Comparative skeletal muscle fibre morphometry among wild birds with different locomotor behaviour (original) (raw)
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Descriptive and functional morphometry of skeletal muscle fibres in wild birds
Canadian Journal of Zoology, 1999
The fibre types of four forelimb and two hind-limb muscles involved in locomotion were morphometrically analyzed in three species of wild birds: the mallard (Anas platyrhynchos), common coot (Fulica atra), and yellowlegged gull (Larus cachinnans). Fibre cross-sectional area and perimeter, maximal diffusion distance, and number of capillaries per fibre were measured and the functional implications and physiological demands of the muscles of each species were inferred. In general, all morphometric values were lower in oxidative fibres than in anaerobic fibres, indicating that the supply of oxygen and metabolites available to aerobically working muscles is enhanced. The lower level of activity required during gliding as opposed to flapping flight, and the need to maintain the wings in an outstretched position, presumably by means of isometric contractions, may explain the greater size of the oxidative fibres of the pectoralis and scapulotriceps muscles of the gull. In contrast, the high oxidative demand imposed on mallards and coots by sustained flapping flight is met by small oxidative fibres, possibly at the expense of a reduction in the ability of each fibre to generate force. Anaerobic fibres of the gastrocnemius muscle had greater cross-sectional areas in the mallard and coot than in the gull. This is interpreted as an adaptive response to force generation during burst locomotion, which is usually performed by both mallards and coots, in sharp contrast to the buoyant swimming and postural activities undertaken by gull's legs. The fast oxidative fibres of the gastrocnemius muscle were, in general, larger than those of the iliotibialis muscle in the three species, which matches the different mechanical and functional roles of these muscles during swimming. Résumé : Les types de fibres dans les muscles responsables de la locomotion, quatre muscles des membres antérieurs et deux muscles des membres postérieurs, ont fait l'objet d'une analyse morphométrique chez trois espèces d'oiseaux en nature, le Canard colvert (Anas platyrhynchos), la Foulque macroule (Fulica atra) et le Goéland leucophée (Larus cachinnans). La surface des fibres en coupe transversale, leur périmètre, les distances maximales de diffusion et le nombre de capillaires par fibre ont été mesurés et ces mesures ont permis de déduire les conditions de fonctionnement, de même que les besoins physiologiques des muscles de chaque espèce. En général, toutes les mesures morphométriques se sont avérées plus basses dans les fibres oxydatives que dans les fibres anaérobies, ce qui indique que la quantité d'oxygène et de métabolites fournie aux muscles à fonctionnement aérobie est supérieure. L'activité moins importante reliée au vol plané par opposition au vol avec battements d'ailes et la nécessité de maintenir les ailes étendues, probablement par l'intermédiaire de contractions isométriques, explique probablement la taille plus grande des fibres oxydatives du pectoralis et des scapulotriceps chez le goéland. En revanche, le besoin important d'oxygène pour assurer le battement des ailes chez le colvert et la foulque est fourni par les fibres oxydatives de petite taille, ce qui se traduit probablement par une diminution de la force que peut générer chaque fibre. Chez le Canard colvert et chez la foulque, les fibres anaérobies du gastrocnémien ont une surface plus grande en coupe transversale que celles du goéland. Il semble qu'il s'agisse là d'une adaptation au déploiement d'une force au cours d'un déplacement subit, une tactique utilisée couramment par le colvert et la foulque, tactique totalement différente de la nage par flottaison et des activités reliées à la posture associées aux pattes du goéland. Les fibres oxydatives rapides du gastrocnémien sont en général plus grosses que celles du muscle iliotibialis chez les trois espèces, ce qui correspond aux rôles mécanique et fonctionnel de ces muscles au cours de la nage.
Fiber type homogeneity of the flight musculature in small birds
Comparative Biochemistry and Physiology B-biochemistry & Molecular Biology, 2009
Studies of medium- and large-bodied avian species have suggested that variation in flight muscle composition is related to differences in flight behavior. For example, slow-twitch or tonic fibers are generally found only in the flight muscles of non-volant or soaring/gliding birds. However, we know comparatively little about fiber composition of the muscles of the smallest birds. Here we describe the fiber composition of muscles from the wings, shoulders, and legs of two small avian species, which also display very high wingbeat frequencies: Anna's hummingbirds (Calypte anna) and zebra finches (Taeniopygia guttata). All flight muscles examined in both species contained exclusively fast oxidative glycolytic (FOG) fibers. These unique results suggest that fast oxidative fibers are both necessary and sufficient for the full range of flight behaviors in these small-bodied birds. Like all other studied birds, the zebra finch gastrocnemius, a tarsometatarsal extensor, contained a mixture of FOG (27.1%), slow oxidative (SO, 12.7%), and fast glycolytic (FG, 60.2%) fibers. By contrast, the hummingbird gastrocnemius lacked FG fibers (85.5% FOG, 14.5% SO), which may reflect the reduced role of the hindlimb during take-off. We further hypothesize that thermogenic requirements constrain fiber type heterogeneity in these small endothermic vertebrates.
Innervation Distribution Pattern, Nerve Ending Structure, and Fiber Types in Pigeon Skeletal-Muscle
Anatomical Record, 1993
Six muscles of the mallard duck (Anas platyrhynchos), the common coot (Fulica atra) and the yellow-legged gull (Larus cachinnans) were analysed morphometrically, with special emphasis on their functional implications and physiological needs. Oxidative fibres always had significantly smaller size than anaerobic fibres, although no differences in the number of capillaries per fibre were found. This resulted in greater capillary counts per unit of fibre area and perimeter in oxidative than anaerobic fibres, which indicates that the greater demand for oxygen supply may be achieved by decreasing the size of the muscle fibre rather than by increasing the number of associated capillaries. Fast oxidative fibres of the pectoralis and the triceps of the gull had greater sizes than the fast oxidative fibres of the mallard and the coot, which correlates with the difference in energetic demands between flapping and gliding flight. Greater fibre cross-sectional areas and perimeters seem suited to afford the long-lasting activity with low metabolic demands required during gliding. By contrast, mallards and coots attain a high oxidative metabolism, during sustained flapping flight, by reducing fibre size at the expense of a diminished ability for force generation. Between-species comparisons of the hindlimb muscles only yielded differences for the anaerobic fibres of the gastrocnemius, as an important adaptive response to force generation during burst locomotion. The need to manage sustained swimming abilities effectively may result in similar FOG fibre morphometry of the hindlimb muscles studied, indicating that a compromise between the oxygen flux to the muscle cell and the development of power is highly optimised in oxidative fibres of the bird species studied.
Journal of Morphology, 2000
Twenty-three species within the avian family Alcidae are capable of wing-propelled flight in the air and underwater. Alcids have been viewed as Northern Hemisphere parallels to penguins, and have often been studied to see if their underwater flight comes at a cost, compromising their aerial flying ability. We examined the anatomy and histochemistry of select wing muscles (Mm. pectoralis, supracoracoideus, latissimus dorsi caudalis, coracobrachialis caudalis, triceps scapularis, and scapulohumeralis caudalis) from Atlantic puffins (Fratercula arctica) to assess if the muscle fiber types reveal the existence of a compromise associated with "dual-medium" flight. Pectoralis was found to be proportional in size with that of nondiving species, although the supracoracoideus was proportionally larger in puffins. Muscle fiber types were largely aerobic in both muscles, with two distinct fasttwitch types demonstrable: a smaller, aerobic, moderately glycolytic population (FOg), and a larger, moderately aerobic, glycolytic population (FoG). The presence of these two fiber types in the primary flight muscles of puffins suggests that aerial and underwater flight necessitate a largely aerobic fiber complement. We suggest that alcids do not represent an adaptive compromise, but a stable adaptation for wing-propelled locomotion both in the air and underwater.
Ratios, adaptations, and the differential metabolic capability of avian flight muscles
Journal of Avian Biology, 2014
The eared grebe Podiceps nigricollis shows seasonal variation in the relative size of the major flight muscles that lift and lower the wing: respectively, supracoracoideus (s) and pectoralis (p). S/p ratios are low (≈0.07-0.12) when grebes are in flying condition, higher (≈0.11-0.15) when staging and flightless, and extreme (to 0.29) when starving. Shifts were driven by changes in the protein content in the pectoralis; intramuscular fat had little effect. S/p ratios also vary seasonally in the red knot Calidris canutus and are higher in birds newly arrived in breeding areas than at other times. If that increase was an adaptive response to promote wing-lifting in association with various breeding behaviors as suggested, one would expect it to result from an absolute increase in the post-arrival size of the supracoracoideus, which was not observed. Instead, we propose that it is unrelated to enhancing the upstroke but results from a decrease in the size of the pectoralis, which is a consequence of the greater rate at which this muscle is catabolized in times of exertion and stress, as at the end of a long migration or during starvation. Fuller data on the size, morphology and physiology of individual muscles at various stages of the annual cycle and migration will help to clarify how ratio changes are achieved, and evaluate potential adaptive significance.
Increased fiber capillarization in flight muscle of finch at altitude
Respiration Physiology, 1998
We examined fiber capillarization and ultrastructure in the highly aerobic flight muscle of six gray crowned rosy finches (Leucosticte arctoa; mass 22.99 0.5 (SE) g) living at altitude (A; White Mountains of Eastern California; 4000 m) compared to eight sea-level (SL) house finches (Carpodacus mexicanus, mass, 19.8 9 0.6 g) of the same subfamily, Carduelinae. Capillary length per fiber volume (A, 10 400 9 409 mm − 2 ; SL, 75139 423; P B0.001) and capillary-tofiber ratio (A, 2.32 90.07; SL, 1.85 90.06; PB0.001) were significantly greater in A, with no difference in fiber cross-sectional area compared to SL. Capillary geometry was significantly different in A, yielding a greater contribution of tortuosity and branching to capillary length than in SL. Capillary-to-fiber surface ratio and fiber mitochondrial volume were both greater in A, but their ratio was similar to SL, indicating a proportional increase in the size of the capillary to fiber interface and fiber mitochondrial volume in A to sustain high levels of aerobic capacity while living at altitude.
Journal of Morphology, 2008
Birds utilize one of two hindlimb postures during flight: an extended posture (with the hip and knee joints flexed, while the ankle joint is extended caudally) or a flexed posture (with the hip, knee, and ankle joints flexed beneath the body). American Avocets (Recurvirostra americana) and Black-necked Stilts (Himantopus mexicanus) extend their legs caudally during flight and support them for extended periods. Slow tonic and slow twitch muscle fibers are typically found in muscles functioning in postural support due to the fatigue resistance of these fibers. We hypothesized that a set of small muscles composed of high percentages of slow fibers and thus dedicated to postural support would function in securing the legs in the extended posture during flight. This study examined the anatomy and histochemical profile of eleven hindlimb muscles to gain insight into their functional roles during flight. Contrary to our hypothesis, all muscles possessed both fast twitch and slow twitch or slow tonic fibers. We believe this finding is due to the versatility of dynamic and postural functions the leg muscles must facilitate, including standing, walking, running, swimming, and hindlimb support during flight. Whether birds use an extended or flexed hindlimb flight posture may be related to the aerodynamic effect of leg position or may reflect evolutionary history.
Journal of Anatomy, 2019
During flight, birds employ one of two hindlimb postures. Perching birds utilize a flexed posture with their folded legs tucked beneath the body, whereas shorebirds and raptors use an extended posture with straightened legs trailing behind the body. Maintenance of either posture during flight requires the hindlimbs to hold their position for prolonged periods. Slow contracting fibers are known for their fatigue-resistant properties and are often found in high percentages in muscles utilized for postural actions. Given the similar actions required of the hip and knee flexors used during flight, we hypothesized that the equivalent postural muscles of perching birds (flexed posture) would contain similar percentages of slow fibers as shorebirds (extended posture). We investigated the anatomy and fiber type composition of seven hindlimb muscles in yellow-headed and red-winged blackbirds and revealed that they possess a smaller percentage of slow fibers than we found previously in the same muscles of American avocets and black-necked stilts. The comparably smaller body size of yellow-headed and red-winged blackbirds could mitigate the need for more slow fibers. In addition, the biomechanical placement of the weight force in the flexed posture may require less muscle force for postural support during flight and, therefore, fewer slow fibers.
Rapid Atrophy and Hypertrophy of an Avian Flight Muscle
The Auk, 1990
A•3STRACT.-Eared Grebes (Podiceps nigricollis) use Mono Lake in eastern California as a rest stop during spring migration. Some nonbreeders remain for the summer, and in the autumn the lake becomes a staging area that may accommodate 750,000 returning breeders and young of the year. There the birds become obese by feeding on invertebrates and, if they have not already done so, molt. Most grebes remain several months until a decline in prey populations stimulates further migration. During this period the birds become flightless, and the flight muscles may lose up to 50% of their mass. Myofibers from atrophic birds show evidence of mitochondrial division (or fusion). Even severely atrophic fibers retain a high mitochondrial density (27% vs. 33% in migratory condition), so that relative volume remains stable although absolute volume is reduced. In contrast, intracellular triglyceride droplets are extremely sparse in atrophic fibers, even though most of the birds are carrying >200 g of subcutaneous fat. Mean myofiber diameter increases and decreases with atrophy and hypertrophy. In late autumn, as food availability declines, the birds engage in conspicuous flapping exercises. In the same period, intracellular lipid reappears in the muscles. Within several weeks the muscles are rebuilt to full size and the grebes emigrate. The benefits, if any, of this cycle of muscle atrophy and concomitant obesity, followed by muscle hypertrophy and weight loss, remain obscure.
Capillary-to-fiber geometry and mitochondrial density in hummingbird flight muscle
Respiration physiology, 1992
We investigated structural characteristics for high O2 flux in hummingbird flight muscle, i.e. the most O2 demanding skeletal muscle per unit tissue mass among vertebrates. Pectoralis and supracoracoideus muscles of 3-4 g hummingbirds (Selaphorus rufus) were perfusion fixed in situ, processed for electron microscopy and analyzed by morphometry. Small fiber size (group mean +/- SE, 201 +/- 14 microns 2 at 2.1 microns sarcomere length), large capillary length per fiber volume (8947 +/- 869 mm-2) and high mitochondrial volume density per volume of muscle fiber (34.5 +/- 0.9%) were characteristic features of the muscles. Considering capillary supply and mitochondrial volume on an individual fiber basis showed that the size of the capillary-to-fiber interface (i.e. capillary surface per fiber surface) was also high in the muscles. Comparison with mammalian hindlimb pointed to a major role of the size of the capillary-to-fiber interface in providing a great potential for O2 flux rate from...