Exploring relationships between heat tolerance and tenderness in Bos indicus-influenced cattle
Breeds well known for their superior ability to regulate body temperature in hot climates.
By Tracy Scheffler
Bos indicus breeds are well known for their superior ability to regulate body temperature in hot climates. Crossbreeding utilizing Bos indicus breeds is one approach to incorporating genetics that improve heat tolerance and adaptability of more heat sensitive breeds. However, Bos indicus breeds like Brahman present some challenges as they have a reputation for more reactive behavior, slow growth and meat quality issues.
These challenges decrease the acceptability and value of Bos indicus-influenced cattle and represent obstacles to greater utilization of Bos indicus. This also indicates there may be some antagonism between growth, meat quality and heat tolerance. Identifying genotypes and phenotypes that benefit heat tolerance without sacrificing growth and beef quality is important to maintaining beef production in a changing climate.
Thermoneutral zone and heat toleranceLike people, other mammals, and birds, cattle generate heat from body metabolism to maintain a constant body temperature. When body temperature is greater than ambient temperature, heat produced by the animal can be dissipated to the environment. Thermoneutral zone is the temperature range where heat production and heat loss from the animal’s body are about the same, and in this “comfort zone,” performance is maximized.
At temperatures or thermal loads outside the thermoneutral zone (cold stress or heat stress), the animal must expend energy (increase metabolic rate) to maintain body temperature, energy that could otherwise go to more economical uses such as growth or milk production. The thermoneutral zone depends on several factors, such as animal age, size and stage of production.
Heat tolerant animals have an improved ability to regulate their body temperature in response to high environmental temperatures. Evaluating heat tolerance typically involves monitoring body temperature and respiration, which is relatively feasible under controlled experimental conditions and facilities. However, this becomes much more challenging under field conditions.
Small temperature logging devices may be used to record temperature data over a set period. These devices may be placed in blank internal release devices for recording vaginal temperature in females (spent CIDRs work well); alternatively, devices may be placed in the ear (tympanic temperature) or surgically implanted into the body cavity.
Regulation of body temperature is a function of heat flow between the animal and its environment, and the heat produced by metabolism. Heat transfer from the animal and its environment is related to several factors.
For example, greater surface relative to weight increases the capacity for heat loss. Smaller animals have more body surface area per unit weight, which in turn, means they will tend to lose heat to a cooler environment faster than large animals. Consequently, the small animal must increase its metabolic rate to maintain constant body temperature. Along these lines, the abundance of loose skin on Brahman is thought to increase surface area and promote heat loss. The temperature difference between the animal and the air, and the properties of the hair coat also affect heat loss.
Heat productionHeat produced by the animal is dictated by body metabolic rate. The various tissues of the body differ in their metabolic activity, which is related to their activity on a per unit basis as well as their overall contribution to body weight. For example, the heart represents a small proportion of body weight (<1%), but due to its constant activity, contributes a larger proportion to body metabolic activity.
On the other hand, skeletal muscles make up a large proportion of body mass (~30-40%) but compared to heart or liver, skeletal muscles are relatively less active on a per unit basis. Further, the metabolic rate of muscle depends on physical activity, which may vary based on individual, housing and management system, and other factors.
In turn, the metabolic rate determines the nutrient or energy requirements, and growth rates of livestock. A portion of the nutrients the animal consume are lost through feces, urine or methane; the remaining metabolizable energy is allocated for the energy needed for cellular functions within the animal (basal energy expenditure), and the energy for work. Once the energy requirements for digestion of food and physical activity are met, the leftover energy can be dedicated to production.
Animals that are highly productive, e.g., animals with high gains and lactating dairy cows, produce more heat from metabolism, which shifts their thermoneutral zone; this makes them more tolerant to cold, but less tolerant to heat and humidity.
On a cellular level, nutrients from the diet are metabolized to accomplish vital functions, including protein synthesis, muscular contraction and the maintenance of ion gradients across membranes. However, the energy demand does not come from these processes; rather the additional energy required for cellular maintenance is due to processes that oppose these functions (Rolfe & Brown, 1997). These opposing or uncoupling processes include protein degradation, muscle relaxation and ion leaks. Consequently, decreasing any of these uncoupling processes would be expected to decrease the animal’s metabolic rate and energy requirements. Accordingly, the decrease in metabolic rate would be dictated by which organs are impacted, as well as the extent to which uncoupling processes are reduced.
Phenotypes, genes and heat toleranceCompared to Bos taurus cattle, Bos indicus cattle have improved ability to regulate their temperature in response to high temperatures. Dikmen et al. (2018) suggested that a minimum of 50% Brahman was needed to increase ability of heifers to regulate body temperature, while at least 75% Brahman was needed if heat stress was severe. These findings were based on data collected from an Angus-Brahman ‘multibreed’ herd at the University of Florida. The cattle represent a continuous spectrum from 100% Angus to 100% Brahman.
Using the same herd, Sarlo Davila et al. (2019) indicated that increasing percentage of Brahman coincided with shorter hair length and decrease in core body temperature at high environmental temperature and humidity. The hair coat color is also an important contributor to heat load (Gebremedhin et al., 2011). As expected, cattle with dark hair are more affected by temperature changes and peak temperatures than those with light colored hair, and they are at greater risk of mortality (Brown-Brandl et al., 2003; Gaughan et al., 2010).
In the case of the Angus Brahman multibreed herd, hair coat properties would be expected to represent an extreme range, from the relatively long black hair representative of Angus to the light, slick, and short hair of the Brahman. The hair coat characteristics of Brahman not only promote heat flow from the animal but also reflect solar radiation, which limits heat absorption.
There have also been efforts to utilize specific genotypes in order to determine how hair coat properties affect physiology and productivity. One such mutation, the SLICK1 allele, is a single base change in the DNA coding for the prolactin receptor, which results in a short, slick haircoat (Littlejohn et al., 2014). This mutation is found in criollo breeds and Senepol, and crossbreeding has been used to incorporate the SLICK1 mutation into other breeds.
Holstein heifers with and without the SLICK1 allele were evaluated in both California and Florida (Carmickle et al., 2022). The hot and humid conditions in Florida contributed to more severe heat stress; and in this case, slick animals exhibited reduced rectal temperatures, supporting that the SLICK1 allele helped improve thermotolerance. As prolactin is a hormone that contributes to other biological functions, it is also critical to determine how this receptor mutation may alter other physiological parameters.
Decreased heat production also appears to contribute to heat tolerance of Bos indicus. In the Florida multibreed herd, calves with greater fraction Brahman were more efficient but grew more slowly than those with greater Angus influence (Elzo, Lamb, et al., 2012). For ruminants, the liver and gastrointestinal tract contribute to roughly 20% of body weight but more than 40% of the heat production at rest (Caton et al., 2000).
In the multibreed herd, dressing percentage increased with greater proportion of Brahman (Elzo, Johnson, et al., 2012). Since dressing percentage is calculated as carcass weight relative to live weight, a proportionally smaller gastrointestinal tract could be associated with greater dressing percentage. This serves as an indirect indicator that smaller gastrointestinal tract may contribute to decreased heat production with greater Brahman influence.
There is also interest in identifying factors that influence the cellular response to heat stress. Several proteins affect cellular function and survival in response to heat stress.
For example, heat shock proteins (HSPs) are a family of proteins that are widely recognized for their role in response to heat as well as other cellular stresses. The HSPs serve various roles in preserving function of other proteins by facilitating folding, stabilization, and transport. The ability of cells to increase HSP levels in response to heat stress contributes to heat tolerance at the cellular level, indicating the activity of factors that control the amount of HSPs is also important.
While some DNA markers have been associated with heat tolerance and the cellular response, there has been little progress in identifying specific genetic differences that confer cellular resistance to heat stress.
Tenderness and Bos indicusClearly, Bos indicus possess characteristics that are well suited to hot environments, and crossbreeding is a means of incorporating heat tolerant traits in more sensitive breeds. Yet, hurdles remain to wider utilization of Bos indicus: their reputation of for greater toughness has hurt their acceptability at the rail.
This is evidenced by discrimination against Bos indicus influence in branded beef programs; currently, an astounding 66/70 (>94%) of programs require that carcasses have ≤ 2 inches hump (USDA, 2022), which is approximately 25% Bos indicus (Sherbeck et al., 1996). In conjunction, 51/70 branded beef programs (~73%) specify a black hide, which is associated with Angus phenotype. Thus, the obstacles for improving heat tolerance of feedlot cattle are compounded because there is strong demand for black-hided cattle yet clear discrimination against Bos indicus cattle. Improving tenderness and consistency of Bos indicus influenced beef is paramount for improving their acceptability.
Beef tenderness is a complex trait impacted by intrinsic muscle properties, and the conditions during harvest, processing, and aging. Beef tenderness is a function of connective tissue (Purslow, 2014) , marbling or intramuscular fat (Platter et al., 2003), and postmortem protein degradation (Huff Lonergan et al., 2010). Age of animal, as well as location of the meat cut, explain a large proportion of connective tissue-related differences in beef tenderness.
In contrast, when considering the same cut from carcasses within an age (maturity) group, marbling and protein degradation are key contributors to variation in eating quality. While marbling remains a challenge in Bos indicus influenced beef, toughness is largely attributed to altered activity of protein degradation systems during meat aging.
The primary factor governing protein breakdown in postmortem muscle is the calpain-calpastatin system (Geesink et al., 2006; Koohmaraie & Geesink, 2006). Calpain cuts proteins into fragments, which disrupts the structure and integrity of muscle cells, and contributes to tenderization of beef. Calpastatin specifically inhibits the degradative action of calpain. Calpain also cleaves calpastatin; these calpastatin fragments retain inhibitory activity, which declines during the subsequent aging period.
Bos indicus cattle are well-documented to possess elevated calpastatin content in muscle, which inhibits protein degradation and results in tougher beef (Wheeler et al., 1990; Whipple et al., 1990). Classically, the ratio of calpain: calpastatin activity is considered a predictor of tenderness, and this ratio is also generally less favorable in Bos indicus cattle. Yet, it is important to note there is also greater variation in tenderness in Brahman; in fact, some Brahman are very tender. Calpastatin is a contributing factor, but it does not completely explain the variability in tenderness.
It is possible the greater calpastatin observed in muscle of Brahman and Bos indicus breeds may be a way of limiting protein degradation in the animal, thereby restricting metabolic heat production. Muscle growth is an energetically demanding process; to increase muscle mass, proteins must be synthesized as well as degraded, which is also known as protein turnover. The net balance of synthesis and degradation dictates the gain in muscle mass. The calpain-calpastatin system is one of several systems that contribute to protein degradation in living muscle.
As indicated earlier, relatively small changes in metabolic heat production in skeletal muscle could have a more meaningful contribution to body heat production due to the overall mass of muscle in the body. It is also possible that other organs of Bos indicus cattle possess mechanisms to restrict protein degradation, but these data have not been reported. Further, this highlights that efforts to improve meat quality can impact characteristics of muscle growth in the living animal, and changes may not be mutually beneficial to growth and meat quality.
In living muscle, calpain and calpastatin action are tightly regulated to have precise control over protein degradation. While the content of calpain and calpastatin is important in dictating the breakdown of muscle, the function or activity is also significant.
These mechanisms are studied intensively in living muscle with regard to agricultural production and human health, but understanding regulation of activity in the changing environment of postmortem muscle is quite complex. At slaughter, muscle does not immediately become meat; rather, a number of changes occur during the “conversion of muscle to meat.”
The physical, biochemical and energetic changes that occur in muscle after slaughter are critical for determining the development of meat quality attributes. For instance, the loss of oxygen supply leads to a shift in metabolism and a gradual depletion of available energy resources. In turn, the loss of energy results in rigor, or the stiffness of death. Meanwhile, the pH of muscle becomes more acidic, with pH declining from approximately 7.4 to 5.6, and carcasses slowly cool from body temperature (101°F) to <40°F at 24 hours postmortem.
The rate and extent by which these changes occur influence development of beef tenderness. Although refrigerated storage of meat for several weeks after slaughter (aging) improves beef tenderness, the majority of tenderization caused by protein degradation occurs in the first 24-72 hours postmortem. During this time, changes in pH, temperature and calcium, affect calpain activity. Specifically, increases in calcium trigger activation of calpain and initiation of protein degradation.
Muscle characteristics and tenderizationShifting muscle characteristics could be important to regulating overall body metabolism and heat tolerance. So, this raises the question: what else might be different in Bos indicus influenced muscle?
Muscle is a heterogeneous tissue, and the properties of individual cells vary in order meet specific functional demands. Muscle fibers (cells) are classified according to their contractile and metabolic properties, which is dictated by functional demands. There is an association between fiber type characteristics and meat tenderness. Further, certain fiber types tend to have greater calpastatin content, which is linked to growth rate and function of specific muscles within the animal.
However, when comparing the same muscle, the type of contractile proteins expressed in Bos taurus and Bos indicus is not significantly different (Crouse et al., 1989; Wright et al., 2018), and thus likely does not explain variation in either calpastatin content or tenderness.
The expectation is that Bos indicus muscle possesses additional mechanisms to maintain or protect the cell in the face of adverse physiological circumstances. Metabolic characteristics and regulation of metabolism may be important for the adaptability of Bos indicus muscle.
Mitochondria content may be greater in Brahman (Wright et al., 2018), and functional aspects of mitochondria may also differ (Ramos et al., 2020). Considering mitochondria are the energy “powerhouses” of the cell, this has potential ramifications for metabolic heat production and heat tolerance, as well as postmortem tenderization. In living muscle, increased coupling of respiration and energy production increases efficiency and lowers heat production by mitochondria.
From a postmortem perspective, there are a couple possibilities for how mitochondria may influence tenderization. First, mitochondria can sequester calcium; in turn, this could prevent increases in calcium within the cell, thereby delaying the activation of calpain. Moreover, mitochondria participate in pathways that initiate cell death, which are expected to hasten postmortem metabolism and instigate protein breakdown.
The HSPs have also attracted attention for their link to cellular stress, protein degradation, and tenderness (Gagaoua et al., 2015, 2021). Elevated levels of HSPs have been suggested to protect proteins from degradation during meat aging, thereby contributing to toughness.
ConclusionsHeat tolerance is a complex trait related to heat exchange between the animal and its environment, and the heat production by the body. Bos indicus breeds are often utilized via crossbreeding to impart heat tolerance and adaptability for production in hot, humid climates. However, their reputation for slow growth and greater variation in eating quality has created distinct marketing disadvantages and poses obstacles to greater utilization of Bos indicus.
There are several possible connections between cellular heat production, stress response and tenderness, including protein degradation (calpastatin), mitochondria function and heat shock proteins.
It is important to continue to work to define the phenotypes and genotypes that impart heat tolerance and adaptability, and to determine relationships between heat tolerance, growth and meat quality. Ultimately, this can improve resiliency of cattle without sacrificing production of high quality beef.
References available upon request.
Scheffler is an associate professor in the Department of Animal Sciences, University of Florida.
