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

Abstract

Birds in subtropical deserts face significant thermoregulatory challenges because environmental temperatures regularly exceed avian body temperature. To understand the differing susceptibility of desert birds to increasing temperatures, we examined thermoregulatory performance and estimated heat tolerance limits (HTLs) for three Sonoran Desert nesting bird species -Gambel's quail, mourning doves and white-winged doves. Using flow-through respirometry we measured daytime resting metabolism, evaporative water loss and real-time body temperature at air temperatures (T air ) from 30°C to 66°C. We found marked increases in resting metabolism at the upper critical temperature (T uc ), which was significantly lower in the quail (T air =41.1°C) than in both dove species (T air =45.9-46.5°C). Gambel's quail maintained low resting metabolic rates and low rates of evaporative water loss at their T uc (0.71 W and 1.20 g H 2 O h −1 , respectively), but were more sensitive to increasing air temperature, reaching their HTL at T air of 52°C. Mourning doves and white-winged doves maintained low resting metabolic rates (0.66 and 0.94 W), but higher rates of evaporative water loss (1.91 and 2.99 g H 2 O h −1 ) at their T uc and reached their HTL at T air of 58-60°C. Mass-specific evaporative water loss in white-winged doves (147 g) and mourning doves (104 g) was 45% and 30% greater, respectively, than the rate observed in Gambel's quail (161 g) at T air of 48°C. Higher rates of evaporation and higher T uc made the doves exceptionally heat tolerant, allowing them to maintain body temperatures at least 14°C below air temperatures as high as 60°C (140°F).

The thermoregulatory role of relative bill and leg surface areas in a Mediterranean population of Great tit (Parus major)

“…The Great tit's maximum cooling efficiency, 0.83 ± 0.06, was in accordance with previous values reported for passerines (Bartholomew et al, 1968 ; McKechnie et al, 2017 ; Smith et al, 2015 ; Whitfield et al, 2015 ) for which the maximum EHL/MHP value was <2. At high T a (40°C), Great tit males displayed a positive relationship between the EHL/MHP ratio and tarsi surface index.…”

“…The behavioral mechanisms regulating T b in the studied Great tit population have never been investigated systematically, but this population must exploit the thermal heterogeneity in their environment by selecting microhabitats with favorable T a s. We also observed, for example, Great tits adopting wing drooping inside the metabolic chambers at ~34°C (NPM pers. The Great tit's maximum cooling efficiency, 0.83 ± 0.06, was in accordance with previous values reported for passerines (Bartholomew et al, 1968;McKechnie et al, 2017;Smith et al, 2015;Whitfield et al, 2015) for which the maximum EHL/MHP value was <2. At high T a (40°C), Great tit males displayed a positive relationship between the EHL/MHP ratio and tarsi surface index.…”

The thermoregulatory role of relative bill and leg surface areas in a Mediterranean population of Great tit (Parus major)

“…The Great tit's maximum cooling efficiency, 0.83 ± 0.06, was in accordance with previous values reported for passerines (Bartholomew et al, 1968 ; McKechnie et al, 2017 ; Smith et al, 2015 ; Whitfield et al, 2015 ) for which the maximum EHL/MHP value was <2. At high T a (40°C), Great tit males displayed a positive relationship between the EHL/MHP ratio and tarsi surface index.…”

“…The behavioral mechanisms regulating T b in the studied Great tit population have never been investigated systematically, but this population must exploit the thermal heterogeneity in their environment by selecting microhabitats with favorable T a s. We also observed, for example, Great tits adopting wing drooping inside the metabolic chambers at ~34°C (NPM pers. The Great tit's maximum cooling efficiency, 0.83 ± 0.06, was in accordance with previous values reported for passerines (Bartholomew et al, 1968;McKechnie et al, 2017;Smith et al, 2015;Whitfield et al, 2015) for which the maximum EHL/MHP value was <2. At high T a (40°C), Great tit males displayed a positive relationship between the EHL/MHP ratio and tarsi surface index.…”

Avian thermoregulation in the heat: evaporative cooling capacity of arid-zone caprimulgiforms from two continents

“…These findings support the notion that members of the Caprimulgiformes have evolved heat tolerance and evaporative cooling abilities that are unusual among birds (Dawson and Fisher, 1969;O'Connor et al, 2017). Our data also reveal considerable variation within this order; maximum EHL/ MHP in the three species we examined here varied from 2.4 (owletnightjar), a value not far above the range typical for passerines (Whitfield et al, 2015;McKechnie et al, 2017), up to 4.2, one of the highest avian values yet documented (Smith et al, 2015;McKechnie et al, 2016a,b;O'Connor et al, 2017). In the following discussion, we address the performance of each of these Owlet-nightjar Summary Fig.…”

Avian thermoregulation in the heat: evaporative cooling capacity and thermal tolerance in two Australian parrots

“…Dawson and Fisher (1982) reported maximum T b of 43-44.2°C in galahs held at T a =47-48°C for 6-8 h; these birds were held at lower T a values for much longer periods compared with the present study, but exhibited similar maximum T b values. Maximum T b values recorded in the present study were within the same range as those recently reported for southern African passerines (Whitfield et al, 2015), columbids from southern Africa and North America (McKechnie et al, 2016b;Smith et al, 2015) and a southern African sandgrouse (McKechnie et al, 2016a), with all these studies involving the same methods as we used here. The present study therefore confirms that the approximate upper T b limit to physiological function in psittaciform birds under acute heat exposure conditions is similar to that in most avian taxa.…”

The thermoregulatory role of relative bill and leg surface areas in a Mediterranean population of Great tit (Parus major)

“…The Great tit's maximum cooling efficiency, 0.83 ± 0.06, was in accordance with previous values reported for passerines (Bartholomew et al, 1968 ; McKechnie et al, 2017 ; Smith et al, 2015 ; Whitfield et al, 2015 ) for which the maximum EHL/MHP value was <2. At high T a (40°C), Great tit males displayed a positive relationship between the EHL/MHP ratio and tarsi surface index.…”

“…The behavioral mechanisms regulating T b in the studied Great tit population have never been investigated systematically, but this population must exploit the thermal heterogeneity in their environment by selecting microhabitats with favorable T a s. We also observed, for example, Great tits adopting wing drooping inside the metabolic chambers at ~34°C (NPM pers. The Great tit's maximum cooling efficiency, 0.83 ± 0.06, was in accordance with previous values reported for passerines (Bartholomew et al, 1968;McKechnie et al, 2017;Smith et al, 2015;Whitfield et al, 2015) for which the maximum EHL/MHP value was <2. At high T a (40°C), Great tit males displayed a positive relationship between the EHL/MHP ratio and tarsi surface index.…”

Avian thermoregulation in the heat: evaporative cooling capacity of arid-zone caprimulgiforms from two continents

“…These findings support the notion that members of the Caprimulgiformes have evolved heat tolerance and evaporative cooling abilities that are unusual among birds (Dawson and Fisher, 1969;O'Connor et al, 2017). Our data also reveal considerable variation within this order; maximum EHL/ MHP in the three species we examined here varied from 2.4 (owletnightjar), a value not far above the range typical for passerines (Whitfield et al, 2015;McKechnie et al, 2017), up to 4.2, one of the highest avian values yet documented (Smith et al, 2015;McKechnie et al, 2016a,b;O'Connor et al, 2017). In the following discussion, we address the performance of each of these Owlet-nightjar Summary Fig.…”

Avian thermoregulation in the heat: evaporative cooling capacity and thermal tolerance in two Australian parrots

“…Dawson and Fisher (1982) reported maximum T b of 43-44.2°C in galahs held at T a =47-48°C for 6-8 h; these birds were held at lower T a values for much longer periods compared with the present study, but exhibited similar maximum T b values. Maximum T b values recorded in the present study were within the same range as those recently reported for southern African passerines (Whitfield et al, 2015), columbids from southern Africa and North America (McKechnie et al, 2016b;Smith et al, 2015) and a southern African sandgrouse (McKechnie et al, 2016a), with all these studies involving the same methods as we used here. The present study therefore confirms that the approximate upper T b limit to physiological function in psittaciform birds under acute heat exposure conditions is similar to that in most avian taxa.…”

The thermoregulatory role of relative bill and leg surface areas in a Mediterranean population of Great tit (Parus major)

“…The Great tit's maximum cooling efficiency, 0.83 ± 0.06, was in accordance with previous values reported for passerines (Bartholomew et al, 1968 ; McKechnie et al, 2017 ; Smith et al, 2015 ; Whitfield et al, 2015 ) for which the maximum EHL/MHP value was <2. At high T a (40°C), Great tit males displayed a positive relationship between the EHL/MHP ratio and tarsi surface index.…”

“…The behavioral mechanisms regulating T b in the studied Great tit population have never been investigated systematically, but this population must exploit the thermal heterogeneity in their environment by selecting microhabitats with favorable T a s. We also observed, for example, Great tits adopting wing drooping inside the metabolic chambers at ~34°C (NPM pers. The Great tit's maximum cooling efficiency, 0.83 ± 0.06, was in accordance with previous values reported for passerines (Bartholomew et al, 1968;McKechnie et al, 2017;Smith et al, 2015;Whitfield et al, 2015) for which the maximum EHL/MHP value was <2. At high T a (40°C), Great tit males displayed a positive relationship between the EHL/MHP ratio and tarsi surface index.…”

Avian thermoregulation in the heat: evaporative cooling capacity of arid-zone caprimulgiforms from two continents

“…These findings support the notion that members of the Caprimulgiformes have evolved heat tolerance and evaporative cooling abilities that are unusual among birds (Dawson and Fisher, 1969;O'Connor et al, 2017). Our data also reveal considerable variation within this order; maximum EHL/ MHP in the three species we examined here varied from 2.4 (owletnightjar), a value not far above the range typical for passerines (Whitfield et al, 2015;McKechnie et al, 2017), up to 4.2, one of the highest avian values yet documented (Smith et al, 2015;McKechnie et al, 2016a,b;O'Connor et al, 2017). In the following discussion, we address the performance of each of these Owlet-nightjar Summary Fig.…”

Avian thermoregulation in the heat: evaporative cooling capacity and thermal tolerance in two Australian parrots

“…Dawson and Fisher (1982) reported maximum T b of 43-44.2°C in galahs held at T a =47-48°C for 6-8 h; these birds were held at lower T a values for much longer periods compared with the present study, but exhibited similar maximum T b values. Maximum T b values recorded in the present study were within the same range as those recently reported for southern African passerines (Whitfield et al, 2015), columbids from southern Africa and North America (McKechnie et al, 2016b;Smith et al, 2015) and a southern African sandgrouse (McKechnie et al, 2016a), with all these studies involving the same methods as we used here. The present study therefore confirms that the approximate upper T b limit to physiological function in psittaciform birds under acute heat exposure conditions is similar to that in most avian taxa.…”