Strategies and Mechanisms of Thermal Compensation in Newborn Water Buffaloes

Abstract

Hypothermia is one of the principal causes of perinatal mortality in water buffaloes and can range from 3% to 17.9%. In ruminants, factors affecting hypothermia in newborns may be of intrinsic (e.g., level of neurodevelopment, birth weight, vitality score, amount of brown fat, skin features) or extrinsic origin (e.g., maternal care, environmental conditions, colostrum consumption). When newborn buffaloes are exposed to cold stress, thermoregulatory mechanisms such as peripheral vasoconstriction and shivering and non-shivering thermogenesis are activated to prevent hypothermia. Due to the properties of infrared thermography (IRT), as a technique that detects vasomotor changes triggered by a reduction in body temperature, evaluating the central and peripheral regions in newborn buffaloes is possible. This review aims to analyze behavioral, physiological, and morphological strategies and colostrum consumption as thermal compensation mechanisms in newborn water buffalo to cope with environmental changes affecting thermoneutrality. In addition, the importance of monitoring by IRT to identify hypothermia states will be highlighted. Going deeper into these topics related to the water buffalo is essential because, in recent years, this species has become more popular and is being bred in more geographic areas.

Keywords: Bubalus bubalis; non-shivering thermogenesis; ruminant hypothermia; shivering thermogenesis; thermoregulation.

Figure 1

Differences in dermal structure between Bubalus bubalis and Bos taurus. Water buffaloes have a thicker epidermis and stratum corneum, as well as more melanocytes, giving them dark skin. These are properties that contribute to providing resistance to cold in adult animals. However, the density and size of sweat glands, as well as the number of hair follicles, makes them susceptible to heat stress in adulthood.

Figure 2

Neonatal vitality parameters in ruminants.

Figure 3

Thermoregulation mechanisms that are activated in response to cold stress. In general, when mammals face acute cold, a sequence of events begins whose purpose is to preserve heat or produce it. In the first instance, vasomotor control (vasoconstriction) and piloerection are mechanisms at the skin level to preserve heat. Thermogenesis by shivering or by using adipose tissue is considered a second mechanism for producing heat when the body is unable to control heat loss. UCP1: uncoupling protein 1.

Figure 4

Thermogenesis by activation of brown adipose tissue. When thermoreceptors located in the periphery of newborns detect decreases in temperature (mainly TRPA1 and TRPM8), these cold-sensitive neurons transduce and transmit the thermal signal to the DRG of the spinal cord. Through the LPBel, the signal is in the thermoregulatory center (POA), from which sympathetic neurons are directed towards the IML and towards the BAT. In this adipose tissue, the interaction of NE (released by sympathetic neurons) generates lipogenesis and heat production in the BAT mitochondria, thanks to the activation of UCP1 receptors. AC: adenyl cyclase; β3-AR: beta-3 adrenergic receptor; cAMP: cyclic AMP; DMH: dorsomedial hypothalamus; DRG: dorsal root ganglion; FA: fatty acids; Glu: glutamate; LPBel: external lateral part of the lateral parabrachial nucleus; NE: norepinephrine; PKA: protein kinase A; POA: preoptic area; rRPA: rostral raphe pallidus; TRPA: transient receptor potential ankyrin 1; TRPM8: transient potential receptor melastatin 8. TG: triglycerides; UCP1: uncoupling protein 1.

Figure 5

Shivering thermogenesis. Shivering, caused by skeletal muscle contractions in response to activation of α and γ motor neurons, is initiated by activation of cold-sensing neurons. These transmit the information to higher centers such as the DMH and the DA at the POA. Through projections from the POA to the rRPA and VH, motoneurons generate repeated contractions that lead to heat production. DA: dorsal hypothalamic area; DH: dorsal horn; DMH: dorsomedial hypothalamus; DRG: dorsal root ganglion; Glu: glutamate; LPBel: external lateral part of the lateral parabrachial nucleus; POA: preoptic area; rRPA: rostral raphe pallidus; TRPA: transient receptor potential ankyrin 1; TRPM8: transient receptor potential melastatin 8; VH: ventral horn.

Figure 6

Neonatal behavior and standing/suckling latencies. SD: standard deviation.

Figure 7

Vascularization of the newborn ruminant and its relationship with infrared thermography. Infrared thermography, as a technique that detects changes in blood flow, depends on the circulatory system of animals and the changes associated with the perception of cold.

Figure 8

Thermal response in newborn water buffalo with different birth weights and different thermal windows at day 0. (A) the periocular thermal window (El1) and the pelvic limb thermal window (El2) can be seen. (B) shows the temperature values in different thermal windows according to the weight of the newborn buffalo divided by quartiles on day zero. Maximal temperature is indicated with a red triangle and the minimal with a blue triangle. ** Indicate significant differences between groups (p < 0.01).

Figure 9

Thermal response in newborn water buffalo with different birth weights and different thermal windows at day 5. (A) the surface temperature of the thermal windows in the water buffalo is presented for day 5 postpartum, and it is observed that in the periocular region (El1) it was 36 °C and in the limb pelvic region (El2) it was 31.7 °C. (B) shows the temperature values in different thermal windows according to the weight of the newborn buffalo divided by quartiles on day five after birth. Maximal temperature is indicated with a red triangle and the minimal with a blue triangle. * Indicates significant differences between groups (p < 0.05).

Figure 10

Thermal response of newborn water buffalo calf and postpartum mother. (A) Newborn calf. The periocular (El1) and nasal (El3) surface temperatures are presented, where it is possible to observe mean surface temperatures of 36.8 °C and 35.4 °C, respectively; this response may be associated with hypothermia due to the presence of amniotic fluid. (B) Postpartum mother. Like the offspring, the thermal response of the periocular (El2) and nasal (El1) regions is presented, where average surface temperatures of 35.5 °C and 34.7 °C, respectively, were presented. From a comparative perspective, it can be observed that the overall surface temperatures of the different thermal windows in the mother were lower by 1.3 °C in the periocular region and 0.7 °C in the nasal region. This could be due to the mother’s perception of acute pain. The activation of the SNS causes the neurosecretion of catecholamines, producing peripheral vasoconstriction, which reduces heat radiation, while this same response of the ANS in the calf allows an increase in temperature due to the different mechanisms of thermogenesis and the vasomotor control of temperature in the central windows. Maximal temperature is indicated with a red triangle and the minimal with a blue triangle. Radiometric images were obtained using a T1020 FLIR thermal camera. Image resolution 1024 × 768; up to 3.1 MP with UltraMax. FLIR Systems, Inc. Wilsonville, OR, USA.

Figure 11

Effect of birth weight on the thermal response of different thermal windows in newborn water buffaloes during the first 5 days of life. Graph (A) shows the IRT for the surface temperature of the periocular region thermal window in relation to the weights of the calves on the day of birth. Graph (B) shows the IRT for the surface temperature of the thermal window of the pelvic limb. In panel (C), the IRT is shown for the surface temperature of the thermal window of the nasal region. In Graph (D), the IRT is shown for the surface temperature of the thermal window of the thoracic limb. ^a,b Different literals indicate significant differences between groups of high- and low-weight buffalo calves (p < 0.05).