A heterothermic spectrum in hummingbirds

Abstract

Many endotherms use torpor, saving energy by a controlled reduction of their body temperature and metabolic rate. Some species (e.g., arctic ground squirrels, hummingbirds) enter deep torpor, dropping their body temperatures by 23-37°C, while others can only enter shallow torpor (e.g., pigeons, 3-10°C reductions). However, deep torpor in mammals can increase predation risk (unless animals are in burrows or caves), inhibit immune function, and result in sleep deprivation, so even for species that can enter deep torpor, facultative shallow torpor might help balance energy savings with these potential costs. Deep torpor occurs in three avian orders, but the trade-offs of deep torpor in birds are unknown. Although the literature hints that some bird species (mousebirds and perhaps hummingbirds) can use both shallow and deep torpor, little empirical evidence of such an avian heterothermy spectrum within species exists. We infrared imaged three hummingbird species that are known to use deep torpor, under natural temperature and light cycles, to test if they were also capable of shallow torpor. All three species used both deep and shallow torpor, often on the same night. Depending on the species, they used shallow torpor for 5-35% of the night. The presence of a heterothermic spectrum in these bird species indicates a capacity for fine-scale physiological and genetic regulation of avian torpid metabolism.

Ecological drivers and evolutionary consequences of torpor in Andean hummingbirds

“…Recent studies of torpor have revealed that torpor can be either “deep” or “shallow” (Mckechnie & Lovegrove 2002; Schleucher 2004; Ruf & Geiser 2015; Shankar et al . 2022).…”

“…The copyright holder for this preprint this version posted December 12, 2022. ; https://doi.org/10.1101/2022.12.08.519654 doi: bioRxiv preprint conditions such as changes in ambient temperature (Spence & Tingley 2021), weather (Calder & Booser 1973), migration status (Carpenter & Hixon 1988), nutrition (Hainsworth et al 1977;Powers et al 2003), and season (Hiebert 1991). Moreover, the use of torpor appears to be distributed along a continuum (Schleucher 2004;Ruf & Geiser 2015;Shankar et al 2022), and subtle modifications in the frequency of torpor and bout duration are crucial to birds' ability to save energy (Shankar et al 2020b;Wolf et al 2020). As a consequence, the use of torpor varies across species (Krüger et al 1982;Bech et al 1997;Shankar et al 2020b;Wolf et al 2020), within species (Schleucher 2004;Shankar et al 2019Shankar et al , 2020bSpence & Tingley 2021), and even within individuals (e.g.…”

“…2003), and season (Hiebert 1991). Moreover, the use of torpor appears to be distributed along a continuum (Schleucher 2004; Ruf & Geiser 2015; Shankar et al . 2022), and subtle modifications in the frequency of torpor and bout duration are crucial to birds’ ability to save energy (Shankar et al .…”

Re-examining extreme sleep duration in bats: implications for sleep phylogeny, ecology, and function

“…One possibility is that sleep duration in these experiments was influenced by torpor. Like many small endotherms [ 68–71 ], bats can become heterothermic to alleviate the high energetic demands of maintaining a constant body temperature. This results in the expression of torpor, an energy conserving physiological state in which metabolic rate is decreased and body temperature, ventilation and heart rate are depressed [ 72 , 73 ].…”

Variation in sexual size dimorphism and fit to Rensch's rule in 45 species of Costa Rican hummingbirds

“…Males and females have distinctive reproductive roles and polygynous reproductive systems, where leks are prevalent. Hummingbirds may have reached the upper energetic limits of miniaturization of any group of ying vertebrates, adapting their physiology to conserve heat in cold nights (Shankar et al 2022). Their high metabolic rates force them to secure almost constant access to high-energy food sources, in addition to placing severe constraints on their ability to deal with environmental variation, although this has not been an obstacle for the colonization of high-altitude habitats (Altshuler and Dudley 2002).…”