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.
ABSTRACT. We describe a new collaborative network, the Motus Wildlife Tracking System (Motus; https://motus.org), which is an international network of researchers using coordinated automated radio-telemetry arrays to study movements of small flying organisms including birds, bats, and insects, at local, regional, and hemispheric scales. Radio-telemetry has been a cornerstone of tracking studies for over 50 years, and because of current limitations of geographic positioning systems (GPS) and satellite transmitters, has remained the primary means to track movements of small animals with high temporal and spatial precision. Automated receivers, along with recent miniaturization and digital coding of tags, have further improved the utility of radio-telemetry by allowing many individuals to be tracked continuously and simultaneously across broad landscapes. Motus is novel among automated arrays in that collaborators employ a single radio frequency across receiving stations over a broad geographic scale, allowing individuals to be detected at sites maintained by others. Motus also coordinates, disseminates, and archives detections and associated metadata in a central repository. Combined with the ability to track many individuals simultaneously, Motus has expanded the scope and spatial scale of research questions that can be addressed using radio-telemetry from local to regional and even hemispheric scales. Since its inception in 2012, more than 9000 individuals of over 87 species of birds, bats, and insects have been tracked, resulting in more than 250 million detections. This rich and comprehensive dataset includes detections of individuals during all phases of the annual cycle (breeding, migration, and nonbreeding), and at a variety of spatial scales, resulting in novel insights into the movement behavior of small flying animals. The value of the Motus network will grow as spatial coverage of stations and number of partners and collaborators increases. With continued expansion and support, Motus can provide a framework for global collaboration, and a coordinated approach to solving some of the most complex problems in movement biology and ecology.Le Système de suivi de la faune Motus : un réseau de recherche collaboratif visant à mieux comprendre le déplacement des animaux RÉSUMÉ. Le Système de suivi de la faune Motus (Motus; https://motus.org), un nouveau réseau collaboratif de chercheurs internationaux, repose sur un ensemble coordonné de stations automatisées de radiotélémétrie pour étudier le déplacement de petits organismes volant, comme les oiseaux, les chauves-souris et les insectes, aux échelles locales et régionales, et à celle de l'hémisphère. Pierre angulaire pour les études de suivi depuis plus de 50 ans, la radiotélémétrie est encore le principal moyen de suivre le déplacement de petits animaux avec une grande précision temporelle et spatiale, en raison des limites que présentent les émetteurs basés sur le système de positionnement géographique (GPS) ou satellite. Des stations réceptrices automatisées,...
Plasma metabolite profiling offers a potential means to assess stopover refueling performance of migratory birds from a single capture. However, this method has not previously been validated where site quality has been determined independently using analysis of capture data. We captured and blood sampled six passerine bird species refueling at known high-quality (BASE) and low-quality (TIP) sites at Long Point, Ontario, Canada. Plasma triglyceride, an indicator of fat deposition, was higher at the BASE in three early-season species: the hermit thrush, the American robin, and the white-throated sparrow. Plasma B-OH-butyrate, an indicator of fasting and lipid utilization, was lower at the BASE in the same three species. Plasma glycerol was lower at the BASE in American robins, and plasma phospholipid did not differ between sites. No metabolite suggested better conditions at the TIP in any species. Regression of size-corrected mass on time of day also indicated better refueling performance at the BASE in some species, but metabolite profiling was generally more sensitive to site differences. The relationship between plasma glycerol and triglyceride was U-shaped, indicating high glycerol production during both lipolysis (as was previously known) and rapid fat deposition. Our results confirm the validity of metabolite profiling to assess stopover habitat quality and individual performance in refueling migrants.
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.
Although migration is a widespread and taxonomically diverse behaviour, the ecological factors shaping migratory behaviour are poorly understood. Like other montane taxa, many birds migrate along elevational gradients in the tropics. Forty years ago, Alexander Skutch postulated that severe storms could drive birds to migrate downhill. Here, we articulate a novel mechanism that could link storms to mortality risks via reductions in foraging time and provide, to our knowledge, the first tests of this hypothesis in the White-ruffed Manakin (Corapipo altera), a small partially migratory frugivore breeding on the Atlantic slope of Costa Rica. As predicted, variation in rainfall was associated with plasma corticosterone levels, fat stores, plasma metabolites and haematocrit. By collecting data at high and low elevation sites simultaneously, we also found that high-elevation residents were more adversely affected by storms than low elevation migrants. These results, together with striking temporal capture patterns of altitudinal migrants relative to storms, provide, to our knowledge, the first evidence that weather-related risks incurred by species requiring high food intake rates can explain altitudinal migrations of tropical animals. These findings resolve conflicting evidence for and against food limitation being important in the evolution of this behaviour, and highlight how endogenous and exogenous processes influence life-history trade-offs made by individuals in the wild. Because seasonal storms are a defining characteristic of most tropical ecosystems and rainfall patterns will probably change in ensuing decades, these results have important implications for understanding the ecology, evolution and conservation of tropical animals.
. Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird. Am J Physiol Regulatory Integrative Comp Physiol 282: R1405-R1413, 2002; 10.1152/ ajpregu.00267.2001.-We developed an ELISA to measure heart-type fatty acid binding protein (H-FABP) in muscles of the western sandpiper (Calidris mauri), a long-distance migrant shorebird. H-FABP accounted for almost 11% of cytosolic protein in the heart. Pectoralis H-FABP levels were highest during migration (10%) and declined to 6% in tropically wintering female sandpipers. Premigratory birds increased body fat, but not pectoralis H-FABP, indicating that endurance flight training may be required to stimulate H-FABP expression. Juveniles making their first migration had lower pectoralis H-FABP than adults, further supporting a role for flight training. Aerobic capacity, measured by citrate synthase activity, and fatty acid oxidation capacity, measured by 3-hydroxyacylCoA-dehydrogenase and carnitine palmitoyl transferase activities, did not change during premigration but increased during migration by 6, 12, and 13%, respectively. The greater relative induction of H-FABP (ϩ70%) with migration than of catabolic enzymes suggests that elevated H-FABP is related to the enhancement of uptake of fatty acids from the circulation. Citrate synthase, 3-hydroxyacyl-CoA-dehydrogenase, and carnitine palmitoyl transferase were positively correlated within individuals, suggesting coexpression, but enzyme activities were unrelated to H-FABP levels. endurance exercise; fuel selection; lipid transport; metabolism THE INSTANTANEOUS COST OF flight is high relative to other forms of locomotion; flying birds expend energy at 10 to 15 times basal metabolic rate (BMR), and the minimum cost of flight may be twice the aerobic limit (V O 2 max ) of similarly sized running mammals (4, 38). In the special case of migratory flight, during which this intensity of exercise is maintained for as long as 50 or even 100 h, energy metabolism is almost completely dominated (85-95%) by the oxidation of exogenous fatty acids (FA) delivered to flight muscles from extramuscular adipose tissue (21,23,44). The use of stored fat as a metabolic fuel makes migratory flight possible, yet there currently exists no general mechanistic understanding of how birds achieve the high rates of exogenous FA transport and oxidation required to support such high-intensity endurance exercise.The most complete information on fuel selection during exercise comes from studies of running mammals (including humans). Generally, the relative contribution of FA oxidation to total fuel demand declines as exercise intensity increases, with the balance of energy derived mainly from carbohydrate oxidation (36). Exogenous FA contribute only a small fraction of the energy needed for exercise of even moderate intensity, and near V O 2 max exogenous FA oxidation contributes ϳ10% of energy demand (43, 45). The rate of utilization of exogenous FA appears to be most limited by transport across the sa...
Billions of animals migrate each year. To successfully reach their destination, migrants must have evolved an appropriate genetic program and suitable developmental, morphological, physiological, biomechanical, behavioral, and life-history traits. Moreover, they must interact successfully with biotic and abiotic factors in their environment. Migration therefore provides an excellent model system in which to address several of the "grand challenges" in organismal biology. Previous research on migration, however, has often focused on a single aspect of the phenomenon, largely due to methodological, geographical, or financial constraints. Integrative migration biology asks 'big questions' such as how, when, where, and why animals migrate, which can be answered by examining the process from multiple ecological and evolutionary perspectives, incorporating multifaceted knowledge from various other scientific disciplines, and using new technologies and modeling approaches, all within the context of an annual cycle. Adopting an integrative research strategy will provide a better understanding of the interactions between biological levels of organization, of what role migrants play in disease transmission, and of how to conserve migrants and the habitats upon which they depend.
Although fat is the primary fuel for migratory flight in birds, protein is also used. Catabolism of tissue protein yields five times as much water per kilojoule as fat, and so one proposed function of protein catabolism is to maintain water balance during nonstop flights. To test the protein-for-water hypothesis, we flew Swainson's thrushes (Catharus ustulatus) in a climatic wind tunnel under high- and low-humidity conditions at 18°C for up to 5 hours. Flight under dry conditions increased the rates of lean mass loss and endogenous water production and also increased plasma uric acid concentration. These data demonstrate that atmospheric humidity influences fuel composition in flight and suggest that protein deposition and catabolism during migration are, in part, a metabolic strategy to maintain osmotic homeostasis during flight.
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