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.
We used stable isotopes of C in breath, blood, feces and feathers to identify intra-individual changes in diet and the timescale of diet changes in free-living songbirds at a stopover site. Because accurate interpretation of differences between the delta13C of breath, plasma, and red blood cells (RBCs) relative to diet requires knowing the turnover rate of C within them, we determined the rate of change of C in breath, plasma and RBCs for yellow-rumped warblers (Dendroica coronata). Half-lives of C in breath, plasma, and RBCs were 4.4+/-2.1 h, 24.8+/-12.3 h and 10.9+/-3.2 days, respectively, for yellow-rumped warblers. delta13C of breath, plasma, RBCs and feces from wild-caught golden-crowned kinglets (Regulus satrapa), ruby-crowned kinglets (R. calendula) and gray catbirds (Dumetella carolinensis) indicated that they had maintained an isotopically consistent diet for an extended period of time. However, delta13C of breath and plasma indicated that white-throated sparrows (Zonotrichia albicollis) had recently expanded their diet to include a C4 dietary component. Likewise, delta13C of breath, plasma, RBCs and feces indicated that some wild-caught yellow-rumped warblers had consumed foods with a more enriched protein signature prior to their arrival on Block Island, and since arrival, they had consumed mostly northern bayberry (Myrica pensylvanica). Therefore, comparisons of the delta13C of breath, plasma, RBCs, feces and feathers from individual songbirds can indicate changes in diet and provide an estimate of the timescale of the diet change.
Ecological and evolutionary physiology has traditionally focused on aspects of physiology one at a time. Here, we discuss the implications of considering physiological regulatory networks (PRNs) as integrated wholes, a perspective that reveals novel roles for physiology in organismal ecology and evolution. For example, evolutionary response to changes in resource abundance might be constrained by the role of dietary micronutrients in immune response regulation, given a particular pathogen environment. Because many physiological components impact more than one process, organismal homeostasis is maintained, individual fitness is determined, and evolutionary change is constrained (or facilitated) by interactions within PRNs. We discuss how PRN structure and its system-level properties could determine both individual performance and patterns of physiological evolution. GlossaryAlternative physiological structures -Different PRN structures that would produce equivalent functional and fitness outcomes for a given species in a given environment. Which structure evolves might be largely random, but might have consequences for long-term evolution of PRN structure.Cytokines -Small cell-signalling proteins involved in intercellular communication. Regulatory cascades of cytokines are particularly critical in the immune system. Dysregulation -A breakdown over time in the ability of an individual's PRN to maintain homeostasis; possibly in response to chronic stress or infection, and possibly a root cause of aging.3 Homeostasis -A state of healthy physiological equilibrium, including appropriate anticipation of and responses to changing conditions.Integrator -A PRN molecule that has a particularly crucial role in synthesizing information (internal or external) and thereby determining multiple aspects of PRN functioning (e.g., a 'hub' or 'keystone' PRN molecule) Physiological Regulatory Network (PRN) -The network of molecules and their regulatory relationships that maintain and adjust homeostasis and facilitate performance at the wholeorganism level.PRN Molecule -PRN molecules are the subset of molecules that maintain homeostasis at the organism level via their regulatory relationships with other molecules. In most cases, these molecules are the nodes (vertices) in a PRN, and regulatory relationships between them are the links (edges). In some cases, several related molecules (e.g., circulating steroid, receptors, binding globulins) may be grouped together as a single node for measurement purposes, or gene activation may be a node in some contexts. Flexibility of node definition is common in other biological networks-for example, nodes in ecological networks can be species, groups of species, life stages, or other categories (e.g., detritus). PRN state -The concentrations of all PRN molecules at a given moment for a given individual in a particular context (e.g. age, time of year, life history stage). More generally, "changes in PRN state" describe joint adjustments in molecule concentrations in anticipation of or respo...
Managing oxidative stress is an important physiological function for all aerobic organisms, particularly during periods of prolonged high metabolic activity, such as long-distance migration across ecological barriers. However, no previous study has investigated the oxidative status of birds at different stages of migration and whether that oxidative status depends on the condition of the birds. In this study, we compared (1) energy stores and circulating oxidative status measures in (a) two species of Neotropical migrants with differing migration strategies that were sampled at an autumn stopover site before an ecological barrier; and (b) a species of trans-Saharan migrant sampled at a spring stopover site after crossing an ecological barrier; and (2) circulating oxidative measures and indicators of fat metabolism in a trans-Saharan migrant after stopovers of varying duration (0–8 nights), based on recapture records. We found fat stores to be positively correlated with circulating antioxidant capacity in Blackpoll Warblers and Red-eyed Vireos preparing for fall migration on Block Island, USA, but uncorrelated in Garden Warblers on the island of Ponza, Italy, after a spring crossing of the Sahara Desert and Mediterranean Sea. In all circumstances, fat stores were positively correlated with circulating lipid oxidation levels. Among Garden Warblers on the island of Ponza, fat anabolism increased with stopover duration while oxidative damage levels decreased. Our study provides evidence that birds build antioxidant capacity as they build fat stores at stopover sites before long flights, but does not support the idea that antioxidant stores remain elevated in birds with high fuel levels after an ecological barrier. Our results further suggest that lipid oxidation may be an inescapable hazard of using fats as the primary fuel for flight. Yet, we also show that birds on stopover are capable of recovering from the oxidative damage they have accrued during migration, as lipid oxidation levels decrease with time on stopover. Thus, the physiological strategy of migrating songbirds may be to build prophylactic antioxidant capacity in concert with fuel stores at stopover sites before a long-distance flight, and then repair oxidative damage while refueling at stopover sites after long-distance flight.
SUMMARY Most migrating birds accumulate lipid stores as their primary source of energy for fueling long distance flights. Lipid stores of birds during migration are composed of mostly unsaturated fatty acids; whether such a fatty acid composition enhances exercise performance of birds is unknown. We tested this hypothesis by measuring metabolic rate at rest and during intense exercise in two groups of red-eyed vireos, a long-distance migratory passerine, fed either a diet containing 82% unsaturated fat (82%U), or one containing 58% unsaturated fat (58%U). Vireos fed the 82%U diet had fat stores containing (77%) unsaturated fatty acids, whereas vireos fed the 58% U diet had fat stores containing less (66%) unsaturated fatty acids. Blood metabolites measured prior to and immediately following exercise confirmed that vireos were metabolizing endogenous fat during intense exercise. Mass-specific resting metabolic rate (RMR) was similar for vireos fed the 58%U diet (2.75±0.32 ml O2 g–1h–1) and for vireos fed the 82%U diet (2.30±0.30 ml O2 g–1 h–1). However,mass-specific peak metabolic rate (MRpeak) was 25% higher in vireos fed the 58%U diet (28.55±1.47 ml O2 g–1h–1) than in vireos fed the 82%U diet (21.50±1.76 ml O2 g–1 h–1). Such whole-animal energetic effects of fatty acid composition of birds suggest that the energetic cost of migration in birds may be affected by the fatty acid composition of the diet.
During fall migration many songbirds switch from consuming primarily insects to consuming mostly fruit. Fruits with more carbohydrates and less protein may be sufficient to rebuild expended fat stores, but such fruits may be inadequate to replace catabolized protein. We manipulated the concentrations and isotopic signatures of macronutrients in diets fed to birds to study the effects of diet quality on metabolic routing of dietary nutrients. We estimated that approximately 45% and 75%, respectively, of the carbon in proteinaceous tissue of birds switched to high- or low-protein diets came from nonprotein dietary sources. In contrast, we estimated that approximately 100% and 20%-80%, respectively, of the nitrogen in proteinaceous tissues of birds switched to high- or low-protein diets was attributable to dietary protein. Thus, the routing and assimilation of dietary carbon and nitrogen differed depending on diet composition. As a result, delta (15)N of tissues collected from wild animals that consume high-quality diets may reliably indicate the dietary protein source, whereas delta (13)C of these same tissues is likely the product of metabolic routing of carbon from several macronutrients. These results have implications for how isotopic discrimination is best estimated and how we can study macronutrient routing in wild animals.
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