Move That Fatty Acid: Fuel Selection and Transport in Migratory Birds and Bats

Abstract

The metaphor of marathon running is inadequate to fully capture the magnitude of long-distance migratory flight of birds. In some respects a journey to the moon seems more appropriate. Birds have no access to supplementary water or nutrition during a multi-day flight, and they must carefully budget their body fat and protein stores to provide both fuel and life support. Fatty acid transport is crucial to successful non-stop migratory flight in birds. Although fat is the most energy-dense metabolic fuel, the insolubility of its component fatty acids makes them difficult to transport to working muscles fast enough to support the highly aerobic exercise required to fly. Recent evidence indicates that migratory birds compensate for this by expressing large amounts of fatty acid transport proteins on the membranes of the muscles (FAT/CD36 and FABPpm) and in the cytosol (H-FABP). Through endogenous mechanisms and/or diet, migratory birds may alter the fatty acid composition of the fat stores and muscle membranes to improve endurance during flight. Fatty acid chain length, degree of unsaturation, and placement of double bonds can affect the rate of mobilization of fatty acids from adipose tissue, utilization of fatty acids by muscles, and whole-animal performance. However, there is great uncertainty about how important fatty acid composition is to the success of migration or whether particular types of fatty acids (e.g., omega-3 or omega-6) are most beneficial. Migratory bats provide an interesting example of evolutionary convergence with birds, which may provide evidence for the generality of the bird model to the evolution of migration by flight in vertebrates. Yet only recently have attempts been made to study bat migration physiology. Many aspects of their fuel metabolism are predicted to be more similar to those of migrant birds than to those of non-flying mammals. Bats may be distinct from most birds in their potential to conserve energy by using torpor between flights, and in the behavioral and physiological trade-offs they may make between migration and reproduction, which often overlap.

Differential gene expression in seasonal sympatry: mechanisms involved in diverging life histories

“…As the primary fuel for most migratory songbirds, lipids provide more energy per wet mass than other sources of energy [21]. Lipids are stored in muscle and adipose tissue in preparation for migration and are mobilized in the form of fatty acids to fuel migratory flight [21][22][23] and transported in circulation [24,25]. L-3-hydroxyacyl-Coenzyme A dehydrogenase and long-chain-acyl-CoA dehydrogenase, which are involved in fatty acid oxidation, were expressed more in migrants.…”

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

“…For decades, it was widely accepted that fat fueled the migratory flight of birds, without clear recognition of how impossible it should be based on what was known about mammalian exercise. Many studies of muscle enzymes of migrant birds emphasized that fatty acid oxidation capacity increased and how important this was, yet the key limitation is not oxidation but transport (Guglielmo, 2010). The paradox of fatty acids stored in adipose fat (triacylglycerol) as fuel for flying migrants such as birds and bats, is that the property that makes them ideal for storing energy (hydrophobicity), also makes them difficult to metabolize at the very high rates needed for flight.…”

“…Many excellent reviews summarize aspects of fat storage and utilization in migratory birds (Bairlein, 2002;Berthold, 1993;Biebach, 1996;Blem, 1976Blem, , 1980Guglielmo, 2010;Jenni and Jenni-Eiermann, 1998;McWilliams et al, 2004;Newton, 2008;Pierce and McWilliams, 2014;Price, 2010;Ramenofsky, 1990;Weber, 2009), with occasional information on bats (Blem, 1980;Fleming and Eby, 2003;McGuire and Guglielmo, 2009). The purpose of this Review is to use recent findings to compare the role of fat as a fuel for migration of birds and bats.…”

“…2 toward long-duration activity requires a change in fuel supply, and this is where stored fat becomes most important. Using fat to fuel high-intensity exercise requires a suite of changes to pathways of fatty acid transport and oxidation, which appear to be characteristic of long-distance migrants (Guglielmo, 2010;see below). Fat is the preferred fuel for migration because the highly reduced nature and hydrophobicity of fatty acids result in fat providing approximately eight times more energy per unit wet mass (∼37 kJ g −1 ) than carbohydrates or protein (∼4-5 kJ g −1 ; Blem, 1990;Jenni and Jenni-Eiermann, 1998).…”

Landscape structure, human disturbance and crop management affect foraging ground selection by migrating geese

“…Migrating birds depend mostly on the availability of resources at stopover sites that influence survival and recuperation (Bauer et al 2008;Alerstam 2011). Although many studies have focused on the physiology of migration and strategies for energy refuelling (e.g., Tinkler et al 2009;Guglielmo 2010), much less is known about site choice where birds forage (Newton 2006).…”