Cold-hearted bats: uncoupling of heart rate and metabolism during torpor at subzero temperatures

Abstract

Many hibernating animals thermoregulate during torpor and defend their body temperature () near 0°C by an increase in metabolic rate. Above a critical temperature (), animals usually thermoconform. We investigated the physiological responses above and below for a small tree-dwelling bat (, ∼14 g) that is often exposed to sub-zero temperatures during winter. Through simultaneous measurement of heart rate () and oxygen consumption ( ), we show that the relationship between oxygen transport and cardiac function is substantially altered in thermoregulating torpid bats between 1 and -2°C, compared with thermoconforming torpid bats at mild ambient temperatures ( 5-20°C). for this species was at a of 0.7±0.4°C, with a corresponding of 1.8±1.2°C. Below, animals began to thermoregulate, as indicated by a considerable but disproportionate increase in both and The maximum increase in was only 4-fold greater than the average thermoconforming minimum, compared with a 46-fold increase in The differential response of and to low was reflected in a 15-fold increase in oxygen delivery per heart beat (cardiac oxygen pulse). During torpor at low, thermoregulating bats maintained a relatively slow and compensated for increased metabolic demands by significantly increasing stroke volume and tissue oxygen extraction. Our study provides new information on the relationship between metabolism and in an unstudied physiological state that may occur frequently in the wild and can be extremely costly for heterothermic animals.

Optimizing dissection, sample collection and cell isolation protocols for frugivorous bats

“…Here we characterized sample collection and utilization of almost all tissues from fruit bats. While multiple groups have used bats in in vivo scientific studies for physiology (Chen, Zhu, Jones, Zhang, & Sun, 2013;Harrison & Roberts, 2000;Suarez, Hanna, & Herrera, 2009;Suarez, Welch, Hanna, & Herrera, 2009b), metabolism (Arévalo, Pérez-Suárez, & Lóapez-Luna, 1991;Bell, Price, Balthes, Cordon, & Wormell, 2019;Brunet-Rossinni, 2004;Foley et al, 2018;Funakoshi & Kunisaki, 1991;Healy et al, 2014;Hernández-Arciga et al, 2018;McMichael et al, 2016McMichael et al, , 2015Peng et al, 2017;Podlutsky, Khritankov, Ovodov, & Austad, 2005), evolution (Currie, Stawski, & Geiser, 2018;Moreno-Santillán, Machain-Williams, Hernández-Montes, & Ortega, 2019;Pollard et al, 2019;Seim et al, 2013;Shen et al, 2010) or immunological/virological studies (Aguilar-Setién et al, 2008;Ahn et al, 2019;Aída, Herrera, Flores-Martínez, & Welch, 2016;Allen, Sims, & Singht, n.d.;Barr et al, 2012;Chakravarty & Paul, 1987;Halpin et al, 2011;Davis et al, 2005;Cabrera-Romo et al, 2014;Hughes et al, 2006;Jones et al, 2015;Kandeil et al, 2019;Mackie et al, 2017;Obregón-Morales et al, 2017;…”

“…Here we characterized sample collection and utilization of almost all tissues from fruit bats. While multiple groups have used bats in in vivo scientific studies for physiology (Chen, Zhu, Jones, Zhang, & Sun, ; Harrison & Roberts, ; Suarez, Hanna, & Herrera, ; Suarez, Welch, Hanna, & Herrera, ), metabolism (Arévalo, Pérez‐Suárez, & Lóapez‐Luna, ; Bell, Price, Balthes, Cordon, & Wormell, ; Brunet‐Rossinni, ; Foley et al, ; Funakoshi & Kunisaki, ; Healy et al, ; Hernández‐Arciga et al, ; McMichael et al, , ; Peng et al, ; Podlutsky, Khritankov, Ovodov, & Austad, ), evolution (Currie, Stawski, & Geiser, ; Moreno‐Santillán, Machain‐Williams, Hernández‐Montes, & Ortega, ; Pollard et al, ; Seim et al, ; Shen et al, ) or immunological/virological studies (Aguilar‐Setién et al, ; Ahn et al, ; Aída, Herrera, Flores‐Martínez, & Welch, ; Allen, Sims, & Singht, n.d.; Barr et al, ; Chakravarty & Paul, ; Halpin et al, ; Davis et al, ; Cabrera‐Romo et al, ; Hughes et al, ; Jones et al, ; Kandeil et al, ; Mackie et al, ; Obregón‐Morales et al, ; Paweska et al, ; Perea‐Martínez et al, ; Sarkar & Chakravarty, ; Sullivan, Grimes, Eads, Menzies, & Irons, ; Swanepoel et al, ; Tong et al, ; Watanabe et al, ; Weise, Czirják, Lindecke, Bumrungsri, & Voigt, ; Yob et al, ), there is no detailed description of the methods required for efficient processing. Consistent, fast, methodology will benefit comparative biology studies on bats across multiple disciplines.…”

Bat population recoveries give insight into clustering strategies during hibernation

“…For each bat, laboratory experiments show that there exists a minimal torpor temperature, usually between 1 and 10°C, where its energy expenditure is lowest [2]. Hibernating at lower than critical temperatures requires thermoregulation to prevent freezing and at higher temperatures bats conserve less energy resources [11,12]. Microclimate at the specific roost thus affects long-term energy expenditure during torpor.…”

“…Microclimate at the specific roost thus affects long-term energy expenditure during torpor. Bats hibernating in tree hollows, under bark, or in shallow rock crevices face high risk that the ambient temperature at the hibernaculum will fluctuate daily over about 10°C and could drop below zero [11,13]. While deep underground hibernacula present more stable microclimates, cave-dwelling bats are able to choose different roosts, resulting in exposure to temperatures differing by more than 7°C [14].…”

Valuable carcasses: postmortem preservation of fatty acid composition in heart tissue

“…Bats in particular experience immense fluctuations in metabolism and cardiovascular function over short time frames with changes in heart rate from 5 bpm during torpor, to upwards of 1000 bpm during flight (Studier and Howell, 1969; Currie et al , 2018). Yet, PUFA composition as it pertains to the cardiovascular system of bats remains understudied.…”