Abstract
Heat stress (HS) poses significant challenges to broiler production, negatively influencing growth performance and meat quality. This study explores the resilience and the meat quality of hybrid chickens with dwarf size and frizzled feather traits to HS. We investigated F1 progeny derived from a crossbreed of dwarf yellow chickens (DYCs) with Yuexi frizzled feather chickens. Following a rearing period of 12 weeks, we randomly assigned 72 chickens into two distinct environmental conditions: a HS group subjected to 35 ± 1 °C for 8 h per day, and a control group (CN) maintained at 26 ± 1 °C. Seven days post-HS, multiple tissue samples were collected to assess meat quality attributes and measure expression levels of heat shock proteins (HSPs), muscle growth-related genes and cytokines. The results demonstrated a substantial reduction in weight gain of the F1 chickens exposed to HS, along with decreased expression of insulin-like growth factor-1 (IGF-1) and its receptor (IGF-1R) in the liver. Furthermore, HS exposure significantly increased muscle shear force and the expression of HSP70 in both liver and pectoral muscle tissues (p < .05). Despite these changes, there were no significant alterations in the other meat quality indices, or indicators of splenic and hepatic tissue injury. Likewise, expression levels of growth hormone receptor (GHR) and cytokines remained stable, implying a lack of heightened inflammation. These observations suggest an inherent thermotolerance in the chickens possessing dwarf size and frizzled feather traits, warranting further exploration for their potential in heat-stress-prone poultry production environments.
Dwarf and frizzled feather traits in crossbreed chickens show potential for improved heat tolerance in poultry production.
Heat stress had limited impact on meat quality parameters, suggesting resilience of these local chicken traits.
Understanding the genetic basis of thermotolerance can inform breeding strategies for climate-resilient chickens.
Highlights
Introduction
Chicken serves as one of the most consumed protein sources worldwide, contributing significantly to the escalating demand for animal protein. However, the decline in growth performance observed under high ambient temperatures indicates the adverse impact of global warming on livestock productivity (Gonzalez-Rivas et al. Citation2020; Saracila et al. Citation2021). Within the poultry sector, mitigating the effects of elevated temperatures is critical for maximising profitability and ensuring food security. Despite their homeothermic nature, fast-growing broiler lines are vulnerable to heat stress (HS) owing to their lack of sweat glands and elevated metabolic rates, a consequence of artificial selection (Nawaz et al. Citation2021; Shakeri and Le Citation2022). The implications of HS are multifaceted, encompassing changes in behaviour (e.g., lethargy, reduced feed intake, panting), metabolism (increased fat accumulation, decreased skeletal muscle mass), inflammation and oxidative stress (Nawaz et al. Citation2021; Fernandes et al. Citation2023). HS negatively impacts the effectiveness of broiler production and the quality of their meat. It leads to stunted growth and deterioration of meat quality due to lower pH levels and increased drip loss in meat, altering its typical colour, flavour and texture (Song and King Citation2015; Zaboli et al. Citation2019). Previous research has demonstrated that HS alters the impact of myogenic regulatory factors, insulin-like growth factor-1 (IGF-1) and heat-shock proteins (HSPs), thereby impairing skeletal muscle growth and development (Nawab et al. Citation2018; Nawaz et al. Citation2023). To counteract the deleterious effects of HS on chicken health and productivity, concerted efforts from both the poultry industry and scientific community have been undertaken to identify viable solutions.
The continued threat of global warming to poultry farming in tropical and subtropical regions is particularly alarming. Commercial birds, with specific genotypes optimised for temperate climates, often face substantial economic losses when reared in hotter tropical regions (Brugaletta et al. Citation2022; Fernandes et al. Citation2023). Some studies have proposed that local chicken breeds exhibiting traits such as dwarfism, frizzled feathers and naked necks, which reduce body size and feather coverage, display enhanced thermoregulation and could be instrumental in addressing HS issues (Yunis and Cahaner Citation1999; Sharifi et al. Citation2010; Nawaz et al. Citation2023). Commercial breeds often exhibit accelerated growth due to increased metabolic activity, which unfortunately leads to heightened metabolic heat production and drastically diminished performance under hot conditions (Gonzalez-Rivas et al. Citation2020; Shakeri and Le Citation2022). Interestingly, certain local chicken breeds that exhibit superior thermoregulation have been identified. These breeds characterised by slower growth rates, smaller bodies and reduced feather mass, exhibit better function under HS due to their decreased size and lower metabolic heat production. Specifically, it has been reported that dwarf chickens (Sharifi et al. Citation2010) and the native South Chinese breed of Yuexi frizzled feather chicken (also known as Kirin chickens) (Adu-Asiamah et al. Citation2021) exhibit enhanced performance under HS. Previous research has revealed that chicken dwarfism can be attributed to a 1.7 kb deletion mutation in the growth hormone receptor (GHR) gene (Ouyang et al. Citation2012), while the frizzled feather trait arises from a 15 bp deletion mutation in exon 2 of the KRT75L4 gene (Dong et al. Citation2018). Notably, the dwarf yellow chicken (DYC) and Yuexi frizzled feather chicken, both indigenous to the Guangdong province in South China, display superior heat tolerance capabilities (Nawaz et al. Citation2023).
The study aims to explore whether specific traits, such as dwarfism and frizzled feathers in crossbreed chickens, can enhance heat tolerance, ameliorate the negative effects of HS on growth performance and meat quality, and provide potential solutions for poultry production in high-temperature environments. This study hypothesise that chickens with dwarf and frizzled feather traits may exhibit resilience to HS, potentially benefiting poultry production in elevated temperature conditions.
Materials and methods
Animal ethics
The hatching of the crossbreed was carried out at the Guangdong Ocean University experimental station. The Animal Care and Use Committee of Guangdong Ocean University, Zhanjiang, China (SYXK-2019-0140), authorised animals and procedures are involved in this study.
Animals and crossbreeding
DYC was acquired from the Guangxi Zhuang Autonomous Region’s Animal Husbandry Research Institute and is characterised by low body weight and a shorter shank length. Yuexi frizzled feather chicken, characterised by frizzled feathers, was purchased from the Wannong Company based in Guangdong province, China. Fertilised eggs for hatching were obtained by crossbreeding DYC male chickens with Yuexi frizzled feather female chickens. The specific breeding design is as follows: 50 dwarf male chickens and 200 Yuexi frizzled feather female chickens were used for crossbreeding to obtain 500 F1 chicks. The GHR gene is present on the sex chromosome ‘Z’, while the KRT75L4 gene is present on chromosome number ‘33’ in chickens. In the F1 generation, male chickens did not display the dwarf phenotype since all of them contained heterozygous genes for both traits. However, all female chickens in the F1 generation were heterozygous for the frizzled trait and homozygous for the dwarf trait, meaning they possessed both the genes associated with dwarfism and frizzled feathers. Thereby, only female birds carrying both traits were used in the HS experiment (Supplementary Figure 1) and individuals with non-conforming phenotypic characteristics or disabilities were removed before the HS experiment.
Heat stress experiment
For the first 12 weeks of the trial, the birds were reared in cages (80 cm × 80 cm × 50 cm) housing six subjects each under controlled environmental conditions (26 ± 1 °C and 60 ± 5% relative humidity). Each cage was equipped with nipple waterers for ad libitum water access. A standard commercial broiler diet (Table ) was provided to all the chickens for all the trial. Subsequently, the 12-week-old birds (n = 72) with similar body weights (560.50 ± 8.50 g) were randomly distributed into two groups (HS and CN) consisting of six cages (replicates) each. All birds were checked for general health conditions, confirming that none of the birds in both groups showed any signs of bacterial, viral or parasitic infection. CN chickens were housed at a constant ambient temperature of 26 ± 1 °C, whereas HS group was raised in a separate room with 16 h at 26 ± 1 °C and eight consecutive hours at 35 ± 1 °C for seven days.
Table 1. Diet composition and its nutritional values given to experimental birds.
Sample collection
At the end of the HS experiment, one bird per cage, approximately the average weight of the replicate (n = 6), was randomly selected and humanely slaughtered through exsanguination. For gene expression analysis, samples of the liver, hypothalamus and pectoral muscle (the left side of the pectoralis major) were collected and kept in RNAlater solution for 24 h at 4 °C. Afterward, the solution was removed, and the samples were stored at −80 °C.
Body weight gain, body organ index and feed consumption
After seven days of HS, the final live weight and feed intake of each group were measured. Six randomly chosen birds from each group were humanely slaughtered through exsanguination, and the remaining broilers were reweighed after removing their feathers and viscera. Samples of the carcass, liver, pectoralis major and thigh muscle were taken and kept for further procedures. The feed intake, protein efficiency ratio, weight gain ratio and body organ index were calculated using the following formulas, respectively: feed intake (g/chicken/d) = feed consumed (g)/total number of birds/total days of experiment, protein efficiency ratio = chicken weight gain (g)/total protein intake (g), weight gain ratio (%) = (final body weight (g) – initial body weight (g))/initial body weight (g) × 100% and body organ index (%) = organ weight (g)/total carcass weight (g) × 100%.
Meat quality tests
The meat colour, including lightness (L*), redness (a*) and yellowness (b*) of both pectoral and thigh muscle samples, was measured using a colorimeter (CR-20, Konica Minolta Inc., Tokyo, Japan). Strips of meat 1 cm thick and 0.5 cm long (without tendons, fascia or fat) were used to assess the muscle shear force with a C-LM2 type muscle tenderness metre (Bulader Technology Development Co., Ltd., Beijing, China).
The water loss rate was determined using the pressurised gravimetric method. Pectoral and thigh muscle samples were cut into thin slices and weighed (W1). Each sample was then placed between layers of filter paper, secured with a rigid plastic plate, and subjected to a pressure of 343 N (equivalent to 35 kg) in RH-1000 meat pressure metre (Runhu Instrument Co., Ltd., Guangzhou, China) for 5 min. After removing the pressure, the sample was reweighed (W2), and the water loss rate was calculated using the formula: water loss rate (%) = (W1 – W2)/W1 × 100%.
Cooking loss was determined by weighing 20 g of muscle tissue sample within 45 min after slaughter (W1). These weighed samples were placed into a cooking pot, steamed for 0.5 h at 80 °C, cooled for 2 h, and then reweighed (W2). The cooking loss was calculated using the formula: cooking loss (%) = (W2 – W1)/W1 × 100%.
For drip loss, about 10 g (W1) of each meat sample was suspended vertically with a wire inside an inflatable and airtight plastic bag, and then placed in a refrigerator at 4 °C for 24 h. After 24 h, the sample was taken out of the refrigerator, reweighed (W2) and drip loss was calculated using the formula: drip loss (%) = (W1 – W2)/W1 × 100%.
Haematoxylin and eosin staining and microscopic analysis
Liver tissue samples were collected from each replicate of both control and HS groups for histopathological examination (Adu-Asiamah et al. Citation2021). An Olympus light microscope (Shinjuku City, Japan) was used for slide examination, and digital images of the slides were captured using a Nikon DS-U3 camera (Minato City, Japan) connected to a Nikon Eclipse CI upright optical microscope.
RNA extraction, cDNA synthesis and quantitative real-time PCR analysis
RNA was isolated from the liver, hypothalamus and pectoral muscle tissues using HiPure Universal RNA kits with Trizol reagent (Magen Biotech Co. Ltd., Guangzhou, China) following the manufacturer’s instructions. The integrity and purity of the RNA were confirmed using Nanodrop 2000 (Thermo Fisher, Waltham, MA). Subsequently, the RNA was transcribed into cDNA using a PrimeScript RT Reagent Kit (TaKaRa, Kyoto, Japan). The resulting cDNA was diluted four times with RNase-free water and stored at −20 °C for future use. Real-time quantitative PCR was conducted using an Applied Biosystems StepOne Plus™ Real-Time PCR system (Applied Biosystems, Foster City, CA) with TransStart Green qPCR SuperMix (Transgen Co., Ltd., Beijing, China) according to the provided directions. The specific primers for the target genes used in this study were synthesised based on primer blast (Table ). The mRNA expression level of the target gene was normalised to the mRNA expression level of GAPDH, following the method described before (Kim et al. Citation2020). The ΔΔCT was adjusted against an average from the control group (CN). All samples were run in triplicate, and the relative expression levels of the target genes were reported as the fold difference between the CN and HS groups.
Table 2. Gene primer sequences for quantitative RT-PCR.
Statistical analysis
Data relating to each chicken’s growth performance and gene expression analysis were analysed using general linear model of SPSS version 20.0 (SPSS, Chicago, IL). Results were presented as mean ± SEM (standard error of the mean). An unpaired Student’s t-test was used to calculate the SEM and p value of data related to gene expression, meat quality and growth performance. Statistically significant differences were considered at p < .05.
Results
Effects of seven-day HS on feed intake and growth parameters
After seven days of heat treatment, a greatly significant decrease in the weight gain ratio was observed in birds subjected to HS (p < .01). However, both feed intake and total protein intake did not exhibit any significant changes (p > .05) (Table ). Both the protein efficiency ratio and total protein intake per day were highly significantly lower in heat-stressed chickens as compared to the CN group (p < .01). Interestingly, HS did not result in a significant alteration in the weight of various organs, including the spleen, liver, pectoral and thigh muscles (p > .05). Although a decreasing trend in pectoral muscle gain was observed in birds subjected to HS after seven days, the reduction was not statistically significant (p > .05) (Table ).
Table 3. Feed consumption and growth performance of crossbreed after seven-day heat stress (HS).
Histopathological alterations in liver and spleen tissues after seven-day HS
Histopathological examination of spleen tissue from the CN group revealed regular morphological characteristics including the white pulp (WP), red pulp (RP) and central arteriole (CA) (Figure ). In contrast, the HS groups exhibited mild to moderate histological changes (Figure ). In the liver tissue from the CN group, regular histological features such as the central vein (CV), sinusoid (S) and hepatocytes (H) were observed (Figure ). However, the HS group demonstrated tissue necrosis, mononuclear cell infiltration, inflammation and nuclear degeneration, along with dilated sinusoids and CV. Additionally, there was an accumulation of inflammatory cells, vacuole degeneration, congestion of mononuclear, and a few binuclear cells (Figure ).
Figure 1. Histological effect induced by heat stress (HS) on the liver and spleen of crossbreed. Magnification was 20×, and scale denotes 50 μm. Control groups illustrate WP (white pulp), RP (red pulp) and CA (central artery) in spleen (a1) and the central vein (CV), sinusoidal cells (S) and hepatocytes in liver (b1). Panels a2–a4 and b2–b4 are HS groups of spleen and liver tissues, respectively. For histological comparison, different shapes were used to depict the pathological changes. Spleen (a2–a4): (
) represents mild vacuole degeneration, (
) shows red blood cell hyperplasia, (
) shows degeneration of red and white pulp. Liver (b2–b4): b2 depicts tissue inflammation with mononuclear cell infiltration (
) and vacuolar degeneration (
); b3 shows dilated CV with mild hyperplasia (
), tissue haemorrhages with necrosis (
) and mild inflammatory cells infiltration (
); b4 shows dilation in portal area with red blood cells hyperplasia (
), mononuclear cell infiltration (
) and vacuolar degeneration (
).
Expression levels of somatotropic pathway genes and heat shock proteins
Quantitative real-time PCR analysis revealed that HS significantly affected the mRNA levels of both IGF-1 and IGF-1R in liver tissue (p < .05), while GHR expression levels remained unchanged (p > .05) (Figure ). HS notably upregulated the mRNA expression levels of HSP70 but not HSP90 in both liver (p < .01) and pectoral (p < .05) tissues (Figure ), though no significant changes of them were observed in the hypothalamus (Figure ).
Figure 2. Relative mRNA expression levels of somatotropic genes related to muscle growth and heat shock proteins in liver and pectoralis major muscle tissues isolated after seven days of heat stress (HS). X-axis represents the treatments (HS or CN) and respective genes, while Y-axis shows the relative mRNA expression level. Relative mRNA expression of growth hormone receptor (GHR), insulin growth factor-1 (IGF-1) and its receptor (IGF-1R) in liver (a) and pectoral muscles (b). Relative mRNA expression of HSP70 and HSP90 in liver (c), pectoral muscle (d) and hypothalamus (e). Significant difference at (p < .01) is shown with **, while * depicts significant difference of p < .05. CN and HS represent control group and heat stress group, respectively.
Impact of HS on the immune and oxidative status of chicken
The effects of HS on the immune and oxidative status of crossbred chickens were evaluated by examining the mRNA expression levels of antioxidant and immune genes. HS did not significantly affect the relative mRNA expression of SOD, CAT and other cytokines in the liver compared to the CN group (p > .05) (Figure ). However, a significant increase was observed in SOD gene expression in the pectoralis major tissues of the HS group compared to the CN group (p < .05), while CAT mRNA expression remained unchanged (p > .05) (Figure ). Similarly, no significant changes were observed in the mRNA expression levels of IL-4, IL-6, IL-10 and IL-1β (Figure ). These findings indicate that the cytokine genes remained unchanged in the HS group of crossbred chickens compared to the CN.
Figure 3. Effect of heat stress (HS) on antioxidant and immune status of crossbreed chicken. Relative mRNA expression levels of superoxide dismutase (SOD) and catalase (CAT) in liver (a) and in pectoral muscle (b). Relative mRNA expression levels of IL-4, IL-6 (c), IL-10 and IL-1β (d) in hepatic tissues. *Significant difference at p < .05. CN and HS represent control group and heat stress group, respectively.
Meat quality parameters after heat stress
To understand the impact of HS on the meat quality of crossbred chickens, we evaluated meat colour, water loss, cooking loss, and drip loss for pectoral and thigh muscles after seven days of HS treatment. Our results indicated that seven-day HS significantly reduced the a*-value of thigh muscle (p < .05), but did not significantly affect other meat colour parameters of pectoral and thigh muscles compared to the CN group (p > .05) (Table ). For both pectoral and thigh meat quality, HS significantly increased shear force (p < .05), while drip loss, cooking loss and water loss remained unchanged between the HS and CN groups (p > .05) (Table ). These results suggest that HS had a limited impact on the meat quality parameters of crossbred chickens.
Table 4. Effect of heat stress on meat colour parameters after seven days of heat stress.
Table 5. Effect of heat stress on drip loss, cook loss, water holding capacity, and shear force of pectoral and thigh muscle after seven days of heat stress.
Discussion
This study aimed to examine the effects of HS on crossbreed chickens, focusing on various aspects such as growth parameters, tissue damage, gene expression, oxidative status and meat quality. By investigating the impacts of HS on poultry, particularly in crossbreed chickens with dwarf and frizzled feather traits, our findings contribute to the growing body of evidence on this subject. The study provides valuable insights into potential resilience factors in these specific chicken breeds, shedding light on how they respond to HS conditions.
In accordance with previous research (Adu-Asiamah et al. Citation2021; Malila et al. Citation2021; Qaid and Al-Garadi Citation2021; Saracila et al. Citation2021), our study also observed a significant reduction in weight gain ratio and feed intake in chickens exposed to HS. These findings validate the existing understanding that animals exposed to high temperatures tend to decrease their feed intake as a means to limit metabolic heat production. The consistency in these results across different studies further reinforces the importance of considering the impact of HS on poultry and its potential implications for poultry farming practices. The substantial reduction in weight gain observed in our study can be primarily attributed to the decreased feed intake, as suggested by earlier studies (Mashaly et al. Citation2004; Souza et al. Citation2016). However, contrary to previous studies, our investigation found that HS did not significantly affect parameters other than weight gain ratio in crossbreed chickens. Interestingly, our results suggest that the presence of dwarf and frizzled feather traits in these chickens may provide some degree of heat resistance, which could potentially explain the limited impact of HS on other parameters. This highlights the importance of considering genetic factors and specific breed characteristics in understanding the response of chickens to HS conditions.
The study also provided valuable insights into the implications of HS on tissue damage. Histopathological analysis revealed significant alterations in liver and spleen tissues, characterised by inflammatory cell infiltration, hyperplasia and degradation. These observations indicate that HS can cause substantial tissue damage, which aligns with previous studies (Zeng et al. Citation2014; Adu-Asiamah et al. Citation2021). The consistency of these findings across studies further emphasises the detrimental effects of HS on the physiological health of chickens and underscores the importance of understanding and mitigating the impacts of HS in poultry farming practices. Indeed, our findings revealed that the extent of tissue damage in crossbreed chickens under HS was moderate, indicating that they may possess some level of resilience to severe tissue damage in such conditions. Additionally, the study demonstrated that HS significantly reduced IGF-1 mRNA expression levels, while the expression levels of GHR and IGF-1R remained stable. This intriguing observation suggests that the presence of dwarf and frizzled traits in these chickens might confer a degree of adaptability to growth in hot environments as previously suggested before (Ferdaus et al. Citation2016). These results open new avenues for future research on the thermotolerance of chickens and highlight the importance of understanding genetic factors that may influence their ability to cope with HS.
Furthermore, our study found that HS led to a significant increase in the expression of HSP70, a heat shock protein (HSP), in both liver and pectoral tissues. This finding is consistent with previous research that also reported elevated expression of HSPs in high-temperature environments (Shankar and Mehendale Citation2014; Cedraz et al. Citation2017; Sejian et al. Citation2018). However, contrary to previous studies, we observed no significant change in HSP90 mRNA expression levels in response to HS. The oxidative status of chickens under HS was also evaluated in this study. Similarly, the significant increase in SOD expression in the pectoral muscle tissue of HS-treated crossbreed chickens contradicts certain earlier findings reporting a decrease in CAT and SOD activities under chronic HS conditions (Zeng et al. Citation2014; Pejić et al. Citation2016). These contrasting results indicate that the response of crossbreed chickens to oxidative stress and HS may differ from that of other chicken populations. It suggests that crossbreed chickens might possess superior antioxidant capabilities, potentially enabling them to cope better with oxidative stress induced by heat.
Several studies found that HS had a pivotal effect in performance parameters (lower a*-value, drip loss and compression force), and body weight (Quinteiro-Filho et al. Citation2010; Sohail et al. Citation2012; Rocchi et al. Citation2022). Our investigation under HS revealed a significant reduction in the redness (a*-value) of thigh muscle, with no significant changes in lightness (L*-value) and yellowness (b*-value). This is partially in contrast with some previous studies that found changes in all three parameters due to HS (Wang et al. Citation2017; Xing et al. Citation2019; Zhang et al. Citation2019). However, our findings are consistent with earlier research that suggested chickens with the F gene can produce better-quality meat in hot environments (Yunis and Cahaner Citation1999; Deeb and Cahaner Citation2001, Citation2002). This study provides valuable insights into the multifaceted effects of HS on the growth, health and meat quality of crossbred chickens. The observed implications of specific genetic traits in conferring resilience to HS highlight the potential for genetic selection strategies aimed at enhancing HS tolerance in poultry. Unfortunately, our study only examined HS for one week (from days 84 to 91), in contrast to earlier research on long-term HS that encompassed three weeks (from days 21 to 42) (Ruff et al. Citation2020), five consecutive weeks (from days 7 to 42) (Rocchi et al. Citation2022) and six weeks (from days 1 to 42) (Sohail et al. Citation2012). Our study’s experimental period was quite short, which means that several performance parameters and physiological indicators did not alter significantly. However, an acute HS with 36 °C for one hour could also result in lower pH value and higher L*-value of broilers meat quality (Wang et al. Citation2017). Therefore, more research is necessary to understand the underlying processes of the intricate physiological responses to HS in chickens.
Conclusions
In conclusion, our study provides valuable insights into the physiological responses of crossbreed chickens with dwarf and frizzled feather traits, under HS. The findings highlight that a seven-day HS period led to a decrease in the overall weight gain ratio of the crossbreed chickens. Interestingly, despite the reduction in overall weight gain, there was no significant decrease in pectoral muscle mass. This suggests that HS might have a differential impact on various growth parameters in these chickens.
Notably, the preservation of meat quality characteristics in crossbreed chickens, despite exposure to extreme heat, is a noteworthy observation. This finding suggests that these particular genetic traits, such as the dwarf and frizzled feather features, might contribute to inherent heat resistance ability in these local chicken breeds. Such inherent heat resistance could potentially be harnessed to improve poultry production in environments that regularly experience high temperatures. One of this study’s limitations is that the HS experiment was only conducted for seven days, which may have hampered the potential to identify long-term effects on various parameters. Although this study sheds light on the potential benefits of small body size and frizzled feather traits in dealing with HS, it is indeed just the beginning of our understanding of the intricate mechanisms of thermotolerance in these chickens. Further research is essential to fully elucidate the underlying physiological and genetic mechanisms that contribute to the observed heat tolerance, thereby enhancing our ability to breed chickens that can thrive in a warming climate.
Author contributions
Conceptualisation, methodology, A.H.N., L.Z., S.L.; investigation, Z.J., F.W., W.Z., J.Z., J.S.; resources, Z.Z.; validation, visualisation, A.H.N., Z.J.; project administration, L.Z.; writing – original draft preparation, A.H.N., S.L.; writing – review and editing, L.Z., S.L.; supervision, L.Z.; funding acquisition, L.Z., S.L.
Supplemental Material
Download MS Word (74.4 KB)Disclosure statement
No potential conflict of interest was reported by the author(s).
Data availability statement
No new data were created in this study.
Additional information
Funding
References
- Adu-Asiamah P, Zhang Y, Amoah K, Leng QY, Zheng JH, Yang H, Zhang WL, Zhang L. 2021. Evaluation of physiological and molecular responses to acute heat stress in two chicken breeds. Animal. 15(2):100106. doi: 10.1016/j.animal.2020.100106.
- Brugaletta G, Teyssier JR, Rochell SJ, Dridi S, Sirri F. 2022. A review of heat stress in chickens. Part I: insights into physiology and gut health. Front Physiol. 13:934381. doi: 10.3389/fphys.2022.934381.
- Cedraz H, Gromboni JGG, Garcia AAP, Farias Filho RV, Souza TM, Oliveira ERd, Oliveira EBd, Nascimento CSd, Meneghetti C, Wenceslau AA. 2017. Heat stress induces expression of HSP genes in genetically divergent chickens. PLOS One. 12(10):e0186083. doi: 10.1371/journal.pone.0186083.
- Deeb N, Cahaner A. 2001. Genotype-by-environment interaction with broiler genotypes differing in growth rate: 2. The effects of high ambient temperature on dwarf versus normal broilers. Poult Sci. 80(5):541–548. doi: 10.1093/ps/80.5.541.
- Deeb N, Cahaner A. 2002. Genotype-by-environment interaction with broiler genotypes differing in growth rate. 3. Growth rate and water consumption of broiler progeny from weight-selected versus nonselected parents under normal and high ambient temperatures. Poult Sci. 81(3):293–301. doi: 10.1093/ps/81.3.293.
- Dong J, He C, Wang Z, Li Y, Li S, Tao L, Chen J, Li D, Yang F, Li N, et al. 2018. A novel deletion in KRT75L4 mediates the frizzle trait in a Chinese indigenous chicken. Genet Sel Evol. 50(1):68. doi: 10.1186/s12711-018-0441-7.
- Ferdaus AJM, Bhuiyan MSA, Hassin BM, Bhuiyan AKFH, Howlider MAR. 2016. Phenotypic characterization and productive potentialities of indigenous dwarf chicken of Bangladesh. Bang J Anim Sci. 45(1):52–61. doi: 10.3329/bjas.v45i1.27489.
- Fernandes E, Raymundo A, Martins LL, Lordelo M, de Almeida AM. 2023. The naked neck gene in the domestic chicken: a genetic strategy to mitigate the impact of heat stress in poultry production—a review. Animals. 13(6):1007. doi: 10.3390/ani13061007.
- Gonzalez-Rivas PA, Chauhan SS, Ha M, Fegan N, Dunshea FR, Warner RD. 2020. Effects of heat stress on animal physiology, metabolism, and meat quality: a review. Meat Sci. 162:108025. doi: 10.1016/j.meatsci.2019.108025.
- Kim WS, Ghassemi Nejad J, Peng DQ, Jung US, Kim MJ, Jo YH, Jo JH, Lee JS, Lee HG. 2020. Identification of heat shock protein gene expression in hair follicles as a novel indicator of heat stress in beef calves. Animal. 14(7):1502–1509. doi: 10.1017/S1751731120000075.
- Malila Y, Jandamuk A, Uopasai T, Buasook T, Srimarut Y, Sanpinit P, Phasuk Y, Kunhareang S. 2021. Effects of cyclic thermal stress at later age on production performance and meat quality of fast-growing, medium-growing and Thai native chickens. Animals. 11(12):3532. doi: 10.3390/ani11123532.
- Mashaly MM, Hendricks GL, Kalama MA, Gehad AE, Abbas AO, Patterson PH. 2004. Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult Sci. 83(6):889–894. doi: 10.1093/ps/83.6.889.
- Nawab A, Ibtisham F, Li G, Kieser B, Wu J, Liu W, Zhao Y, Nawab Y, Li K, Xiao M, et al. 2018. Heat stress in poultry production: mitigation strategies to overcome the future challenges facing the global poultry industry. J Therm Biol. 78:131–139. doi: 10.1016/j.jtherbio.2018.08.010.
- Nawaz AH, Amoah K, Leng QY, Zheng JH, Zhang WL, Zhang L. 2021. Poultry response to heat stress: its physiological, metabolic, and genetic implications on meat production and quality including strategies to improve broiler production in a warming world. Front Vet Sci. 8:699081. doi: 10.3389/fvets.2021.699081.
- Nawaz AH, Lin S, Wang F, Zheng J, Sun J, Zhang W, Jiao Z, Zhu Z, An L, Zhang L. 2023. Investigating the heat tolerance and production performance in local chicken breed having normal and dwarf size. Animal. 17(3):100707. doi: 10.1016/j.animal.2023.100707.
- Ouyang J, Xie L, Nie Q, Zeng H, Peng Z, Zhang D, Zhang X. 2012. The effects of different sex-linked dwarf variations on Chinese native chickens. J Integr Agric. 11(9):1500–1508. doi: 10.1016/S2095-3119(12)60150-6.
- Pejić S, Stojiljković V, Todorović A, Gavrilović L, Pavlović I, Popović N, Pajović SB. 2016. Antioxidant enzymes in brain cortex of rats exposed to acute, chronic and combined stress. Folia Biol. 64(3):189–195. doi: 10.3409/fb64_3.189.
- Qaid MM, Al-Garadi MA. 2021. Protein and amino acid metabolism in poultry during and after heat stress: a review. Animals. 11(4):1167. doi: 10.3390/ani11041167.
- Quinteiro-Filho WM, Ribeiro A, Ferraz-de-Paula V, Pinheiro ML, Sakai M, Sá LRM, Ferreira AJP, Palermo-Neto J. 2010. Heat stress impairs performance parameters, induces intestinal injury, and decreases macrophage activity in broiler chickens. Poult Sci. 89(9):1905–1914., doi: 10.3382/ps.2010-00812.
- Rocchi A, Ruff J, Maynard CJ, Forga AJ, Señas-Cuesta R, Greene ES, Latorre JD, Vuong CN, Graham BD, Hernandez-Velasco X, et al. 2022. Experimental cyclic heat stress on intestinal permeability, bone mineralization, leukocyte proportions and meat quality in broiler chickens. Animals. 12(10):1273. doi: 10.3390/ani12101273.
- Ruff J, Barros TL, Tellez G Jr, Blankenship J, Lester H, Graham BD, Selby CAM, Vuong CN, Dridi S, Greene ES, et al. 2020. Research note: evaluation of a heat stress model to induce gastrointestinal leakage in broiler chickens. Poult Sci. 99(3):1687–1692. doi: 10.1016/j.psj.2019.10.075.
- Saracila M, Panaite TD, Papuc CP, Criste RD. 2021. Heat stress in broiler chickens and the effect of dietary polyphenols, with special reference to Willow (Salix spp.) bark supplements—a review. Antioxidants. 10(5):686. doi: 10.3390/antiox10050686.
- Sejian V, Bhatta R, Gaughan JB, Dunshea FR, Lacetera N. 2018. Review: adaptation of animals to heat stress. Animal. 12(Suppl. 2):S431–S444. doi: 10.1017/S1751731118001945.
- Shakeri M, Le HH. 2022. Deleterious effects of heat stress on poultry production: unveiling the benefits of betaine and polyphenols. Poultry. 1(3):147–156. doi: 10.3390/poultry1030013.
- Shankar K, Mehendale HM. 2014. Heat-shock proteins. In: Philip W, editor. Encyclopedia of toxicology. 3rd ed. Elsevier, Bethesda, MD, USA: US National Library of Medicine; p. 830–831. doi: 10.1016/B978-0-12-386454-3.00320-1. https://www.sciencedirect.com/science/article/abs/pii/B9780123864543003201?via%3Dihub. ISBN: 9780123864543.
- Sharifi AR, Horst P, Simianer H. 2010. The effect of frizzle gene and dwarf gene on reproductive performance of broiler breeder dams under high and normal ambient temperatures. Poult Sci. 89(11):2356–2369. doi: 10.3382/ps.2010-00921.
- Sohail MU, Hume ME, Byrd JA, Nisbet DJ, Ijaz A, Sohail A, Shabbir MZ, Rehman H. 2012. Effect of supplementation of prebiotic mannan-oligosaccharides and probiotic mixture on growth performance of broilers subjected to chronic heat stress. Poult Sci. 91(9):2235–2240. doi: 10.3382/ps.2012-02182.
- Song DJ, King AJ. 2015. Effects of heat stress on broiler meat quality. Worlds Poult Sci J. 71(4):701–709. doi: 10.1017/S0043933915002421.
- Souza Ld, Espinha LP, Almeida EAd, Lunedo R, Furlan RL, Macari M. 2016. How heat stress (continuous or cyclical) interferes with nutrient digestibility, energy and nitrogen balances and performance in broilers. Livest Sci. 192:39–43. doi: 10.1016/j.livsci.2016.08.014.
- Wang RH, Liang RR, Lin H, Zhu LX, Zhang YM, Mao YW, Dong PC, Niu LB, Zhang MH, Luo X. 2017. Effect of acute heat stress and slaughter processing on poultry meat quality and postmortem carbohydrate metabolism. Poult Sci. 96(3):738–746. doi: 10.3382/ps/pew329.
- Xing T, Gao F, Tume RK, Zhou G, Xu X. 2019. Stress effects on meat quality: a mechanistic perspective. Compr Rev Food Sci Food Saf. 18(2):380–401. doi: 10.1111/1541-4337.12417.
- Yunis R, Cahaner A. 1999. The effects of the naked neck (Na) and frizzle (F) genes on growth and meat yield of broilers and their interactions with ambient temperatures and potential growth rate. Poult Sci. 78(10):1347–1352. doi: 10.1093/ps/78.10.1347.
- Zaboli G, Huang X, Feng X, Ahn DU. 2019. How can heat stress affect chicken meat quality? A review. Poult Sci. 98(3):1551–1556. doi: 10.3382/ps/pey399.
- Zeng T, Li J, Wang D, Li G, Wang G, Lu L. 2014. Effects of heat stress on antioxidant defense system, inflammatory injury, and heat shock proteins of Muscovy and Pekin ducks: evidence for differential thermal sensitivities. Cell Stress Chaperones. 19(6):895–901. doi: 10.1007/s12192-014-0514-7.
- Zhang M, Zhu L, Zhang Y, Mao Y, Zhang M, Dong P, Niu L, Luo X, Liang R. 2019. Effect of different short-term high ambient temperature on chicken meat quality and ultra-structure. Asian-Australas J Anim Sci. 32(5):701–710. doi: 10.5713/ajas.18.0232.