Ratios,adaptations, and the differential metabolic capability of avian flight muscles

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.     

Myoglobin levels and mATPase activity in pectoral muscles of spruce and ruffed grouse (Aves: Tetraoninae)

Myoglobin concentration and myosin ATPase activity were measured in the pectoral muscle of wild spruce grouse (Dendragapus canadensis) and ruffed grouse (Bonasa umbellus), together with the weight of the Mm. pectoralis, supracoracoideus and heart. mATPase activities were similar in both species, but spruce grouse contained 15 times more myoglobin in the pectoralis muscle and the heart was three times heavier than that of the ruffed grouse. The relative mass of the flight muscles and wing loading were similar between species. Characteristics of the pectoral muscle of both grouse species reflect adaptations to predation and advertising displays. The glycolytic nature of the ruffed grouse pectoral muscle and small heart size is an adaptation to a sedentary existence within a small home range. The more oxidative pectoral muscle of spruce grouse together with its larger heart are adaptations to seasonal dispersals requiring more sustained flight.     

Fibre types in primary ‘flight’ muscles of the African Penguin (Spheniscus demersus)

The African penguin (Spheniscus demersus) is an endangered seabird that resides on the temperate southern coast of Africa. Like all penguins it is flightless, instead using its specialized wings for underwater locomotion termed ‘aquatic flight’. While musculature and locomotion of the large Antarctic penguins have been well studied, smaller penguins show different biochemical and behavioural adaptations to their habitats. We used histochemical and immunohistochemical methods to characterize fibre type composition of the African penguin primary flight muscles, the pectoralis and supracoracoideus. We hypothesized the pectoralis would contain predominantly fast oxidative–glycolytic (FOG) fibres, with mainly aerobic subtypes. As the supracoracoideus and pectoralis both power thrust, we further hypothesized these muscles would have a similar fibre type complement. Our results supported these hypotheses, also showing an unexpected slow fibre population in the deep parts of pectoralis and supracoracoideus. The latissimus dorsi was also examined as it may contribute to thrust generation during aquatic flight, and in other avian species typically contains definitive fibre types. Unique among birds studied to date, the African penguin anterior latissimus dorsi was found to consist mainly of fast fibres. This study shows the African penguin has specialized flight musculature distinct from other birds, including large Antarctic penguins.     

Geographical variation of protein reserves in birds: the pectoral muscle mass of Dunlins Calidris alpina in winter

Pectoral muscle size (as an index of protein reserves) was measured in Dunlins during midwinter on five British estuaries, and examined in relation to latitude and midwinter air temperature. In adults, pectoral muscle size was greater on more northerly and colder estuaries. Pectoral muscle size of juveniles varied less than that of adults between estuaries. For both ages, pectoral muscle size correlations were stronger with temperature than with latitude. The size of protein reserves in the pectoral muscles differed by 26% (adults) and 14% (juveniles) between warmest (Menai Straits) and coldest (Firth of Forth) sites studied. Both pectoralis major and supracoracoideus muscles contributed to the protein store, but the supracoracoideus formed only 12% of the total pectoral muscle mass. The age-difference appeared not to arise through the selective death of some juveniles. We propose that juveniles have a set-point for pectoral muscle size in winter adapted to the broad geographical area within which they may settle. The set-point may then be altered according to the weather conditions experienced at the site where they settle and return as adults.     

Anatomy and histochemistry of flight muscles in a wing-propelled diving bird, the Atlantic puffin, Fratercula arctica

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 fast-twitch 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.     

Gliding flight in the American Kestrel (Falco sparverius): An electromyographic study

Electromyographic (EMG) activity was studied in American Kestrels (Falco sparverius) gliding in a windtunnel tilted to 8 degrees below the horizontal. Muscle activity was observed in Mm. biceps brachii, triceps humeralis, supracoracoideus, and pectoralis, and was absent in M. deltoideus major and M. thoracobrachialis (region of M. pectoralis). These active muscles are believed to function in holding the wing protracted and extended during gliding flight. Quantification of the EMG signals showed a lower level of activity during gliding than during flapping flight, supporting the idea that gliding is a metabolically less expensive form of locomotion than flapping flight. Comparison with the pectoralis musculature of specialized gliding and soaring birds suggests that the deep layer of the pectoralis is indeed used during gliding flight and that the slow tonic fibers found in soaring birds such as vultures represents a specialization for endurant gliding. It is hypothesized that these slow fibers should be present in the wing muscles that these birds use for wing protraction and extension, in addition to the deep layer of the pectoralis. © 1993 Wiley-Liss, Inc.     

Phenotypic flexibility of body composition associated with seasonal acclimatization in passerine birds

Improved winter cold tolerance is widespread among small birds overwintering in cold climates and is associated with improved shivering endurance and elevated summit metabolic rate (M_sum). Phenotypic flexibility resulting in elevated M_sum could result from either increased skeletal muscle mass (perhaps with support from similar adjustments in “nutritional organs”) and/or cellular metabolic intensity. We investigated seasonal changes in body composition of three species of passerine birds resident in cold winter climates, all of which show large seasonal variations in M_sum (>25%); white-breasted nuthatch (Sitta carolinensis), black-capped chickadee (Poecile atricapillus), and house sparrow (Passer domesticus). All three species displayed significant winter increases in pectoralis and heart masses, and supracoracoideus mass also increased in winter chickadees. Gizzard mass increased in winter for all three species, but masses of other nutritional organs did not vary consistently with season. These data suggest that winter increases in pectoralis and heart masses are important contributors to elevated thermogenic capacity and cold tolerance, but seasonal variation in nutritional organ masses, other than gizzard, which is likely associated with dietary changes, are not universally associated with seasonal phenotypes. The winter increases in pectoralis and heart masses are consistent with data from other small passerines showing marked seasonal changes in cold tolerance and support the Variable Maximum Model of seasonal phenotypic flexibility, where physiological adjustments that promote improved cold tolerance, also result in elevated M_sum.     

The morphological development of the locomotor and cardiac muscles of the migratory barnacle goose (Branta Leucopsis)

The masses of the locomotor and acardiac muscles of wild barncale goose gollings, from migratory population, were examined systematically during development and their values compared to those of pre-migratory geese. Pre-flight development was typified by approximately linear increases of body, leg, and heart ventricular mass with respect to age. Flight muscle showed an exponential increase in mass. Pectoralis muscle mass was 14.2 ± 0.3% of body mass (1297 ± 73g, n=7) in early flying goslings compared to 16.6 ± 0.3% of body mass (2318 ± 109g, n=8) in pre-migratory geese. Post-flight development was typified by stasis of leg muscle mass but hypertrophy of Ventricular and pectoralis muscle mass in proportion to body mass. Ventricular mass relative to body mass showed the lowest values at 5 weeks of age (0.62 ± 0.01%) with peak values at 1 week of age (10.4 ± 0.04%). The latter may be associated with both requirements of thermoregualation in these precocial, arctic breeding geese and the need to forage approximately 24 hours post-hatch. Peak values for leg muscle mass, relative to body mass, were found at 3 weeks of age (12.7 ± 0.36%), with lowest values in the pre-migratory geese (6.7 ± 0.21%), while peak values for pectoralis muscle mass were expressed in the premigratory geese with lowest values at 1 week of age (0.94 ± 0.07%). Ventricular mass was proportional to leg muscle mass up to 5 weeks of age (M_v= 0.38M_t^0.68, r²=0.95), but subsequent increase in ventricular mass was proportional to pectoralis muscle mass (M_v= 0.25M_p^0.73, r²= 0.81).     

Ontogeny of flight in the little brown bat,Myotis lucifugus: behavior,morphology, and muscle histochemistry

Summary Postnatal changes in wing morphology, flight ability, muscle morphology, and histochemistry were investigated in the little brown bat, Myotis lucifugus. The pectoralis major, acromiodeltoideus, and quadriceps femoris muscles were examined using stains for myofibrillar ATPase, succinate dehydrogenase (SDH), and mitochondrial -glycerophosphate dehydrogenase (-GPDH) enzyme reactions. Bats first exhibited spontaneous, drop-evoked flapping behavior at 10 days, short horizontal flight at 17 days, and sustained flight at 24 days of age. Wing loading decreased and aspect ratio increased during postnatal development, each reaching adult range before the onset of sustained flight. Histochemically, fibers from the three muscles were undifferentiated at birth and had lower oxidative and glycolytic capacities compared to other age groups. Cross-sectional areas of fibers from the pectoralis and acromiodeltoideus muscles increased significantly at an age when dropevoked flapping behavior was first observed, suggesting that the neuromuscular mechanism controlling flapping did not develop until this time. Throughout the postnatal growth period, pectoralis and acromiodeltoideus muscle mass and fiber cross-sectional area increased significantly. By day 17 the pectoralis muscle had become differentiated in glycolytic capacity, as indicated by the mosaic staining pattern for -GPDH. By contrast, the quadriceps fibers were relatively large at birth and slowly increased in size during the postnatal period. Fiber differentiation was evident at the time young bats began to fly, as indicated by a mosaic pattern of staining for myosin ATPase. These results indicate that flight muscles (pectoralis and acromiodeltoideus) are less well developed at birth and undergo rapid development just before the onset of flight. By contrast the quadriceps femoris muscle, which is required for postural control, is more developed at birth than the flight muscles and grows more slowly during subsequent development.     

Anatomy and histochemistry of spread-wing posture in birds. 3. Immunohistochemistry of flight muscles and the "shoulder lock" in albatrosses

As a postural behavior, gliding and soaring flight in birds requires less energy than flapping flight. Slow tonic and slow twitch muscle fibers are specialized for sustained contraction with high fatigue resistance and are typically found in muscles associated with posture. Albatrosses are the elite of avian gliders; as such, we wanted to learn how their musculoskeletal system enables them to maintain spread-wing posture for prolonged gliding bouts. We used dissection and immunohistochemistry to evaluate muscle function for gliding flight in Laysan and Black-footed albatrosses. Albatrosses possess a locking mechanism at the shoulder composed of a tendinous sheet that extends from origin to insertion throughout the length of the deep layer of the pectoralis muscle. This fascial "strut" passively maintains horizontal wing orientation during gliding and soaring flight. A number of muscles, which likely facilitate gliding posture, are composed exclusively of slow fibers. These include Mm. coracobrachialis cranialis, extensor metacarpi radialis dorsalis, and deep pectoralis. In addition, a number of other muscles, including triceps scapularis, triceps humeralis, supracoracoideus, and extensor metacarpi radialis ventralis, were found to have populations of slow fibers. We believe that this extensive suite of uniformly slow muscles is associated with sustained gliding and is unique to birds that glide and soar for extended periods. These findings suggest that albatrosses utilize a combination of slow muscle fibers and a rigid limiting tendon for maintaining a prolonged, gliding posture.     

Morphology, Velocity, and Intermittent Flight in Birds

Body size, pectoralis composition, aspect ratio of the wing,and forward speed affect the use of intermittent flight in birds.During intermittent non-flapping phases, birds extend theirwings and glide or flex their wings and bound. The pectoralismuscle is active during glides but not during bounds; activityin other primary flight muscles is variable. Mechanical power,altitude, and velocity vary among wingbeats in flapping phases;associated with this variation are changes in neuromuscularrecruitment, wingbeat frequency, amplitude, and gait. Speciesof intermediate body mass (35–158 g) tend to flap-glideat slower speeds and flap-bound at faster speeds, regardlessof the aspect ratio of their wings. Such behavior may reducemechanical power output relative to continuous flapping. Smallerspecies (<20 g) with wings of low aspect ratio may flap-boundat all speeds, yet existing models do not predict an aerodynamicadvantage for the flight style at slow speeds. The behaviorof these species appears to be due to wing shape rather thanpectoralis physiology. As body size increases among species,percent time spent flapping increases, and birds much largerthan 300 g do not flap-bound. This pattern may be explainedby adverse scaling of mass-specific power or lift per unit poweroutput available from flight muscles. The size limit for theability to bound intermittently may be offset somewhat by thescaling of pectoralis composition. The percentage of time spentflapping during intermittent flight also varies according toflight speed.     

Post-hatching growth and development of the pectoral and pelvic limbs in the black noddy, Anous minutus

The black tern (Anous minutus) uses a semi-precocial growth strategy. Terrestrial locomotor capacity occurs soon after hatching, but pectoral limb development is delayed and flight is not possible until about post-hatching day 50. A growth series (hatchlings to fledglings) was used to explore how limb musculoskeletal development varied with body mass. In the pelvic limb, bone lengths scaled isometrically or with negative allometry. Gastrocnemius muscle mass and the failure load and stiffness of the tibiotarsus scaled isometrically. In the pectoral limb, pectoralis and supracoracoideus muscle masses increased with strong positive allometry that was mirrored by increases in wing bone strength and stiffness. Bending strength (sigma(ult)) and modulus (E) remained fairly constant throughout development to fledging for all limb bones. The moment of inertia (I) scaled with negative allometry for the tibiotarsus and with strong positive allometry in the wing bones. Differences in sigma(ult) and E of the tibiotarsus between pre-fledged chicks and adults was due, primarily, to increases in bone density rather than increases in the moment of inertia of the skeletal elements, whereas sigma(ult) of wing bones was a function of increases in both bone density and I. Early development of functional pelvic limbs in tree-nesting birds is relatively unusual, and presumably reflects a familial trait that does not appear to compromise breeding success in this species.     

Post-hatching growth and development of the pectoral and pelvic limbs in the black noddy, Anous minutus.

The black tern (Anous minutus) uses a semi-precocial growth strategy. Terrestrial locomotor capacity occurs soon after hatching, but pectoral limb development is delayed and flight is not possible until about post-hatching day 50. A growth series (hatchlings to fledglings) was used to explore how limb musculoskeletal development varied with body mass. In the pelvic limb, bone lengths scaled isometrically or with negative allometry. Gastrocnemius muscle mass and the failure load and stiffness of the tibiotarsus scaled isometrically. In the pectoral limb, pectoralis and supracoracoideus muscle masses increased with strong positive allometry that was mirrored by increases in wing bone strength and stiffness. Bending strength (sigma(ult)) and modulus (E) remained fairly constant throughout development to fledging for all limb bones. The moment of inertia (I) scaled with negative allometry for the tibiotarsus and with strong positive allometry in the wing bones. Differences in sigma(ult) and E of the tibiotarsus between pre-fledged chicks and adults was due, primarily, to increases in bone density rather than increases in the moment of inertia of the skeletal elements, whereas sigma(ult) of wing bones was a function of increases in both bone density and I. Early development of functional pelvic limbs in tree-nesting birds is relatively unusual, and presumably reflects a familial trait that does not appear to compromise breeding success in this species.     

Effects of the sex-linked dwarf gene (dw) on the expression of the muscular dystrophy gene (am) in chicken.

The sex-linked dwarf gene (dw) was introduced into companion muscular dystrophic (am) and nondystrophic (Am+) New Hampshire chicken lines to investigate influences of the dwarf gene on breast muscle weights, muscle fiber area, and the histological expression of muscular dystrophy. Dystrophic and nondystrophic chickens within dwarf or nondwarf genotypes were similar in body and carcass weights. Pectoralis and supracoracoideus muscle weights (as a percentage of adjusted carcass weight) were similar in nondystrophic dwarf and nondwarf males and females. In addition, pectoralis weight was similar in dystrophic dwarf males and dystrophic nondwarf males and females. However, pectoralis weight was significantly smaller in dystrophic dwarf females than in dystrophic nondwarf females, whereas supracoracoideus weight was significantly larger in dystrophic dwarf males than in dystrophic nondwarf males. Supracoracoideus weight was similar in dystrophic dwarf males and females and dystrophic nondwarf females. Pectoralis muscle fiber area was influenced by sex and by dwarf and dystrophy genotype. Muscle fiber area was larger in females than in males, smaller in dwarfs than in nondwarfs, and smaller in dystrophic than in nondystrophic muscles. Muscle fiber degeneration and adipose infiltration was more extensive in dystrophic than in nondystrophic females and males, and it was more advanced in dwarfs than in nondwarfs. Excessive acetylcholinesterase staining patterns were characteristic of dystrophic muscle in both dwarf and nondwarf genotypes. Nondystrophic and dystrophic dwarf male and female chickens are comparable substitutes for nondwarfs as biomedical models with respect to pectoralis histology, acetylcholinesterase staining pattern, and pectoralis muscle hypertrophy.     

Comparative histology, histochemistry and innervation of striated muscle fibers of the greater pectoralis muscle and supracoracoid muscle in birds

The morphology of the pectoralis major muscle and the supracoracoideus muscle was compared in three Galliformes and five Passeriformes, in relation to partial behavioral characteristics. In all species, two fibres types are observed. The frequencies of these fibres are different, especially between Galliformes and Passeriformes, but also between Coturnix and other Galliformes. All fibres show phasic innervation. A relation of the extent between synaptic gutters and muscle activity is suggested.     

Influence of physical exercise after long-lasting hypodynamia on the morphological parameters of muscle fibers

The purpose of this research was morphometric ultrastructure evaluation of the fibers in muscles taking part in the flight of pigeons forced to exercise after a long period of hypodynamia. It was found that following physical exercise, after 12 and 18 months of mobility limitation, there appeared marked qualitative and quantitative changes: a diminution of the volume fraction and number of mitochondria, increase of smooth sarcoplasmic reticulum and sarcoplasm, and a significant decrease of the number of glycogen granules as compared with those after 18 months hypodynamia. The above described changes were more pronounced in the supracoracoideus than in the pectoralis muscle.     

Changes in myoglobin and lactate dehydrogenase in muscle tissues of a diving bird, the Pigeon Guillemot, during maturation

1. The concentration of myoglobin (Mb) and the isozymic distribution and activity of lactate dehydrogenase (LDH) in heart and pectoralis muscle were investigated at three stages of maturation of the Pigeon Guillemot, Cepphus columba. 2. Mb is not detectable in chick pectoralis; it is present in fledgling pectoralis muscle and increases four-fold in adult pectoralis. Mb concentration in heart muscle is similar in chick and fledgling and doubles in the adult. 3. LDH activities in pectoralis muscle of fledgling and adult increase to about three times that of the chick. LDH activities in heart of chick, fledgling and adult are similar to one another. 4. All five isozymes of LDH are present in both heart and pectoralis muscle at all stages; the heart muscle shows predominantly LDH-1 isozyme, and the pectoralis, LDH-5. The relative amounts of the five isozymes in the heart extract were constant during maturation but pectoralis LDH isozymes changed during maturation towards a more even distribution of the five isozymes in the adult. 5. Changes in Mb and LDH in the Pigeon Guillemot correlate with the animal's maturation from a sedentary nest sitter to an active diver and flyer. The adult pectoralis muscle probably has both aerobic function for wing-propelled short dives and flying and anaerobic capacity for longer dives.     

Histology, immunocytology, histochemistry and muscle fiber innervation of the pectoralis major and supracoracoideus muscles of Excalfactoria chinensis chinensis (L.)]

The morphology of the pectoralis major muscle and its antagonist, the supracoracoideus muscle, of the Chinese quail was studied in comparison with the Japanese quail, in relation to behavioral characteristics. The actomyosin ATPase reaction after alkaline and acid preincubation reveals two fibre types. The indirect immunofluorescence, using specific antibodies against 'slow' (twitch) myosin from the human vastus lateralis muscle, provokes a weak reaction. All fibres observed show focal, monoaxonal 'en plaques' endings, typical of the phasic motor system. For the two quail species, the muscle structure seems adequate in relation to the movement characteristics, meaning muscle activity of migratories, flying long distances.     

A histochemical comparison of fibre types in the M. pectoralis and M. supracoracoideus of the great skua Catharacta skua and the herring gull Larus argentatus with reference to kleptoparasitic capabilities

Skuas, which are closely related to gulls, frequently use a specialized feeding method (kleptoparasitism) by which they rob other seabirds of their food. This paper tests the idea that skuas have evolved as specialist kleptoparasites.
The fibre type composition of the M. pectoralis, M. supracoracoideus and M. iliofibularis of a great skua Catharacta skua (Brünn.) and a herring gull Larus argentatus (Pontopp.) was determined by three enzyme histochemical methods commonly used for mammalian fibre classification; the reactions for alphaGPDH, NADH-TR and mATPase activity.
In both species slow fibres were present only in the M. iliofibularis, and fast twitch glycolytic fibres were not present in any of the muscles. The M. pectoralis and M. supracoracoideus of both species consisted entirely of the fast twitch oxidative-glycolytic fibres.
The overall metabolic enzyme activities of the muscles were assessed in terms of the proportions of fibres with high, intermediate and low metabolic enzyme activity. The overall levels of oxidative and glycolytic enzyme activity were significantly higher in the M. pectoralis than in the M. supracoracoideus and significantly higher in both of these than in the M. iliofibularis. This was true of both species.
The oxidative and glycolytic activities of all three muscles of the great skua were significantly higher than those of the homologous muscles of the herring gull. This was particularly true of the M. pectoralis and M. supracoracoideus. It is suggested that this difference between great skuas and herring gulls enables the former to be more effective aerial kleptoparasites than the latter.     

Breeding biology of the Madagascar Paradise Flycatcher,Terpsiphone mutata,with special reference to plumage variation in males

This study was undertaken to understand the migratory strategies of the Dunlins (Calidris alpina) caught in Eilat, Israel, before and after they accomplish the crossing of the combined ecological barrier of the Sinai, Sahara and Sahel deserts. Between 1999–2001, a total of 410 adults and 342 juveniles were banded. The significant difference in mean wing length between birds caught in autumn and spring reflects the degree of abrasion of the outer primaries during over-wintering in Africa. Dunlins caught in Eilat in autumn and early winter had a mean wing length 1.4–1.9mm longer than in the spring. The rate of body mass increase was comparatively high and the mean body mass of the heaviest 10% of Dunlin at Eilat was 56.2g (SE ± 0.6, N = 80). The heaviest birds from Eilat carried on average about 10g of fat with a lipid index (fat mass as a percentage of total body mass) of 18%. These reserves allow a flight of approximately 1 000km, which is probably sufficient for continued migration to more southerly wintering grounds.