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, 9 (12), e115724
eCollection

Bats on a Budget: Torpor-Assisted Migration Saves Time and Energy

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Bats on a Budget: Torpor-Assisted Migration Saves Time and Energy

Liam P McGuire et al. PLoS One.

Abstract

Bats and birds must balance time and energy budgets during migration. Migrating bats face similar physiological challenges to birds, but nocturnality creates special challenges for bats, such as a conflict between travelling and refueling, which many birds avoid by feeding in daylight and flying at night. As endothermic animals, bats and birds alike must expend substantial amounts of energy to maintain high body temperatures. For migratory birds refueling at stopovers, remaining euthermic during inactive periods reduces the net refuelling rate, thereby prolonging stopover duration and delaying subsequent movement. We hypothesized that bats could mitigate similar ambient-temperature dependent costs by using a torpor-assisted migration strategy. We studied silver-haired bats Lasionycteris noctivagans during autumn migration using a combination of respirometry and temperature-sensitive radiotelemetry to estimate energy costs incurred under ambient temperature conditions, and the energy that bats saved by using torpor during daytime roosting periods. All bats, regardless of sex, age, or body condition used torpor at stopover and saved up to 91% of the energy they would have expended to remain euthermic. Furthermore, bats modulated use of torpor depending on ambient temperature. By adjusting the time spent torpid, bats achieved a rate of energy expenditure independent of the ambient temperature encountered at stopover. By lowering body temperature during inactive periods, fuel stores are spared, reducing the need for refuelling. Optimal migration models consider trade-offs between time and energy. Heterothermy provides a physiological strategy that allows bats to conserve energy without paying a time penalty as they migrate. Although uncommon, some avian lineages are known to use heterothermy, and current theoretical models of migration may not be appropriate for these groups. We propose that thermoregulatory strategies should be an important consideration of future migration studies of both bats and birds.

Conflict of interest statement

Competing Interests: In-kind support was provided by Lotek Wireless Inc. There are no patents, products in development, or marketed products to declare. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials.

Figures

Figure 1
Figure 1. Torpid and euthermic metabolic rates measured by open flow respirometry.
Silver-haired bats were held at a range of temperatures similar to local conditions. Open circles and dashed regression line indicate resting metabolic rate (RMR) and filled circles and solid regression line indicate torpid metabolic rate (TMR).
Figure 2
Figure 2. Temperature profiles of free-living silver-haired bats during autumn migration.
Vertical lines indicate sunrise and sunset, horizontal dashed line indicates the individually determined threshold below which the bat was considered torpid (see Materials and Methods), black dots indicate skin temperature, and gray dots indicate ambient temperature. The amount of time spent torpid depended on ambient conditions. Mean ambient temperature over the period of observation was 27.4°C (Sept 3), 21.9°C (Aug 28), and 18.3°C (Sept 8) in panels (a), (b), and (c) respectively. Accordingly, in (a) the bat spent only a brief period of the morning in torpor, whereas at cooler temperatures bats spent most (b) or all (c) of the day torpid.
Figure 3
Figure 3. Relative energy savings of daytime torpor use during stopover.
(a) On cooler days, when the energetic cost of defending normal body temperature would be greater, bats spent more time in torpor. (b) Bats saved 12–91% of the estimated energy required to remain euthermic, and saved more energy on cooler days.
Figure 4
Figure 4. Estimated field metabolic rate of migrating bats calculated for the entire daytime period of observation.
Metabolic rate was determined from ambient temperature and the regression lines from respirometry trials (Fig. 1) accounting for periods of torpor and euthermia. The lines correspond to the expected field metabolic rate if the bats had remained strictly euthermic (dashed line), or torpid (solid line) based on respirometry trials. The secondary y-axis converts metabolic rate to the mass of fat required.

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References

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Grant support

Funding was provided to CGG by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada and a Leaders Opportunity Fund Grant from the Canada Foundation for Innovation and Ontario Research Fund (CFI 11826). LPM and KAJ were supported by Canada Graduate Scholarships from the Natural Sciences and Engineering Research Council of Canada. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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