Insectivorous bats at northern latitudes need to cope with long periods of no food for large parts of the year. Hence, bats which are resident at northern latitudes throughout the year will need to undergo a long hibernation season and a short reproductive season where foraging time is limited by extended daylight periods. Eptesicus nilssonii is the northernmost occurring bat species worldwide and hibernates locally when ambient temperatures (Ta) limit prey availability. Therefore, we investigated the energy spent maintaining normothermy at different Ta, as well as how much bats limit energy expenditure while in torpor. We found that, despite being exposed to Ta as low as 1.1°C, bats did not increase torpid metabolic rate, thus indicating that E. nilssonii can survive and hibernate at low ambient temperatures. Furthermore, we found a lower critical temperature (Tlc) of 27.8°C, which is lower than in most other vespertilionid bats, and we found no indication of any metabolic response to Ta up to 37.1°C. Interestingly, carbon dioxide production increased with increasing Ta above the Tlc, presumably caused by a release of retained CO2 in bats that remained in torpor for longer and aroused at Ta above the Tlc. Our results indicate that E. nilssonii can thermoconform at near-freezing Ta, and hence maintain longer torpor bouts with limited energy expenditure, yet also cope with high Ta when sun exposed in roosts during long summer days. These physiological traits are likely to enable the species to cope with ongoing and predicted climate change.

At high latitudes in the northern hemisphere, small bats are faced with seasonal environmental challenges throughout the year (Boyles et al., 2020; Fjelldal et al., 2023). Animals with a large surface area to volume ratio must deal with energetic challenges when faced with low ambient temperatures (Ta), as the increased ratio increases heat loss (Andreasson et al., 2020), and small body size provides limited possibilities for fat storage (McGuire et al., 2018). In the short time-window for reproduction and growth during summer, Ta can vary substantially depending on the weather conditions and sun exposure.

Being nocturnal, insectivorous bats foraging on aerial insects are also challenged by decreasing Ta, as prey availability decreases substantially when Ta drops below 14°C (Speakman et al., 2000). Accordingly, bats at high latitudes are frequently exposed to challenging thermal conditions both during the active season and during the hibernation season. As they are heterothermic, bats at high latitudes frequently enter the energy-saving state of torpor, defined as a period of controlled and reversible reduction of metabolic rate (Geiser, 2021), and decrease body temperature (Tb) to be almost equal to, or slightly higher than Ta (i.e. thermoconforming; Geiser, 2021). Hence, heterothermic bats employ torpor on a day-to-day basis when environmental conditions are unfavorable during the active season (Boyles et al., 2016; Fjelldal et al., 2023), and for extended periods during winter (Jonasson and Willis, 2012; Czenze et al., 2017; McGuire et al., 2022).

Available foraging time for nocturnal animals in northern summers is also restricted by day length as the sun never sets above the Arctic circle (>66°N), and night length and level of darkness decrease gradually with increasing latitude. Thus, the ability of bats to forage can be limited to as little as 2 h per night (Frafjord, 2021), although topography (Siivonen and Wermundsen, 2008; Michaelsen et al., 2011) and cluttered habitat (Michaelsen et al., 2018) may allow for extended foraging opportunities. As the hibernation season can last for up to 9.5 months at the northern extreme (Frafjord, 2021; Hranac et al., 2021), female bats at northern latitudes will have little time to prepare for their reproductive period after emerging from hibernation, and may thus start fetal development with low available energy reserves.

With maternity colonies stretching as far north as 69°N, the northern bat (Eptesicus nilssonii) is the bat species that is reproductively active at the highest latitude globally (Speakman et al., 2000; Frafjord, 2013a; López-Baucells and Burgin, 2019). As an aerial-hawking predator (Rydell, 1993), E. nilssonii forages frequently in open areas related to water (de Jong, 1994; Siivonen and Wermundsen, 2008), and often utilizes street lamps which attract insects (Rydell, 1992; Rydell et al., 2020). To date, most research studying the biology of E. nilssonii has been limited to circadian rhythm and habitat use (Rydell, 1992, 1993; de Jong, 1994; Speakman et al., 2000; Frafjord, 2013a,b, 2021; Michaelsen, 2016, 2017; Rydell et al., 2020; Smirnov et al., 2020, 2021; Vasko et al., 2020; Blomberg et al., 2021). Thus, little work has been done to understand the thermoregulatory physiology of E. nilssonii, and how individuals react metabolically to different Ta, and to what extent individual bats utilize steady-state torpor.

With ongoing climate change (Rantanen et al., 2022), bats are predicted to expand their distribution range northward as a result of increasing environmental temperatures (Humphries et al., 2002; Sherwin et al., 2013; Novella-Fernandez et al., 2021). Therefore, E. nilssonii is predicted to experience increased competition as other aerial-hawking species with similar habitat preferences are expected to expand northward (Rebelo et al., 2010; Novella-Fernandez et al., 2021). Because populations of E. nilssonii are living at the northern margin of the range of any bat species and are both predicted to decline (Rebelo et al., 2010; Sherwin et al., 2013) and reported to be declining (Frafjord, 2013b; Rydell et al., 2018, 2020), we set out to quantify how the species copes with both low and high Ta by measuring energy consumption over a wide range of temperatures. The experimental setup was twofold. First, we performed experiments over a shorter time span during daytime, where we measured resting metabolic rate [RMR, values below the lower critical temperature (Tlc), a resting animal outside of their thermoneutral zone (TNZ)] and basal metabolic rate (BMR, a resting, post-absorptive animal within the TNZ) by exposing the bats to an increasing temperature profile from approximately 15°C to 39°C for 7–8 h. Second, we performed experiments over longer time spans, where we measured variation in metabolic rates by exposing bats to 5°C overnight, followed by an increasing temperature profile from approximately 0°C to 39°C over 10–11 h. Using a wide range of Ta, we expected to expose bats to Ta below the temperatures at which they have been found hibernating (Wermundsen and Siivonen, 2010), as well as Ta within their TNZ. Our overall aim was to quantify how E. nilssonii respond to a wide range of Ta, as this will help to increase our understanding of life at the northern margin of bat distribution globally and aid in the further conservation of this species.

List of symbols and abbreviations

     
  • BMR

    basal metabolic rate

  •  
  • Mb

    body mass

  •  
  • RMR

    resting metabolic rate

  •  
  • Ta

    ambient temperature

  •  
  • Tlc

    lower critical temperature

  •  
  • TMR

    torpid metabolic rate

  •  
  • TNZ

    thermoneutral zone

  •  
  • Tset

    set temperature

  •  
  • CO2

    rate of carbon dioxide production

  •  
  • O2

    rate of oxygen consumption

Study area and study species

We studied Eptesicus nilssonii (Keyserling and Blasius 1839) in Norway and captured 18 bats in and around Trondheim Municipality, Trøndelag County (63°25′49″N, 10°23′43″E), and 3 bats in Nittedal Municipality, Viken County (60°4′23″N, 10°52′20″E; Fig. 1). All bats were captured in 2020 or 2021 during the season in which they are most active at northern latitudes (early June to early September). Permission to capture bats was granted by the Norwegian Food Safety Authority (FOTS ID 23284) and the Norwegian Environment Agency (ref. 2018/4899).

Fig. 1.

Global distribution of Eptesicusnilssonii. The dark grey areas in Eurasia illustrate northern bat distribution (from López-Baucells and Burgin, 2019). The two red triangles in the left frame show the two study areas used in the present study. The distance between the northern and southern study area is approximately 370 km.

Fig. 1.

Global distribution of Eptesicusnilssonii. The dark grey areas in Eurasia illustrate northern bat distribution (from López-Baucells and Burgin, 2019). The two red triangles in the left frame show the two study areas used in the present study. The distance between the northern and southern study area is approximately 370 km.

Field methods

Bats were captured between early June and early September using mist nets placed in areas used for foraging or as commuting routes for E. nilssonii. Following removal from the net, bats were placed in individual cloth bags before being measured. We measured body mass (Mb) to the nearest 0.1 g (Aweigh MB-50) and forearm length to the nearest 0.1 mm (RS Pro 150 mm Digital Caliper 0.03 mm), and determined sex and reproductive status (i.e. pregnancy based on palpated abdomen, lactation based on enlarged fur-free nipples, or post-lactation based on enlarged nipples with bite marks and new fur growing). To check for potential recaptures, we photographed both wings of all bats captured and checked the wing membrane using a standard DSLR camera and an external flash (see Amelon et al., 2017; Sørås et al., 2022). No individuals were captured more than once.

As reproduction in bats can have profound effects on metabolic rates (Kurta et al., 1989; Otto et al., 2015), we specifically targeted non-reproductively active bats for the present study (7 females, 14 males). If suitable for analysis (i.e. non-reproductively active, not captured before and not born the same year), all (N=6 females, N=12 males) bats captured around Trondheim were brought back to an indoor flight cage (2 m×4 m×2 m) at the campus of the Norwegian University of Science and Technology. Suitable bats captured in Nittedal (N=1 female, N=2 males) were brought back to a local outdoor flight cage (2.5 m×5 m×2 m; see Sørås et al., 2022, for more details). As we were only able to measure the metabolic rate of one individual per day, some bats were kept in captivity for up to 4 days. All bats were released at the site of capture on the evening following measurement. In captivity, bats were handfed mealworms (Tenebrio molitor) until satiated once or twice per day, while water was provided ad libitum.

Metabolic measurements

We measured oxygen consumption (O2) and carbon dioxide production (CO2) by placing the bat in an airtight chamber (325 ml) that we supplied with a set supply of dry air (i.e. open flow respirometry) depending on the activity level of the bat. If active, the flow rate through the chamber was 315 ml min−1. If in torpor, the flow rate was reduced to 101–248 ml min−1. The air was provided by an outside pump (Eheim 100, EHEIM GmbH & Co., Deizisau, Germany), and passed through tubes of Drierite before and after passing through the chamber for removal of humidity, before entering a FOXBOX analyser (Sable Systems International, Las Vegas, NV, USA), which analysed the fractional content of O2 and CO2. Data recorded were logged and saved in the software Expedata (Sable Systems International) every minute. The gas analyser was zeroed (O2) and span-calibrated (CO2) at the onset of both field seasons using stock gas consisting of 99.4% nitrogen and 0.6% CO2. Oxygen was span-calibrated to 20.95% O2 during the first baseline at the onset of each experiment. Ta in the metabolic chamber was measured using an iButton (model DS1923-F5, Dallas Semiconductor Inc., Dallas, TX, USA) placed in the bottom of the chamber. To verify that the iButtons did not emit ultrasound (see Willis et al., 2009), we checked for potential emission of ultrasound beforehand using a heterodyne bat detector (Model D200, Petterson Elektronik AB, Uppsala, Sweden).

To better estimate O2 and CO2 when bats were either thermoconforming (i.e. not defending Tb) or thermoregulating (i.e. defending Tb), we performed two different experimental protocols. For the shorter experiments that examined individual RMR and BMR, bats (N=16) were held in the flight cage overnight. The following morning, they were weighed and handfed up to 5 mealworms to facilitate the bats to not enter torpor, which generally resulted in a less than 0.5 g Mb increase. After feeding, we measured Mb again to the nearest 0.1 g before placing the bat in the chamber, which was situated in a temperature-controlled chamber at a set temperature (Tset) of 15°C. Subsequently, Tset was increased at predetermined increments every hour (Tset=15, 21, 26, 30, 33, 36, 38, 40°C), but Ta tended to fluctuate slightly below Tset within the metabolic chamber. Throughout the text, we therefore refer to the actual measured temperature in the chamber as Ta and to the set point temperature as Tset. The experiment consisted of 6–8 experimental hours with a mean (±s.d.) duration of 410±38 min. As transit time in big brown bats (Eptesicus fuscus), with a mean (±s.d.) Mb of 17.4±3.1 g, averages 122±16 min (Luckens et al., 1971), and transit time decreases with Mb in bats (Cabrera-Campos et al., 2021), we assume that E. nilssonii will be post-digestive after approximately 120 min given the low food quantity they were provided with.

Each experimental hour consisted of a 15 min baseline where the air went through an identical, but empty, reference chamber. This was followed by a 45 min measurement period in which O2 and CO2 were measured. The bats in the short measurement protocol period experiment were exposed to a minimum Ta of 15.9±1.9°C and a maximum of 37.1±1.4°C. After the experiment ended, bats were removed from the chamber, weighed, and handfed mealworms until satiated, and given water ad libitum.

For the longer experiments investigating torpid metabolic rate (TMR) across a wide temperature gradient, bats were immediately placed into the metabolic chamber after arriving in the flight cage, on the same night as they were captured. Hence, bats were not handfed, but were likely to have foraged before being captured. At a Tset of 5°C bats were facilitated to enter torpor. At approximately 09:00 h the following morning, Tset was reduced to 0°C for 1 h, before being increased at predetermined increments every hour (Tset=0, 5, 10, 15, 20, 25, 28, 31, 34, 37, 39°C). As in the shorter experiments, Ta fluctuated slightly below Tset, except at Tset=0°C, where Ta fluctuated slightly above Tset. The experiment consisted primarily of 11 experimental hours with a mean duration of 908±221 min (including the hours at night when the bat was in the chamber prior to when Tset was reduced to 0°C). The bats in the long experimental protocol were exposed to a minimum Ta of 1.9±0.7°C and a maximum Ta of 35.8±1.2°C. All bats in the long measurement protocol were captured and measured in Trondheim, Norway.

O2 and CO2 were measured in 21 bats; 19 of these were measured only once with one of the two experimental protocols, while two were first exposed to the long experimental protocol, before being exposed to the short protocol 3 days later. Thus, we made 23 measurements (N=7 long, N=16 short). In total, 12 out of 16 bats exposed to the short experimental protocol entered torpor, while all seven bats in the long experimental protocol entered torpor.

O2 was calculated by extracting a series of stable measurements over at least 5 min at each Tset. We then calculated the lowest 5 min mean value within each series of measurements from each Tset using the runMean() function in the TTR package (https://CRAN.R-project.org/package=TTR) in R (v.4.1.3). Accordingly, we selected the same 5 min means in the CO2 dataset. We calculated O2 and CO2 using eqns 10.5 and 10.6, respectively, in Lighton (2018).

Bats were weighed immediately before being put into the chamber, and immediately after being removed from the chamber (i.e. before being given food and water). We estimated the loss of body mass per minute based on the actual CO2 values relative to the total CO2 produced using the equation:
formula
(1)
where Mcur is the calculated mass at a certain (current) minute, Mprev is the calculated mass in the previous minute, CO2 is the CO2 production in the current minute, CO2,tot is the total CO2 production over the entire experiment, and Mt is the total loss of body mass over the entire experiment (Sørås et al., 2022).

Data analyses

All data analyses for estimating metabolism were performed using R, and results are presented in the language of evidence as suggested by Muff et al. (2022).

We chose to analyse the thermoconforming (i.e. in torpor) and thermoregulating (i.e. normothermic) measurements of O2 and CO2 separately. We estimated Tlc in a stepwise procedure. First, we fitted a linear regression model using the lm() function with all normothermic O2 from both experimental protocols as the response variable, and Ta as fixed effect. Second, we performed a Davies test on the fitted linear model using the davies.test() function to check for the presence of an inflection point. Thus, if an inflection point was found, we performed a broken stick regression with all normothermic O2 measurements using the segmented() function and used the inflection point as an estimate of Tlc. Both functions were from the segmented package (Muggeo, 2008). All data points from euthermic and thermoregulating individuals at Ta above this estimated Tlc were assigned as BMR, while all data points at Ta below the estimated Tlc were assigned as RMR.

To estimate what causes variation in BMR, we fitted a linear mixed-effects model using the lmer() function from the lmerTest package (Kuznetsova et al., 2017). First, we fitted a global model including all normothermic O2 measurements above the Tlc as the response variable, and Ta and estimated Mb were added as fixed effects. Additionally, as bats in the short experimental protocol were fed a small supply of food prior to the experiment, we added duration from the start of the experiment as a fixed effect to account for possible differences between the experimental protocols. Individual bat ID was added as a random effect. Although there was only a weak correlation between estimated Mb per data point and forearm length (t65=0.25, P=0.043), we did not include forearm length in the models as forearm length only explains a minor variation in Mb (see McGuire et al., 2018). Second, as there was strong evidence of higher Mb at the start of the experiment (t8.7=3.0, P=0.015) in females (10.3±1.1 g) than in males (9.0±0.5 g), we ran a separate model that included sex as a fixed effect instead of Mb. Third, we performed model selection by identifying the best models using the dredge() function in the MuMIn package (https://CRAN.R-project.org/package=MuMIn). The best-fit model and all models with a ΔAICc<2 are presented in Table 1. The same procedure was repeated using all O2 measurements below the Tlc as the response variable and the same fixed effects to estimate variation in RMR. The same steps of analysis were repeated for all normothermic CO2 measurements (see Table 2).

Table 1.

Fitted models and model statistics of oxygen consumption in Eptesicus nilssonii

Fitted models and model statistics of oxygen consumption in Eptesicus nilssonii
Fitted models and model statistics of oxygen consumption in Eptesicus nilssonii
Table 2.

Fitted models and model statistics of carbon dioxide production in Eptesicus nilssonii

Fitted models and model statistics of carbon dioxide production in Eptesicus nilssonii
Fitted models and model statistics of carbon dioxide production in Eptesicus nilssonii

We continued to fit an exponential curve to all data points where the bats expressed steady-state torpor (i.e. TMR) using the nls() function in R. We also fitted a linear mixed model with the lowest TMR measured per individual as the response variable, and Ta and estimated Mb as fixed effects. Similarly, we ran a separate model that included sex instead of Mb as a fixed effect.

Immediately before being placed in the metabolic chamber, bats had an average Mb of 9.4±1.0 g (N=23). At the end of the experiment, immediately after being removed from the chamber, bats had an average Mb of 8.6±1.0 g (N=23). Energy consumption differed widely between thermoregulating and thermoconforming bats, and bats in the short and long experimental protocol lost on average 9.6±0.4% and 8.0±0.4% of Mb, respectively, over the entire experiment.

The metabolic cycle of the 19 experiments in which bats entered torpor consisted of five stages (Fig. 2A,C). While in the metabolic chamber, (1) bats remained normothermic for a varying amount of time before (2) commencing torpor entry. After completing torpor entry, (3) bats remained in steady-state torpor until (4) aroused, after which bats (5) remained normothermic for the rest of the experiment. In the four experiments in which the bats did not enter torpor, the bats remained normothermic for the entire duration of the experiment (Fig. 2B).

Fig. 2.

Example graphs of three individual E.nilssonii. (A) The metabolic rate (CO2) of a bat in the long experimental protocol from the time when the bat was placed in the chamber until it was taken out, 1110 min later. Black circles illustrate when the bat was normothermic, red when the bat entered torpor, green when the bat was in steady-state torpor, and blue when the bat aroused from torpor. The grey dots show the ambient temperature (Ta). (B,C) CO2 of two bats from the short experimental protocol. B shows CO2 of a bat that did not enter torpor. The graph also illustrates how it was active on multiple occasions during the experiment. C shows CO2 of a bat that entered torpor for 2 h out of the first 3 h of the experiment. Gaps with missing data points represent when baseline measurements were done.

Fig. 2.

Example graphs of three individual E.nilssonii. (A) The metabolic rate (CO2) of a bat in the long experimental protocol from the time when the bat was placed in the chamber until it was taken out, 1110 min later. Black circles illustrate when the bat was normothermic, red when the bat entered torpor, green when the bat was in steady-state torpor, and blue when the bat aroused from torpor. The grey dots show the ambient temperature (Ta). (B,C) CO2 of two bats from the short experimental protocol. B shows CO2 of a bat that did not enter torpor. The graph also illustrates how it was active on multiple occasions during the experiment. C shows CO2 of a bat that entered torpor for 2 h out of the first 3 h of the experiment. Gaps with missing data points represent when baseline measurements were done.

Thermoregulation

When investigating potential estimates for the Tlc, an inflection point was initially revealed in all normothermic measurements by the Davies test (P<0.0001). The following broken stick regression of O2 revealed a break point at 27.8±0.76°C (estimate±s.e.; confidence interval, CI 26.3–29.3°C, F=444.9, r2=0.96, P<0.0001), which can be considered a best estimate of Tlc. For CO2, broken stick regression revealed a break point at 29.4±0.74°C (CI 28.0–30.9°C, F=432.9, r2=0.86, P<0.0001). Although exposed to Ta up to 37.1±1.4°C (range: 34.8–39.3°C) and 35.9±1.1°C (34.0–37.5°C) in the short and long experimental protocol, respectively, there were no indications of any increase in metabolism at higher Ta. Thus, our results indicate a TNZ expanding from 27.8°C to at least 37.1°C (Fig. 3A).

Fig. 3.

Metabolic rate as a function of Ta. (A) O2 (red circles, normothermia; black circles, torpor) with the black line below 27.6°C showing the decrease in O2 with increasing Ta (i.e. resting metabolic rate, RMR) of normothermic bats (y=103.4−3.24Ta, N=14 bats, n=26 measurements, P<0.0001). The black line above 27.8°C shows the metabolic rate above lower critical temperature (Tlc), with a mean of 13.47 ml O2 h−1 (N=23, n=66). The blue line shows the increase in torpid metabolic rate (TMR) with increasing Ta (y=0.16+1., N=19, n=74, P<0.0001). (B) CO2 (red circles, normothermia; black circles, torpor) below 29.4°C (y=79.9–2.42Ta, N=16, n=29, P<0.005), CO2 above 29.4°C (y=0.90+0.29Ta, N=23, n=61, P=0.005), and increasing TMR with increasing Ta (y=0.17+1., N=19, n=69, P<0.0001). The dashed grey lines show the width of the confidence interval (CI) of the estimated Tlc in both A (Tlc=27.8°C, CI: 26.3–29.3°C) and B (Tlc=29.4°C, CI: 28.0–30.9°C).

Fig. 3.

Metabolic rate as a function of Ta. (A) O2 (red circles, normothermia; black circles, torpor) with the black line below 27.6°C showing the decrease in O2 with increasing Ta (i.e. resting metabolic rate, RMR) of normothermic bats (y=103.4−3.24Ta, N=14 bats, n=26 measurements, P<0.0001). The black line above 27.8°C shows the metabolic rate above lower critical temperature (Tlc), with a mean of 13.47 ml O2 h−1 (N=23, n=66). The blue line shows the increase in torpid metabolic rate (TMR) with increasing Ta (y=0.16+1., N=19, n=74, P<0.0001). (B) CO2 (red circles, normothermia; black circles, torpor) below 29.4°C (y=79.9–2.42Ta, N=16, n=29, P<0.005), CO2 above 29.4°C (y=0.90+0.29Ta, N=23, n=61, P=0.005), and increasing TMR with increasing Ta (y=0.17+1., N=19, n=69, P<0.0001). The dashed grey lines show the width of the confidence interval (CI) of the estimated Tlc in both A (Tlc=27.8°C, CI: 26.3–29.3°C) and B (Tlc=29.4°C, CI: 28.0–30.9°C).

Analysis of the causes of variation in O2 versus CO2 provided similar results with some variation. For metabolism above Tlc (BMR) based on O2, the top-ranked model did not include any fixed effects (i.e. intercept-only model, Table 1). All measurements of O2 above 27.8°C had a mean metabolic rate of 13.47±3.07 ml O2 h−1 (N=23, n=66 measurements in all individuals). As there was no evidence for Mb explaining any variation in metabolism (Table 1), we estimated mass-specific metabolism above Tlc, which had a mean of 1.56±0.40 ml O2 h−1 g−1. In contrast, the best-fit model for CO2 only included Ta as an explanatory variable (Table S2), and did not differ with duration of the experiment or Mb. All measurements above 29.4°C had a mean metabolic rate of 10.80±2.14 ml CO2 h−1 (N=23, n=60). In this subset of data, CO2 increased at 0.33 ml CO2 h−1 °C−1 (CO2=−0.44+0.33Ta ml CO2 h−1, P=0.002; Table 2, Fig. 3B). When including sex as a fixed effect instead of Mb, the top ranked model included sex as a fixed effect (Table S1). However, there was no evidence of sex explaining any variation in O2 (Table 1). Sex was not included as a fixed effect in the top ranked model for CO2 (Table S2).

The best-fit model for O2 below Tlc (RMR) included Ta and Mb as fixed effects (Table S1). Of these explanatory variables, there was strong evidence that RMR increased with decreasing Ta (P<0.001; Table 1), and there was no evidence that RMR was affected by Mb (P=0.13). To investigate why Mb was included in the top ranked model, we repeated the analysis on O2 below Tlc after excluding the measurements from the long experiment (N=3, n=5), as these bats were measured toward the end of their active season (18–23 August), and had a relatively high Mb of 10.5±0.7 g. Similarly, the most parsimonious model contained the same fixed effects (Table S1), but there was moderate evidence that bats with a higher estimated Mb had a higher RMR (Table 1). To visualize the relationship, we fitted a simple linear mixed effects model with only Ta as a fixed effect and individual bat ID as a random effect. O2 below 27.8°C increased with decreasing Ta at 3.24 ml O2 h−1 °C−1 (O2=103.4−3.24Ta ml O2 h−1, N=14, n=26; Fig. 3A). CO2 below 29.4°C increased with decreasing Ta (P<0.0001), with Mb not having a similar effect to that for O2 (Table 2). When including sex instead of Mb as a fixed effect, the top ranked models for both O2 and CO2 always included sex as a fixed effect, but we found no evidence that sex explained any variation.

Thermoconformity

Changes in TMR across the temperature range were similar for O2 and CO2, and increased exponentially with increasing Ta (O2=0.16×1. ml O2 h−1, N=19, n=74; and CO2=0.17×1. ml CO2 h−1, N=19, n=74; Fig. 3). Despite being exposed to Ta as low as 1.9±0.7°C, bats in the long experimental protocol did not increase metabolism at the lowest Ta. The minimum measured torpid O2 and CO2 decreased with decreasing Ta at 0.17 ml O2 h−1 °C−1 (F=10.8, P=0.044, N=19) and 0.12 ml CO2 h−1 °C−1 (F=24.4, P=0.0001, N=19), respectively. The minimum TMR was not affected by Mb (Tables S1 and S2).

We provide the first measurements of energy consumption in normothermic E. nilssonii and show that the species can maintain a steady metabolic rate within the TNZ spanning almost 10°C. Additionally, we provide results which indicate that E. nilssonii can tolerate Ta approaching 0°C without increasing energy expenditure during torpor, thus indicating a critical set-point temperature below 1.9°C outside the hibernation season. To compare our results with those of other species in the northern hemisphere, we reassessed the papers reviewed in Skåra et al. (2021), as well as more recent papers (Czenze et al., 2022; Sørås et al., 2022) for details on BMR and the TNZ. Our results reveal a wide TNZ in E. nilssonii compared with that in other species of bats in the northern hemisphere, primarily consisting of bats of the family Vespertilionidae (Table 3).

Table 3.

Overview of general physiological traits of bats

Overview of general physiological traits of bats
Overview of general physiological traits of bats

Eptesicus nilssonii in our study had a Tlc of 27.8°C based on O2, which is approximately 2°C lower than that predicted based on Mb (see Speakman and Thomas, 2003; Fristoe et al., 2015). Although Tlc has been reported to scale with Mb in bats, regardless of taxon, with Mb ranging from 4.2 to 739.2 g (Speakman and Thomas, 2003), limited data on Tlc are available for species of the family of Vespertilionidae (Fristoe et al., 2015; Skåra et al., 2021). In the data summarized here (see Table 3), vespertilionid bats had an average Tlc of 31.8±2.0°C (range: 26.7–34.5°C, N=12), while Mb averaged 12.5±6.5 g (range: 4.4–25.3 g, N=12). Given the limited availability of data on Tlc, we did not perform any statistical analysis on the effects of Mb on Tlc in vespertilionid bats. However, the average value of 31.8°C for the vespertilionid bats highlights the relatively low Tlc of E. nilssonii compared with that of most other vespertilionid bats. Estimation of Tlc based on CO2 provided a 1.6°C higher inflection point than that predicted based on O2. However, as bats often aroused at Ta close to Tlc, the higher Tlc based on CO2 may be due to retained CO2 during torpor being released following arousal (Milsom and Jackson, 2011; Sprenger and Milsom, 2022).

The estimation of Tlc based on O2 and CO2 in our study had a CI spanning 3.0 and 2.9°C, respectively. Interestingly, six individuals remained torpid above our estimated Tlc. This may be related to the among-individual variation in Tlc, as bats that remained torpid above the Tlc may have a higher individual Tlc. Given the experimental setup used in this study, we were unable to estimate individual estimates for Tlc. This is due to limited sample sizes within individuals, and because many individuals remained in torpor until Ta was close to the estimated Tlc. Generally, the TNZ, and hence Tlc, is often considered to be a species-specific trait. However, intraspecific variation in the thermoregulatory curve has been documented in small mammals (Stawski et al., 2017; van Baarsfeld et al., 2021; Ramirez et al., 2022) and other endotherms (reviewed in Burton et al., 2011). Although few bat species have been studied on larger geographical scales, some intraspecific variation has been identified. For example, the TMR of E. fuscus can differ between southern and northern populations (Dunbar and Brigham, 2010), while evaporative water loss varies geographically in E. fuscus (Klüg-Baerwald and Brigham, 2017) and other species of bats (McGuire et al., 2021). As animals adapted to northern temperate climates of high seasonal variation have been predicted (Janzen, 1967), and documented (Ghalambor et al., 2006; Pollock et al., 2021), to exhibit a wider TNZ than animals adapted to more stable environments (Bozinovic et al., 2014), future studies should investigate intraspecific variation in bats. Given the large geographical range of E. nilssonii (see Fig. 1), the species is exposed to a varied range of environmental pressures across its distribution and could thus serve as a good model species for studying intraspecific variation, as different populations are adapted to differing climates across Eurasia.

The average BMR within the TNZ of E. nilssonii reported here is 106% of that predicted for a vespertilionid bat weighing 9.4 g (Skåra et al., 2021). In small mammals, latitude has been reported to correlate with BMR, with the highest values observed in the northern hemisphere (Lovegrove, 2003). Although no such effects have been found for vespertilionid bats (Skåra et al., 2021), the available data consist of a relatively small number of species, and only species between 30° and 60° from both the southern and northern hemispheres. However, in future studies, these should ideally be tested separately as the seasonal variation in the southern hemisphere is much lower because of the buffering effect of the ocean on winter temperatures (Addo-Bediako et al., 2000).

Below the Tlc, the resting metabolic rate decreased significantly with increasing Ta for O2. Interestingly, Mb was included in the top ranked model that explained the variation in RMR (Table 1), despite the lack of strong evidence that Mb explains any variation. By excluding three individual bats that were exposed to the long experimental protocol at the latter end of their active season (18–23 August), we found that there was moderate evidence for heavier bats having a higher RMR below the Tlc.

Although all our measurements of O2 and CO2 were performed outside the hibernation season, we found that no individual bat showed any increase in metabolism when torpid at low Ta, despite being exposed to temperatures close to freezing. Therefore, bats did not increase metabolism to prevent Tb from decreasing below a certain critical temperature and this suggests that they do not alter their thermoregulatory curve seasonally, although further studies are needed to test this. Eptesicus nilssonii can hibernate at a wide range of temperatures, with records ranging from −5.3°C (Masing and Lusar, 2007) to 3.7°C (Wermundsen and Siivonen, 2010). Therefore, E. nilssonii can hibernate at particularly low temperatures, which is probably necessary given the length of time they need to hibernate in the north with relatively small fat stores (see McGuire et al., 2018). This is exemplified by a study by Anufriev and Revin (2006) in which two E. nilssonii captured in Yakutia, Russia, and measured over approximately 5.5 months spent 97% of their time in torpor, with torpor bouts lasting an average of 214.8±23.9 h (mean±s.d., range: 93.0–428.0), and did not show any increase in metabolism at low temperatures.

Previous studies have shown that TMR in bats can differ with season (Geiser, 2021), but not necessarily with latitude or climate zones (Fjelldal et al., 2022; McGuire et al., 2022). Additionally, to what extent bats defend Tb at low Ta can be state dependent, as animals can delay torpor entry (Matheson et al., 2010), arouse more frequently (Bieber et al., 2014) or at lower Ta (Sørås et al., 2022), or defend a higher Tb (Zervanos et al., 2013), if an individual's condition facilitates it. The low minimum TMR of E. nilssonii is similar to that in species of similar sizes (Willis et al., 2005a,b; for review, see Fjelldal et al., 2022), and the lack of any increase in TMR at the lowest Ta is similar to what has been found in other species, such as little brown bats (Myotis lucifugus; Hock, 1951; McGuire et al., 2022).

Overall, our results indicate that E. nilssonii has a relatively wide zone of thermoneutrality, and can cope with Ta down to 1.9°C without increasing metabolic rate in torpor. Furthermore, E. nilssonii can be exposed to Ta up to 37.1°C without showing any sign of increased heat dissipation. However, despite this phenotypic flexibility, E. nilssonii in Scandinavia are declining (Frafjord, 2013b; Rydell et al., 2020,), presumably as a result of a generally decreasing insect abundance (Hallmann et al., 2017), loss of insect-attracting streetlamps (Rydell et al., 2020) that previously worked as foraging hotspots (Rydell, 1992), and a predicted increase in competition from Pipistrellus pygmaeus (Rebelo et al., 2010; Rydell et al., 2020). As day length can be considered a limiting factor for bat distribution, with increasing strength at higher latitudes (Michaelsen et al., 2011; Boyles et al., 2016; Frafjord, 2021, Fjelldal et al., 2023), the extent to which increased competition will affect E. nilssonii across the width of its distribution is unknown. However, irrespective of decreasing prey availability, understanding how future populations and distribution of E. nilssonii and other species will adapt to and survive ongoing climate change requires a more detailed understanding of species-specific physiological traits. In particular, given recent studies that indicate the state dependence of individual responses to environmental effects (Matheson et al., 2010; Zervanos et al., 2013; Bieber et al., 2014; Sørås et al., 2022), future studies should investigate how variation in an individual's state can predict their ability to cope with extreme weather events, such as extreme low and high temperatures, and prolonged periods of bad weather. This is particularly important to understand during the reproductive season, as failing to cope with environmental challenges during this period can lead to population collapse.

We thank Helene M. Hannestad for assistance during fieldwork. The Norwegian Environment Agency and the Norwegian Food Safety Authority granted permission to capture and hold bats. We also thank the Norwegian University of Science and Technology for financial support for the study.

Author contributions

Conceptualization: R.S., C.S.; Methodology: R.S., M.A.F., C.B., C.S.; Validation: C.B.; Formal analysis: R.S., M.A.F., C.B., K.E.; Resources: J.v.d.K., K.E., C.S.; Data curation: R.S., M.A.F., J.v.d.K.; Writing - original draft: R.S.; Writing - review & editing: R.S., M.A.F., C.B., J.v.d.K., K.E., C.S.; Visualization: R.S.; Supervision: K.E., C.S.; Project administration: C.S.; Funding acquisition: C.S.

Funding

Funding for this research was provided by Norges Teknisk-Naturvitenskapelige Universitet.

Data availability

The data collected and analysed during the current study are available from the corresponding author on reasonable request.

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Competing interests

The authors declare no competing or financial interests.

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