Ontogeny of sex differences in the energetics and kinematics of terrestrial locomotion in leghorn chickens (Gallus gallus domesticus).

Sex differences in locomotor performance may precede the onset of sexual maturity and/or arise concomitantly with secondary sex characteristics. Here, we present the first study to quantify the terrestrial locomotor morphology, energetics and kinematics in a species, either side of sexual maturation. In domestic leghorn chickens (Gallus gallus domesticus) sexual maturation brings about permanent female gravidity and increased male hind limb muscle mass. We found that the sexes of a juvenile cohort of leghorns shared similar maximum sustainable speeds, while in a sexually mature cohort maximum sustainable speeds were greater by 67% (males) and 34% (females). Furthermore, relative to that in juveniles of the same sex, the absolute duration of leg swing was longer in mature males and shorter in mature females. Consequently, the proportion of a stride that each limb was in contact with the ground (duty factor) was higher in sexually mature females compared to males. Modulation of the duty factor with the development of secondary sex characteristics may act to minimize mechanical work in males; and minimise mechanical power and/or peak force in females. A greater incremental response of mass-specific metabolic power to speed in males compared to females was common to both age cohorts and, therefore, likely results from physiological sexual dimorphisms that precede sexual maturation.

Kinematics and energetics of swimming performance during acute warming in brown trout Salmo trutta.

This study examined how acute warming of water temperature affects the mechanical efficiency of swimming and aerobic capabilities of the brown trout Salmo trutta. Swimming efficiency was assessed using the relationship between swimming kinematics and forward speed (U), which is thought to converge upon an optimum range of a dimensionless parameter, the Strouhal number (St ). Swim-tunnel intermittent stopped-flow respirometry was used to record kinematics and measure oxygen consumption (MO2) of S. trutta during warming and swimming challenges. Salmo trutta maintained St between 0·2 and 0·3 at any given U over a range of temperatures, irrespective of body size. The maintenance of St within the range for maximum efficiency for oscillatory propulsion was achieved through an increase in tail-beat frequency (ftail) and a decrease in tail-beat amplitude (A) as temperature increased. Maintenance of efficient steady-state swimming was fuelled by aerobic metabolism, which increased as temperature increased up to 18° C but declined above this temperature, decreasing the apparent metabolic scope. As St was maintained over the full range of temperatures whilst metabolic scope was not, the results may suggest energetic trade-offs at any given U at temperatures above thermal optima.

Locomotory abilities and habitat of the Cretaceous bird Gansus yumenensis inferred from limb length proportions.

The relative length proportions of the three bony elements of the pelvic (femur, tibiotarsus and tarsometatarsus) and pectoral (humerus, ulna and manus) limbs of the early Cretaceous bird Gansus yumenensis, a well-represented basal ornithuromorph from China, are investigated and compared to those of extant taxa. Ternary plots show that the pectoral limb length proportions of Gansus are most similar to Apodiformes (swifts and hummingbirds), which plot away from all other extant birds. In contrast, the pelvic limb length proportions of Gansus fall within the extant bird cluster and show similarities with the neornithine families Podicipedidae (grebes), Diomedeidae (albatross) and Phalacrocoracidae (cormorants). Although it does have some of the pelvic limb features of grebes and cormorants, the femur of Gansus is more gracile and is thus more consistent with an albatross-like shallow-diving mode of life than a strong foot-propelled diving movement pattern. The position of Gansus in pectoral limb ternary morphospace is largely due to its elongated manus. In contrast to apodiformes, where the humerus and ulna are short and robust, an adaptation, which provides a stiff wing for their demanding fast agile and hovering flight (respectively), the wing-bones of Gansus are slender, indicating a less vigorous flapping flight style. The suite of characters exhibited by Gansus mean it is difficult to completely interpret its likely ecology. Nevertheless, our analyses suggest that it is probable that this bird was both volant and capable of diving to some degree using either foot-propelled or, perhaps, both its wings and its feet for underwater locomotion.

Size scaling and stiffness of avian primary feathers: implications for the flight of Mesozoic birds.

The primary feathers of birds are subject to cyclical forces in flight causing their shafts (rachises) to bend. The amount the feathers deflect during flight is dependent upon the flexural stiffness of the rachises. By quantifying scaling relationships between body mass and feather linear dimensions in a large data set of living birds, we show that both feather length and feather diameter scale much closer to predictions for geometric similarity than they do to elastic similarity. Scaling allometry also indicates that the primary feathers of larger birds are relatively shorter and their rachises relatively narrower, compared to those of smaller birds. Two-point bending tests indicated that larger birds have more flexible feathers than smaller species. Discriminant functional analyses (DFA) showed that body mass, primary feather length and rachis diameter can be used to differentiate between different magnitudes of feather bending stiffness, with primary feather length explaining 63% of variance in rachis stiffness. Adding fossil measurement data to our DFA showed that Archaeopteryx and Confuciusornis do not overlap with extant birds. This strongly suggests that the bending stiffness of their primary feathers was different to extant birds and provides further evidence for distinctive flight styles and likely limited flight ability in Archaeopteryx and Confuciusornis.

The primary feather lengths of early birds with respect to avian wing shape evolution.

We examine the relationships between primary feather length (f(prim)) and total arm length (ta) (sum of humerus, ulna and manus lengths) in Mesozoic fossil birds to address one aspect of avian wing shape evolution. Analyses show that there are significant differences in the composition of the wing between the known lineages of basal birds and that mean f(prim) (relative to ta length) is significantly shorter in Archaeopteryx and enantiornithines than it is in Confuciusornithidae and in living birds. Based on outgroup comparisons with nonavian theropods that preserve forelimb primary feathers, we show that the possession of a relatively shorter f(prim) (relative to ta length) must be the primitive condition for Aves. There is also a clear phylogenetic trend in relative primary feather length throughout bird evolution: our analyses demonstrate that the f(prim)/ta ratio increases among successive lineages of Mesozoic birds towards the crown of the tree ('modern birds'; Neornithes). Variance in this ratio also coincides with the enormous evolutionary radiation at the base of Neornithes. Because the f(prim)/ta ratio is linked to flight mode and performance in living birds, further comparisons of wing proportions among Mesozoic avians will prove informative and certainly imply that the aerial locomotion of the Early Cretaceous Confuciusornis was very different to other extinct and living birds.

Evidence for energy savings from aerial running in the Svalbard rock ptarmigan (Lagopus muta hyperborea).

Svalbard rock ptarmigans were walked and run upon a treadmill and their energy expenditure measured using respirometry. The ptarmigan used three different gaits: a walking gait at slow speeds (less than or equal to 0.75 m s(-1)), grounded running at intermediate speeds (0.75 m s(-1) < U < 1.67 m s(-1)) and aerial running at high speeds (greater than or equal to 1.67 m s(-1)). Changes of gait were associated with reductions in the gross cost of transport (COT; J kg(-1) m(-1)), providing the first evidence for energy savings with gait change in a small crouched-postured vertebrate. In addition, for the first time (excluding humans) a decrease in absolute metabolic energy expenditure (rate of O(2) consumption) in aerial running when compared with grounded running was identified. The COT versus U curve varies between species and the COT was cheaper during aerial running than grounded running, posing the question of why grounded running should be used at all. Existing explanations (e.g. stability during running over rocky terrain) amount to just so stories with no current evidence to support them. It may be that grounded running is just an artefact of treadmill studies. Research investigating the speeds used by animals in the field is sorely needed.

Energetics and kinematics of walking in the barnacle goose (Branta leucopsis).

Barnacle geese were walked on a treadmill at speeds ranging from 0.25 to 1.25 ms(-1), which was their highest sustainable speed. No evidence for a gait change was found. The gait of a barnacle goose appears to conform to the classical pendulum mechanics based model of walking, with the kinetic energy of forward motion (horizontal kinetic energy, E(kh)) out-of-phase with the sum of the gravitational potential (E(p)), and vertical kinetic (E(kv)) energies of the centre of mass at all speeds. Why barnacle geese are unable to aerial run when other 'waddling' species do show an aerial phase (e.g., mallard ducks) is unclear. Presumably, however, it is likely to relate to the amount of lateral kinetic energy generated, which is a feature of 'waddling'. We predict that lateral kinetic energy generated by barnacle geese and other waddling species that cannot aerial run, is higher than in those that can. Due to competing selection pressures for swimming and flight, barnacle geese are mechanically and energetically inefficient walkers relative to more specialist cursorial birds. Their upper walking speed, however, appears to be limited by morphology (via kinematics) and not metabolic capacity (energetics).

The shape of pterosaur evolution: evidence from the fossil record.

Although pterosaurs are a well-known lineage of Mesozoic flying reptiles, their fossil record and evolutionary dynamics have never been adequately quantified. On the basis of a comprehensive data set of fossil occurrences correlated with taxon-specific limb measurements, we show that the geological ages of pterosaur specimens closely approximate hypothesized patterns of phylogenetic divergence. Although the fossil record has expanded greatly in recent years, collectorship still approximates a sigmoid curve over time as many more specimens (and thus taxa) still remain undiscovered, yet our data suggest that the pterosaur fossil record is unbiased by sites of exceptional preservation (lagerstätte). This is because as new species are discovered the number of known formations and sites yielding pterosaur fossils has also increased - this would not be expected if the bulk of the record came from just a few exceptional faunas. Pterosaur morphological diversification is, however, strongly age biased: rarefaction analysis shows that peaks of diversity occur in the Late Jurassic and Early Cretaceous correlated with periods of increased limb disparity. In this respect, pterosaurs appear unique amongst flying vertebrates in that their disparity seems to have peaked relatively late in clade history. Comparative analyses also show that there is little evidence that the evolutionary diversification of pterosaurs was in any way constrained by the appearance and radiation of birds.

An interspecific test of allen's rule: evolutionary implications for endothermic species.

Ecogeographical rules provide potential to describe how organisms are morphologically constrained to climatic conditions. Allen's rule (relatively shorter appendages in colder environments) remains largely unsupported and there remains much controversy whether reduced surface area of appendages provides energetic savings sufficient to make this morphological trend truly adaptive. By showing for the first time that Allen's rule holds for closely related endothermic species, we provide persuasive support of the adaptive significance of this trend for multiple species. Our results indicate that reduction of thermoregulatory cost during the coldest part of the breeding season is the most likely mechanism driving Allen's rule for these species. Because for 54% of seabird species examined, rise in seasonal maximum temperature over 100 years will exceed that for minimum temperatures, an evolutionary mismatch will arise between selection for limb length reduction and ability to accommodate heat stress.

Flight of Sharovipteryx mirabilis: the world's first delta-winged glider.

The 225 million-year-old reptile Sharovipteryx mirabilis was the world's first delta-winged glider; this remarkable animal had a flight surface composed entirely of a hind-limb membrane. We use standard delta-wing aerodynamics to reconstruct the flight of S. mirabilis demonstrating that wing shape could have been controlled simply by protraction of the femora at the knees, and by variation in incidence of a small forelimb canard. Our method has allowed us to address the question of how identifying realistic glide performance can be used to set limits on aerodynamic design in this small animal. Our novel interpretation of the bizarre flight mode of S. mirabilis is the first based directly on interpretation of the fossil itself and the first grounded in aerodynamics.

Limb disparity and wing shape in pterosaurs.

The limb proportions of the extinct flying pterosaurs were clearly distinct from their living counterparts, birds and bats. Within pterosaurs, however, we show that further differences in limb proportions exist between the two main groups: the clade of short-tailed Pterodactyloidea and the paraphyletic clades of long-tailed rhamphorhynchoids. The hindlimb to forelimb ratios of rhamphorhynchoid pterosaurs are similar to that seen in bats, whereas those of pterodactyloids are much higher. Such a clear difference in limb ratios indicates that the extent of the wing membrane in rhamphorhynchoids and pterodactyloids may also have differed; this is borne out by simple ternary analyses. Further, analyses also indicate that the limbs of Sordes pilosus, a well-preserved small taxon used as key evidence for inferring the extent and shape of the wing membrane in all pterosaurs, are not typical even of its closest relatives, other rhamphorhynchoids. Thus, a bat-like extensive hindlimb flight membrane, integrated with the feet and tail may be applicable only to a small subset of pterosaur diversity. The range of flight morphologies seen in these extinct reptiles may prove much broader than previously thought.

Scaling of body frontal area and body width in birds.

By analyzing a homogenous dataset we show, in contradiction to a previous study, that the scaling of body frontal area (S(b)) with body mass (m(b)) does not differ between passerine and nonpasserine birds. It is likely that comparison of data collected from live passerines with data collected from frozen nonpasserines had led to the incorrect conclusion that the scaling of S(b) varied between the taxa. We suggest that body dimensions collected from frozen specimens, or specimens stored in alcohol, are not applicable to live birds, and that both the current equations presented in the literature for predicting S(b) from m(b) may lead to inaccurate estimates. Using data from preserved specimens, we found that S(b) scales isometrically with m(b) (S(b) proportional, variant m(b) (0.66)), and therefore we found no evidence for larger birds being more streamlined than smaller birds. S(b) scales with negative allometry against wingspan (b), however, and b scales with positive allometry against m(b), so larger birds have smaller S(b) relative to b. In addition, it appears that dorsoventral flattening of the body is a general characteristic of bird's bodies but that it is more pronounced in larger birds, suggesting perhaps a function in terms of increased lift during forward flight. It appears that bird's bodies obey the surface-to-area geometric scaling law, but bird body shape may vary in relation to aerodynamic function. We suggest that a large-scale study, simultaneously measuring S(b) and m(b) in live passerines and nonpasserines, is required to improve the predictive power of S(b) upon m(b) scaling equations, which play a key role in the estimation of mechanical power consumption in flight in birds. Furthermore, the relations between bird body shape and axial skeleton dimensions, with reference to aerodynamic adaptation, warrant further investigation.

Forelimb proportions and the evolutionary radiation of Neornithes.

Analysis of a comprehensive dataset demonstrates that the brachial index (BI = humerus length/ulna length) of modern birds (Neornithes) varies significantly between clades at all taxonomic levels, yet is strongly correlated with recent phylogenetic hypotheses. Variance in BI at the infraclass level is low, but increases rapidly during the proposed major radiation of neornithines in the Palaeocene and Eocene. Although a BI of greater than 1 is primitive for Neornithes, more basal groups of Mesozoic birds (Confuciusornithidae and some members of the diverse Enantiornithidae) had BIs comparable with those of 'higher' modern clades. It is possible that occupation of ecological niches by these Mesozoic clades precluded the divergence of some groups of neornithines until after the Cretaceous-Tertiary boundary. We suggest that with further analysis and data collection the relationships between flight behaviour, ecology and BI can be determined. Hence, BI may provide a useful tool for characterizing the ecology of fossil birds.

The energetic cost of short flights in birds.

Many small birds perform short flights, for which take-offs, ascents and descents form a large component of the total flight time and which are characterised by low airspeeds. Using the doubly-labelled water technique, zebra finches Taeniopygia guttata engaging in repeated short flights were found to expend 13.65 kJ more than 'non-flying' controls, which equated to a flight expenditure of 27.8 times their basal metabolic rate. This is over three times the predicted flight expenditure derived from existing aerodynamic models. These data were used to determine a coefficient (0.11) for converting the mechanical power derived from aerodynamic models into metabolic power. An equation is presented, based on body mass, which can be used to predict the costs of short flights in ecological and behavioural studies of birds.