Poultry industry supports the livelihoods and food security of billions of people worldwide. Both poultry meat and egg are globally highly regarded as the most efficient protein sources, with high organoleptic quality, relatively inexpensive, and without religious taboos (Barroeta, 2007; Cavani et al., 2009; Marangoni et al., 2015). However, poultry production sustainability is facing several challenges from a steep projected increase in global demand for high animal protein quality and the need to adapt to the pressure on natural resource availability and environmental constraints. In fact and according to the Food and Agriculture Organization (FAO) of the United Nations (Food and Agriculture Organization [FAO], 2018) and to the 2019 World Population Prospect (United Nations, 2019), it is predicted that the world human population will increase by 10% over the next decade, reaching approximately 9.7 billion in 2050. This, in turn, is estimated to drive a significant rise in the demand for food (∼73% in meat and 58% in dairy products), which require greater animal production including poultry that is projected to double by 2050.

Doubling poultry production within “planetary boundaries” to feed the growing global population will be challenging. It is clear that climate changes drive the earth system into a much warmer state (Alley et al., 2005; Chen et al., 2011). Indeed, unusual warm season with widespread and more intense heat waves have increased markedly over the past decades, and are likely to be larger in the future (Mora et al., 2013). Modern broiler chickens are highly thermo-sensitive and cannot cope well with high environmental temperatures because they are covered with feathers, they have high core body temperature (∼40°C) and high metabolic activity, and they lack sweat gland (Settar et al., 1999; Caulfield et al., 2014; Nawab et al., 2018). The strong adverse effect of heat stress-induced by high environmental temperature on broilers are well documented. Heat stress alters bird’s well-being by inducing stress (Star et al., 2008; Gu et al., 2012), depressing feed intake (Flees et al., 2017; Rajaei-Sharifabadi et al., 2017), inducing thirst (Belay et al., 1993), causing immunosuppression (Ghazi et al., 2012; Monson et al., 2018), reducing performance (Quinteiro-Filho et al., 2010; Lara and Rostagno, 2013), and in extreme case increasing mortality rate by spiraling hyperthermia (Furlan et al., 1998). For example, the European heat wave of summer 2003 resulted in the death of more than one million chickens in France (Fouillet et al., 2008). Another heat wave in 2015 killed more than 17 million birds in India (Bhadauria et al., 2016). In addition to welfare and performance issue, heat stress is a significant economic burden to the industry (St-Pierre et al., 2003), and it is a major thrust of intense research effort to identify effective strategies to ameliorate heat stress productivity loss.

Seminal works and various nutritional and/or managerial strategies were applied to mitigate heat stress, yet the poultry productivity losses are still high during hot seasons. Although they are known for more than 60 years in traditional medicine (for review see Panossian and Wikman, 2011), the use of in feed-adaptogens in livestock just begins to gain popularity (Selvam et al., 2018). Adaptogens, plant extracts, also known as stress response modifiers, are defined as metabolic regulators, which increase the ability of an organism to adapt to environmental stressors and to avoid damage from such stressors (Wagner et al., 1994; Panossian and Wikman, 2009, 2010). We undertook the present study to assess the effect of the adaptogen NR-PHY-30 (Natural Remedies, Bengaluru, India) on growth performance and carcass quality in broilers exposed to chronic cyclic heat stress.

The experiment has been conducted from January 21 to March 3, 2021 for 42 days. The weather cast (temperature and RH) is shown in Figures 1A,B. The average temperature was approximately 10°C and the RH was about 60–70%, which is typical in Arkansas during that season. The average temperature and the RH inside of the barn (but outside of the chambers) were ∼20°C and 30–40%, respectively (Figures 1A,B). The temperature inside of the environmental chambers was accurately manipulated to reach 35°C from 9:30 am to 5:30 pm and return to 24°C during the rest of the day each day from d29 to d42, creating a cyclic heat stress condition as planned (Figure 1C). The RH inside the chambers was ∼16–20% until d29 and then increased during heat stress to reach ∼45–60% (Figure 1D).

As expected, heat stress significantly increased the broiler body core temperature by ∼0.5°C compared to TN conditions (Figure 2A). The supplementation of the herbal adaptogen (NR-PHY-30) increased further the body core temperature of heat-stressed broilers, although the difference was not statistically discernable (Figure 2A). Similarly, the infrared thermal imaging showed that the surface temperature was significantly higher in heat-stressed broilers fed with control- and adaptogen-supplemented diets compared to birds maintained at TN conditions (Figures 2B,C). There was no significant difference in the mortality rate between all groups (7.73, 6.54, 5.95, and 7.14% in C-TN, C-HS, NR-PHY-500HS, and NR-PHY-1000HS, respectively).

As shown in Figures 3A–C, heat stress significantly reduced feed intake and body weight compared to TN conditions. Adaptogen supplementation significantly increased feed intake and body weight in a dose-dependent manner in heat-stressed broilers compared to those fed control diet and exposed to heat stress (Figures 3A,B). Adaptogen supplementation averaged 65.95 and 83.25 g better SW (Table 2) and 5 and 10 points better FCR at low (500 g/1000 kg diet) and high dose (1 kg/1000 kg diet), respectively, compared to heat-stressed birds (Figure 3D). Heat stress significantly reduced body part weights (HCW, CCWG, breast, tender, wings, and leg) (Table 2). Although it was not significant, except for tender, adaptogen supplementation increased, in a dose-dependent manner, breast weight (by ∼20 and 27.28 g), tender weight (by ∼2.66 and 5.18 g), and leg weight (by ∼7.42 and 15.94 g) at low and high doses, respectively, compared to heat-stressed birds fed control diet (Table 2).

Heat stress did not affect the pH of breast meat at both processing and 24 h postmortem (Table 3). However, adaptogen supplementation at both doses significantly increased pH at processing only, and not at 24 h postmortem (Table 3). Heat stress significantly reduced breast meat b^∗ value at processing, and did not affect any other color value (Table 4). Breasts from adaptogen-fed birds exhibited significant higher processing L^∗ and b^∗ values compared to those from heat-stressed birds fed a control diet (Table 4). Meat color parameters (L^∗, a^∗, and b^∗) did not differ between all groups at 24 h postmortem and after cook (Table 4). Cook loss was significantly reduced by heat stress, and increased to normal levels by adaptogen supplementation (Table 5). Adaptogen supplementation at high dose (1 kg/1000 kg diet) significantly increased MORSE compared to birds fed control diet and maintained under both TN and heat stress conditions (Table 5).

Heat stress did not elicit any change to free amino acid profile in breast tissues compared to TN environment in our experimental conditions (Table 6). Supplementation of adaptogen at both doses significantly reduced breast cysteine levels compared to heat-stressed birds fed with control diet (Table 6). High dose (1 kg/1000 kg diet) of adaptogen significantly decreased the breast levels of glutamic acid, glycine, serine, and threonine compared to heat-stressed birds fed with control diet (Table 6).

There is a monumental pressure on farm animals to increase production to feed the future and meet the growing global demand for high-quality animal proteins. Due to various constraints, including extreme environmental conditions, this will be very challenging. Heat load is one of the most challenging stressor to poultry industry worldwide because of its strong adverse effects on welfare, feed intake, growth, immunity, meat yield, and mortality (Star et al., 2008; Quinteiro-Filho et al., 2010; Ghazi et al., 2012; Lara and Rostagno, 2013; Flees et al., 2017; Rajaei-Sharifabadi et al., 2017; Monson et al., 2018; Liu et al., 2019). Over the past decades, widespread extreme heat waves have occurred repeatedly and caused great losses across the globe (Rotter and Van de Geijn, 1999; St-Pierre et al., 2003; Thornton et al., 2009; Nardone et al., 2010; Reynolds et al., 2010). These heat anomalies are projected to increase in the future and their strong adverse effects will likely take a heavy toll and large amplitude (Meehl and Tebaldi, 2004; Sherwood and Huber, 2010; Liu et al., 2017; Mora et al., 2017). There is, therefore, a critical need to identify new effective strategies (management, nutrition, etc.) to mitigate these adverse effects and ameliorate heat stress productivity losses.

Fueled by consumer preferences for natural products, there is growing interest in using phytobiotic feed additives in the animal food system (American Meat Science Association [AMSA], 2012). Although they are known for more than 60 years in medicine and pharmacosanation (Wagner et al., 1994), and their original plant sources have been used for centuries in traditional medicine (Wagner et al., 1994; Panossian and Wikman, 2011), adaptogens are just recently begin to be used as feed additive in poultry (Selvam et al., 2018; Marimuthu et al., 2020). Herbal adaptogens are plant-derived biologically active substances originally defined as stress-response modifiers and metabolic regulators that increase the ability of an organism to adapt to environmental stressors and, thereby, protect against cellular damage from such stressors (Duraisami et al., 2010; Giri et al., 2011, 2013; Singh et al., 2017). In this study, we sought to assess the effect of the herbal adaptogen NR-PHY-30, formulated by Natural Remedies Private Limited, Bengaluru, India, on growth performance, carcass quality and breast amino acid profile in heat-stressed broilers.

NR-PHY-30 contains Indian gooseberry (Emblica officinalis), holy basil (Ocimum sanctum), and winter cherry (Withania somnifera) (Natural Remedies, personal communication), and the adaptogenic properties of these plants have been already reported (Wagner et al., 1994; Panossian and Wikman, 2011) as well as their beneficial therapeutic effects (Pattanayak et al., 2010; Malik et al., 2016; Dutta et al., 2019). As expected and in agreement with previous studies, including our own (Flees et al., 2017; Rajaei-Sharifabadi et al., 2017; Liu et al., 2020; Tabler et al., 2020; Wasti et al., 2020), heat stress increased both surface and body core temperatures and reduced feed intake and body weight in modern broilers. Interestingly, although it increased further the surface and body core temperatures, the herbal adaptogen NR-PHY-30 enhanced feed intake and body weight and improved FCR in heat-stressed broilers. This suggests one of the two following potential scenarios: (1) While it is known that the body experiences a temperature-dependent variation in energy needs that should be reflected in feed intake (reduction under heat stress conditions) (Brobeck, 1948; Jakubczak, 1976), the effect of the adaptogen NR-PHY-30 on appetite and feed intake in our experimental conditions was probably independent from the thermostatic mechanism (Brobeck, 1948). For instance, it has been shown that intracerebroventricular administration of IL-1 raised body core temperature without affecting feed intake in rodents indicating that feed intake regulation could be uncoupled from the thermoregulatory mechanisms (McCarthy et al., 1986). (2) Although it was not measured in the present study, as the adaptogen was supplemented from d1 post hatch, it is probable that NR-PHY-30 increased the body core temperature at early age, which mimics a repeated mild exposure and low stress dose that resulted in increased resistance and better adaptation to heat stress (thermo-tolerance) at later age. This second scenario might be supported also by previous thermal conditioning studies showing that temporarily elevated brooding temperatures at early post-hatch or at embryonic age impart long-term resistance to heat stress in broilers, which survive and grow better at higher environmental temperatures (De Basilio et al., 2003; Gunal, 2013; Loyau et al., 2013, 2015; Zaboli et al., 2017).

The increased body weight was accompanied by an enhanced weights of body parts, including breast and tender weights along with a significant reduction in breast levels of free alanine, arginine, cysteine, glutamic acid, glycine, and serine. This indicates that the adapotogen NR-PHY-30 might stimulate amino acid incorporation and use by the muscle for protein synthesis. Previous studies have shown the key role of alanine (Perez-Sala et al., 1987), arginine (Wang et al., 2018), cysteine (Chua et al., 1984), glutamic acid (Brodsky et al., 2017), glycine (Wang et al., 2014), and serine (Galbraith and Buse, 1981) in protein synthesis. What downstream pathways used by the adaptogen to enhance muscle protein synthesis under heat stress condition is not known and merit further in depth investigation.

Although heat stress did not affect the breast meat pH, it reduced the b^∗ (yellowness) value, which corroborated previous studies (McKee and Sams, 1997; Aksit et al., 2006). This might be associated with heat stress-induced disruption of muscle membrane integrity, denaturation of muscle proteins, and in turn increased light scattering (Owens et al., 2000; Sandercock et al., 2001). Interestingly, the adaptogen supplementation increased the pH at processing and increased the L^∗ value, suggesting potential improvement of meat color. Although the underlying mechanisms are not known at this time, it is possible that the adaptogen supplementation improved the antioxidant status of the breast muscle (Arif et al., 2016), which in turn improve meat quality. Intriguingly, heat stress reduced cook loss and the adaptogen supplementation reverse this parameter to the same levels of breast from TN birds fed with control diet. Similarly, MORS total energy (MORSE) was not altered by heat stress, but increased with the adaptogen supplementation, indicating that the adaptogen reduced breast meat tenderness. Although it was not measured here, and in addition to collagen and tissue connective content in the breast, tenderness might be affected by the sarcomere length, muscle fiber diameter, stromal proteins, and collagen solubility (Koohmaraie et al., 2002), all of which might be modified by the adaptogen administration, which warrant further investigations.

Supplementation of the herbal adaptogen NR-PHY-30 stimulated appetite and feed intake, and in turn improved growth performance in a dose-dependent manner (average 66–83 g in body weight and 5–10 points better FCR) in cyclic heat-stressed broilers, which make it a promising nutritional strategy. However, further in depth investigation are needed to define its mode of action and its underlying molecular mechanisms.

The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author/s.

The animal study was reviewed and approved by the University of Arkansas.

SD designed the experiment and purchased the reagents. EG and SD conducted the trial and processed the animals at the end of trial. EG and CM measured and analyzed the meat quality parameters. SD wrote the manuscript with input from EG, CM, CO, and J-FM. All the 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.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.