Exhaled air temperature and water conservation in lizards

doi:10.1016/0034-5687(70)90079-4

Respiration Physiology

Volume 10, Issue 2, September 1970, Pages 151-158

Respiration Physiolo...

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Abstract

Studies of the desert iguana (Dipsosaurus dorsalis) show that a significant amount of water can be saved by exhaling air at temperatures below body temperature. When body temperature is near-equal to ambient air temperature the exhaled air is about 0.5 °C below body temperature, but when body temperature is higher than ambient air temperature (as in nature when the lizards bask in the sun) the exhaled air is cooled by several degrees. For example, a lizard with its body temperature maintained at 42 °C in air at 30 °C (r.h., 25 %) exhales air at 35 °C and recovers 31 % of the water that would have been lost if air were exhaled saturated at body temperature. The mean body temperature of active lizards in the field has been found to be about 42 °C (even when the air is much cooler), and the ability to exhale air at a lower temperature is therefore of great importance in their water balance.

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The function of conchae garnered extensive interest in the 1960s and 1970s with the seminal works of Jackson and Schmidt-Nielsen (1964), Schmidt-Nielsen et al. (1970), and Collins et al. (1971) laying the groundwork for nasal passage function and the role of respiratory conchae in maintaining heat and water balance. Several studies later validated these conchal functions across a broad range of species within Amniota (Schmidt-Nielsen et al., 1969; Murrish and Schmidt-Nielsen, 1970; Murrish, 1973; Langman et al., 1979; Schmidt-Neilsen et al., 1981; Schroter and Watkins, 1986). The role of conchae in maintaining body temperature and reducing respiratory evaporative water loss (REWL), coupled with the generally more complicated conchae observed in mammals and birds has led to the hypothesis that respiratory conchae—and the turbinates on which they rest—may be a necessity for the evolution of tachymetabolic endothermy (Hillenius, 1992, 1994; Ruben, 1995; Ruben et al., 1996; Hillenius and Ruben 2004).
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Immunolocalization of aquaporins 1, 3, and 5 in the nasal respiratory mucosa of a panting species, the sheep (Ovis aries)
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Heat and water added upon inspiration is lost to the environment upon expiration (Murrish, 1973). The nasal mucosal epithelium is the primary site for respiratory evaporative water loss (REWL) (Hales, 1973; Murrish, 1973; Murrish and Schmidt-Nielsen, 1970), and the efficiency of REWL depends on the continuous replacement of water that is evaporated from the mucosal surface by water passaging from the blood to the respiratory surfaces (Cauna and Cauna, 1975). How that water reaches the surface epithelium is unknown.
The nasal respiratory mucosa is the primary site for evaporative water loss in panting species, necessitating the movement of water across the nasal epithelium. Aquaporins (AQP) are protein channels that facilitate water movement in various fluid transporting tissues of non-panting species. Whether the requirement for enhanced capacity for transepithelial water movement in the nasal respiratory mucosa of panting species has led to differences in AQP localization is unknown. Using immunohistochemistry, we report the localization of AQP1, 3, and 5 in the nasal respiratory mucosa of sheep being exposed to ambient temperatures of ~21 °C or ~38 °C for 4.5 h before death (n=3/treatment). Exposure to either treatment resulted in panting. While exposure to ~38 °C resulted in a higher respiratory frequency (mean difference: 82 breaths min⁻¹; P<0.001) than exposure to ~21 °C, there was no difference in the localization of AQPs. Connective tissue and vascular endothelial cells expressed AQP1. Glandular acini expressed AQP1 and apically localized AQP5, which was also present in glandular duct cells. Ciliated columnar epithelial cells expressed AQP5 apically and AQP3 basolaterally. Basal cells expressed AQP3. The distribution and co-localization of AQPs in the ovine nasal respiratory mucosa is different to that reported in non-panting species and may reflect the physiological demands associated with enhanced respiratory evaporation. We propose that AQP1, 3, and 5 may constitute a transepithelial water pathway via glandular secretions and across the surface epithelium, which provides a possible means for rapid and controllable water movement in the nasal respiratory mucosa of a panting species.
Respiratory cooling and thermoregulatory coupling in reptiles
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Comparative physiological research on reptilies has focused primarily on the understanding of mechanisms of the control of breathing as they relate to respiratory gases or temperature itself. Comparatively less research has been done on the possible link between breathing and thermoregulation. Reptiles possess remarkable thermoregulatory capabilities, making use of behavioural and physiological mechanisms to regulate body temperature. The presence of thermal panting and gaping in numerous reptiles, coupled with the existence of head–body temperature differences, suggests that head temperature may be the primary regulated variable rather than body temperature. This review examines the preponderance of head and body temperature differences in reptiles, the occurrence of breathing patterns that possess putative thermoregulatory roles, and the propensity for head and brain temperature to be controlled by reptiles, particularly at higher temperatures. The available evidence suggests that these thermoregulatory breathing patterns are indeed present, though primarily in arid-dwelling reptiles. More importantly, however, it appears that the respiratory mechanisms that have the capacity to cool evolved initially in reptiles, perhaps as regulatory mechanisms for preventing overheating of the brain. Examining the control of these breathing patterns and their efficacy at regulating head or brain temperature may shed light on the evolution of thermoregulatory mechanisms in other vertebrates, namely the endothermic mammals and birds.
Respiratory heat exchange in mammals
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The dimensions of the maxillo-turbinate structures of a number of medium-sized and large mammals were determined using morphometric techniques. Estimates were obtained of the variation of gap width, perimeter and airway cross-sectional area along the organ. The time required for heat exchange in the turbinates of each animal was then determined for flow in a simple model based on that developed by Collins et al. (1971) and compared to the expected transit time for respired air. In all cases it was found that there was ample time for heating and humidification of the air when breathing at rest or moderate exercise. It was also shown that narrowing the air gap increased the effective time available for heat exchange despite the resulting reduction in transit time.
Panting in dogs: Paths of air flow in response to heat and exercise
1981, Respiration Physiology
Panting is the major avenue of evaporative cooling in dogs exposed to heat and/or exercise. We found modulation of evaporation was achieved by varying the paths of airflow during inhalation and exhalation.
The direction of airflow through the nose and mouth was determined by measuring pressure changes and temperatures at the openings of one nostril and the mouth in three dogs (av. weight 22 kg). Rates of oxygen consumption of respiratory evaporation were measured simultaneously.
Three patterns of panting were observed as the demand for respiratory evaporation increased:
- 1.
  (I), inhalation and exhalation through nose;
- 2.
  (II), inhalation through nose, exhalation through nose and mouth; and
- 3.
  (III), inhalation through nose and mouth, exhalation through nose and mouth.
Pattern I was observed in resting dogs when ambient temperature was below 26 °C and when animals rat at slow speeds in the cold (e.g. m·s⁻¹ at 10°C). Patterns II and III were observed when dogs rested quietly at ambient temperatures above 30°C and during exercise except when dogs ran slowly at very low temperatures. Patterns II and III rarely occurred independently for long periods of time. Instead, there was normally a continual oscillation between the two. The proportion of the time the dog used Pattern III instead of Pattern II increased as temperature and/or speed were increased; but the correlation between rate of respiratory evaporation and the percentage of time Pattern III was utilized was weak (r² = 0.63).
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A steady-state model, based on a combination of empirical and mechanistic relationships, is developed to predict respiratory water loss from terrestrial vertebrates. Model parameters are evaluated from published data for the banner-tail kangaroo rat (Dipodomys spectabilis). A three-dimensional representation of model behavior is presented, emphasizing the interaction of organismal and environmental variables. The model makes possible the calculation of respiratory water and heat losses for animals in both artificial and natural environments.

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^☆: Supported by NIH Research Grant HE-02228 and NIH Research Career Award 1-K6-GM-21,522 to KSN.

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Exhaled air temperature and water conservation in lizards☆

Abstract

Comp. Biochem. Physiol.

Respir. Physiol.

Comp. Biochem. Physiol.

Am. J. Med.

Thermorégulation and eccritic body temperatures in Mexican lizards of the genus Sceloporus

Anales del Inst. de Biol. Mexico