Partitioning of evaporative water loss in white-winged doves: plasticity in response to short-term thermal acclimation

Abstract

We investigated changes in the relative contributions of respiratory evaporative water loss (REWL) and cutaneous evaporative water loss (CEWL) to total evaporative water loss (TEWL) in response to short-term thermal acclimation in western white-winged doves Zenaida asiatica mearnsii. We measured REWL, CEWL, oxygen consumption and carbon dioxide production in a partitioned chamber using flow-through respirometry. In doves housed for 2-4 weeks in a room heated to ca. 43°C during the day, TEWL increased from 5.5±1.3·mg·g -1 ·h -1 at an air temperature (Ta) of 35°C to 19.3±2.5·mg·g -1 ·h -1 at Ta=45°C. In doves housed at room temperature for the same period, TEWL increased from 4.6±1.1·mg·g -1 ·h -1 at Ta=35°C to 16.1±4.6·mg·g -1 ·h -1 at Ta=45°C. The CEWL of heat-acclimated doves increased from 3.6±1.2·mg·g -1 ·h -1 (64% of TEWL) at 35°C to 15.0±2.1·mg·g -1 ·h -1 (78% of TEWL) at Ta=45°C. Cool-acclimated doves exhibited more modest increases in CEWL, from 2.7±0.7·mg·g -1 ·h -1 at Ta=35°C to 7.8±3.4·mg·g -1 ·h -1 at Ta=45°C, with the contribution of CEWL to TEWL averaging 53% over this Ta range. Cool-acclimated doves became mildly hyperthermic (body temperature Tb=42.9±0.4°C) and expended 35% more energy relative to heat-acclimated doves (T b=41.9±0.6°C) at Ta=45°C, even though TEWL in the two groups was similar. In each of the two groups, metabolic rate did not vary with Ta, and averaged 7.1±0.5·mW·g -1 in cool-acclimated doves and 6.3±0.8·mW·g -1 in heat-acclimated doves. The differences in TEWL partitioning we observed between the two experimental groups resulted from a consistently lower skin water vapour diffusion resistance (rv) in the heatacclimated doves. At Ta=45°C, rv in the cool-acclimated doves was 120±81·s·cm -1 , whereas rv in the heatacclimated doves was 38±8·s·cm -1 . Our data reveal that in Z. a. mearnsii, TEWL partitioning varies in response to short-term thermal acclimation.

Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert doves and quail

“…For mourning doves in this study, RMR was 6.1 mW g −1 at the T uc , which is less than the BMR of 7.1 mW g −1 observed in birds at higher humidities and acclimated to 25°C (Hudson and Brush, 1964;appendix A of McNab, 2009). For white-winged doves in this study, RMR was 6.5 mW g −1 at the T uc , which compares favorably with the metabolic rate (6.3±0.8 mW g −1 ; n=15; 35°C≤T air ≤45°C) found for birds acclimated to 43°C (McKechnie and Wolf, 2004).…”

Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert doves and quail

“…For mourning doves in this study, RMR was 6.1 mW g −1 at the T uc , which is less than the BMR of 7.1 mW g −1 observed in birds at higher humidities and acclimated to 25°C (Hudson and Brush, 1964;appendix A of McNab, 2009). For white-winged doves in this study, RMR was 6.5 mW g −1 at the T uc , which compares favorably with the metabolic rate (6.3±0.8 mW g −1 ; n=15; 35°C≤T air ≤45°C) found for birds acclimated to 43°C (McKechnie and Wolf, 2004).…”

Phenotypic flexibility in heat production and heat loss in response to thermal and hydric acclimation in the zebra finch, a small arid-zone passerine

“…It should be noted that Marder and co-workers acclimated rock pigeons to T a 's exceeding their T b . Similar flexible adjustments of CEWL were also reported in other Columbiformes (McKechnie and Wolf 2004b). However, if drinking water is limited, increased EWL in the heat can lead to greater risk of dehydration.…”

Avian thermoregulation in the heat: efficient evaporative cooling allows for extreme heat tolerance in four southern Hemisphere columbids

“…and B.O.W., unpublished data), whereas the corresponding value for seven columbids is just 1.46±0.19°C (Hoffman and Walsberg, 1999;McKechnie and Wolf, 2004;Withers and Williams, 1990; present study). The smaller increase among columbids supports the notion that the CEWL-predominated evaporative cooling of the former group provides the physiological basis for more effective maintenance of T b below T a compared with the REWLpredominated evaporative cooling of the latter group, although the larger M b of the columbids compared with passerines potentially confounds this comparison.…”

“…Among seven passerines, the mean ratio of RMR at T a =48°C compared with T a =35°C is 1.38±0.22 (Tieleman et al, 2002a;Whitfield et al, 2015;Wolf and Walsberg, 1996; B.S., M.C.W., A.E.M. and B.O.W., unpublished data), whereas the corresponding value for seven columbids is 1.07±0.09 (Hoffman and Walsberg, 1999;McKechnie and Wolf, 2004;Withers and Williams, 1990; present study). The smaller fractional increases in RMR among columbids compared with passerines between T a =35 and 48°C support the notion that evaporative cooling predominated by CEWL is more energetically efficient than REWL-predominated cooling.…”

Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert doves and quail

“…For mourning doves in this study, RMR was 6.1 mW g −1 at the T uc , which is less than the BMR of 7.1 mW g −1 observed in birds at higher humidities and acclimated to 25°C (Hudson and Brush, 1964;appendix A of McNab, 2009). For white-winged doves in this study, RMR was 6.5 mW g −1 at the T uc , which compares favorably with the metabolic rate (6.3±0.8 mW g −1 ; n=15; 35°C≤T air ≤45°C) found for birds acclimated to 43°C (McKechnie and Wolf, 2004).…”

Phenotypic flexibility in heat production and heat loss in response to thermal and hydric acclimation in the zebra finch, a small arid-zone passerine

“…It should be noted that Marder and co-workers acclimated rock pigeons to T a 's exceeding their T b . Similar flexible adjustments of CEWL were also reported in other Columbiformes (McKechnie and Wolf 2004b). However, if drinking water is limited, increased EWL in the heat can lead to greater risk of dehydration.…”

Avian thermoregulation in the heat: efficient evaporative cooling allows for extreme heat tolerance in four southern Hemisphere columbids

“…and B.O.W., unpublished data), whereas the corresponding value for seven columbids is just 1.46±0.19°C (Hoffman and Walsberg, 1999;McKechnie and Wolf, 2004;Withers and Williams, 1990; present study). The smaller increase among columbids supports the notion that the CEWL-predominated evaporative cooling of the former group provides the physiological basis for more effective maintenance of T b below T a compared with the REWLpredominated evaporative cooling of the latter group, although the larger M b of the columbids compared with passerines potentially confounds this comparison.…”

“…Among seven passerines, the mean ratio of RMR at T a =48°C compared with T a =35°C is 1.38±0.22 (Tieleman et al, 2002a;Whitfield et al, 2015;Wolf and Walsberg, 1996; B.S., M.C.W., A.E.M. and B.O.W., unpublished data), whereas the corresponding value for seven columbids is 1.07±0.09 (Hoffman and Walsberg, 1999;McKechnie and Wolf, 2004;Withers and Williams, 1990; present study). The smaller fractional increases in RMR among columbids compared with passerines between T a =35 and 48°C support the notion that evaporative cooling predominated by CEWL is more energetically efficient than REWL-predominated cooling.…”

Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert doves and quail

“…For mourning doves in this study, RMR was 6.1 mW g −1 at the T uc , which is less than the BMR of 7.1 mW g −1 observed in birds at higher humidities and acclimated to 25°C (Hudson and Brush, 1964;appendix A of McNab, 2009). For white-winged doves in this study, RMR was 6.5 mW g −1 at the T uc , which compares favorably with the metabolic rate (6.3±0.8 mW g −1 ; n=15; 35°C≤T air ≤45°C) found for birds acclimated to 43°C (McKechnie and Wolf, 2004).…”

Phenotypic flexibility in heat production and heat loss in response to thermal and hydric acclimation in the zebra finch, a small arid-zone passerine

“…It should be noted that Marder and co-workers acclimated rock pigeons to T a 's exceeding their T b . Similar flexible adjustments of CEWL were also reported in other Columbiformes (McKechnie and Wolf 2004b). However, if drinking water is limited, increased EWL in the heat can lead to greater risk of dehydration.…”

Avian thermoregulation in the heat: efficient evaporative cooling allows for extreme heat tolerance in four southern Hemisphere columbids

“…and B.O.W., unpublished data), whereas the corresponding value for seven columbids is just 1.46±0.19°C (Hoffman and Walsberg, 1999;McKechnie and Wolf, 2004;Withers and Williams, 1990; present study). The smaller increase among columbids supports the notion that the CEWL-predominated evaporative cooling of the former group provides the physiological basis for more effective maintenance of T b below T a compared with the REWLpredominated evaporative cooling of the latter group, although the larger M b of the columbids compared with passerines potentially confounds this comparison.…”

“…Among seven passerines, the mean ratio of RMR at T a =48°C compared with T a =35°C is 1.38±0.22 (Tieleman et al, 2002a;Whitfield et al, 2015;Wolf and Walsberg, 1996; B.S., M.C.W., A.E.M. and B.O.W., unpublished data), whereas the corresponding value for seven columbids is 1.07±0.09 (Hoffman and Walsberg, 1999;McKechnie and Wolf, 2004;Withers and Williams, 1990; present study). The smaller fractional increases in RMR among columbids compared with passerines between T a =35 and 48°C support the notion that evaporative cooling predominated by CEWL is more energetically efficient than REWL-predominated cooling.…”