Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective

Abstract

Unlike exercising mammals, migratory birds fuel very high intensity exercise (e.g., flight) with fatty acids delivered from the adipose tissue to the working muscles by the circulatory system. Given the primary importance of fatty acids for fueling intense exercise, we discuss the likely limiting steps in lipid transport and oxidation for exercising birds and the ecological factors that affect the quality and quantity of fat stored in wild birds. Most stored lipids in migratory birds are comprised of three fatty acids (16:0, 18:1 and 18:2) even though migratory birds have diverse food habits. Diet selection and selective metabolism of lipids play important roles in determining the fatty acid composition of birds which, in turn, affects energetic performance during intense exercise. As such, migratory birds offer an intriguing model for studying the implications of lipid metabolism and obesity on exercise performance. We conclude with a discussion of the energetic costs of migratory flight and stopover in birds, and its implications for bird migration strategies. Migration poses distinct physiological challenges for birds. For example, long-distance migrants rely virtually entirely on stored energy and nutrients to fuel each flight, and then must rapidly restore the necessary energy and nutrients at stopover sites along their migration route. Solutions to the physiological challenges associated with alternating intense exercise without feeding and then intense feeding and refueling at stopover sites are often physiologically incompatible. Determining how birds overcome these physiological challenges requires understanding how the physiological capabilities of exercising and fasting birds relate to the ecological conditions encountered during migration. This review focuses on the nutritional and physiological ecology of birds during migration. We discuss the current model of how birds fuel the costs of migration and the likely limiting steps in lipid transport and oxidation for exercising birds, and how lipid metabolism in birds is different from that in other vertebrates. We then place these aspects of the biochemistry and metabolism of birds during migration within an ecological context. We review selected aspects of the nutritional ecology of birds during migration with an emphasis on how birds accumulate fat stores, how fatty acid composition of diet influences composition of fat stores, and the effect of fatty acid composition of fat # JOURNAL OF AVIAN BIOLOGY REVIEW Reviews provide an opportunity to summarize existing knowledge within ornithological research, especially in areas where rapid and significant advances are occurring. Reviews should be concise and should cite all key references. An abstract is required.

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

“…The adipose triacylglycerol in nonmigratory and migratory birds is predominately composed of 16 and 18 carbon fatty acids that are saturated (no double bonds, 18:0, 16:0) and monounsaturated (MUFA, one double bond with 'n' indicating the position of the first double bond relative to the methyl end, e.g. 16:1n-7 or 18:1n-9; Blem, 1976;McWilliams et al, 2004). The most abundant constituents are usually 16:0 and 18:1n-9, comprising 10-37% and 17-61% of the total adipose fatty acids, respectively, in migratory songbirds and waterbirds (Blem, 1976;Klaiman et al, 2009;Maillet and Weber, 2006;McWilliams et al, 2004;Napolitano and Ackman, 1990;.…”

“…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.…”

“…Although there is empirical support for such an adjustment of muscle mass with changing body mass (Lindström et al, 2000;Schwilch et al, 2002), most of the lean mass catabolized in flight is usually derived from digestive and other organs, which have inherently greater protein turnover rates than muscle (Battley et al, 2000;Bauchinger and McWilliams, 2009;Bauchinger et al, 2005), suggesting that the maintenance of metabolic and osmotic homeostasis are the primary causes of lean mass catabolism in flight. Empirical measurements made in the field and laboratory by body composition analysis, respirometry and stable isotopic analysis show that fat usually provides ∼90% and protein ∼10% of the energy for long-distance flights of migratory birds (Jenni and Jenni-Eiermann, 1998;McWilliams et al, 2004).…”

Physiological regulatory networks: ecological roles and evolutionary constraints

“…In birds, fatty acid composition during migration appears to be adjusted to optimize energy-to-weight ratio, even at a cost of increased oxidative damage [63]. The strong force of selection on weight during migration will thus likely result in conserved or convergent evolution of fatty acid composition, rather than in alternative strategies for fatty acid metabolism, though the details have yet to be confirmed.…”

A Puzzling Migratory Detour: Are Fueling Conditions in Alaska Driving the Movement of Juvenile Sharp-Tailed Sandpipers?

“…Higgins and Davies (1996) presented data on Sharp-tailed Sandpipers banded in Australia, and there seems to be no significant prevalence of males there. Being the larger sex, males may have a longer flight range (McWilliams et al 2004) and may thus be more able to make a long detour en route to the nonbreeding grounds than can females (cf. O'Hara et al 2006).…”