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

Abstract

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.

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

“…Migration-related changes were again complicated by sex differences: 22:6n-3 increased and 18:2n-6 decreased in migrant females, whereas the opposite occurred in males. Although total unsaturation did not change during migration, the double-bond index decreased in males and increased in females, and the n-6/n-3 ratio increased in males and decreased in females (McGuire et al, 2013a). Thus, no general pattern emerges regarding migrationrelated changes in the fatty acid composition of muscle membranes of free-living migratory birds and bats, except that changes in longchain n-3 PUFA appear to be offset by opposite changes in n-6 PUFA so that overall unsaturation remains stable (Guglielmo et al, 2002b;Maillet and Weber, 2006;McGuire et al, 2013a).…”

“…In studies of insectivorous bats sampled during autumn migration, fat loads were ∼25% of body mass whereas a frugivorous species had ∼12% body fat (Blem, 1980;Fleming and Eby, 2003). McGuire et al (2013a) found that female hoary bats were fatter during spring migration (16% of the total body mass) than during the summer (11%), but that males were lean in both seasons (11-12%). Fat stores of bats cannot be assessed visually owing to their thick fur; however, non-invasive QMR analysis has greatly increased our understanding of their fat storage (McGuire and Guglielmo, 2010).…”

“…The fatty acid composition of hoary bat fat stores changed slightly between summer and migration, and sex was a significant factor. Total unsaturation and the double-bond index increased during migration, driven by decreased 16:0 and 16:1n-7, increased 18:2n-6 and 18:3n-3, and 18:1n-9 increasing slightly in females and decreasing in males (McGuire et al, 2013a). Like the fat stores of birds, the fat stores of migratory bats appear to contain ∼70% unsaturated fatty acids.…”

“…The total body lipids of three migratory Myotis species had low relative amounts of 18:0 (1.5-3.5%) and high levels of 16:0 (12-18%), 16:1n-7 (9-17%), 18:1n-9 (31-49%) and 18:2n-6 (10-19%), with ∼5-6% 18:3n-3 (Ewing et al, 1970). McGuire et al (2013a) analyzed adipose triglycerides of migratory hoary bats and found similarly high levels of 16:0 (∼25%) and 18:1n-9 (∼57%), but lower levels of 16:1 (∼2%), 18:0 (∼3%), 18:2n-6 (∼8%) and 18:3n-3 (∼5%). The fatty acid composition of hoary bat fat stores changed slightly between summer and migration, and sex was a significant factor.…”

“…Although the individual fatty acids ( particularly PUFA) in bird flight muscle phospholipids may change dramatically between winter and migration, total unsaturation or the double-bond index tend to decrease slightly, and the ratio of n-6/n-3 PUFA may increase or decrease (Guglielmo et al, 2002b;Klaiman et al, 2009;Price et al, 2010). McGuire et al (2013a) reported that the fatty acid composition of the flight muscle phospholipids of hoary bats differed substantially from adipose triacylglycerol by having more 18:0 (8% versus 2%), and by the presence and high abundance of 20 and 22 carbon PUFA (up to ∼20% 22:6n-3). Migration-related changes were again complicated by sex differences: 22:6n-3 increased and 18:2n-6 decreased in migrant females, whereas the opposite occurred in males.…”