The insectivorous bat Pipistrellus nathusii uses a mixed-fuel strategy to power autumn migration

SUMMARYMany species of bats migrate long distances, but the physiological challenges of migration are poorly understood. We tested the hypothesis that migration is physiologically demanding for bats by examining migration-related phenotypic flexibility. Both bats and birds are endothermic, flying vertebrates; therefore, we predicted that migration would result in similar physiological tradeoffs. We compared hoary bats (Lasiurus cinereus) during spring migration and summer non-migratory periods, comparing our results with previous observations of birds. Migrating bats had reduced digestive organs, enlarged exercise organs, and fat stores had higher proportions of polyunsaturated fatty acids (PUFAs). These results are consistent with previous studies of migrating birds; however, we also found sex differences not typically associated with bird migration. Migrating female hoary bats increased the relative size of fat stores by reducing lean body components, while males maintained the same relative amount of fat in both seasons. The ratio of n-6 to n-3 PUFA in flight muscle membrane increased in migrating males and decreased in migrating females, consistent with males using torpor more frequently than females during spring migration. Enlarged exercise organs, reduced digestive organs and changes in adipose tissue composition reflect the elevated energetic demands of migration. Sexspecific patterns of fat storage and muscle membrane composition likely reflect challenges faced by females that migrate while pregnant. Our results provide some of the first insights into the physiological demands of bat migration and highlight key differences between bats and birds.

Section: Organ Sizescontrasting

confidence: 54%

Section: Introductionmentioning

confidence: 99%

Phenotypic flexibility in migrating bats: seasonal variation in body composition, organ sizes and fatty acid profiles

McGuire

Fenton

Guglielmo

2013

“…Recent studies employing 13 C-breath testing have revealed that different classes of purified nutrients exhibit unique oxidative kinetics when fed to birds (McCue et al, , 2011a, rodents and bats (Voigt et al, 2012). The general pattern observed is that exogenous amino acids are oxidized much sooner and to a greater extent than exogenous fatty acids during the postprandial period (Welch et al, 2015).…”

Section: Introductionmentioning

confidence: 98%

Digesting pythons quickly oxidize the proteins in their meals and save the lipids for later

McCue

Guzman

Passement

2015

Pythons digesting rodent meals exhibit up to 10-fold increases in their resting metabolic rate (RMR); this increase in RMR is termed specific dynamic action (SDA). Studies have shown that SDA is partially fueled by oxidizing dietary nutrients, yet it remains unclear whether the proteins and the lipids in their meals contribute equally to this energy demand. We raised two populations of mice on diets labeled with either [ 13 C]leucine or [ 13 C]palmitic acid to intrinsically enrich the proteins and lipids in their bodies, respectively. Ball pythons (Python regius) were fed whole mice (and pureed mice 3 weeks later), after which we measured their metabolic rates and the δ 13 C in the breath. The δ 13C values in the whole bodies of the protein-and lipid-labeled mice were generally similar (i.e. 5.7±4.7‰ and 2.8±5.4‰, respectively) but the oxidative kinetics of these two macronutrient pools were quite different. We found that the snakes oxidized 5% of the protein and only 0.24% of the lipids in their meals within 14 days. Oxidation of the dietary proteins peaked 24 h after ingestion, at which point these proteins provided ∼90% of the metabolic requirement of the snakes, and by 14 days the oxidation of these proteins decreased to nearly zero. The oxidation of the dietary lipids peaked 1 day later, at which point these lipids supplied ∼25% of the energy demand. Fourteen days after ingestion, these lipids were still being oxidized and continued to account for ∼25% of the metabolic rate. Pureeing the mice reduced the cost of gastric digestion and decreased SDA by 24%. Pureeing also reduced the oxidation of dietary proteins by 43%, but it had no effect on the rates of dietary lipid oxidation. Collectively, these results demonstrate that pythons are able to effectively partition the two primary metabolic fuels in their meals. This approach of uniquely labeling the different components of the diet will allow researchers to examine new questions about how and when animals use the nutrients in their meals.

“…However, whether the fat used under these conditions is entirely supplied from adipose, as is required for long migratory flights, or involves intramuscular fat stores is unknown. Migratory bats may instead use a mixed fuel strategy where flight is fueled by stored fat and ingested nutrients (Jonasson, 2017;Voigt et al, 2012). Bats normally feed at night on insects, fruit or nectar, making it possible for them to feed before initiating a migratory flight or to pause to feed as they travel (Jonasson, 2017).…”

Section: Introductionmentioning

confidence: 99%

Obese super athletes: fat-fueled migration in birds and bats

Guglielmo

2018

123

112

Migratory birds are physiologically specialized to accumulate massive fat stores (up to 50-60% of body mass), and to transport and oxidize fatty acids at very high rates to sustain flight for many hours or days. Target gene, protein and enzyme analyses and recent -omic studies of bird flight muscles confirm that high capacities for fatty acid uptake, cytosolic transport, and oxidation are consistent features that make fat-fueled migration possible. Augmented circulatory transport by lipoproteins is suggested by field data but has not been experimentally verified. Migratory bats have high aerobic capacity and fatty acid oxidation potential; however, endurance flight fueled by adipose-stored fat has not been demonstrated. Patterns of fattening and expression of muscle fatty acid transporters are inconsistent, and bats may partially fuel migratory flight with ingested nutrients. Changes in energy intake, digestive capacity, liver lipid metabolism and body temperature regulation may contribute to migratory fattening. Although control of appetite is similar in birds and mammals, neuroendocrine mechanisms regulating seasonal changes in fuel store set-points in migrants remain poorly understood. Triacylglycerol of birds and bats contains mostly 16 and 18 carbon fatty acids with variable amounts of 18:2n-6 and 18:3n-3 depending on diet. Unsaturation of fat converges near 70% during migration, and unsaturated fatty acids are preferentially mobilized and oxidized, making them good fuel. Twenty and 22 carbon n-3 and n-6 polyunsaturated fatty acids (PUFA) may affect membrane function and peroxisome proliferator-activated receptor signaling. However, evidence for dietary PUFA as doping agents in migratory birds is equivocal and requires further study.