Temporal patterns of foraging by silver-haired bats during migratory stopover revealed by isotopic analyses (δ13C) of breath CO2.

The extent to which migratory bats forage at stopover sites or while in migratory flight is poorly understood. Endogenous fat stores have lower δ13C values relative to the dietary substrates from which they were synthesized, and so, the fed versus fasted state of bats should be discernable by comparing their breath δ13C at capture to that after a known period of fasting. We captured silver-haired bats (Lasionycteris noctivagans) at a stopover site at Long Point, Ontario, Canada, during spring and fall migration. We collected breath samples at capture and after fasting in captivity for 12 h, providing a fasted-state δ13C value corresponding to metabolism of fat stores. We also collected and weighed fecal pellets produced while in captivity. Breath δ13C values at capture were positively correlated with mass of feces produced. During spring migration, δ13C values of breath CO2 at capture were low and similar to fasting values, but increased with date consistent with increased foraging at stopover and reliance on exogenous dietary nutrients as the season progressed. The opposite temporal pattern was found during fall migration. Our findings suggest that bats forage during migratory stopover when environmental conditions permit despite potential time trade-offs between feeding and travel, and the energy savings resulting from torpor during roosting. This study provides insight into the eco-physiology of bat migration and shows the importance of foraging habitat for migratory bats.

Testing the "Fasting While Foraging" Hypothesis: Effects of Recent Feeding on Plasma Metabolite Concentrations in Little Brown Bats (Myotis lucifugus).

Plasma metabolite concentrations can be used to understand nutritional status and foraging behavior across ecological contexts including prehibernation fattening, migration refueling, and variation in foraging habitat quality. Generally, high plasma concentrations of the ketone ß-hydroxybutyrate, a product of fat catabolism, indicate fasting, while triglycerides indicate recent feeding and fat accumulation. In recent studies of insectivorous bats, triglyceride concentration increased after feeding as expected, but ß-hydroxybutyrate also unexpectedly increased rather than decreased. An aerial-hawking foraging strategy is energetically demanding, and thus it has been hypothesized that foraging by insectivorous bats requires catabolism of stored fat. We tested this hypothesis by quantifying plasma ß-hydroxybutyrate and triglyceride concentration following feeding in little brown bats (Myotis lucifugus) that were temporarily housed in individual cages to prevent flight. We provided a fixed amount of food and collected blood samples at different intervals after feeding to produce variation in plasma metabolite concentrations. Plasma triglyceride concentration responded as predicted, but similar to previous studies and contrary to our prediction, when flight was eliminated plasma ß-hydroxybutyrate concentration responded similarly to triglyceride. Thus, it is unlikely that the unexpected plasma ß-hydroxybutyrate patterns observed in previous studies were related to flight. The mechanism underlying this unexpected pattern remains unknown, but the response has been consistent in all studies to date. Thus, plasma metabolite analysis provides an effective tool for studies of nutritional status, although more work is needed to understand why insectivorous bats respond differently than other taxa.

Energetics of migratory bats during stopover: a test of the torpor-assisted migration hypothesis.

The torpor-assisted migration hypothesis posits that migration is facilitated in bats by the use of torpor during stopover roosting periods, and predicts that at stopover, bats regulate time in torpor facultatively so that daily energy expenditure is independent of ambient roosting temperature. Energy savings can thus be directed to migratory movement. However, direct measurements of total roosting energy expenditure in relation to ambient and body temperature are lacking. We captured migratory silver-haired bats (Lasionycteris noctivagans; ∼11 g) at Long Point, ON, Canada, in spring and autumn 2016. We used quantitative magnetic resonance analysis to measure body composition change and energy expenditure over a 12 h roosting period in a ventilated incubator at 10, 17 and 25°C. We assessed the effects of season, body mass, sex and age on energy expenditure. We found that daily energy expenditure was independent of roosting temperature, and that this was achieved by flexible use of torpor. Variation in body mass at capture was driven mainly by differences in fat, and the amount of body fat was negatively related to torpor use, particularly in spring. Season, sex and age also affected torpor use and energy expenditure, notably with pregnant females being generally fatter and using less torpor than males in spring. We estimate that stopover contributes only 15-20% to the total energy costs of migration in bats compared with 70% or more in typical birds. This study provides support for the torpor-assisted migration hypothesis, and furthers our understanding of the energy budgets of migratory bats.

Metabolic rate, latitude and thermal stability of roosts, but not phylogeny, affect rewarming rates of bats.

Torpor is an adaptation that allows many endotherms to save energy by abandoning the energetic cost of maintaining elevated body temperatures. Although torpor reduces energy consumption, the metabolic heat production required to arouse from torpor is energetically expensive and can impact the overall cost of torpor. The rate at which rewarming occurs can impact the cost of arousal, therefore, factors influencing rewarming rates of heterothermic endotherms could have influenced the evolution of rewarming rates and overall energetic costs of arousal from torpor. Bats are a useful taxon for studies of ecological and behavioral correlates of rewarming rate because of the widespread expression of heterothermy and ecological diversity across the >1200 known species. We used a comparative analysis of 45 bat species to test the hypothesis that ecological, behavioral, and physiological factors affect rewarming rates. We used basal metabolic rate (BMR) as an index of thermogenic capacity, and local climate (i.e., latitude of geographic range), roost stability and maximum colony size as ecological and behavioral predictors of rewarming rate. After controlling for phylogeny, high BMR was associated with rapid rewarming while species that live at higher absolute latitudes and in less thermally stable roosts also rewarmed most rapidly. These patterns suggests that some bat species rely on passive rewarming and social thermoregulation to reduce costs of rewarming, while others might rely on thermogenic capacity to maintain rapid rewarming rates in order to reduce energetic costs of arousal. Our results highlight species-specific traits associated with maintaining positive energy balance in a wide range of climates, while also providing insight into possible mechanisms underlying the evolution of heterothermy in endotherms.