Thermoregulatory Mechanisms in Altricial and Precocial Species: Comparison
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Thermoregulation in newborn mammals is an essential species-specific mechanism of the nervous system that contributes to their survival during the first hours and days of their life. When exposed to cold weather, which is a risk factor associated with mortality in neonates, pathways such as the hypothalamic–pituitary–adrenal axis (HPA) are activated to achieve temperature control, increasing the circulating levels of catecholamine and cortisol. Consequently, alterations in blood circulation and mechanisms to produce or to retain heat (e.g., vasoconstriction, piloerection, shivering, brown adipocyte tissue activation, and huddling) begin to prevent hypothermia. Determined mainly by physiological maturity, mammals can be classified into altricial and precocial species. Although altricial and precocial newborns have several mechanisms to maintain a stable body temperature, a sudden drop in temperature experienced at birth reduces vigor and affects their feeding ability. Consequently, the acquisition of immunoglobulins and the ingestion of nutrients that fuel thermogenesis are compromised.

  • thermoregulation
  • body temperature
  • brown adipose tissue
  • animal welfare
  • neonate welfare
  • fetal welfare
  • puppy
  • foal welfare
  • buffalo newborn
  • IRT
  • Thermoregulation
  • Infrared thermography

1. Introduction

Neonatal mortality in domestic animals such as lambs, calves, foals, piglets, and rodents responds to several maternal and offspring factors. Within these, hypothermia caused by excessive heat loss or inhibition of thermoregulation and heat production is considered a major element that causes mortality of newborn animals [1][2][3]. Hypothermia is mainly the result of starvation when the offspring is unable to suckle [1]. Neonatal survival within the first 24 to 72 hours is highly related to decreased body temperature experienced at birth. At this moment, the offspring abruptly transitions from a warm, nutritious, sterile, and controlled environment in utero to the extrauterine environment, usually at a much colder temperature (1 to 2 °C below), exposed to novel microorganisms and deprived of a nutrient supply via placenta [4][5][6][7]. These physical and physiological changes can generate hypoglycemia, hypoalbuminemia, energy alterations, or acid-base alterations leading to growth retardation or multiorgan failure [8].
The separate evolution of endothermy in mammals and birds is considered an important transition in vertebrate evolution. It is a unique case of convergence between these two groups, essential to their rapid spread across the planet and their ecological success [9][10]. Rezende et al. [10] observed that when metabolism increases, the sizes of the individuals decrease (and that is why dinosaurs gave rise to birds). In endotherm animals, thermoregulation is a homeostatic and dynamic process between the internal response of an organism and its external environment [11][12][13]. This internal response triggers a series of thermoregulatory mechanisms that are modulated by the preoptic area of the hypothalamus (POA) [14], and they are aimed at promoting energy conservation in the neonate, using this mechanism for growth, development, and cellular functions [15][16]. However, newborn’s interspecies characteristics, such as the presence or absence of thermogenic cells, e.g., brown adipocyte tissue its acronym is BAT; the presence of fur at birth, the thickness of the dermis, behavior at birth, locomotor abilities, and general organ development, can either facilitate or hinder thermoregulation [17].
These interspecies differences respond to physiological maturity, known as the newborn’s capacity to cope with the transition between the intrauterine life and the external environment. Such maturity involves activating several neuroendocrinological and behavioral changes. Nonetheless, nutrition, genetic selection, and pharmacology can also influence maturity at birth. Similarly, factors leading to the activation of the hypothalamic–pituitary–adrenal axis (HPA) [18], increasing the catecholamine and cortisol concentrations either in the fetus or the newborn animal [19], will cause changes in blood flow that will ultimately compromise the newborn’s thermoregulation capacity [20].

12. Brown Adipose Tissue Activation (BAT)

Among the three types of adipose cells found in mammals (brown, white, and beige), BAT represents the least abundant but the one with the greatest thermogenic capacity, especially at birth [21]. Nonetheless, its quantity depends on the fetal development during gestation, the species (altricial or precocial), and the deposited anatomical site [22]. Unlike WAT, BAT has more mitochondria, high cytochrome Cc content, a vast vascular network [23][24], and BAT activation is mediated by uncoupling protein 1 (UCP1) [8]. UCP1s respond to the secretion of norepinephrine (NE) released by the sympathetic nerves and its action on β3 adrenoreceptors, whose effect is reversible through vagal stimulation (parasympathetic) [11][25]. Among other actions, NE promotes the proliferation of preadipocytes, the differentiation of mature adipocytes, regulates the expression of genes that encode UCP1, and increases mitochondrial mass. Altogether, NE actions contribute to heat generation through ATP synthesis by UCP1 [26] and lipolysis [27]. In the case of altricial species such as laboratory rodents, the relative percentage of BAT and white adipocytes can vary, depending on environmental and nutritional conditions, sex, and age. However, its remarkable plasticity allows retroperitoneal WAT to transform to BAT when exposed to cold [28]. An example of this was reported in 27 newborn deer mice (Peromyscus maniculatus) kept at a temperatures of 5 °C. BAT utilization increased by 42% (measured in terms of oxygen consumption), suggesting it is the only mechanism responsible for maintaining thermal stability during the first days of life [29]. Likewise, prenatal exposure to temperatures of 15 ± 4.2 °C on a female Darwin´s leaf-eared mouse (Phyllotis darwini) was shown to improve the thermoregulatory capacity of neonates, achieving higher body temperatures (32.3 ± 2.41 °C) compared to animals acclimated to an ambient temperature of 30 °C, which can be attributed to higher amounts of BAT and the increased expression of UCP1 in adipocytes [30]. Nevertheless, the characteristics and the properties of BAT may differ between lines of the same species. In a comparative study between B6 and A/J mice, it was found that cold stress only induced BAT activation in A/J mice due to genetic variability in the expression of UCP1 and adipogenesis. B6 mice are an inbred strain used to study obesity, a trait associated with BAT [31], while A/J mice are another strain with susceptibility to obesity and, together with B6 mice, have shown regional differences after adrenergic stimulation of UCP1 [32]. In B6 mice, a resistance of BAT induction has been reported by adrenergic stimulation, contrary to the A/J strain. In A/J mice, the UCP1 expression in the retroperitoneal fat at 60 days of age was higher than in B6 mice, with an induced activity of 71%, more active than interscapular BAT. In contrast, in B6 mice, the presence of BAT was lower than that found in A/J mice at one month of birth [33]. Additionally, the mother’s diet and body condition have also been associated with the functionality and pre- and post-natal development of BAT. A study with female C57/BL mice of 10 to 12 weeks of age observed that obese mothers fed a high-fat diet presented a deficient activity of BAT as a thermoregulator, where the activation and the expression of UCP1 and other proteins responsible for lipolysis had a lower oxygen consumption. In contrast, a deficient BAT activation was not observed in mice from dams with balanced diets [34]. On the other hand, species that are born with a low birth weight in relation to the average birth weight of the species or breed, like canine puppies, are more exposed to hypothermia because they have less adipose tissue. Moreover, when there is competition with littermates for access to a nipple/teat or a deficiency in colostrum intake at birth, there is a higher risk of hypoglycemia, which has important repercussions on neonatal survival [35][36].

2. Thermoregulation in Precocial Animals

Precocial animals, such as ruminants usually present a greater development of thermoregulatory mechanisms at birth, allowing them to maintain a constant body temperature, even in cold environments [37]. In these species, non-shivering thermogenesis is the most used mechanism in neonates. For example, in lambs (O. aries), approximately half of the cold-induced summit metabolic rate comes from non-shivering thermogenesis. The presence of metabolic-active BAT during the early postnatal period is essential [38]. However, adipose tissue distributed in the pre-scapular, inguinal, and prerenal regions represents only 2% of the total body weight [25][39]. The thermogenic activity has been measured in perirenal adipose tissue from newborn lambs (O. aries) for up to 33 days. In these animals, the impact of cold acclimatization of the pregnant dams can influence the thermogenic capacity of the offspring. In lambs from mothers exposed to cold climates, they had a 21% greater perirenal fat, increased metabolic activity (40%), and higher oxygen consumption in cold temperatures (16%). Additionally, the thermogenesis responses of these lambs were due solely to non-shivering thermogenesis, in contrast to lambs from dams not climatized to the cold [40]. The activation of BAT tissue responds to an increase in blood levels of cortisol, NE, and epinephrine. These catecholamines bind to beta-3-adrenergic receptors located in BAT, activating the UCP1 in the inner mitochondrial membrane. UCP1 and thermogenin increase the H+ ion flux at the mitochondrial level without ATP production [41]. Similarly, during birth, the plasma levels of hormones such as triiodothyronine (T3) and thyroxine (T4), triggered by the release of thyroid-stimulating hormone (TSH), increase metabolic consumption of adipose tissue to produce non-shivering thermogenesis [42]. In lambs, Schermer et al. [43] studied the thermoregulatory capacity of newborn lambs with fetal thyroidectomy. According to Litten et al. [44] and Silva [45], the thyroid hormone pathway for heat production is more developed in precocial species. Thyroid hormones are critical for the generation and the maintenance of body basal temperature (BBT), and even slight changes in hormone levels can affect BBT [45]. It has been observed that minor changes in thyroxine (T4) concentrations significantly impact body temperature [45][46]. BAT contains multiple enzymes called deiodinases, essential for converting T4 to active triiodothyronine (T3). In other words, BAT can generate T3, which is crucial for producing ATP and heat [47]. When exposed to cold stimuli, the enzyme 5-deiodinase type II is activated, converting T4 to T3. However, if T3 is not produced, UCP1 synthesis is blocked, leading to hypothermia [48]. Due to the influence of thyroid hormones in thermoregulation [44][45], thyroidectomized animals presented lower colon temperatures (up to 2.35 °C) than control animals. For example, Berthon et al. [49] found that in pigs, lower plasma levels of T4 are present in animals with a lower rectal temperature after birth. Likewise, the thyroidectomized animals had a lower oxygen consumption rate and a higher incidence of shivering thermogenesis, which coincides with a lower activity of the perirenal adipose tissue, lower levels of uncoupling protein, and a higher lipid content. In most mammals, concurrently with non-shivering thermogenesis, colostrum intake in the first hours of life represents an energy resource that contributes to maintaining a stable temperature in neonates [2]. In particular, the nutrients present in colostrum provide water, bioactive compounds, growth factors, digestive enzymes, and immunoglobulins, and one of its main roles during the first days after birth is the supplement of energy in the form of kcal/L. Although it is said that the nutritional properties of colostrum and milk are similar during the first days of life, the energy value of colostrum can be 20–30% higher than the values registered after three days or two weeks [50]. Additionally, colostrum intake and glucose absorption prevent hypoglycemia due to the low fat and glycogen storage in newborns [51], maintaining normal glucose levels that can support thermogenesis [52]. For example, in calves, colostrum provides large amounts of glucose and amino acids, equivalent to 6.7 MJ/g, that can be used to produce heat [42][53]. Piglets (S. scrofa) are a species born with low amounts of BAT; their main ways of heat production rely on shivering and colostrum intake shortly after birth [54]. Furthermore, several molecular (e.g., the presence of uncoupling proteins 1, 2, or 3, the responsible for non-shivering thermogenesis), ultrastructural (e.g., number of mitochondria in longissimus thoracis and rhomboideus muscle per unit tissue area), biochemical (e.g., fat oxidation, mitochondrial processes), physiological, and metabolic adaptations in the maturation of the energy production of the musculoskeletal system in piglets are an adaptive thermoregulatory mechanism [54]. Additionally, newborn piglets use their body fat and glycogen stores to survive in the first 12 to 24 h after birth [55]. On the other hand, the fetal development of BAT, the mother’s diet during gestation, and the influence of hormones such as melatonin have been shown to influence the thermoregulation capacity of the newborn. The case of 5 to 6-day-old lambs born from dams with low melatonin profiles and exposed to 4 °C showed a reduction in BAT temperature of approximately 39.8 °C compared to the control group of 40 °C and elevated NE concentrations greater than 1000 pg/ml, as a result of thermal stress [56]. Thermogenesis by BAT activation is essential in the neonate of most species, and it is also essential in hibernating animals such as American black bears (Ursus americanus) [57][58], which represents the first resource during the postnatal period. However, for species with limited energy reserves at birth, such as newborn piglets with low amounts of BAT or rodent pups with non-fully developed interscapular BAT, colostrum intake and other mechanisms to preserve heat are critical to prevent hypothermia.

3. Shivering

Shivering is the universal thermogenic mechanism through the repetitive and rapid contraction of the skeletal muscle when the body is exposed to cold environments or when there is hypothermia. The muscle fibers are from resistant aerobic muscles that can produce repeated contractions [59]. This process utilizes the oxidation of carbohydrates, lipids, and proteins obtained from muscle reserves and the circulating blood [60]. Despite being a mechanism for heat production, shivering includes consequences such as an increase in oxygen consumption of up to 20-fold, increasing the aerobic capacity of muscle fibers, and leading to fatty acid oxidation [59]. Other consequences include an increased intracranial pressure and metabolic demand, causing poor ventilation synchronization [61]. This hypoxic effect has been reported in newborns. For example, in deer mice (P. maniculatus), high-altitude habitats (4350 m.a.s.l.) reduce the capacity to generate heat by shivering. The capacity is reduced by 30%, and only when deer mice pups reach 27 days-old do they develop an aerobic muscle phenotype, predisposing them to hypothermia and mortality. However, this characteristic is also considered a physiological adaptation to reduce energy expenditure by thermoregulation [62]. One of the main differences in thermogenic capacity through shivering between altricial and precocial species is caused by species-specific morphological features. For example, the intensity of shivering depends on the percentage of body fat, the surface-to-volume ratio, and the ATP necessary to maintain contractions [60]. In the case of dogs, the mechanism of shivering thermogenesis is poor or absent, having a greater risk of hypothermia. Additionally, dog puppies (Canis lupus familiaris) have only 1.3% body fat [63]; therefore, they rely on milk intake and constant maternal care to properly thermoregulate [64][65]. A similar case is seen in cubs of polar bears (Ursus maritimus), where they are born in temperatures as low as −25 °C. Over time they increase the ability to shiver, improve their insulation traits and, in some cases, develop BAT [66], or resort to other methods such as vasomotor control to maintain an adequate body temperature. As stated before, thermogenesis through rapid and oscillating muscle contractions or twitching of skeletal muscle is an involuntary mechanism that produces energy released in heat [41]. Although for most precocial species it is the most efficient method for heat production and thermal equilibrium when exposed to cold environments [67], it cannot be used as a primary method due to the immaturity of the muscle tissue observed in some species, such as ruminants) [37]. In this sense, shivering heat production in piglets has been associated with a decrease in muscle glycogen up to 47%, as well as a decrease in total lipid content, a decrease in lactate in blood, and better muscle cytochrome oxidase activity (by 20% more), indicating the increase in muscle potential with exposure to cold [68]. According to Alexander and Williams [69], in one-day-old Merino lambs and one-month-old lambs, the mechanisms of thermogenesis by shivering, in comparison with the mechanisms that use BAT, are considered the basis of its thermoregulation in the first days of life. Similarly, shivering is considered a complementary mechanism activated in the first four days of birth because newborns suffer rapid thermoregulatory alterations when the adipose tissue is insufficient to maintain thermal comfort [40]. On the other hand, in piglets exposed to low temperatures (25 °C), thermogenesis by shivering increased its activity. However, their temperatures remained slightly lower than newborns exposed to thermoneutral temperatures (34 °C) [68]. In a recent study, Schmitt et al. [70] evaluated the piglets’ thermoregulation efficiency from two divergent lines for the residual feed intake (high feed efficiency and less feed efficiency). Rectal temperature, infrared thermography of ear base and tip and back were recorded. Vigor, evaluated by respiration, mobility, vocalization, and morphology, was also registered by weight, length, width, and circumference. The researchers observed that both vigor and morphology did not vary between piglet lines, but it was possible to observe a greater weight gain in the efficient lines (7.1 ± 1.3 g) compared to the less efficient (3.6 ± 1.3 g). Likewise, animals with a higher efficiency had a lower temperature in the ear region (24.7 ± 0.37 °C vs. 26.3 ± 0.36 °C). All of the above allows researchers to establish that thermogenesis through shivering is a mechanism that depends on the type of muscle fiber of the newborn. In this process, efficient feeding is essential since neonates use their feed intake as a source of energy to maintain vital function and, consequently, survival. However, if the source of hypothermia is not addressed, continued shivering can have adverse consequences for the neonate.

4. Vasomotor Control

Another sympathetic-dependent response to hypothermia is vasomotor shifts in the peripheral circulation [71]. When exposed to a cold stimulus, the cold-sensitive neurons located in the POA and the activation of the HPA axis induce the secretion of catecholamines (epinephrine and NE) and other neurotransmitters such as neuropeptide and ATP [41]. Consequently, they activate receptors in the blood vessels to produce vasoconstriction [72][73] to divert blood flow from the limbs or peripheral structures to vital organs [74][75][76]. Solomon et al. [77] demonstrated this in four Long Evans rats (Rattus norvegicus) subjected to motility frustration (e.g., not being able to use an activity wheel). These animals showed restlessness, and the stress caused low paw temperatures due to sustained vasoconstriction. In precocial species, some differences in thermoregulation between breeds have been reported. In pigs (S. scrofa), 2 to 4-hour-old Meishan piglets (Sus domesticus) have greater development at birth than piglets of the European breed. For example, in Meshian piglets, cardiovascular responses to cold (vasoconstriction) were observed on birth/1 day/2 days after birth. In contrast, in Pietrain, Landrace, and Large White crossbred piglets, the vasomotor response capacity was not observed until five days after birth [78]. However, these differences cannot only be associated with the vasomotor response. Renaudeau et al. [79] have studied the thermoregulatory differences between European (Large White) and Caribbean (Creole) pigs regarding breed, season, and skin histology. The dermis of Creole pigs was thicker than Large White (3.60 vs. 3.13 mm) and they had a higher density of sweat glands (32.0 and 25.4 glands per mm2, respectively). Although these traits can be associated with enhanced adaptability of Creole pigs as a heat-tolerant breed, they may also influence the thermoregulatory efficiency in piglets during the first days of life or the growing stage, but this needs further studies [80]. As a possible assessment of this vasoconstriction during hypothermia, infrared thermography (IRT) has been implemented, which reflects the peripheral blood flow through the emitted radiation [81]. Kammersgaard et al. [82] evaluated the thermal response in 91 newborn piglets under three different environmental temperatures (15 °C, 20 °C and 25 °C) through IRT and rectal temperature from birth to 48 h after parturition. They observed a positive correlation between the ear and rectal body temperature. For example, when the piglet’s IRT indicated a temperature of 30 °C, the rectal temperature was 32 °C or less, with an IRT confidence of 91.3%. Similarly, McCoard et al. [83] evaluated the thermal response by IRT and rectal temperature after birth in 10 newborn lambs. Continuous thermograms were recorded during the evaluation of a 30-min sequential baseline (11–18 °C), 30-min cold exposure (0° C), and 30-min recovery (11–18 °C) time evaluation. They observed that the rectal temperature decreased between 0.4–1 °C from the baseline to the end of the recovery period, while there were no changes in IRT during the baseline event. Five minutes after cold exposure, a rapid decrease of 5 °C was observed. These researchers attribute that the observed linear thermal response is due to the change in surface blood flow in response to cold to preserve heat. This result makes it possible to suggest IRT as a valuable tool because of its non-invasive nature and the correlation between the decrease in peripheral blood flow caused by hypothermia.

5. Behavior and Postural Changes

Besides the metabolic and physiological mechanisms of thermoregulation, animals perform certain behaviors and postural changes to minimize heat loss [84]. Some examples are warmth seeking, nesting, burrowing, huddling, basking, and calling for the mother [85][86]. Most of the thermoregulatory behavioral changes observed in animals are innate activities. However, there is evidence that learning is another adaptative mechanism to adverse environmental conditions, as observed in rats who have shown their capability to learn and light lamps to generate heat [87]. It is believed that these behavior and postural changes involve the activation of the POA; however, it has not yet been established [11]. In pigs (S. scrofa), it has been observed that adopting postures such as huddling with littermates [88] or assuming a sternal position reduces the contact surface with the ground and prevents heat loss at birth [89]. In European rabbit kits (O. cuniculus), the most frequent behaviors are huddling, rooting, climbing, and maintaining close contact with the rest of the littermate. These behaviors seek to retain a better position within the nest, ensuring a source of heat and food [90]. In this same sense, García-Torres et al. [91] have studied the relationship between BAT, triglyceride concentrations, and huddling of the chinchilla-strain rabbits (O. cuniculus, F. domestica). Researchers determined that BAT is the main activation mechanism of thermogenesis in newborn rabbits, and that posture changes are vital in preserving their body temperature. They reported that kits positioned on the group’s periphery had lower BAT reserves and low triglyceride concentrations (101.7 ± 24.8 mg/dL), suggesting that these animals were exposed to a greater thermal and metabolic challenge than the rabbit neonates found in central positions. IRT is a tool not limited to evaluating vasomotor thermoregulation mechanisms, and there are reports that this tool can record BAT or muscle activity in laboratory animals in different settings [92].  In precocial species such as lambs, behavior at birth greatly contributes to their thermoregulation. One of its first reflexes is standing from the floor and seeking the udder to suckle and to consume colostrum. Getting up off the ground reduces heat loss, while the vitality and they speed with which the newborn finds the nipple promote early colostrum intake necessary for energy production [2]. Unlike lambs, kids (newborn goats) are considered more sensitive to hypothermia during the first hours of life. Giannetto et al. [93] have reported in Maltese kids that the circadian system is the predominant mechanism for maintaining homeostasis after birth due to the development of this system and the genetic and phenotypic differences with lambs. In newborn piglets, vitality, and suckle capacity influence their survival rate after birth and determine their thermoregulation efficiency [94]. Together with animals’ weight and size, vitality influences thermoregulation [95]. Moreover, it has been reported in newborn moose (Alces alces) that, in addition to the amount of BAT present at birth, newborns require feeding an average of 8 times a day in 130 second sessions to obtain nutrients and to thermoregulate [96]. Similarly, blue foxes (Alopex lagopus) in artic environments can reduce heat loss through postural and behavioral changes, increasing metabolic heat production to prevent heat transfer from the core to the surface [97].

6. Diving Air-Breathing Marine Vertebrates

Air-breathing marine vertebrates need to maintain thermal homeostasis in an oxygen-limited aquatic environment. That is why these animals, thanks to their phylogeny and thermoregulatory adaptations, have managed to survive in environments with changing temperatures using morphological, physiological, and behavioral traits [98][99][100]. Sirenians, for example, are the only herbivorous marine mammals with relevant thermoregulatory implications. They have a very slow metabolism, limiting their capacity for thermogenesis and making them sensitive to cold [101]. Marine mustelids and ursides are also exposed to extreme climatological challenges. Small marine mammals such as otters (Enhydra lutris) inhabit places with cold temperature climates to subarctic waters, while polar bears (Ursus maritimus) live in the arctic [102]. Another example is penguins (Aptenodytes patagonicus), which with their adaptations can lower their abdominal and subcutaneous temperature to −25 °C and then return to their normal temperature through subsequent rewarming [103].

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