was supplemented at 2.5 or 5 g/kg diet	Animals were housed in temperature-controlled rooms for 12 weeks at either 22 ± 2 °C for 24 h per day considered as thermoneutral or under 34 ± 2 °C for 8 h per day, followed by 22 °C for 16 h considered as heat-stress (HS).	Taurine supplementation, especially at higher dose(5 g/kg) improved the production performance, nutrient digestion, and ileal nutrient transport in HS quails	[74]
L-Theanine
Male WENS yellow-feathered broilers	Birds received a corn soybean meal basal diet in mash form or a basal diet supplemented with 800 mg/kg L-theanine	At 24, 25 and 26 days of age, birds were intra-abdominally injected with 0.2 mL sterile saline or LPS (Escherischia coli serotype O127:B8) dissolved in saline at adequate doses of 600 mg/kg BW	L-theanine exerted a protective role on the growth performance of LPS-challenged broilers and attenuated LPS-induced immune stress	[17]
Arbor Acre broilers	Basal diets were supplemented with different concentrations of L-theanine at 0, 100, 200 and 300 mg/kg feed	Experimental birds were divided into 4 treatments groups of control and 3 levels of L-theanine supplementation	Supplementation of L-theanine up to 200 mg/kg enhanced the growth performance, meat quality, immune response, and anti-oxidant status of broilers but reduced the total serum cholesterol levels. However, higher dose up to 300 mg/kg L-theanine may pose deleterious effects on the performance and health of birds.	[75]
Arbor Acre broilers	L-theanine was mixed in basal diets at different concentrations at 0, 100, 200, and 300 mg/kg feed	Experimental treatments included control (basal diet); basal diet + 100mg L-theanine/kg diet; basal diet + 200mg L-theanine/kg diet; and basal diet + 300mg L-theanine/kg diet	L-theanine promoted immune and growth responses by favoring the abundance of beneficial gut microbes and downregulating the expression of inflammatory mediators	[76]
Yellow-feathered broilers	L-theanine was provided at four different levels of 100, 200, 400 and 800 mg/kg	Broilers were grouped as the control group (basal diet); antibiotic group; and four L-theanine test groups at different levels of 100, 200, 400 and 800 mg/kg diet. The test period was 49 d.	L-theanine had no adverse effects on the production performance and immune organ index of yellow feather broilers at different production stages	[77]
Egg laying chickens	L-theanine was provided as 200 mg/kg in the basal diets	The ambient room temperature of experimental chickens was controlled at 32 ± 3 °C, and 70% RH. The trial period lasted for 28 d	L-theanine had no significant effect on the growth performance of chickens. However, L-theanine increased the catalase activity but reduced malondialdehyde content in various tissues providing antioxidant effects	[78]
Chaohu ducks	Basal diets were supplemented with 0 (control), 300, 600, 900 and 1500 mg/kg of L-theanine	Room temperature was between 27 to 36 °C, with 70% RH. Lighting period was 23 h/d and the trial lasted for 28 d	L-theanine yielded significant improvements in immune function and jejunum morphology and antioxidant capacity of ducks. The optimum inclusion levels of L-theanine was 600 to 900 mg/kg based on the current experimental condition	[79]
Male Ross 308 broilers	Dietary L-theanine was supplemented at 600 mg/kg of diet	Broilers were subjected to 3 protocols of 0-h transport (control group), 3-h transport, and 3-h transport + dietary L-theanine supplementation	L-theanine alleviated transport-stress-impairment of immune organ indexes and meat quality of broilers. L-theanine reversed the detrimental effects of transport stress on muscle antioxidant capacity and glycolysis metabolism.	[80]
Betaine
Hens and roosters of Mandarah strain	Dietary supplementation of 1000 mg/kg betaine	Control conditions: 22–24 °C; 45–55% RH or Chronic HS at 38 ± 1 °C; 55–65% RH from 11:00 to 15:00 h for 3 weeks	Betaine supplementation during chronic HS improved the body weight gain, survival rate, laying rate, egg mass and feed intake	[81]
Mandarah (a dual-purpose breed) chickens	Basal diet supplemented with 1000 mg/kg of betaine	Thermoneutral conditions of 22–24 °C, 45–55% RH or chronic HS (38 ± 1 °C; 55–65% RH) for three successive days a week, from 11:00 to 15:00 h	Betaine supplementation alleviated the adverse effects of chronic HS by improving the semen characteristics, fertility, physiological, haematological indices, antioxidant status, wellbeing, and intestinal DNA functions of breeder roosters	[82]
Male White Ross breed broiler chickens	Daily oral administration of betaine hydrochloride at 250 mg/kg for 42 d	Hot dry season having dry-bulb temperature (28.33-35.67 °C), relative humidity (69.0-93.0%), and THI (27.85-36.1)	Betaine and its co-administration with ascorbic acid decreased fearfulness in birds and increased antioxidant enzymes activities of SOD and GPx activity in broiler chickens	[83]
Female Japanese quails	Dietary supplementation of betaine at 2 g/kg of feed	Dry season conditions with highest mean dry-bulb temperature of 32.0 to 32.1 °C, highest mean THI of 85.4­-85.5 and highest mean RH of 79.6%	Dietary enrichment with betaine and ascorbic acid improved activities of serum sex and stress hormones, and erythrocytic parameters of Japanese quails during thermally stressful dry season.	[84]
Day-old broiler chicks	Betaine (Betafin.), was administered at the dose rate of 50 g/50 kg of feed from the first day of experiment	Hot summer season (average temperature, 34.6 °C) where HS birds were managed without using desert cooler	Betafin improved the growth performance and immunity of birds during heat stress	[85]
Ross 308 male broiler chickens	1 g/kg feed of betaine was added in powder form on top of the basal diets	HS chickens were housed in a chambers at 34 °C for 8 h (9:00–17:00 h).	Dietary betaine improved the growth performance (ADG, EPI, FCR) and humoral immunity against NDV and infectious bronchitis virus in heat-stressed broilers	[86]
Yellow-feathered male broilers (Huaixiang chickens)	Basal diets supplemented with 500, 1000, 2000 mg/kg betaine	Birds were exposed to thermoneutral conditions of 26 ± 1 °C or cyclic HS of 32 ± 1 °C for 8 h/d from 9:00 to 17:00 h with 65–75% RH	Dietary betaine alleviated the impacts of long term HS on the growth performance, digestive function, and carcass traits in indigenous yellow-feathered broilers.	[87]
Meat-type ducks	Betaine was supplemented at 700, 1000 and 1300 ppm betaine	From 22 to 42 days of age, heat wave was applied at 11:00 to 17:00 h, 33 to 43 °C, and 70% RH, followed by maintaining at 22 to 26 °C from 17:00 to 11:00 h, 50% RH	Betaine supplementation had beneficial effects on the short chain fatty acid levels, hematological parameters, and body weight of heat stressed ducks.	[88]
Hy-line Brown laying hens	3.0 or 6.0 g/kg of purified betaine was supplemented to the basal diet at the expense of celite.	Hens were raised during the hot season with 25.8 ± 2.0 °C average daily room temperature, 74.8 ± 7.3% RH, and heat stress index of 76	Dietary betaine improved the hen-day egg production, decreased the broken and shell-less egg production and selectively modified the jejunal tight junction-related genes in laying hens raised under hot environment	[89]
Male broiler chickens (Cobb × Cobb)	Betaine (Betafin®) was supplied in the drinking water (50 g/kg) or feed (100 g/kg)	Broilers were subjected to 34 ± 1 °C, 75% RH for 4 h in environmental chambers at 35 day, then increased to 36 ± 1 °C for 4 h/d from d 36 to 41.	Study revealed that birds supplemented with betaine via drinking water had better resistance against high ambient temperatures than birds fed betaine in diets	[28]
L-Citrulline
Ross 308 broiler chickens	Dietary supplementation with 1% L-Citrulline of basal diet	Broilers were subjected to two environments, either thermoneutral at 24 °C or HS at 35 °C for 5 h, 60% RH	L-Citrulline affected the body temperature, antioxidant status, heat shock response and nitric oxide regeneration of broilers during HS and at thermoneutrality	[24]
Hy-Line Brown laying hens	Dietary addition at 0.25%, 0.5%, and 1% L-citrulline to basal diets	Summer season with average daily minimum and maximum temperatures of 25.02 °C and 31.01 °C	Dietary L-Citrulline did not influence the production performance, and rectal temperature of laying hen. L-Citrulline modulated systemic arginine metabolism, nitric oxide synthesis, and antioxidant defences of laying hens	[90]
Hy-Line Brown laying hens	Diets were offered as a reduced protein diet deficient in Arginine supplemented with 0.35% L-Citrulline at the expense of wheat	Birds were fed commercial diets 16 to 20 weeks of age and experimental diets started from 21 to 40 weeks of age.	Supplementation of either L-Citrulline to reduced protein diets did not affect the egg quality, protein and energy digestibilities of hens but tended to increase the Haugh unit and lower the shell breaking strength of eggs	[91]
KUB Chicks	Oral administration of L-citrulline at 3.75, 7.5 and 15 mmol/kg body weight.	5 days old chicks received L-Citrulline orally	L-Citrulline did not influence the feed intake, body temperature or plasma metabolites in chicks.	[92]
Male layer chicks (Julia)	Chicks received oral administration of L-Cit (15 mmol/10 mL/kg body weight) as single or double doses	Birds were exposed to HS (35 ± 1 °C) or thermoneutral temperature (30 ±1 °C) for 180 mins.	Single L-citrulline administration caused persistent hypothermia and lowered plasma glucose without affecting food intake. Dual administration of L-Citrulline afforded thermotolerance without a significant change in plasma nitric oxide of chicks	[23]
Male layer chicks (Julia)	L-Citrulline was administered as i.c.v. injection at 1 μmol/10 μL dosage. Orally administered L-citrulline was at 3.75, 7.5 or 15 mmol/10 mL/kg body weight	Exp. 1 was an intracerebroventricular (i.c.v.) injection while Exp. 2 was the oral administration of L-citrulline	Central citrulline did not alter body temperature, whereas, peripheral L-citrulline had a hypothermic effect in a dose responsive manner. Rectal temperature was decreased at 30, 60 and 120 mins after injection of the highest dose of L-Citrulline.	[93]
Male layer chicks (Julia)	Oral administration of watermelon rind extract (1.6 mL) or L-Cit (15 mmol/10 mL)	Chickens were treated with dual oral administration of (1.6 mL) watermelon rind extract or L-Cit (15 mmol/10 mL and exposed to high ambient temperature (35 ± 1 °C, 2 h) for 120 mins	Watermelon rind extract reduced rectal temperatures under control and heat stressed conditions in a similar fashion as high L-citrulline treatment	[94]
Male layer chicks (Julia)	Watermelon rind dried powder (WRP) was mixed with commercial starter diet to prepare a 9% WRP mash diet.	WRP mash diet was fed to 3- to 15-day-old chicks	Chronic supplementation of the WRP mash diet increased plasma L-citrulline levels, but did not affect the body temperature in chicks	[95]
Layer chicks	Oral administration of either a medium containing L-Citrulline producing live bacteria and 277 mmol/L L-Citrulline or an equimolar amount of L-Citrulline	In Exp. 1, chicks were orally administered treatments at 7-day-old and in Exp. 2, chicks were subjected to chronic treatment from 7 to 13 days of age	Acute or chronic administration of the media containing L-citrulline-producing live bacteria decreased the rectal and surface body temperatures of chicks, but an equimolar amount of L-citrulline elicited no changes	[96]
Ross 308 cockerels	L-citrulline was supplemented to low protein deficient in Arg at two levels of 0.238% and 0.476% L-Citrulline	Dietary treatments included eight groups assigned as normal-protein diet; low-protein diet deficient in Arginine (LP) and LP with two levels of either Arginine (0.238% and 0.476%), guanidinoacetic acid (0.309% and 0.618%) or Citrulline (0.238% and 0.476%).	L-Citrulline supplementation to low protein diets increased the body weight gain, carcass yield, bone length, diameter and ash but did not increase the ileal energy or nitrogen digestibility	[97]