Limits...
Trapped in the darkness of the night: thermal and energetic constraints of daylight flight in bats.

Voigt CC, Lewanzik D - Proc. Biol. Sci. (2011)

Bottom Line: Bats are one of the most successful mammalian groups, even though their foraging activities are restricted to the hours of twilight and night-time.We conclude that increased flight costs only render diurnal bat flights profitable when the relative energy gain during daytime is high and risk of predation is low.Ancestral bats possibly have evolved dark-skinned wing membranes to reduce nocturnal predation, but a low degree of reflectance of wing membranes made them also prone to overheating and elevated energy costs during daylight flights.

View Article: PubMed Central - PubMed

Affiliation: Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Straße 17, 10315 Berlin, Germany. voigt@izw-berlin.de

ABSTRACT
Bats are one of the most successful mammalian groups, even though their foraging activities are restricted to the hours of twilight and night-time. Some studies suggested that bats became nocturnal because of overheating when flying in daylight. This is because--in contrast to feathered wings of birds--dark and naked wing membranes of bats efficiently absorb short-wave solar radiation. We hypothesized that bats face elevated flight costs during daylight flights, since we expected them to alter wing-beat kinematics to reduce heat load by solar radiation. To test this assumption, we measured metabolic rate and body temperature during short flights in the tropical short-tailed fruit bat Carollia perspicillata at night and during the day. Core body temperature of flying bats differed by no more than 2°C between night and daytime flights, whereas mass-specific CO(2) production rates were higher by 15 per cent during daytime. We conclude that increased flight costs only render diurnal bat flights profitable when the relative energy gain during daytime is high and risk of predation is low. Ancestral bats possibly have evolved dark-skinned wing membranes to reduce nocturnal predation, but a low degree of reflectance of wing membranes made them also prone to overheating and elevated energy costs during daylight flights. In consequence, bats may have become trapped in the darkness of the night once dark-skinned wing membranes had evolved.

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Carbon dioxide production rate (; ml min−1) measured by indirect calorimetry in relation to  (ml min−1) measured by the Na-bicarbonate method. Total bicarbonate pool size was estimated by either the plateau (filled circles) or the intercept method (open circles).
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RSPB20102290F2: Carbon dioxide production rate (; ml min−1) measured by indirect calorimetry in relation to (ml min−1) measured by the Na-bicarbonate method. Total bicarbonate pool size was estimated by either the plateau (filled circles) or the intercept method (open circles).

Mentions: Bats of the validation experiment weighed on average 22.1 ± 1.4 g. Within a few minutes after IP injection of the labelled Na-bicarbonate, the 13C label equilibrated in the bats' body bicarbonate pool (figure 1a). On average, peak 13C enrichments above baseline levels (5.87 ± 1.23 atom%) occurred 11.3 ± 2.4 min post-injection. Intercept values of maximum AP13CE equalled 7.37 ± 1.74 atom%. After the peak, kc averaged 0.078 ± 0.016 min−1 and the dynamics of the reaction progress variable suggested a linear decline, and thus a single pool involved in the washout of the 13C label for a 30 min post-peak period (figure 1b). The comparison between respirometry and the Na-bicarbonate method revealed that the Na-bicarbonate method yielded higher values than the indirect calorimetry (figure 2). averaged 0.73 ± 0.37 ml min−1 when measured with indirect calorimetry, while averaged 1.84 ± 0.91 and 1.40 ± 0.71 ml min−1 based on the intercept and the plateau approach of the Na-bicarbonate method, respectively. Thus, the Na-bicarbonate method exceeded the respirometric value by 151 ± 26 and 89 ± 18 per cent, respectively. Despite this discrepancy, the coefficient of determination for the relationship between as measured with the Na-bicarbonate method and respirometry was high, equalling 94 and 97 per cent when using the intercept and the plateau method, respectively. Because of the higher r2 value, we used the plateau method for calculating of flying bats.Figure 1.


Trapped in the darkness of the night: thermal and energetic constraints of daylight flight in bats.

Voigt CC, Lewanzik D - Proc. Biol. Sci. (2011)

Carbon dioxide production rate (; ml min−1) measured by indirect calorimetry in relation to  (ml min−1) measured by the Na-bicarbonate method. Total bicarbonate pool size was estimated by either the plateau (filled circles) or the intercept method (open circles).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3119008&req=5

RSPB20102290F2: Carbon dioxide production rate (; ml min−1) measured by indirect calorimetry in relation to (ml min−1) measured by the Na-bicarbonate method. Total bicarbonate pool size was estimated by either the plateau (filled circles) or the intercept method (open circles).
Mentions: Bats of the validation experiment weighed on average 22.1 ± 1.4 g. Within a few minutes after IP injection of the labelled Na-bicarbonate, the 13C label equilibrated in the bats' body bicarbonate pool (figure 1a). On average, peak 13C enrichments above baseline levels (5.87 ± 1.23 atom%) occurred 11.3 ± 2.4 min post-injection. Intercept values of maximum AP13CE equalled 7.37 ± 1.74 atom%. After the peak, kc averaged 0.078 ± 0.016 min−1 and the dynamics of the reaction progress variable suggested a linear decline, and thus a single pool involved in the washout of the 13C label for a 30 min post-peak period (figure 1b). The comparison between respirometry and the Na-bicarbonate method revealed that the Na-bicarbonate method yielded higher values than the indirect calorimetry (figure 2). averaged 0.73 ± 0.37 ml min−1 when measured with indirect calorimetry, while averaged 1.84 ± 0.91 and 1.40 ± 0.71 ml min−1 based on the intercept and the plateau approach of the Na-bicarbonate method, respectively. Thus, the Na-bicarbonate method exceeded the respirometric value by 151 ± 26 and 89 ± 18 per cent, respectively. Despite this discrepancy, the coefficient of determination for the relationship between as measured with the Na-bicarbonate method and respirometry was high, equalling 94 and 97 per cent when using the intercept and the plateau method, respectively. Because of the higher r2 value, we used the plateau method for calculating of flying bats.Figure 1.

Bottom Line: Bats are one of the most successful mammalian groups, even though their foraging activities are restricted to the hours of twilight and night-time.We conclude that increased flight costs only render diurnal bat flights profitable when the relative energy gain during daytime is high and risk of predation is low.Ancestral bats possibly have evolved dark-skinned wing membranes to reduce nocturnal predation, but a low degree of reflectance of wing membranes made them also prone to overheating and elevated energy costs during daylight flights.

View Article: PubMed Central - PubMed

Affiliation: Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Straße 17, 10315 Berlin, Germany. voigt@izw-berlin.de

ABSTRACT
Bats are one of the most successful mammalian groups, even though their foraging activities are restricted to the hours of twilight and night-time. Some studies suggested that bats became nocturnal because of overheating when flying in daylight. This is because--in contrast to feathered wings of birds--dark and naked wing membranes of bats efficiently absorb short-wave solar radiation. We hypothesized that bats face elevated flight costs during daylight flights, since we expected them to alter wing-beat kinematics to reduce heat load by solar radiation. To test this assumption, we measured metabolic rate and body temperature during short flights in the tropical short-tailed fruit bat Carollia perspicillata at night and during the day. Core body temperature of flying bats differed by no more than 2°C between night and daytime flights, whereas mass-specific CO(2) production rates were higher by 15 per cent during daytime. We conclude that increased flight costs only render diurnal bat flights profitable when the relative energy gain during daytime is high and risk of predation is low. Ancestral bats possibly have evolved dark-skinned wing membranes to reduce nocturnal predation, but a low degree of reflectance of wing membranes made them also prone to overheating and elevated energy costs during daylight flights. In consequence, bats may have become trapped in the darkness of the night once dark-skinned wing membranes had evolved.

Show MeSH
Related in: MedlinePlus