Flight Muscles Of Birds Research Articles

Muscle testosterone supply keeps male birds topped up out of season

Many creatures live life on the energetic limit, so when they don't need a particular organ, they simply allow it to wither away to save energy until required again. Snakes’ digestive tracts atrophy between meals, migrating birds also reduce the mass of their digestive systems while en route and many male birds allow their testes to downsize out of the mating season. But this does not mean that male birds are not able to brag boastfully when their testes are out of action. Male woodpeckers are still capable of high-speed drumming, powered by their strong neck muscles, to warn other males off their territories, which made Eric Schuppe (University of California, San Francisco, USA) and Matthew Fuxjager (Brown University, USA) wonder whether the woodpecker's impressive out-of-season percussive performances could be due to testosterone produced in the muscle itself.Schuppe headed out into the North Carolina woods to capture territorial downy woodpeckers (Dryobates pubescens) during and after the mating season, to measure the quantity of testosterone circulating in their blood and in various tissues – including the powerfully drumming neck muscle and their testes. Back in the lab, Schuppe and Daniel Tobiansky (Brown University) discovered that the levels of testosterone in the drumming muscle during the breading season were six times higher than in the bird's flight muscles, which are required year-round. The testosterone levels even remained high in the percussive muscle during the winter and autumn, when the hormone had all but disappeared from other tissues in the body. And when the team checked for evidence of the key enzymes that are essential for producing the potent hormone from the basic cholesterol building block, all of the key enzymes turned up in the neck muscle at high levels. Woodpeckers are capable of beefing up their masculine drumming neck muscles by producing testosterone within the muscle itself. But could the magnificent performances of other males also benefit from a boost of in situ testosterone?This time, the team turned their attention to chattering male white-breasted nuthatches (Sitta carolinensis) and zebra finches (Taeniopygia guttata), both of which serenade females, to find out whether their superfast voice box muscles benefit from a self-produced shot of testosterone. Sure enough, all of the necessary enzymes for producing the masculine hormone from scratch turned up in the trilling birds’ voice boxes. Serenading nuthatches and zebra finches probably produce testosterone in their voice box muscles to enhance their acoustic pyrotechnics to attract females.Having confirmed that testosterone can be produced in organs that become souped up to catch the attention of passing females, Schuppe, Fuxjager and colleagues wondered whether the hormone could also enhance the performance of other superfast muscles, such as those that drive swift eye swivels. Sure enough, all of the critical enzymes turned up in the fast-contracting eye muscles of lab mice and at much higher levels than occur in other muscles that never contract as fast.It seems that the organs that male birds depend upon when courting females are capable of producing their own internal testosterone supply to enhance their performance, and it turns out that some other muscles that are capable of super-fast contractions can also produce the hormone, which may enhance blisteringly fast contractions. So male woodpeckers, nuthatches and zebra finches don't need to depend on testosterone produced by their testes when defending their territories and serenading females out of season: their own internal muscle supplies keep them topped up and in tip-top condition.

The Long Glu-Rich Segments of Troponin T in Flight Muscles of Birds and Insects

The troponin complex plays a central role in the Ca2+-regulation of striated muscle contraction and relaxation. Molecular evolution and comparative structural studies have identified Glu-rich segments specifically expressed in the T subunit of troponin (TnT) in diverse flying species, such as birds and insects. Avian pectoral muscle TnT has a Glu-rich segment in the N-terminal variable region and insect TnT has one in the C-terminal extension. To understand these structural traits of non-homologous evolutionary origins, which may have been selected for analogous functions of flight muscles, will help to understand the mechanisms of striated muscle contraction for the development of therapeutic improvement of skeletal and cardiac muscle functions. We previously demonstrated a potential function of the N-terminal Glu-rich segment of avian pectoral muscle TnT as a myofilament-associated Ca2+-reservoir (Zhang et al., Biochemistry 43:2645-55 2004). To investigate a novel hypothesis that this function reduces the work load of the Ca2+ handling system in myocytes thus saving energy for sustaining the work of muscle especially during long distance flight, we developed a Drosophila line with the Glu rich C-terminal segment of TnT deleted to test its requirement for muscle function and flight capacity. Engineered drosophila TnT proteins are expressed in E. coli for the characterization of changes in biochemical activities. The results showed that the C-terminal truncated Drosophila TnT retains the capacity of binding to troponin I, troponin C and tropomyosin. Tpnt gene-modified flies expressing the Glu-rich C-terminal segment deleted TnT have been generated for functional studies. Together with the development and characterization of genetically modified mice expressing an insect muscle-like TnT in the heart, our study aims at establishing a novel mechanism to improve cardiac efficiency for the treatment of heart failure.

How the hummingbird wingbeat is tuned for efficient hovering.

Both hummingbirds and insects flap their wings to hover. Some insects, like fruit flies, improve efficiency by lifting their body weight equally over the upstroke and downstroke, while utilizing elastic recoil during stroke reversal. It is unclear whether hummingbirds converged on a similar elastic storage solution, because of asymmetries in their lift generation and specialized flight muscle apparatus. The muscles are activated a quarter of a stroke earlier than in larger birds, and contract superfast, which cannot be explained by previous stroke-averaged analyses. We measured the aerodynamic force and kinematics of Anna's hummingbirds to resolve wing torque and power within the wingbeat. Comparing these wingbeat-resolved aerodynamic weight support measurements with those of fruit flies, hawk moths and a generalist bird, the parrotlet, we found that hummingbirds have about the same low induced power losses as the two insects, lower than that of the generalist bird in slow hovering flight. Previous analyses emphasized how bird flight muscles have to overcome wing drag midstroke. We found that high wing inertia revises this for hummingbirds - the pectoralis has to coordinate upstroke to downstroke reversal while the supracoracoideus coordinates downstroke to upstroke reversal. Our mechanistic analysis aligns with all previous muscle recordings and shows how early activation helps furnish elastic recoil through stroke reversal to stay within the physiological limits of muscles. Our findings thus support Weis-Fogh's hypothesis that flies and hummingbirds have converged on a mechanically efficient wingbeat to meet the high energetic demands of hovering flight. These insights can help improve the efficiency of flapping robots.

Біоморфологічні особливості м’язів, діючих на плечовий суглоб, деяких представників ряду горобцеподібних – Ordо Passeriformes

Biomorphological features of muscles that act on the shoulder joint of some representatives of orderPasseriformes are represented in the article. As shoulder joint of birds has many axes, not only the muscles of the shoulder joint provide the movements in it, but some of the muscles of the shoulder girdle and elbow joint. It should be noted that the main flight muscles of birds are the shoulder girdle muscles, including the chest (m. pectoralis) and supra-coracoid muscles. Some muscles of an elbow joint, including m. coracoradialis and m. scapuli triceps, are equally important. However, the amount of muscles that somehow act on the shoulder joint of the investigated birds' species is different, the degree of muscle development in these species is also different. In order to understand the degree of development, particularly mechanisms of differentiation and development of muscle structures, a comprehensive study of the muscles of the shoulder girdle, shoulder and elbow joints was conducted. The material for the research was obtained from the funds of the Department of animal anatomy named after acad. V.G. Kasyanenko of National University of Life and Environmental Sciences of Ukraine, where the studies of muscular structures of the shoulder joint of some representatives of order Passeriformes, including raven (Corvus corax), rook (Corvus fragilegus), waxwings (Bombycilla garrulous), were conducted. Research of muscles of the shoulder joint, shoulder girdle and elbow joint of birds was performed on fresh or fixed in 10% formalin solution cadavers. After describing and defining of fixation points of the muscles, they were dissected to determine the location of the muscle fibers. In addition, in order to determine the degree of development of muscles and muscle groups, each muscle was weighed. During the research, muscles were drawn or pictured to complement the work with illustrative material. There was no larger or smaller muscle neither in muscle group of shoulder, nor elbow joint that should be significantly for each case. There is no clear stability in the development of muscle groups of these joints. At the same time, muscle group of elbow joint is more developed than the muscle group of shoulder joint. All these mentioned features of structure and differentiation of muscles, which act on the shoulder joint of birds, are caused by physical exertion, posed by adaptation to a different type, speed and duration of flight.

Muscle function in avian flight: achieving power and control

Flapping flight places strenuous requirements on the physiological performance of an animal. Bird flight muscles, particularly at smaller body sizes, generally contract at high frequencies and do substantial work in order to produce the aerodynamic power needed to support the animal's weight in the air and to overcome drag. This is in contrast to terrestrial locomotion, which offers mechanisms for minimizing energy losses associated with body movement combined with elastic energy savings to reduce the skeletal muscles' work requirements. Muscles also produce substantial power during swimming, but this is mainly to overcome body drag rather than to support the animal's weight. Here, I review the function and architecture of key flight muscles related to how these muscles contribute to producing the power required for flapping flight, how the muscles are recruited to control wing motion and how they are used in manoeuvring. An emergent property of the primary flight muscles, consistent with their need to produce considerable work by moving the wings through large excursions during each wing stroke, is that the pectoralis and supracoracoideus muscles shorten over a large fraction of their resting fibre length (33-42%). Both muscles are activated while being lengthened or undergoing nearly isometric force development, enhancing the work they perform during subsequent shortening. Two smaller muscles, the triceps and biceps, operate over a smaller range of contractile strains (12-23%), reflecting their role in controlling wing shape through elbow flexion and extension. Remarkably, pigeons adjust their wing stroke plane mainly via changes in whole-body pitch during take-off and landing, relative to level flight, allowing their wing muscles to operate with little change in activation timing, strain magnitude and pattern.

Glycolysis activity in flight muscles of birds according to their physiological function. An experimental model in vitro to study aerobic and anaerobic glycolysis activity separately

An experimental system in vitro is presented to assess the activity of the entire glycolysis in tissue extracts, which allows determining aerobic and anaerobic glycolysis activities separately. Glycolysis activity has been measured in pectoral and supracoracoideus muscles of the homing pigeon and the domestic fowl. These muscles support different aspects of flight in the two birds and are representative models of the two kinds of basic movements, endurance and sprint. The results obtained showed that in type I red fibers (pigeon pectoral), glucose produced a high glycolytic activity, while it was a poor substrate for type IIb white fibers (fowl pectoral and the two supracoracoideus). White fibers, however, attained its maximum glycolytic activity with phosphorylated glucose as substrate. These results demonstrated the validity of the experimental system as a method for assaying the two kinds of glycolytic activity in tissues, and supply new information about the biochemical and physiological features of these types of fibers.

Fatty acid-dependent expression of the muscle FABP gene – comparative analysis of gene control in functionally related, but evolutionary distant animal systems

The heart is the most fatty acid-dependent muscle in mammals, but flight muscles of birds and insects encounter even higher rates of fatty acid oxidation. The amount of the muscle fatty acid binding protein (H-FABP) found in these muscle reflects their metabolic activities, and increased fatty acid metabolism in endurance exercise increases FABP expression further. We have studied the mechanism of fatty acid-dependent expression of the H-FABP gene, taking advantage of the comparative analysis of gene control in functionally related, but evolutionary distant animal systems, i.e., rat heart and locust flight muscle. Luciferase reporter genes with a full-length promoter ( approximately 1 kb) from either the locust or the rat were strongly expressed in L6 myoblasts, and the expression of both constructs was markedly increased by fatty acid treatment. Because of its stronger induction by fatty acids and the absence of other vertebrate transcription factor binding sites, the locust promoter was advantageous for the identification of a fatty acid response element (FARE), an inverted repeat of a hexanucleotide half site reminiscent of steroid hormone receptor binding sites (IR-3). All mammalian H-FABP promoters contain similar sequences, however in reverse orientation (everted repeats, ER-3). Deletion of the FARE eliminated the fatty acid inducibility completely for the locust promoter, but only partly for its mammalian analogue, perhaps because of additional factors or more complex interactions. In gel shift studies, the element binds nuclear proteins from both rat cells and locust flight muscle, further attesting to the far-reaching conservation of this mechanism. Two individual proteins bind to the element, with full binding requiring the presence of free fatty acid. Antibodies to PPARs failed to induce a supershift of the protein-DNA complex, indicating that other transcription factors are responsible for the fatty acid-mediated induction of gene expression of H-FABP.

SLOW-FLYING PIGEONS PUT MORE POWER INTO IT

Bird flight aerodynamics researchers often base their flight models on man-made flying machines. This may work for soaring and gliding birds, but as Jim Usherwood points out, `slow-flapping birds really don't resemble planes'. So Usherwood and his colleagues came up with an innovative approach involving pressure sensors to calculate the aerodynamic power of slow-flapping pigeons(p. 355).`To calculate the aerodynamic power output of a bird's flight muscles you need to know the forces acting on a bird's wing and the speed of the wing'says Usherwood. He explains that there are two non-independent types of force acting when you see a bird flying - those that keep the animal in the air, and those that require muscular work to keep the animal flying. These forces result from pressure differences. `If you know the pressure difference between the top surface and the bottom surface of a bird's wing, you can calculate the force acting on the wing,' says Usherwood. To calculate the forces acting during slow-flapping flight, he needed to measure the pressure at different points on pigeons' wings during flight.Teaming up with Tyson Hedrick, Craig McGowan and Andrew Biewener, Usherwood began adapting pressure sensors so that he could attach them to the birds. The challenge was modifying pressure sensors to stay in place despite the large accelerations of the flapping wings. The team eventually succeeded in pinning pressure sensors through eight feathers on the birds' wings. With the sensors firmly in place, the team used high-speed digital video to record the pigeons'flapping flight as they flew between two perches. The team calculated the birds' aerodynamic power output by combining measurements of the birds' wing speed from the digital videos with simultaneous pressure sensor measurements.The team's novel approach provides a valuable test of the accuracy of direct wing muscle measurements, which until now provided the only method of calculating power output directly. But the team's calculations of the power output of slow-flapping flight are higher than those obtained from direct wing muscle measurements in previous studies. Usherwood emphasizes that each component of his team's power output calculation is reasonable, and slow flight may simply be more energetically expensive and aerodynamically inefficient than previously thought, resulting in higher power outputs than had previously been predicted.Usherwood is enthusiastic about this new approach. `Now that we know that the pressure sensors work, we want to take the set-up outside,' he says;`eventually, we'd like to be able to calculate power output while birds are behaving naturally, such as during migration or foraging.'

Computer Simulation of Fat and Muscle Burn in Long-distance Bird Migration

The mechanical power required from a bird's flight muscles was recalculated at regular intervals (default 6 min), and the energy consumed in the interval was accounted for by reducing fuel reserves, which also reduced the all-up mass and the body cross-sectional area. Part of the energy requirement was met by consuming flight muscle tissue, according to one of three alternative “muscle burn criteria”. These were (1) specific work held constant, (2) power density held constant and (3) muscle mass held constant, i.e. no muscle consumed. Holding the specific work constant produced results in the best agreement with the results of other studies. This criterion was therefore selected to compare simulated flights of three very different species whose flight and migrations have been extensively studied, (1) Thrush Nightingale (Luscinia luscinia), (2) Knot (Calidris canutus) and (3) Whooper Swan (Cygnus cygnus). The ratio of protein to fat consumed ranged from 0.19 to 0.36, depending mainly on the starting value assumed for the muscle fraction. Specific work and starting power density were much higher for the Whooper Swan than for the two smaller species, suggesting that the latter have power to spare for climbing to high cruising altitudes, whereas the swan has not. If all three species were able to reach high cruising altitudes, the result would be a large reduction in journey time, which in turn would result in a small increase in range, due to a saving of energy required for basal metabolism. On current assumptions, the proportion of the fuel energy spent on basal metabolism would be eight times higher in the Thrush Nightingale than in the Whooper Swan, consequently the gain in range due to flying high would be greater in the smaller bird. In order to run the simulation, assumptions have been made at the primary physical level, to calculate the mechanical power required, and also at the secondary physiological level, to convert this into fuel consumption. The physical assumptions mostly take the form of variables whose existence is not in doubt, but whose values are poorly known, whereas in the case of some of the most important physiological variables, even the principles are unknown. Attention is drawn to a number of problems in need of attention, including (1) the mass and energy requirements of respiratory and circulatory organs required to sustain aerobically a given level of mechanical power; (2) the capabilities of bird lungs at high altitudes; (3) the possibility that heart muscle and lung tissue may be consumed in flight; (4) the two “biological constants”, isometric force per myosin fibril and inverse power density of mitochondria; (5) the energy density of different fuels, and the conversion efficiency of the flight muscles; and (6) the manner in which basal metabolism combines with other demands for power in an exercising animal.

Correlation of Flight-Muscle Size and Body Mass in Cooper’s Hawks: A Natural Analogue of Power Training

ABSTRACT Muscle hypertrophy in response to increased load (e.g. power training) is well documented in laboratory animals and in man (see, for example, Thorstensson, 1976; Gonyea, Ericson & Bonde-Peterson, 1977), but this phenomenon has not been quantitatively linked to changes in the use of muscles by wild animals. In free-living animals, and sometimes even in those used in laboratory studies, predicting the stress placed on an individual muscle is difficult. Thus, evaluating a compensatory response in relation to a change in muscle use is also difficult. The flight muscles of birds, however, represent a system in which changes in muscle size can be quantitatively compared to the power output required for flight. We describe here a correlation of flight-muscle mass with body mass in Cooper’s hawks (Accipiter cooperii). We believe this correlation represents a natural analogue of power training. The variation in muscle mass between individuals can be directly related to differences in the power requirements for flight caused by differences in body mass.

Interactions among carnosine, anserine, ophidine and copper in biochemical adaptation

Recent findings indicate that carnosine, anserine and ophidine should chelate copper in the tissues where these dipeptides are present in high concentration. The observations that carnosine, anserine and ophidine are located in skeletal muscles exhibiting active oxidative metabolism and/or glycolysis and that their accumulation appears to occur ontogenetically at the same time as these tissues begin to function suggests that these dipeptides may be involved in the intracellular transport of copper for activation of cytochrome oxidase at the end of the electron transport chain and in the regulation of anaerobic glycolysis. This hypothesis provides explanations for the presence of ophidine in the skeletal muscle of whale, the presence of anserine in the flight muscles of birds, the regulatory mechanism that permits orderly replacement of the primary olfactory neuron within the nasal olfactory epithelium, and the high activity of carnosinase in the uterus.