To survive, all animals have to balance how much energy they take in and how much they use. They must find enough food to fuel the chemical processes that keep them alive – known as their metabolism – and store leftover fuel to use when food is not available. Bats, for example, have a fast metabolism and powerful flight muscles, which require a lot of energy. Some bat species, such as the tent-making bats, survive on fruit juice, and their food sources are often far apart and difficult to find. These bats are likely to starve if they go without food for more than 24 hours, and therefore need to conserve energy while they are resting.

To deal with potential food shortages, bats and other animals can enter a low-energy resting state called torpor. In this state, animals lower their body temperature and slow down their heart rate and metabolism so that they need less energy to stay alive. However, many animals that live in tropical regions, including tent-making bats, cannot enter a state of torpor, as it is too hot to sufficiently lower their body temperature. Until now, scientists did not fully understand how these bats control how much energy they use.

Now, O’Mara et al. studied tent-making bats in the wild by attaching small heart rate transmitters to four wild bats, and measured their heartbeats over several days. Since each heartbeat delivers oxygen and fuel to the rest of the body, measuring the bats’ heart rate indicates how much energy they are using. The experiments revealed for the first time that tent-making bats periodically lower their heart rates while resting (to around 200 beats per minute). This reduces the amount of energy they use each day by up to 10%, and helps counteract heart rates that can reach 900 beats per minute when the bats are flying.

Overall, these findings show that animals have evolved in various ways to control their use of energy. Future research should use similar technology to continue uncovering how wild animals have adapted to survive in different conditions. This knowledge will help us to understand how life has become so diverse in the tropics and the strategies that animals may use as climates change.

Energy intake, incorporation and expenditure are fundamental to animal behavior and evolution (Brown et al., 2004; Weiner, 1992). Animals must balance between generating enough metabolic power to find and acquire food and maintaining sufficient reserves to sustain daily maintenance, and repair and reproduce. This basic requirement of life can drive the foraging strategies of entire clades (Williams et al., 2014) and extensive links among various behavioral and physiological strategies have evolved in response to single ecological pressures including diet and pathogen environments (Cohen et al., 2012). This is largely a consequence of the sequential and linear process of energetic input (feeding), and that energy expenditure is additive across parallel aspects of physiology (Weiner, 1992). Energetic networks then link across physiological systems from mitochondrial oxidation to digestion, to respond to changes in resource availability and maintain physiological integrity. Well-adapted energy metabolisms must then both be able to conserve reserves and deliver enormous energetic power outputs in an efficient and effective manner. However, few animal models currently allow us to follow energy from intake to delivery of energetic currency to fuel metabolism, and finally to the countermeasures taken to slow down energetic expenditure when it is not needed. Furthermore, accumulating evidence shows that data collected in laboratory settings may not reflect the full range of strategies animals employ to deal with this energetic dilemma (Bishop et al., 2015; Bowlin et al., 2005; Calisi and Bentley, 2009; Geiser et al., 2007; Ward et al., 2002). This makes quantitative data from naturally behaving animals in the wild even more important to test the balance and integration of physiological adaptations to energetic limitations.

Flying vertebrates are an excellent example of this balance. While flight is one of the most efficient modes of locomotion per unit distance traveled, it is costlier per unit time than any other mode of locomotion (Norberg, 1990; Schmidt-Nielsen, 1979). To fulfill the exceptional demands of powered flight, both birds and bats have undergone dramatic physiological reorganization that emphasizes the need to supply fuel to large flight muscles (Maina, 2000; Norberg, 1990). Bat flight in particular is an extreme case of vertebrate locomotor energetics. In comparison to those of non-flying mammals of comparable size, hearts and lungs of bats are larger and have higher blood oxygen transport potential, delivering more oxygen per heart beat than non-flying terrestrial mammals (Neuweiler, 2000). Bats use some of the highest mass-specific metabolic rates during flight; 3–5 times greater than any other mammals and maximum increases of 15–16 times minimum resting metabolic rates (Speakman and Thomas, 2003). This may place bats at their energetic ceiling, and integrated physiological networks that allow them to maintain high metabolic rates at or near their limits over extended periods of time may be under equally strong selection to reduce resting energetic expenditure below what is commonly found in mammals.

Bats launch themselves directly into energy-demanding flight at the onset of their activity period and on an empty stomach, fueling flight by limited fat reserves (Voigt et al., 2010). They must then efficiently find and ingest food, and make energy available to their metabolism rapidly, as high metabolic rates and small body size place them at risk of starvation if sufficient food is not found. This risk is enhanced in the many species that specialize on ephemeral food sources. One strategy to cope with this energetic vulnerability is through daily reduction of metabolic rate (torpor) found in small-bodied bat species especially from the temperate zone. By entering a distinct low-energy state characterized by low body temperature, some bats reduce metabolic rates by 99% during torpor when ambient temperatures are lower than their thermoneutral zone (Geiser and Stawski, 2011; Ruf and Geiser, 2015). In tropical and sub-tropical regions where ambient temperatures are high, it may be impossible to lower body temperature beyond these critical minimum temperatures to save energy, therefore reductions in heart rate may reflect reductions in cellular respiration rates and gene expression in multiple pathways and be an effective measure of energetic conservation (Dechmann et al., 2011; Dzal et al., 2015; McNab, 1969; Storey and Storey, 2004). This may be particularly important in those that feed on sugar dense foods as they are at the highest risk of starvation (McNab, 1969; Voigt and Speakman, 2007).

Heart rate has a quadratic relationship with metabolic oxygen consumption (Bishop and Spivey, 2013; Grubb, 1982), and by measuring it directly it is possible to gain insight into energetic expenditure at high temporal resolution. Heart rates in bats may more than double in the transition from rest to flight, reflecting enormous flight power requirements (Thomas, 1975). Controlled experiments in wind tunnels and laboratory conditions have yielded incredible insight into the regulation of metabolism and energy consumption across a wide variety of activities and physiological states. However, heart rates of exercising animals in nature are unpredictable and metabolic rates measured during wind tunnel flight may not indicate the full scope of natural behavior. In a tropical insectivorous bat, heart rate increases from 129 bpm in the roost to 847 bpm during flight, a six-fold increase that is larger than predicted from other captive bats in wind tunnels (Dechmann et al., 2011). Alternatively, heart rates of free-flying animals may be much lower than expected. For example, bar-headed geese traverse the Himalayas with heart rates of 250–475 bpm (Bishop et al., 2015), 20% lower than what is expected from captive measures (Ward et al., 2002), and during migration, heart rates in Swainson’s thrushes are 10% lower than comparable long flights in wind tunnels (Bowlin et al., 2005). This indicates that sustainable metabolic rates possible during exercise may differ greatly from maximal rates or extrapolations in captive studies and we have only been able to get an initial glimpse into the heart rates used by flying bats.

Once they begin to feed, bats fuel their enormous demand for power by directly and rapidly metabolizing ingested food, but this can lead to high risk of starvation via rapid fat turnover (Caviedes-Vidal et al., 2008; Voigt and Speakman, 2007). One mechanism that may help animals to adjust the timing and intensity of shifts in metabolic scopes are glucocorticoids. They are key integrators between the environment and energy balance that ensure rapid response to changes in energetic needs (Cohen et al., 2012). Elevated levels of glucocorticoid hormones in blood plasma suppress glycogen formation and promote gluconeogenesis (Haase et al., 2016), fat oxidation (Brillon et al., 1995), and play a primary role in energy balance (Nieuwenhuizen and Rutters, 2008). Most bats that have been studied show high baseline glucocorticoid concentrations (Reeder et al., 2004; 2006), which indicates that they are in a ready state to rapidly mobilize glucose and glycogen reserves. By manipulating circulating levels of glucocorticoids or those tied to binding globulin, individual use of energy reserves can be modulated (Schneider, 2004).

Bats are then faced with an energetic dilemma where they must rapidly power flight, but quickly switch to conserving energetic stores gained during foraging. To better understand the interplay of energy expenditure and conservation, we describe the daily energetic life of Peters’ tent-making bat (Uroderma bilobatum, family Phyllostomidae) in Gamboa, Panamá. These bats are central-place foragers that leave a stable roost location to feed primarily on juice extracted from ripe figs (Ficus spp). We hypothesized that they would not use torpor during their regular daily life and that their energy intake and turnover rates would be high. Daily energy intake and expenditure should then be closely matched, resulting in a specialized life-style at the energetic edge. Testing our hypotheses was made possible by newly miniaturized heart rate transmitters to describe both the activity patterns of the species and their instantaneous energetic expenditure throughout the day, including the first flying heart rates of free-ranging individuals. We also tested how these bats fuel their metabolism through measurement of metabolic incorporation rates and fat turnover from stable isotope ratios in their breath in short-term captivity (Voigt and Speakman, 2007). In combination with an estimate of energy mobilization potential via elevated circulating cortisol, this allows us a more complete view into how these small-bodied, high-metabolic frugivores meet daily energetic demands.

We tracked the heart rates free-ranging bats throughout the 24 hr period, including foraging, to estimate total energetic costs. As hypothesized, we found that heart rate derived energy expenditure of U. bilobatum during flight is high and this is achieved through rapid incorporation of ingested food into their metabolism. We found flying heart rates that were 4–5 times higher than resting rates during the day and twice the heart rates of bats roosting at night. These bats replace nearly half of their fat reserves within a single day, resulting in short potential starvation times. Uroderma bilobatum counter this high energetic expenditure by spending relatively little time in flight and they have exceptionally low circulating cortisol values at rest during the day. These low basal values promote conservation of glucose reserves, but can be elevated up to 15 times, at least in response to stress, and could be used to generate the high metabolic power needed for flight. Most surprising, we found that by cyclically lowering heart rates during the day, they save 10% of their energy budget. This cyclic bradycardia is a novel strategy that minimizes energetic expenditure at relatively high ambient temperatures and allows U. bilobatum to maintain a FMR expected for their size. Only by completely sampling these high-resolution data from naturally behaving bats were we able to detect these lowered heart rates and quantify their effect on bat energetic strategies.

Using the energetic expenditure derived from median heart rates of resting bats in their natural roosts during the day (0.54 kJ h⁻¹ or 0.27 W) we can estimate a RMR of 13.0 kJ day⁻¹, which closely approximates previous measures of BMR (12.8 kJ day⁻¹ [McNab, 1969]). After commuting to the foraging patch, figs are collected during short flights of 1–2 mins and most of the remaining time is spent more or less at rest in their night feeding roosts resulting in only 30 mins per night in actual flight. Although this may differ among sites or during periods of less favorable food availability, this perch-resting with short fruit collection flights is an important part of their energy saving strategy. The subsequently low heart rates and activity patterns estimate an estimated FMR of ca. 46 kJ day⁻¹ (Bishop and Spivey, 2013), which is within the general predictions for FMR based on body mass from a broad taxonomic sampling of studies using doubly-labeled water (Speakman, 2005). While energetic expenditure met estimates for 16–19 g bats, this was only possible due to U. bilobatum restriction of total active flying time to less than about two hours per night (Figure 3) and the cyclic suppression of heart rates while resting during the day.

The cyclic bradycardia during daytime rest in our study is unprecedented. It is possible that these cycles are linked to REM and pre-REM sleep, but when humans and cats sleep their heart rate slows immediately prior to the elevation of heart rates during REM cycles (Taylor et al., 1985; Verrier et al., 1998). In both taxa the change in heart rate lasts only seconds and amounts to a total change of 3–5% from the resting heart rate as compared to the minutes-long 30% reduction in U. bilboatum. A reversed pattern in heart rate is found in hibernating ground squirrels that show irregular heart rates that speed up for 30–50 s before slowing again to a steady rate (Milsom et al., 1993; Milsom et al., 1999). The regular occurrence of this cyclic bradycardia suggests that it is a standard and regular aspect of the way that U. bilobatum rests and is likely a further extension of the energy conservation of sleep (Benington and Heller, 1995; Kilduff et al., 1993; Schmidt, 2014; Walker et al., 1979). Bradycardia is common aspect of the dive response where diving mammals slow their heart rates to conserve oxygen when submerged for long periods (Noren et al., 2012). Mammals in torpor are also bradycardic (Currie et al., 2014; Dechmann et al., 2011; Elvert and Heldmaier, 2005; Heldmaier et al., 2004), but the cyclic and varying nature of the heart rate depressions we find in U. bilobatum are not characteristic of any of these physiological states. Animals enter torpor and hibernation through controlled reductions of heart rate via increased inter-beat interval and skipped beats (Elvert and Heldmaier, 2005; Milsom et al., 1999). It may be that the slowed heart rates in U. bilobatum reflect the initial descent into short and shallow torpor events with a decrease in heart rate preceding the shift to torpor. Further investigation into the nervous control of bradycardic states in U. bilobatum would clarify both how these reductions are executed and any similarity to a sleep-torpor transition (Milsom et al., 1999).

Thus far, bats and hummingbirds in torpor and at rest have showed low and constant heart rates without any indication of the cycling we observe (Currie et al., 2014; Dechmann et al., 2011; Schaub and Prinzinger, 1999). Species that are capable of daily torpor generally lower their body temperatures to maximize energetic savings, particularly when exposed to cold temperatures (Ruf and Geiser, 2015), and this commonly occurs in tropical and sub-tropical mammals at temperatures below 24°C (Canale et al., 2012; Geiser and Stawski, 2011). However, a similar torpor response is not possible for the tropical U. bilobatum. Instead, they actively defend their body temperatures when exposed to cold, and more than triple metabolic rates to maintain a body temperature of 36°C at ambient temperatures of 10°C vs 30°C (McNab, 1969). In our respirometry calibrations, U. bilobatum maintained a constant body temperature around 37°C across the measured range of heart rates of 300–800 bpm. In fact, they may alter heart rate dynamics independently of body temperature (Tøien et al., 2011). The low heart rates we observed are similar to the minimum resting heart rates of small bats (i.e., 200–400 bpm) in thermonetural conditions (Currie et al., 2015; Kulzer, 1967; Leitner, 1966; Leitner and Nelson, 1967). The thermoneutral zone for U. bilobatum is reported to be 29–35°C (McNab, 1969; Rodríguez-Herrera et al., 2016), which is still slightly higher than the ambient temperature of our field site (mean: 25.87 ± 1.21°C, range: 23.38–28.24°C. It is unclear if the frequency and intensity of the cycling we observed are in response to ecological and energetic interactions, such as lowered foraging success, that decouples resting metabolic rates from overall FMR (Nilsson, 2002; Welcker et al., 2015). Decoupling resting metabolic rates from total energetic expenditure is hypothesized to be found in animals that live near their energetic ceilings (Welcker et al., 2015) with high metabolic rates, like U. bilobatum. We found the number of cycles per hour varied both within and among individuals, but we do not yet have enough information on the relationship between total nightly energy expenditure, energy intake, and the lowering of heart rates. However, it is unclear why these bats move between two apparently stable low energy states at rest. Further investigation into the potential relationship between this heart rate change and more commonly perceived torpor states would help understand energetic adaptations in tropical environments.

There are relatively few data on the heart rates of free-flying animals (Green, 2011) all of which are larger than U. bilobatum. Furthermore, accurately estimating energy consumption during flight under controlled conditions has often been unpractical or impossible due to the conditions needed in wind tunnels and mask respirometry. Our bats' heart rates and metabolic power are surprisingly low and variable when compared to flight tunnel studies. The heart rate derived estimate for cost of flight in U. bilobatum (1.36 ± 0.23 W, range 0.98–2.3 W) was slightly lower than mass loss estimates for bats of similar sizes and wing shapes (1.96–2.45 W: (von Busse et al., 2013; Winter and von Helversen, 1998). However, U. bilobatum show a mass specific power of 76 W kg⁻¹ with a maximum output of 145 W kg⁻¹, which is within the power requirements of bats that are up to 44 times larger (Carpenter, 1986; Thomas, 1975). While our estimates of energy consumption were not directly calibrated with flying bats, they provide the best potential estimates available based on broad patterns of the relationships among heart rate, stroke volume, and oxygen consumption during exercise (Bishop and Spivey, 2013), and must be interpreted with some caution. The large changes in heart rate among activity states remain lower than would be expected based on body size and reinforce the emerging pattern of lower energy consumption by free-flying animals versus those in controlled laboratory conditions (Bishop et al., 2015; Bowlin et al., 2005; Ward et al., 2002). Metabolic power of bat flight may be difficult to predict as a function of body size, but more likely the context in which the animals fly plays a strong role in determining the energy used. Laboratory experiments have been our best window into animals' physiological possibilities, but it is increasingly important to study energetics in relevant ecological settings to understand how these physiological mechanisms evolve.

The ability to rapidly fuel metabolism through ingested food seems to be a common adaptation among hummingbirds and bats with diets of simple carbohydrates and the fastest incorporation rates measured for vertebrates (Welch et al., 2016). Nectarivorous hummingbirds (3–5 g) and bats (10 g) fuel 50% of their metabolism within 3–9 min of feeding (Suarez et al., 2011; Voigt and Speakman, 2007; Welch et al., 2008). At three times their body size, U. bilobatum shows similar fractional incorporation rates. In contrast, other fruit-eating bats use incorporation rates of 10–12 min regardless of body size (Amitai et al., 2010). These comparative data indicate strong pressure on all flying frugivores, regardless of size, to mobilize ingested food to power flight and this is mediated through paracellular absorption (Caviedes-Vidal et al., 2008; Price et al., 2014). While initiating flight on stored energy, U. bilobatum and other sugar-focused bats rely heavily on ingested carbohydrates to supplement rapidly depleted glycogen at the onset of flight, further taxing the sugar oxidation cascade to push energy to muscle as quickly as possible (Suarez et al., 2011; Welch et al., 2016). Frugivorous bats deplete the large glycogen stores in their liver within 24 hr (Pinheiro et al., 2006). Our fat turnover experiments also showed that half of fat and sugar storage is mobilized within a single day. Specialization on foods rich in simple but rapidly incorporated carbohydrates seems to come with high risks that necessitate additional physiological and behavioral strategies to ensure energetic stability.

Uroderma bilobatum further control energetic incorporation and conservation by maintaining exceptionally low baseline cortisol levels that then are elevated to some of the highest recorded naturally induced values for mammals (Sapolsky et al., 2000). Basal glucocorticoid values of other bat species are especially high for mammals of their size (100–800 ng ml⁻¹; (Reeder et al., 2004; 2006) and show large potential maximal output when challenged with ACTH (Lewanzik et al., 2012). However, the difference between baseline and restraint-induced circulating cortisol especially in female U. bilobatum is more similar to the extremes found in lemmings (Lemmus trimucronatus) that seasonally elevate their baseline corticosterone values by 10–80 times to concentrations of over 4000 ng ml⁻¹ (Romero et al., 2008) or in flying squirrels (Glaucomys sp) that elevate cortisol values 38–40% above already high baseline values (Desantis et al., 2016). The low baselines we found may be a consequence of capturing resting or sleeping animals in their day roosts at least 4 hr after sunrise when circulating glucocorticoids were at their lowest (Sapolsky et al., 2000). However, this cannot explain peak values 1.5x greater than those observed in other mammals. We suggest that rapid increases in circulating cortisol levels during the acute stress response act in concert to mobilize energy stores, but more importantly, by suppressing glucocorticoid secretion during rest these bats are able to further minimize energetic expenditure and lower their metabolic rates (Haase et al., 2016; Nieuwenhuizen and Rutters, 2008; Palme et al., 2005) and minimize additional fat oxidation (Brillon et al., 1995).

Unpredictable fruit availability can have dramatic effects on survival and some bats, including U. bilobatum take advantage of their roosts to leverage social information and identify newly available food items (O'Mara et al., 2014a; Ramakers et al., 2016). Furthermore, the potential for rapid declines in food availability has likely shaped conservative physiological strategies in these bats to minimize energy expenditure while allowing for rapid resource mobilization needed for powered flight. These dynamic energetic strategies likely contribute to the success and diversity of the over 1300 bat species throughout the world (Simmons, 2005).

All methods were approved by the Autoridad Nacional del Ambiente, Panama (SE/A-88–13; SE/AP-12–14; SE/A-73–14) and by the Institutional Animal Care and Use Committee of the Smithsonian Tropical Research Institute (2012-060-2015; 2014-0701-2017). All data presented are available at the Dryad Digital Repository (doi: 10.5061/dryad.n821p)

1. 1. M Teague O'Mara
   2. Martin Wikelski
   3. Christian C Voigt
   4. Henry S Pollock
   5. Lanna M Desantis
   6. Gary Burness
   7. Andries Ter Maat
   8. Dina KN Dechmann

   (2017) Cyclic bouts of extreme bradycardia counteract the explosive metabolism of frugivorous bats

   Available at Dryad Digital Repository under a CC0 Public Domain Dedication.

   http://dx.doi.org/10.5061/dryad.n821p

1. 1. Aldridge HDJN
   2. Brigham RM

   (1988) Load carrying and maneuverability in an insectivorous bat: a test of the 5% "rule" of radio-telemetry

   Journal of Mammalogy 69:379–382.

   https://doi.org/10.2307/1381393

   • Google Scholar
2. 1. Amitai O
   2. Holtze S
   3. Barkan S
   4. Amichai E
   5. Korine C
   6. Pinshow B
   7. Voigt CC

   (2010) Fruit bats (Pteropodidae) fuel their metabolism rapidly and directly with exogenous sugars

   Journal of Experimental Biology 213:2693–2699.

   https://doi.org/10.1242/jeb.043505

   • PubMed
   • Google Scholar
3. 1. Barron DG
   2. Brawn JD
   3. Weatherhead PJ

   (2010) Meta-analysis of transmitter effects on avian behaviour and ecology

   Methods in Ecology and Evolution 1:180–187.

   https://doi.org/10.1111/j.2041-210X.2010.00013.x

   • Google Scholar
4. 1. Barske J
   2. Fusani L
   3. Wikelski M
   4. Feng NY
   5. Santos M
   6. Schlinger BA

   (2014) Energetics of the acrobatic courtship in male golden-collared manakins (Manacus vitellinus)

   Proceedings of the Royal Society B: Biological Sciences 281:20132482.

   https://doi.org/10.1098/rspb.2013.2482

   • PubMed
   • Google Scholar
5. 1. Benington JH
   2. Heller HC

   (1995) Restoration of brain energy metabolism as the function of sleep

   Progress in Neurobiology 45:347–360.

   https://doi.org/10.1016/0301-0082(94)00057-O

   • PubMed
   • Google Scholar
6. 1. Bishop CM
   2. Spivey RJ
   3. Hawkes LA
   4. Batbayar N
   5. Chua B
   6. Frappell PB
   7. Milsom WK
   8. Natsagdorj T
   9. Newman SH
   10. Scott GR
   11. Takekawa JY
   12. Wikelski M
   13. Butler PJ

   (2015) The roller coaster flight strategy of bar-headed geese conserves energy during Himalayan migrations

   Science 347:250–254.

   https://doi.org/10.1126/science.1258732

   • PubMed
   • Google Scholar
7. 1. Bishop CM
   2. Spivey RJ

   (2013) Integration of exercise response and allometric scaling in endotherms

   Journal of Theoretical Biology 323:11–19.

   https://doi.org/10.1016/j.jtbi.2013.01.002

   • PubMed
   • Google Scholar
8. 1. Bowlin MS
   2. Cochran WW
   3. Wikelski MC

   (2005) Biotelemetry of New World thrushes during migration: Physiology, energetics and orientation in the wild

   Integrative and Comparative Biology 45:295–304.

   https://doi.org/10.1093/icb/45.2.295

   • PubMed
   • Google Scholar
9. 1. Brillon DJ
   2. Zheng B
   3. Campbell RG
   4. Matthews DE

   (1995)

   Effect of cortisol on energy expenditure and amino acid metabolism in humans

   The American journal of physiology 268:E501–513.

   • PubMed
   • Google Scholar
10. 1. Brown JH
    2. Gillooly JF
    3. Allen AP
    4. Savage VM
    5. West GB

    (2004) Toward a metabolic theory of ecology

    Ecology 85:1771–1789.

    https://doi.org/10.1890/03-9000

    • Google Scholar
11. 1. Calisi RM
    2. Bentley GE

    (2009) Lab and field experiments: are they the same animal?

    Hormones and Behavior 56:1–10.

    https://doi.org/10.1016/j.yhbeh.2009.02.010

    • PubMed
    • Google Scholar
12. Book

    1. Canale C
    2. Levesque DL
    3. Lovegrove BG

    (2012) Tropical heterothermy: does the exception prove the rule or force a re-definition?

    In: Ruf T, Bieber C, Arnold W, Millesi E, editors. Living in a Seasonal World: Thermoregulatory and Metabolic Adaptations. Berlin: Springer. pp. 29–40.

    https://doi.org/10.1007/978-3-642-28678-0_3

    • Google Scholar
13. 1. Canals M
    2. Atala C
    3. Grossi B
    4. Iriarte-Díaz J

    (2005) Relative size of hearts and lungs of small bats

    Acta Chiropterologica 7:65–72.

    https://doi.org/10.3161/1733-5329(2005)7[65:RSOHAL]2.0.CO;2

    • Google Scholar
14. 1. Carpenter RE

    (1986)

    Flight physiology of intermediate-sized fruit bats (Pteropodidae)

    The Journal of Experimental Biology 120:79–103.

    • Google Scholar
15. 1. Caviedes-Vidal E
    2. Karasov WH
    3. Chediack JG
    4. Fasulo V
    5. Cruz-Neto AP
    6. Otani L

    (2008) Paracellular absorption: a bat breaks the mammal paradigm

    PLoS One 3:e1425.

    https://doi.org/10.1371/journal.pone.0001425

    • PubMed
    • Google Scholar
16. 1. Cohen AA
    2. Martin LB
    3. Wingfield JC
    4. McWilliams SR
    5. Dunne JA

    (2012) Physiological regulatory networks: ecological roles and evolutionary constraints

    Trends in Ecology & Evolution 27:428–435.

    https://doi.org/10.1016/j.tree.2012.04.008

    • PubMed
    • Google Scholar
17. 1. Core Team R

    (2016) R: A language and environment for statistical computing: R Foundation for Statistical Computing

    R: A language and environment for statistical computing: R Foundation for Statistical Computing, Vienna, Austria, http://www.r-project.org.

    http://www.r-project.org

    • Google Scholar
18. 1. Currie SE
    2. Körtner G
    3. Geiser F

    (2014) Heart rate as a predictor of metabolic rate in heterothermic bats

    Journal of Experimental Biology 217:1519–1524.

    https://doi.org/10.1242/jeb.098970

    • PubMed
    • Google Scholar
19. 1. Currie SE
    2. Noy K
    3. Geiser F

    (2015) Passive rewarming from torpor in hibernating bats: minimizing metabolic costs and cardiac demands

    AJP: Regulatory, Integrative and Comparative Physiology 308:R34–R41.

    https://doi.org/10.1152/ajpregu.00341.2014

    • PubMed
    • Google Scholar
20. 1. Dechmann DK
    2. Ehret S
    3. Gaub A
    4. Kranstauber B
    5. Wikelski M

    (2011) Low metabolism in a tropical bat from lowland Panama measured using heart rate telemetry: an unexpected life in the slow lane

    Journal of Experimental Biology 214:3605–3612.

    https://doi.org/10.1242/jeb.056010

    • PubMed
    • Google Scholar
21. 1. Desantis LM
    2. Bowman J
    3. Lahoda CV
    4. Boonstra R
    5. Burness G

    (2016) Responses of New World flying squirrels to the acute stress of capture and handling

    Journal of Mammalogy 97:80–88.

    https://doi.org/10.1093/jmammal/gyv156

    • Google Scholar
22. 1. Ditmer MA
    2. Vincent JB
    3. Werden LK
    4. Tanner JC
    5. Laske TG
    6. Iaizzo PA
    7. Garshelis DL
    8. Fieberg JR

    (2015) Bears Show a Physiological but Limited Behavioral Response to Unmanned Aerial Vehicles

    Current Biology 25:2278–2283.

    https://doi.org/10.1016/j.cub.2015.07.024

    • PubMed
    • Google Scholar
23. 1. Dzal YA
    2. Jenkin SE
    3. Lague SL
    4. Reichert MN
    5. York JM
    6. Pamenter ME

    (2015) Oxygen in demand: How oxygen has shaped vertebrate physiology

    Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 186:4–26.

    https://doi.org/10.1016/j.cbpa.2014.10.029

    • PubMed
    • Google Scholar
24. 1. Elliott KH

    (2016) Measurement of flying and diving metabolic rate in wild animals: Review and recommendations

    Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 202:63–77.

    https://doi.org/10.1016/j.cbpa.2016.05.025

    • PubMed
    • Google Scholar
25. 1. Elvert R
    2. Heldmaier G

    (2005) Cardiorespiratory and metabolic reactions during entrance into torpor in dormice, Glis glis

    Journal of Experimental Biology 208:1373–1383.

    https://doi.org/10.1242/jeb.01546

    • PubMed
    • Google Scholar
26. 1. Geiser F
    2. Holloway JC
    3. Körtner G

    (2007) Thermal biology, torpor and behaviour in sugar gliders: a laboratory-field comparison

    Journal of Comparative Physiology B 177:495–501.

    https://doi.org/10.1007/s00360-007-0147-6

    • PubMed
    • Google Scholar
27. 1. Geiser F
    2. Stawski C

    (2011) Hibernation and torpor in tropical and subtropical bats in relation to energetics, extinctions, and the evolution of endothermy

    Integrative and Comparative Biology 51:337–348.

    https://doi.org/10.1093/icb/icr042

    • PubMed
    • Google Scholar
28. 1. Green JA

    (2011) The heart rate method for estimating metabolic rate: review and recommendations

    Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 158:287–304.

    https://doi.org/10.1016/j.cbpa.2010.09.011

    • PubMed
    • Google Scholar
29. 1. Grubb BR

    (1982)

    Cardiac output and stroke volume in exercising ducks and pigeons

    Journal of applied physiology: respiratory, environmental and exercise physiology 53:207–211.

    • PubMed
    • Google Scholar
30. 1. Haase CG
    2. Long AK
    3. Gillooly JF

    (2016) Energetics of stress: linking plasma cortisol levels to metabolic rate in mammals

    Biology Letters 12:20150867.

    https://doi.org/10.1098/rsbl.2015.0867

    • PubMed
    • Google Scholar
31. 1. Heldmaier G
    2. Ortmann S
    3. Elvert R

    (2004) Natural hypometabolism during hibernation and daily torpor in mammals

    Respiratory Physiology & Neurobiology 141:317–329.

    https://doi.org/10.1016/j.resp.2004.03.014

    • PubMed
    • Google Scholar
32. 1. Kilduff TS
    2. Krilowicz B
    3. Milsom WK
    4. Trachsel L
    5. Wang LC

    (1993) Sleep and mammalian hibernation: homologous adaptations and homologous processes?

    Sleep 16:372–386.

    https://doi.org/10.1093/sleep/16.4.372

    • PubMed
    • Google Scholar
33. 1. Kulzer E

    (1967) Die Herztätigkeit bei lethargischen und winterschlafenden Fledermäusen

    Zeitschrift für Vergleichende Physiologie 56:63–94.

    https://doi.org/10.1007/BF00333563

    • Google Scholar
34. 1. Leitner P
    2. Nelson JE

    (1967) Body temperature, oxygen consumption and heart rate in the Australian false vampire bat, Macroderma gigas

    Comparative Biochemistry and Physiology 21:65–74.

    https://doi.org/10.1016/0010-406X(67)90115-6

    • PubMed
    • Google Scholar
35. 1. Leitner P

    (1966) Body temperature, oxygen consumption, heart rate and shivering in the California mastiff bat, Eumops perotis

    Comparative Biochemistry and Physiology 19:431–443.

    https://doi.org/10.1016/0010-406X(66)90152-6

    • Google Scholar
36. 1. Lewanzik D
    2. Kelm DH
    3. Greiner S
    4. Dehnhard M
    5. Voigt CC

    (2012) Ecological correlates of cortisol levels in two bat species with contrasting feeding habits

    General and Comparative Endocrinology 177:104–112.

    https://doi.org/10.1016/j.ygcen.2012.02.021

    • PubMed
    • Google Scholar
37. Book

    1. Lighton JR

    (2008)

    Measuring Metabolic Rates: A Manual for Scientists

    New York: Oxford University Press.

    • Google Scholar
38. 1. Maina JN

    (2000)

    What it takes to fly: the structural and functional respiratory refinements in birds and bats

    The Journal of experimental biology 203:3045–3064.

    • PubMed
    • Google Scholar
39. 1. Martínez Del Rio C
    2. Anderson-Sprecher R

    (2008) Beyond the reaction progress variable: the meaning and significance of isotopic incorporation data

    Oecologia 156:765–772.

    https://doi.org/10.1007/s00442-008-1040-z

    • PubMed
    • Google Scholar
40. 1. McCue MD
    2. Welch KC

    (2016) 13C-Breath testing in animals: theory, applications, and future directions

    Journal of Comparative Physiology B 186:265–285.

    https://doi.org/10.1007/s00360-015-0950-4

    • PubMed
    • Google Scholar
41. 1. McNab BK

    (1969) The economics of temperature regulation in neotropical bats

    Comparative Biochemistry and Physiology 31:227–268.

    https://doi.org/10.1016/0010-406X(69)91651-X

    • PubMed
    • Google Scholar
42. 1. Milsom WK
    2. Burlington RF
    3. Burleson ML

    (1993)

    Vagal influence on heart rate in hibernating ground squirrels

    The Journal of experimental biology 185:25–32.

    • Google Scholar
43. 1. Milsom WK
    2. Zimmer MB
    3. Harris MB

    (1999) Regulation of cardiac rhythm in hibernating mammals

    Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 124:383–391.

    https://doi.org/10.1016/S1095-6433(99)00130-0

    • PubMed
    • Google Scholar
44. Book

    1. Neuweiler G

    (2000)

    The Biology of Bats

    Oxford University Press.

    • Google Scholar
45. 1. Nieuwenhuizen AG
    2. Rutters F

    (2008) The hypothalamic-pituitary-adrenal-axis in the regulation of energy balance

    Physiology & Behavior 94:169–177.

    https://doi.org/10.1016/j.physbeh.2007.12.011

    • PubMed
    • Google Scholar
46. 1. Nilsson JA

    (2002) Metabolic consequences of hard work

    Proceedings of the Royal Society B: Biological Sciences 269:1735–1739.

    https://doi.org/10.1098/rspb.2002.2071

    • PubMed
    • Google Scholar
47. Book

    1. Norberg UM

    (1990)

    Vertebrate Flight: Mechanics, Physiology, Morphology, Ecology and Evolution

    Berlin: Springer-Verlag.

    • Google Scholar
48. 1. Noren SR
    2. Kendall T
    3. Cuccurullo V
    4. Williams TM

    (2012) The dive response redefined: underwater behavior influences cardiac variability in freely diving dolphins

    Journal of Experimental Biology 215:2735–2741.

    https://doi.org/10.1242/jeb.069583

    • PubMed
    • Google Scholar
49. 1. O'Mara MT
    2. Dechmann DKN
    3. Page RA

    (2014a) Frugivorous bats evaluate the quality of social information when choosing novel foods

    Behavioral Ecology 25:1233–1239.

    https://doi.org/10.1093/beheco/aru120

    • Google Scholar
50. 1. O'Mara MT
    2. Wikelski M
    3. Dechmann DKN

    (2014b) 50 years of bat tracking: device attachment and future directions

    Methods in Ecology and Evolution 5:311–319.

    https://doi.org/10.1111/2041-210X.12172

    • Google Scholar
51. 1. Palme R
    2. Rettenbacher S
    3. Touma C
    4. El-Bahr SM
    5. Möstl E

    (2005) Stress hormones in mammals and birds: comparative aspects regarding metabolism, excretion, and noninvasive measurement in fecal samples

    Annals of the New York Academy of Sciences 1040:162–171.

    https://doi.org/10.1196/annals.1327.021

    • PubMed
    • Google Scholar
52. 1. Pinheiro EC
    2. Taddei VA
    3. Migliorini RH
    4. Kettelhut IC

    (2006) Effect of fasting on carbohydrate metabolism in frugivorous bats (Artibeus lituratus and Artibeus jamaicensis)

    Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 143:279–284.

    https://doi.org/10.1016/j.cbpb.2005.11.013

    • PubMed
    • Google Scholar
53. 1. Price ER
    2. Rott KH
    3. Caviedes-Vidal E
    4. Karasov WH

    (2014) Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level

    Journal of Experimental Biology 217:3483–3492.

    https://doi.org/10.1242/jeb.105619

    • PubMed
    • Google Scholar
54. 1. Ramakers JJC
    2. Dechmann DKN
    3. Page RA
    4. O'Mara MT

    (2016) Frugivorous bats prefer information from novel social partners

    Animal Behaviour 116:83–87.

    https://doi.org/10.1016/j.anbehav.2016.03.021

    • Google Scholar
55. 1. Reeder DM
    2. Kosteczko NS
    3. Kunz TH
    4. Widmaier EP

    (2004) Changes in baseline and stress-induced glucocorticoid levels during the active period in free-ranging male and female little brown myotis, Myotis lucifugus (Chiroptera: Vespertilionidae)

    General and Comparative Endocrinology 136:260–269.

    https://doi.org/10.1016/j.ygcen.2003.12.020

    • PubMed
    • Google Scholar
56. 1. Reeder DM
    2. Kosteczko NS
    3. Kunz TH
    4. Widmaier EP

    (2006) The hormonal and behavioral response to group formation, seasonal changes, and restraint stress in the highly social Malayan Flying Fox (Pteropus vampyrus) and the less social Little Golden-mantled Flying Fox (Pteropus pumilus) (Chiroptera: Pteropodidae)

    Hormones and Behavior 49:484–500.

    https://doi.org/10.1016/j.yhbeh.2005.11.001

    • PubMed
    • Google Scholar
57. 1. Rodríguez-Herrera B
    2. Víquez-R L
    3. Cordero-Schmidt E
    4. Sandoval JM
    5. Rodríguez-Durán A

    (2016) Energetics of tent roosting in bats: the case of Ectophylla alba and Uroderma bilobatum (Chiroptera: Phyllostomidae)

    Journal of Mammalogy 97:246–252.

    https://doi.org/10.1093/jmammal/gyv173

    • Google Scholar
58. 1. Romero LM
    2. Meister CJ
    3. Cyr NE
    4. Kenagy GJ
    5. Wingfield JC

    (2008) Seasonal glucocorticoid responses to capture in wild free-living mammals

    AJP: Regulatory, Integrative and Comparative Physiology 294:R614–R622.

    https://doi.org/10.1152/ajpregu.00752.2007

    • PubMed
    • Google Scholar
59. 1. Ruf T
    2. Geiser F

    (2015) Daily torpor and hibernation in birds and mammals

    Biological Reviews 90:891–926.

    https://doi.org/10.1111/brv.12137

    • PubMed
    • Google Scholar
60. 1. Sapir N
    2. Wikelski M
    3. McCue MD
    4. Pinshow B
    5. Nathan R

    (2010) Flight modes in migrating European bee-eaters: heart rate may indicate low metabolic rate during soaring and gliding

    PLoS One 5:e13956.

    https://doi.org/10.1371/journal.pone.0013956

    • PubMed
    • Google Scholar
61. 1. Sapolsky RM
    2. Romero LM
    3. Munck AU

    (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions

    Endocrine Reviews 21:55–89.

    https://doi.org/10.1210/er.21.1.55

    • PubMed
    • Google Scholar
62. 1. Schaub R
    2. Prinzinger R

    (1999) Long-term telemetry of heart rates and energy metabolic rate during the diurnal cycle in normothermic and torpid African blue-naped mousebirds (Urocolius macrourus)

    Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 124:439–445.

    https://doi.org/10.1016/S1095-6433(99)00136-1

    • Google Scholar
63. 1. Schmidt MH

    (2014) The energy allocation function of sleep: a unifying theory of sleep, torpor, and continuous wakefulness

    Neuroscience & Biobehavioral Reviews 47:122–153.

    https://doi.org/10.1016/j.neubiorev.2014.08.001

    • PubMed
    • Google Scholar
64. Book

    1. Schmidt-Nielsen K

    (1979)

    Animal Physiology: Adaptation and Environment

    Cambridge: Cambridge University Press.

    • Google Scholar
65. 1. Schneider JE

    (2004) Energy balance and reproduction

    Physiology & Behavior 81:289–317.

    https://doi.org/10.1016/j.physbeh.2004.02.007

    • PubMed
    • Google Scholar
66. Book

    1. Simmons N

    (2005)

    Order Chiroptera

    In: Wilson D, Reeder D, editors. Mammal Species of the World: A Taxonomic and Geographic Reference. Baltimore: Johns Hopkins University Press. pp. 312–529.

    • Google Scholar
67. Book

    1. Speakman JR
    2. Thomas DW

    (2003)

    Physiological ecology and energetics of bats

    In: Kunz T, Fenton M, editors. Bat Ecology. Chicago: University of Chicago Press. pp. 430–490.

    • Google Scholar
68. 1. Speakman JR

    (2005) Body size, energy metabolism and lifespan

    Journal of Experimental Biology 208:1717–1730.

    https://doi.org/10.1242/jeb.01556

    • PubMed
    • Google Scholar
69. 1. Steiger SS
    2. Kelley JP
    3. Cochran WW
    4. Wikelski M

    (2009) Low metabolism and inactive lifestyle of a tropical rain forest bird investigated via heart-rate telemetry

    Physiological and Biochemical Zoology 82:580–589.

    https://doi.org/10.1086/605336

    • PubMed
    • Google Scholar
70. 1. Stockmaier S
    2. Dechmann DK
    3. Page RA
    4. O'Mara MT

    (2015) No fever and leucocytosis in response to a lipopolysaccharide challenge in an insectivorous bat

    Biology Letters 11:20150576.

    https://doi.org/10.1098/rsbl.2015.0576

    • PubMed
    • Google Scholar
71. 1. Storey KB
    2. Storey JM

    (2004) Metabolic rate depression in animals: transcriptional and translational controls

    Biological Reviews 79:207–233.

    https://doi.org/10.1017/S1464793103006195

    • PubMed
    • Google Scholar
72. 1. Suarez RK
    2. Herrera M LG
    3. Welch KC

    (2011) The sugar oxidation cascade: aerial refueling in hummingbirds and nectar bats

    Journal of Experimental Biology 214:172–178.

    https://doi.org/10.1242/jeb.047936

    • PubMed
    • Google Scholar
73. 1. Tøien Ø
    2. Blake J
    3. Edgar DM
    4. Grahn DA
    5. Heller HC
    6. Barnes BM

    (2011) Hibernation in black bears: independence of metabolic suppression from body temperature

    Science 331:906–909.

    https://doi.org/10.1126/science.1199435

    • PubMed
    • Google Scholar
74. 1. Taylor WB
    2. Moldofsky H
    3. Furedy JJ

    (1985) Heart rate deceleration in REM sleep: an orienting reaction interpretation

    Psychophysiology 22:110–115.

    https://doi.org/10.1111/j.1469-8986.1985.tb01569.x

    • PubMed
    • Google Scholar
75. 1. Thomas SP

    (1975)

    Metabolism during flight in two species of bats, Phyllostomus hastatus and Pteropus gouldii

    The Journal of experimental biology 63:273–293.

    • PubMed
    • Google Scholar
76. 1. Verrier RL
    2. Lau TR
    3. Wallooppillai U
    4. Quattrochi J
    5. Nearing BD
    6. Moreno R
    7. Hobson JA

    (1998)

    Primary vagally mediated decelerations in heart rate during tonic rapid eye movement sleep in cats

    The American journal of physiology 274:R1136–1141.

    • PubMed
    • Google Scholar
77. 1. Voigt CC
    2. Sörgel K
    3. Dechmann DK

    (2010) Refueling while flying: foraging bats combust food rapidly and directly to power flight

    Ecology 91:2908–2917.

    https://doi.org/10.1890/09-2232.1

    • PubMed
    • Google Scholar
78. 1. Voigt CC
    2. Speakman JR

    (2007) Nectar-feeding bats fuel their high metabolism directly with exogenous carbohydrates

    Functional Ecology 21:913–921.

    https://doi.org/10.1111/j.1365-2435.2007.01321.x

    • Google Scholar
79. 1. von Busse R
    2. Swartz SM
    3. Voigt CC

    (2013) Flight metabolism in relation to speed in Chiroptera: testing the U-shape paradigm in the short-tailed fruit bat Carollia perspicillata

    Journal of Experimental Biology 216:2073–2080.

    https://doi.org/10.1242/jeb.081760

    • PubMed
    • Google Scholar
80. 1. Walker JM
    2. Garber A
    3. Berger RJ
    4. Heller HC

    (1979) Sleep and estivation (shallow torpor): continuous processes of energy conservation

    Science 204:1098–1100.

    https://doi.org/10.1126/science.221974

    • PubMed
    • Google Scholar
81. 1. Ward S
    2. Bishop CM
    3. Woakes AJ
    4. Butler PJ

    (2002)

    Heart rate and the rate of oxygen consumption of flying and walking barnacle geese (Branta leucopsis) and bar-headed geese (Anser indicus)

    The Journal of experimental biology 205:3347–3356.

    • PubMed
    • Google Scholar
82. 1. Weiner J

    (1992) Physiological limits to sustainable energy budgets in birds and mammals: Ecological implications

    Trends in Ecology & Evolution 7:384–388.

    https://doi.org/10.1016/0169-5347(92)90009-Z

    • PubMed
    • Google Scholar
83. 1. Welch KC
    2. Herrera M LG
    3. Suarez RK

    (2008) Dietary sugar as a direct fuel for flight in the nectarivorous bat Glossophaga soricina

    Journal of Experimental Biology 211:310–316.

    https://doi.org/10.1242/jeb.012252

    • PubMed
    • Google Scholar
84. 1. Welch KC
    2. Péronnet F
    3. Hatch KA
    4. Voigt CC
    5. McCue MD

    (2016) Carbon stable-isotope tracking in breath for comparative studies of fuel use

    Annals of the New York Academy of Sciences 1365:15–32.

    https://doi.org/10.1111/nyas.12737

    • PubMed
    • Google Scholar
85. 1. Welcker J
    2. Speakman JR
    3. Elliott KH
    4. Hatch SA
    5. Kitaysky AS
    6. Wilson R

    (2015) Resting and daily energy expenditures during reproduction are adjusted in opposite directions in free-living birds

    Functional Ecology 29:250–258.

    https://doi.org/10.1111/1365-2435.12321

    • Google Scholar
86. 1. Williams TM
    2. Wolfe L
    3. Davis T
    4. Kendall T
    5. Richter B
    6. Wang Y
    7. Bryce C
    8. Elkaim GH
    9. Wilmers CC

    (2014) Mammalian energetics. Instantaneous energetics of puma kills reveal advantage of felid sneak attacks

    Science 346:81–85.

    https://doi.org/10.1126/science.1254885

    • PubMed
    • Google Scholar
87. 1. Winter Y
    2. von Helversen O

    (1998) The energy cost of flight: do small bats fly more cheaply than birds?

    Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 168:105–111.

    https://doi.org/10.1007/s003600050126

    • PubMed
    • Google Scholar

Thank you for submitting your article "Cyclic bouts of extreme bradycardia counteract the explosive metabolism of frugivorous bats" for consideration by eLife. Your article has been reviewed by three peer reviewers, one of whom is a member of our Board of Reviewing Editors and the evaluation has been overseen by the Reviewing Editor and Ian Baldwin as the Senior Editor. The following individual involved in review of your submission has agreed to reveal his identity: Fritz Geiser (Reviewer #2).

The reviewers have discussed the reviews with one another and the Reviewing Editor has drafted this decision to help you prepare a revised submission. Whereas we realize the number of essential revisions is rather extensive in this particular case, we believe that rewriting this manuscript such that it is more rigorous is entirely feasible based on the excellent style of the submitted manuscript. In general, we are mostly concerned with overstatements and a lack of essential information needed to place the findings in context; we do not question your key field observations.

Please comply to your best ability to the comments and provide point-by-point responses indicating at the start of every response if you comply, explain, or respectfully disagree.

Summary:

The manuscript by O'Mara et al., reports the discovery of a new cyclic bradycardic state in tropical fruit bats that saves energy by reducing the heart rate to extremely low values for a series of short moments during day rest. This is a unique and exciting find that advances our understanding of the mammalian cardiovascular system and metabolism. The technical accomplishment of measuring heart rate in freely flying individuals over several days in their natural habitat is impressive. Overall the use of heart rate as a measure of energy expenditure in small free-ranging mammals is commendable, the study was well constructed and the manuscript well written. The findings will be of interest to physiologists, ecologists, comparative biomechanists and organismal biologists in general.

Essential revisions:

Overall, we believe that the manuscript needs some careful reorganization to ensure scientific rigor: That the discussion and conclusions are placed within the context of the studies limitations.

Please discuss how estimates of energy expenditure and energy savings are extrapolations from a small sample of HR and MR under limited conditions and a single activity state. Further, the initial calibrations of HR against MR seem limited in that they were only conducted over a short time frame (3hrs) and at a single high ambient temperature very close to the thermoneutral zone. This gives a likelihood that animals with high HR (around 800bpm may have been exhibiting stress associated with the respirometry procedure, which can impact the derived regression equation as stress response alters blood pressure and cardiac output and is not indicative of true resting conditions.

While we agree that these short bouts of bradycardia are unlikely to be representative of torpor. We note that even small reductions in Tb can be reflected in reductions in HR and energy savings. Especially, because at rest many tropical and subtropical bats can reduce their body temperature by up to 6 degrees.

We appreciate the authors may make inferences of the costs of flight based on their resting calibration, however, these extrapolations may be inaccurate and this should be discussed appropriately. Alternatively, the paragraph in the discussion about flight costs (in the Discussion section) could simply be removed altogether without detracting from the findings improving the overall rigor of the manuscript.

To assist the reader please clarify how the regression calculations were conducted. How long were the HR values averaged with VO2? What time of day were the animals placed in the respirometry chamber? And were issues of autocorrelation and repeated measures addressed in the calculation of the regression equation?

Please further clarify the method by which HR was analyzed so the reader does not need to find and read the Cochran and Wikelski, 2005 reference but can simply fully rely on the Materials and methods section of the present manuscript to appreciate both its strengths and limitations.

Please clarify how many male and female bats were sampled for circulating cortisol, reading the manuscript we were confused by the different statements.

Title: An explosive metabolism would interfere with survival of the organisms. Another adjective may be more appropriate.

Bat stress related comments:

Based on the Introduction we wondered how well the bats function with the backpack after the surgical procedure. This also holds for the discussion in the Introduction and Discussion section "truly evolve" (too strong wording). Both the previous wind tunnel and invasive field experiments performed here are stressful to the animals unless habituation and positive reinforcement training have been implemented with all stressors removed. Only non-invasive non-stress experiments may possibly give this insight.

Reading the Materials and methods the 23ga needle is rather large, the metabolism of the bats is high, how quickly are they expected to heal up compared to the duration of the experiment? Please discuss this in the Materials and methods.

The Materials and methods states the backpack weighs 0.8 gram, which seems a high percentage of body weight. Heavy backpacks are a continues stressor of an animal with a high metabolic rate close to starvation. Please give the percentage backpack weight versus body weight and discuss it in the context of bat and bird experiments in which the effect of backpacks on stress, metabolics and general energetics have been studied. Please integrate this in the discussion if the backpack weighs more than 5% (limit for bird studies without recapture) bodyweight, otherwise integration in the Materials and methods section is sufficient.

Figure 2A; there appears to be a data gap beyond 22:00 hours, please explain and discuss. Panel B also appears to overlap with the data of panel A causing another gap, or there is another gap. Please plot the entire data of panel A without gaps from 0-24hrs if possible, otherwise indicate gaps using a gray area / bar with the explanation of why gaps exist.

Materials and Methods: What is the body mass and sample size of the bats? Sample sizes also need to be integrated into the Results section. Also include the average mass and std when discussing backpack mass in the Materials and methods and discuss the size of the backpack with respect to the size measure of the bat.

Table 1: include the mass and a measure of size of the individuals.

Abstract: Clearly much more than the cardiovascular system is involved here, for example digestion among other functions will be crucial in all this.

Introduction: Statement on homeostasis. There are other approaches than simply maintaining homeostasis in animal physiology.

Introduction:. …15-16 times 'of' minimum metabolic rates. Is this in comparison to BMR? If so, state. BTW some small bats at rest and without flight can do 300-400 times of the minimum metabolic rate during torpor.

Introduction: It is more complex than just lowering heart rate and body temperature and bats can reduce metabolic rate during torpor by up to 99% even when compared to BMR and more when compared to RMR at low ambient temperatures. Rephrase.

Introduction: There are published data on reduction of metabolism by 50% within the TNZ. Moreover, tropical bats are not always in thermo-neutrality, see the above reference. The sentence also does not make sense as written because they should be able to lower body temperature outside of thermo-neutral conditions. And reductions in heart rates will not only reduce metabolism. Rephrase.

Introduction: quadratic?

Introduction: Here it appears that all of the energy comes from food, further down stores of glycogen are needed. See also your results. Rephrase.

Introduction: By manipulating circulating levels of what?

Introduction: Define 'central-place forager'

Introduction: The reference in the Indroduction lists a number of phyllostomids using torpor (some described by McNab from lab studies as homeothermic) and also other nectarivorous/frugivorous bat.

Introduction: How would not using torpor result in a high metabolic scope -- should it not be the opposite?

Introduction: Further up it is argued that lab work is no good, now lab work is used. An explanation as to why this needs to be done in the laboratory would help.

Results: Large range in heart rates. To put this into perspective, six–fold is pretty good, but humans can do about four–fold and hibernating bats about eighty–fold.

Results: Were these bats captured or in captivity? If so, where and how?

Discussion: Entire range? Did they not fly over the canal?

Discussion: Replacement of half the fat reserves. The results on this need to be made clearer.

Discussion: 10% is not a lot and perhaps insignificant with regard to FMR.

Discussion: The short foraging times are interesting and are known from other small mammals in the field.

Discussion: Predictions of FMR from body mass?

Discussion: See comments above regarding McNab and reference in the Introduction. Differences between field and laboratory data are not only observed for flight, but also torpor expression and there is even a review on that. Rephrase this section.

Discussion: High sustained metabolic rates. Further up in the Discussion section it is stated their FMR is low.

Discussion: How will cyclic bradycardia maintain a semi-vigilant (and why semi?) state?

Discussion: Fuel metabolism from what?

Discussion: Is 50% of fat a majority?

Materials and methods: The statement is insufficient. In bears it was observed that behavioral responses to stressors can be minimal even if physiological responses are significant:http://www.cell.com/current-biology/abstract/S0960-9822(15)00827-1 Please discuss these issues briefly and fairly.

Materials and methods: Please include detailed information on the following: were animals retrieved during the experiment or after the experiment? Was the heart rate transmitter removed during or after the experiment, was the animal sacrificed or released after the experiment? If it was released in which state was the animal released?

Materials and methods: How was body temperature tracked? Provide details.

Materials and methods: What were the ambient temperatures during field work? If you can, provide daily minima, maxima and averages.

Materials and methods: Address assumptions and define abbreviations.

Materials and methods: Were the Figures and agave nectar analyzed for isotopes?

Materials and methods: This needs more explanation.

Materials and methods: What was in the vacutainers?

Materials and methods: This was queried above, were these in the wild? If so, please describe how bats were found, captured etc.

[Editors' note: further revisions were requested prior to acceptance, as described below.]

Thank you for resubmitting your work entitled "Cyclic bouts of extreme bradycardia counteract the high metabolism of frugivorous bats" for further consideration at eLife. Your revised article has been favorably evaluated by Ian Baldwin (Senior editor), a Reviewing editor, and two reviewers.

The manuscript has been improved but there are some remaining issues that need to be addressed before acceptance, as outlined below:

1) Throughout the results and discussion energy expenditure in free ranging bats should be clarified as estimated, calculated or "HR derived" or equivalent. (E.g. Discussion section and other lines.)

2) The bradycardia experienced by these animals at rest seem to fall within the range expected for basal heart rate and values found for other species of bats of a similar size or smaller (see Kulzer, 1967 and Currie et al., 2015), therefore related statements should be clarified accordingly.

Essential revisions:

Overall, we believe that the manuscript needs some careful reorganization to ensure scientific rigor: That the discussion and conclusions are placed within the context of the studies limitations.

Please discuss how estimates of energy expenditure and energy savings are extrapolations from a small sample of HR and MR under limited conditions and a single activity state. Further, the initial calibrations of HR against MR seem limited in that they were only conducted over a short time frame (3hrs) and at a single high ambient temperature very close to the thermoneutral zone. This gives a likelihood that animals with high HR (around 800bpm may have been exhibiting stress associated with the respirometry procedure, which can impact the derived regression equation as stress response alters blood pressure and cardiac output and is not indicative of true resting conditions.

This is an excellent point, and one we have attempted to circumvent using the allometric relationships based on heart and body mass developed by Bishop & Spivey (2013). Under stress conditions, it is unclear what the relationship between heart rate and oxygen consumption truly is. First, as a semantic distinction it is unclear why the reviewers assume that only high heart rates are indicative of stress. In our experience with frugivorous phyllostomids, such as Uroderma bilobatum, the most dangerous and stressful situations are when these animals enter low energy states, reduce T_b and f_H. While rare, in these stress-induced states, animals are unlikely to recover. Furthermore, high stress can induce torpor conditions in many, including tropical, bat species (e.g., Molossidae). The physiological adjustments animals make to increase blood pressure, mobilize glucose reserves, and hyperventilate, to name only a few, all could yield contradictory energetic results. Furthermore, increased heart rate in these conditions may not have the full cardiac expansion and contraction of exercising heart rates.

One point of confusion that we would like to highlight is how we extrapolated field metabolic rates from the heart rate data. There has been quite a bit of discussion in the literature about the applicability and limitations of respirometry-based calibration of f_H since most animals in these situations are not capable of exercising. Therefore, the calibrations of f_H that we, and many others have used, fail to include exercise values of animals engaging in their typical modes of locomotion. The allometric equations developed by Bishop and Spivey, (2013) are a breakthrough in overcoming this limitation. Instead of the resting-state calibrations we conducted, we instead apply Bishop and Spivey's relationships using body mass and heart mass of our bats. This was noted in the original submission in subsection “Heart rate telemetry and estimated field energy expenditure”, but it was not made clear that this is the fundamental relationship that defined the energetic expenditure of our field study. This has been applied to studies on bar-headed geese (Bishop et al., 2015, Science doi: 10.1126/science.1258732; Hawkes et al., 2014, PloS one doi: 10.1371/journal.pone.0094015), great frigate birds (Wiemerskirch et al., 2016; Science doi: 10.1126/science.aaf4374), and golden-collared manakins (Barske et al., 2014, Proc R Soc B doi: 10.1098/rspb.2013.2482) We have clarified this in the Materials and methods, the Introduction, and in the Results.

Resting calibrations of animals in respirometry have been widely applied using the heart rate methods, and likely over-estimate energy consumption at the low ends of the calibration values, and more importantly dramatically under-estimate energy consumption at high heart rates. Bishop and Spivey, (2013) highlights the work by Dechmann and colleagues (2011) and the implausibly low field metabolic rates due to underestimates of flying energy consumptions via exercise restricted heart rate / metabolic rate calibrations. Outside of Bishop and Spivey’s particularly thorough work, the quadratic relationship driving this is nicely shown by Ward et al., (2002) and the differences in metabolic rates of geese under their primary and non-primary modes of exercise locomotion. There are few data from flying vertebrates that have captured this so completely.

While we agree that these short bouts of bradycardia are unlikely to be representative of torpor. We note that even small reductions in Tb can be reflected in reductions in HR and energy savings. Especially, because at rest many tropical and subtropical bats can reduce their body temperature by up to 6 degrees.

The use of torpor and heterothermy by tropical and subtropical bats when ambient temperature drops below 24°C is an important detail and we have noted this in the Discussion section. In other work, we have even found that a free-tailed bat species in Panama is capable of reducing energetic expenditure to values lower than the minimal torpor metabolic rates of many sub-tropical and temperate zone mammals, but at body temperatures greater than 32°C, largely by lowering heart rate independently of lowered body temperatures (O’Mara et al., in review, Proc R Soc B). We also note in this paragraph that at least in previous work with captive animals by McNab, U. bilobatum actively defends body temperatures and will not undergo heterothermy. It would have been ideal if we were able to also simultaneously measure body temperature of free-ranging bats, but their roosts would not accommodate the PIT tag antenna.

We appreciate the authors may make inferences of the costs of flight based on their resting calibration, however, these extrapolations may be inaccurate and this should be discussed appropriately. Alternatively, the paragraph in the discussion about flight costs (in the Discussion) could simply be removed altogether without detracting from the findings improving the overall rigor of the manuscript.

Flight is obviously the most energetically demanding aspect of a bat’s daily life, and with so few data from free-flying animals we feel that discussing this is worthwhile. We have added a qualifying statement of the difficulty of accurately measuring in-flight metabolic rates in subsection “Heart rate telemetry and estimated field energy expenditure”.

To assist the reader please clarify how the regression calculations were conducted. How long were the HR values averaged with VO2? What time of day were the animals placed in the respirometry chamber? And were issues of autocorrelation and repeated measures addressed in the calculation of the regression equation?

We have clarified this in the Materials and methods to show that heart rates were averaged over the one minute preceding the VO2 measure, as well as the time of day when the experiments were conducted (subsection “Metabolic incorporation rates.”). To account for potential confounds of repeated measures we included individual identity as a random effect. We did not attempt to correct for autocorrelation in the heart rate data, but treated the five-minute samples as independent units.

Please further clarify the method by which HR was analyzed so the reader does not need to find and read the Cochran and Wikelski, 2005 reference but can simply fully rely on the Materials and methods section of the present manuscript to appreciate both its strengths and limitations.

We are unclear to what this comment is referring since the 2005 Cochran & Wikelski chapter focuses on the spatial tracking of thrushes, not physiological sampling. We have added the sampling windows and intervals for how heart rate was previously visually counted in subsection “Metabolic incorporation rates.” so that it is clear how our current method differs.

Please clarify how many male and female bats were sampled for circulating cortisol, reading the manuscript we were confused by the different statements.

This is noted in subsection “Glucocorticoids & energy mobilization” and in Figure 4.

Title: An explosive metabolism would interfere with survival of the organisms. Another adjective may be more appropriate.

We have adjusted the title accordingly to read ‘high metabolism’.

Bat stress related comments:

Based on the Introduction we wondered how well the bats function with the backpack after the surgical procedure. This also holds for the discussion in the Introduction and Discussion sections "truly evolve" (too strong wording). Both the previous wind tunnel and invasive field experiments performed here are stressful to the animals unless habituation and positive reinforcement training have been implemented with all stressors removed. Only non-invasive non-stress experiments may possibly give this insight.

The impact of tag placement on an animal’s behavior is always of concern, and it is unlikely that any tag attachment, no matter how small or streamlined will have no impact on an animal. The best we can do is to minimize this impact on the limited number of animals that we study. The 0.8 g tag we used represents 4-5% of body mass (4.5 ± 0.04%). We have included this summary of body mass and tag mass as a percent of body mass in the Discussion section. We have also revised the wording for the statements. For all studies conducted in wind tunnels extensive habituation and positive reinforcement are needed to get animals to fly in these environments. Animals must be trained to use these devices. We therefore need to acknowledge that the results of these wind tunnel experiments represent normal unstressed states for animals under those conditions. As we note throughout the manuscript, however, the more we learn from free-ranging animals, even those wearing any biologging device, the more we understand that there is great behavioral, mechanical, and physiological flexibility that we have underestimated in these study species.

Reading the Materials and methods the 23ga needle is rather large, the metabolism of the bats is high, how quickly are they expected to heal up compared to the duration of the experiment? Please discuss this in the Materials and methods.

Healing time is difficult to estimate, but we also don't believe that the 23ga needle is large (⌀ = 0.6414 mm). The needle punctures are difficult to find for lead insertion and we expect superficial healing within an hour. In comparison, human insulin needles are typically 26–31 ga (⌀ = 0.4636–0.2604 mm), and most intramuscular and subcutaneous injections for human infants are done with 23ga needles. Furthermore, cannulae used to inject PIT tags that are commonly used on small mice and bats including Uroderma in our study populations are 12ga ((⌀ = 2.769) and no negative impact has been observed. We have added additional statement regarding potential healing time in subsection “Calibration of heart rate versus oxygen consumption.”

The Materials and methods states the backpack weighs 0.8 gram, which seems a high percentage of body weight. Heavy backpacks are a continues stressor of an animal with a high metabolic rate close to starvation. Please give the percentage backpack weight versus body weight and discuss it in the context of bat and bird experiments in which the effect of backpacks on stress, metabolics and general energetics have been studied. Please integrate this in the discussion if the backpack weighs more than 5% (limit for bird studies without recapture) bodyweight, otherwise integration in the Materials and methods section is sufficient.

This additional mass represents 4.5 ± 0.04% of body mass. This, and the general limits of additional loading on flying animals, has been added in the Material and methods.

Figure 2A; there appears to be a data gap beyond 22:00 hours, please explain and discuss. Panel B also appears to overlap with the data of panel A causing another gap, or there is another gap. Please plot the entire data of panel A without gaps from 0-24hrs if possible, otherwise indicate gaps using a gray area / bar with the explanation of why gaps exist.

There are indeed gaps in the data. We have amended Figure 2 to note these gaps and explain in the figure that this is when bats were out of range of radio telemetry (i.e., they flew faster through the forest than we could run) or when they left the roost when recording had been automated.

Materials and Methods: What is the body mass and sample size of the bats? Sample sizes also need to be integrated into the Results section. Also include the average mass and std when discussing backpack mass in the Materials and methods and discuss the size of the backpack with respect to the size measure of the bat.

Noted in subsection “Heart rate telemetry and estimated field energy expenditure”. The sample sizes, both in the number of individuals tracked (or sampled) and the duration of tracking, were integrated in each section in subsections “Activity patterns”; “Field metabolic rates and cyclic bradycardia“, “Metabolic incorporation rates of resting bats“; and Figure 4.

Table 1: include the mass and a measure of size of the individuals.

Added.

Abstract: Clearly much more than the cardiovascular system is involved here, for example digestion among other functions will be crucial in all this.

This has been deleted to simplify.

Introduction: Statement on homeostasis. There are other approaches than simply maintaining homeostasis in animal physiology.

Revised to ‘maintain physiological integrity’.

Introduction:. …15-16 times 'of' minimum metabolic rates. Is this in comparison to BMR? If so, state. BTW some small bats at rest and without flight can do 300-400 times of the minimum metabolic rate during torpor.

Clarified to resting metabolic rate.

Introduction: It is more complex than just lowering heart rate and body temperature and bats can reduce metabolic rate during torpor by up to 99% even when compared to BMR and more when compared to RMR at low ambient temperatures. Rephrase.

Rephrased

Introduction: There are published data on reduction of metabolism by 50% within the TNZ. Moreover, tropical bats are not always in thermo-neutrality, see the above reference. The sentence also does not make sense as written because they should be able to lower body temperature outside of thermo-neutral conditions. And reductions in heart rates will not only reduce metabolism. Rephrase.

Rephrased.

Introduction: quadratic?

Corrected.

Introduction: Here it appears that all of the energy comes from food, further down stores of glycogen are needed. See also your results. Rephrase.

Rephrased.

Introduction: By manipulating circulating levels of what?

Clarified.

Introduction: Define 'central-place forager'

Clarified.

Introduction: The reference in the Indroduction lists a number of phyllostomids using torpor (some described by McNab from lab studies as homeothermic) and also other nectarivorous/frugivorous bat.

This is true; however; McNab has previously shown that this species does not use torpor.

Introduction: How would not using torpor result in a high metabolic scope -- should it not be the opposite?

The breadth of metabolic scope is not a focus for our MS, so we have removed it from this statement.

Introduction: Further up it is argued that lab work is no good, now lab work is used. An explanation as to why this needs to be done in the laboratory would help.

We did not intend to say that lab work is no good – only that what has been seen is that there are substantial differences between the responses of the same species under laboratory conditions and when they are placed into more complicated ecological circumstances. In addition to the work we highlight, this has also been shown by Professor Geiser’s group, and others, regarding torpor and homeothermy expression (e.g, Geiser et al. 2007 doi:10.1007/s00360-007-0147-6; Geiser et al. 2000 doi:10.1007/978-3-662-04162-8_10; and Audet & Thomas 1997 doi: 10.1007/s003600050058). We have added a sentence in the Introduction to hopefully minimize these concerns and reaction about the importance of controlled experiments.

Results: Large range in heart rates. To put this into perspective, six–fold is pretty good, but humans can do about four–fold and hibernating bats about eighty–fold.

Thank you for the additional context.

Results: Were these bats captured or in captivity? If so, where and how?

Clarified.

Discussion: Entire range? Did they not fly over the canal?

This sentence highlights the range of activities, not necessarily spatial range. We have revised accordingly. We did not track the bats across the canal, but were able to maintain radio contact with them due to the large open space and that the bats apparently did not venture far into the forest on the south side of the canal.

Discussion: Replacement of half the fat reserves. The results on this need to be made clearer.

We believe that the results for this are clear in subsection “Glucocorticoids & energy mobilization” and Figure 4B, but we would appreciate further guidance as to what should be clarified.

Discussion: 10% is not a lot and perhaps insignificant with regard to FMR.

We respectfully disagree, particularly in light of the rapid incorporation rates and fat turnover that we also document.

Discussion: The short foraging times are interesting and are known from other small mammals in the field.

We agree, and this seems to be the norm for other frugivorous bats as well.

Discussion: predictions of FMR from body mass?

Clarified.

Discussion: see comments above regarding McNab and reference in the Introduction. Differences between field and laboratory data are not only observed for flight, but also torpor expression and there is even a review on that. Rephrase this section.

We are unclear about the specifics of this comment as the reference in the Discussion section focuses on past work by McNab which shows that U. bilobatum defends Tb across a wide range of temperatures and does not enter classic torpor. We have added reference in the previous sentence that is more focused on lowering Tb in torpor to also include tropical and sub-tropical species. We would like to note as well that torpor appears to be more likely to be document in laboratory conditions than in free-ranging animals.

Discussion: High sustained metabolic rates. Further up in the Discussion section it is stated their FMR is low.

It is high for a mammal of their size, but what is expected for a frugivorous bat. We have rephrased this.

Discussion: How will cyclic bradycardia maintain a semi-vigilant (and why semi?) state?

We have removed this statement.

Discussion: Fuel metabolism from what?

Clarified.

Discussion: Is 50% of fat a majority?

Rephrased.

Materials and methods: The statement is insufficient. In bears it was observed that behavioral responses to stressors can be minimal even if physiological responses are significant:http://www.cell.com/current-biology/abstract/S0960-9822(15)00827-1 Please discuss these issues briefly and fairly.

This is an excellent point and the citation is spot on, particularly since it includes heart rate data. We have added further discussion in the Materials and methods section.

Materials and methods: Please include detailed information on the following: were animals retrieved during the experiment or after the experiment? Was the heart rate transmitter removed during or after the experiment, was the animal sacrificed or released after the experiment? If it was released in which state was the animal released?

3 of the 4 bats were recaptured and the transmitter was removed. Bats lost 0.0–0.5g (0.17 ± 0.29 g) which is within the daily mass fluctuations of 1–2g observed in this species (487 bats 92 of which have been captured more than once; O’Mara, unpublished data).

Materials and methods: How was body temperature tracked? Provide details.

This was described in subsection “Calibration of heart rate versus oxygen consumption” of the original submission. There may be confusion with the word "tracked" in that sentence. We did not measure Tb in free-ranging animals, only in respirometry. This has been clarified.

Materials and methods: What were the ambient temperatures during field work? If you can, provide daily minima, maxima and averages.

Added in subsection “Energetic Mobilization”.

Materials and methods: address assumptions and define abbreviations.

Added.

Materials and methods: Were the Figures and agave nectar analyzed for isotopes?

We measured the value of the agave nectar solution but not the Figures.

Materials and methods: This needs more explanation.

We have expanded these methods and hopefully they are now clear.

Materials and methods: What was in the vacutainers?

Rephrased.

Materials and methods: This was queried above, were these in the wild? If so, please describe how bats were found, captured etc.

We have clarified these methods: These were all wild bats in their natural roost.

[Editors' note: further revisions were requested prior to acceptance, as described below.]

The manuscript has been improved but there are some remaining issues that need to be addressed before acceptance, as outlined below:

1) Throughout the results and discussion energy expenditure in free ranging bats should be clarified as estimated, calculated or "HR derived" or equivalent. (E.g. Discussion section and other lines.).

We have corrected this accordingly by adding ‘heart rate derived’ where appropriate (e.g., Discussion section).

2) The bradycardia experienced by these animals at rest seem to fall within the range expected for basal heart rate and values found for other species of bats of a similar size or smaller (see Kulzer 1967 and Currie et al., 2015), therefore related statements should be clarified accordingly.

This is true and is it interesting how consistent basal heart rates are in bats. We have added detail related to this in the Discussion section that gives the range basal heart rate of small bat species and also notes the thermoneutral zone for U. bilobatum relative to the ambient temperatures of our field site for readers to consider.

Author details

1. M Teague O'Mara

   1. Department of Migration and Immuno-ecology, Max Planck Institute for Ornithology, Radolfzell, Germany
   2. Department of Biology, University of Konstanz, Konstanz, Germany
   3. Smithsonian Tropical Research Institute, Panama City, Panama
   4. Zukunftskolleg, University of Konstanz, Konstanz, Germany

   Contribution

   Conceptualization, Resources, Data curation, Software, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   teague.omara@gmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6951-1648

2. Martin Wikelski

   1. Department of Migration and Immuno-ecology, Max Planck Institute for Ornithology, Radolfzell, Germany
   2. Department of Biology, University of Konstanz, Konstanz, Germany

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

3. Christian C Voigt

   Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany

   Contribution

   Conceptualization, Resources, Formal analysis, Funding acquisition, Validation, Investigation, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

4. Andries Ter Maat

   Department of Behavioural Neurobiology, Max Planck Institute for Ornithology, Starnberg, Germany

   Contribution

   Resources, Software, Formal analysis, Investigation, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

5. Henry S Pollock

   Program in Ecology, Evolution and Conservation Biology, University of Illinois at Urbana-Champaign, Urbana, United States

   Contribution

   Resources, Formal analysis, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

6. Gary Burness

   Department of Biology, Trent University, Peterborough, Canada

   Contribution

   Conceptualization, Resources, Supervision, Funding acquisition, Investigation, Methodology, Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1695-7179

7. Lanna M Desantis

   Environmental and Life Sciences Graduate Program, Trent University, Peterborough, Canada

   Contribution

   Formal analysis, Investigation, Methodology, Writing—original draft

   Competing interests

   No competing interests declared

8. Dina KN Dechmann

   1. Department of Migration and Immuno-ecology, Max Planck Institute for Ornithology, Radolfzell, Germany
   2. Department of Biology, University of Konstanz, Konstanz, Germany
   3. Smithsonian Tropical Research Institute, Panama City, Panama

   Contribution

   Conceptualization, Supervision, Funding acquisition, Investigation, Methodology, Writing—original draft, Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0043-8267

• 4,031

  Page views

• 340

  Downloads

• 42

  Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.