Limited heat tolerance in an Arctic passerine: Thermoregulatory implications for cold‐specialized birds in a rapidly warming world

Abstract

Arctic animals inhabit some of the coldest environments on the planet and have evolved physiological mechanisms for minimizing heat loss under extreme cold. However, the Arctic is warming faster than the global average and how well Arctic animals tolerate even moderately high air temperatures (Ta) is unknown. Using flow‐through respirometry, we investigated the heat tolerance and evaporative cooling capacity of snow buntings (Plectrophenax nivalis; ≈31 g, N = 42), a cold specialist, Arctic songbird. We exposed buntings to increasing Ta and measured body temperature (Tb), resting metabolic rate (RMR), rates of evaporative water loss (EWL), and evaporative cooling efficiency (the ratio of evaporative heat loss to metabolic heat production). Buntings had an average (±SD) Tb of 41.3 ± 0.2°C at thermoneutral Ta and increased Tb to a maximum of 43.5 ± 0.3°C. Buntings started panting at Ta of 33.2 ± 1.7°C, with rapid increases in EWL starting at Ta = 34.6°C, meaning they experienced heat stress when air temperatures were well below their body temperature. Maximum rates of EWL were only 2.9× baseline rates at thermoneutral Ta, a markedly lower increase than seen in more heat‐tolerant arid‐zone species (e.g., ≥4.7× baseline rates). Heat‐stressed buntings also had low evaporative cooling efficiencies, with 95% of individuals unable to evaporatively dissipate an amount of heat equivalent to their own metabolic heat production. Our results suggest that buntings’ well‐developed cold tolerance may come at the cost of reduced heat tolerance. As the Arctic warms, and this and other species experience increased periods of heat stress, a limited capacity for evaporative cooling may force birds to increasingly rely on behavioral thermoregulation, such as minimizing activity, at the expense of diminished performance or reproductive investment.

Limited heat tolerance in a cold-adapted seabird: implications of a warming Arctic

“…Murres increased their RMR at an upper critical temperature ( T uc ) of 29.9°C (95% CI=18.8–34.1°C), which is similar to the T uc of other cold-region birds, including snow buntings (29.8°C, 95% CI=27.9–42.2°C; O'Connor et al, 2021 ), little penguins ( Eudyptula minor , 30.0°C; Stahel and Nicol, 1982 ), Peruvian penguins ( Spheniscus humboldti , 30.0°C; Drent and Stonehouse, 1971 ) and Cassin's auklet ( Ptychoramphus aleuticus , ∼25.0°C; Richman and Lovvorn, 2011 ) and lower than those of arid and semi-arid birds (33.9–46.5°C; McKechnie et al, 2017 ; Smith et al, 2015 ; Smith et al, 2017 ). RMR increased by 1.57-fold from a mean T a =18.8°C to 36.4°C in murres, which is higher than the mean fractional increase in snow buntings (1.4; O'Connor et al, 2021 ) and some desert birds (1.26–2.66; McKechnie et al, 2016 , 2017 , Smith et al, 2017 , McWhorter et al, 2018 , Talbot et al, 2018 , Czenze et al, 2020 ). When we compared mass-specific RMRs in murres above their T uc , the slope was approximately twice as steep as that predicted from their mean M b (0.298 versus 0.146 mW g °C −1 ; Weathers, 1981 ).…”

“…Murres displayed hyperthermia and increased their T b at T a =33.7°C (95% CI=22.2–37.0°C). The inflection point at T a =33.7°C is similar to that in snow buntings ( Plectrophenax nivalis , 32.6°C, 95% CI=31.0–34.4°C; O'Connor et al, 2021 ), the only other Arctic bird for which heat tolerance measurements are available, and is also within the T a range of desert and non-desert avian species ( Tieleman and Williams, 1999 ). Murres' maximum T b (43.3°C) was similar to the mean T b of birds from non-desert (43.3°C, range 41.1–45.8°C) and desert (43.6°C, range 41.5–45.4°C) environments at T a =45.0°C ( Tieleman and Williams, 1999 ).…”

“…(Eudyptula minor, 30.0°C; Stahel and Nicol, 1982), Peruvian penguins (Spheniscus humboldti, 30.0°C; Drent and Stonehouse, 1971) and Cassin's auklet (Ptychoramphus aleuticus, ∼25.0°C; Richman and Lovvorn, 2011) and lower than those of arid and semi-arid birds (33.9-46.5°C; McKechnie et al, 2017;Smith et al, 2015;Smith et al, 2017). RMR increased by 1.57-fold from a mean T a =18.8°C to 36.4°C in murres, which is higher than the mean fractional increase in snow buntings (1.4;O'Connor et al, 2021) and some desert birds (1. 26-2.66;McKechnie et al, 2016, McWhorter et al, 2018, Czenze et al, 2020.…”

“…In comparison, the onset of panting and increased EWL rate occurred at higher air temperatures in snow buntings (33.2°C and 34.6°C, 95% CI=31. 1-36.2°C, respectively;O'Connor et al, 2021) and arid-zone birds ( panting: 38.0-42.3°C, increase in EWL: 36-46.5°C; Smith et al, 2015, O'Connor et al, 2017, Czenze et al, 2020. It is worth noting that a T a of 21.2°C is ecologically relevant, and corresponds to the maximum T a at Coats Island during years in which murres displayed noticeable heat dissipation behaviours and experienced higher rates of mortality and egg loss due to the combination of heat stress and mosquito parasitism (22°C in 1998: Gaston et al, 2002;21.2 and21.3°C in 2011: Gaston andElliott, 2013).…”

“…However, as most avian heat tolerance studies have focused on desert birds ( Gerson et al, 2014 ; Smit and Mckechnie, 2015 ; Whitfield et al, 2015 ), less is known about heat tolerance in Arctic birds. Recent evidence suggests that an Arctic passerine may be limited in its capacity to withstand even moderately high air temperatures ( O'Connor et al, 2021 ). As larger birds have proportionally less surface area to volume ratios, and therefore less surface to dissipate heat, they may be even more sensitive to heat stress.…”