The largest animals are marine filter feeders, but the underlying mechanism of their large size remains unexplained. We measured feeding performance and prey quality to demonstrate how whale gigantism is driven by the interplay of prey abundance and harvesting mechanisms that increase prey capture rates and energy intake. The foraging efficiency of toothed whales that feed on single prey is constrained by the abundance of large prey, whereas filter-feeding baleen whales seasonally exploit vast swarms of small prey at high efficiencies. Given temporally and spatially aggregated prey, filter feeding provides an evolutionary pathway to extremes in body size that are not available to lineages that must feed on one prey at a time. Maximum size in filter feeders is likely constrained by prey availability across space and time.
Developing animals are particularly vulnerable to predation. Hence, precocial young of many taxa develop predator escape performance that rivals that of adults. Ontogenetically unique among vertebrates, birds transition from hind limb to forelimb dependence for escape behaviours, so developmental investment for immediate gains in running performance may impair flight performance later. Here, in a three-dimensional kinematic study of developing birds performing pre-flight flapping locomotor behaviours, wing-assisted incline running (WAIR) and a newly described behaviour, controlled flapping descent (CFD), we define three stages of locomotor ontogeny in a model gallinaceous bird (Alectoris chukar). In stage I (1 -7 days post-hatching (dph)) birds crawl quadrupedally during ascents, and their flapping fails to reduce their acceleration during aerial descents. Stage II (8 -19 dph) birds use symmetric wing beats during WAIR, and in CFD significantly reduce acceleration while controlling body pitch to land on their feet. In stage III (20 dph to adults), birds are capable of vertical WAIR and level-powered flight. In contrast to altricial species, which first fly when nearly at adult mass, we show that in a precocial bird the major requirements for flight (i.e. high power output, wing control and wing size) convene by around 8 dph (at ca 5% of adult mass) and yield significant gains in escape performance: immature chukars can fly by 20 dph, at only about 12 per cent of adult mass.
The evolution of avian flight remains one of biology's major controversies, with a long history of functional interpretations of fossil forms given as evidence for either an arboreal or cursorial origin of flight. Despite repeated emphasis on the 'wing-stroke' as a necessary avenue of investigation for addressing the evolution of flight, no empirical data exist on wing-stroke dynamics in an experimental evolutionary context. Here we present the first comparison of wing-stroke kinematics of the primary locomotor modes (descending flight and incline flap-running) that lead to level-flapping flight in juvenile ground birds throughout development. We offer results that are contrary both to popular perception and inferences from other studies. Starting shortly after hatching and continuing through adulthood, ground birds use a wing-stroke confined to a narrow range of less than 20 degrees , when referenced to gravity, that directs aerodynamic forces about 40 degrees above horizontal, permitting a 180 degrees range in the direction of travel. Based on our results, we put forth an ontogenetic-transitional wing hypothesis that posits that the incremental adaptive stages leading to the evolution of avian flight correspond behaviourally and morphologically to transitional stages observed in ontogenetic forms.
How does agility evolve? This question is challenging because natural movement has many degrees of freedom and can be influenced by multiple traits. We used computer vision to record thousands of translations, rotations, and turns from more than 200 hummingbirds from 25 species, revealing that distinct performance metrics are correlated and that species diverge in their maneuvering style. Our analysis demonstrates that the enhanced maneuverability of larger species is explained by their proportionately greater muscle capacity and lower wing loading. Fast acceleration maneuvers evolve by recruiting changes in muscle capacity, whereas fast rotations and sharp turns evolve by recruiting changes in wing morphology. Both species and individuals use turns that play to their strengths. These results demonstrate how both skill and biomechanical traits shape maneuvering behavior.
Despite recent advances in the study of animal flight, the biomechanical determinants of maneuverability are poorly understood. It is thought that maneuverability may be influenced by intrinsic body mass and wing morphology, and by physiological muscle capacity, but this hypothesis has not yet been evaluated because it requires tracking a large number of free flight maneuvers from known individuals. We used an automated tracking system to record flight sequences from 20 Anna's hummingbirds flying solo and in competition in a large chamber. We found that burst muscle capacity predicted most performance metrics. Hummingbirds with higher burst capacity flew with faster velocities, accelerations, and rotations, and they used more demanding complex turns. In contrast, body mass did not predict variation in maneuvering performance, and wing morphology predicted only the use of arcing turns and high centripetal accelerations. Collectively, our results indicate that burst muscle capacity is a key predictor of maneuverability.DOI: http://dx.doi.org/10.7554/eLife.11159.001
Bird flight is a remarkable adaptation that has allowed the approximately 10 000 extant species to colonize all terrestrial habitats on earth including high elevations, polar regions, distant islands, arid deserts, and many others. Birds exhibit numerous physiological and biomechanical adaptations for flight. Although bird flight is often studied at the level of aerodynamics, morphology, wingbeat kinematics, muscle activity, or sensory guidance independently, in reality these systems are naturally integrated. There has been an abundance of new studies in these mechanistic aspects of avian biology but comparatively less recent work on the physiological ecology of avian flight. Here we review research at the interface of the systems used in flight control and discuss several common themes. Modulation of aerodynamic forces to respond to different challenges is driven by three primary mechanisms: wing velocity about the shoulder, shape within the wing, and angle of attack. For birds that flap, the distinction between velocity and shape modulation synthesizes diverse studies in morphology, wing motion, and motor control. Recently developed tools for studying bird flight are influencing multiple areas of investigation, and in particular the role of sensory systems in flight control. How sensory information is transformed into motor commands in the avian brain remains, however, a largely unexplored frontier.
Summary The biomechanical and neuromuscular mechanisms used by different animals to generate turns in flight are highly variable. Body size and body plan exert some influence, e.g., birds typically roll their body to orient forces generated by the wings whereas insects are capable of turning via left-right wingbeat asymmetries. Turns are also relatively brief and have low repeatability with almost every wingbeat serving a different function throughout the change in heading. Here we present an analysis of Anna’s hummingbirds (Calypte anna) as they fed continuously from an artificial feeder revolving around the outside of the animal. This setup allowed for examination of sustained changes in yaw without requiring any corresponding changes in pitch, roll, or body position. Hummingbirds sustained yaw turns by expanding the wing stroke amplitude of the outer wing during the downstroke and by altering the deviation of the wingtip path during both downstroke and upstroke. The latter led to a shift in the inner-outer stroke plane angle during the upstroke and shifts in the elevation of the stroke plane and in the deviation of the wingtip path during both strokes. These features are generally more similar to how insects, as opposed to birds, turn. However, time series analysis also revealed considerable stroke-to-stroke variation. Changes in the stroke amplitude and the wingtip velocity were highly cross-correlated as were changes in the stroke deviation and the elevation of the stroke plane. As was the case for wingbeat kinematics, electromyogram recordings from pectoral and wing muscles were highly variable, but no correlations were found between these two features of motor control. The high variability of both kinematic and muscle activation features indicates a high level of wingbeat-to-wingbeat adjustments during sustained yaw. The activation timing of the muscles was more repeatable than the activation intensity, which suggests that the former may be constrained by harmonic motion and that the latter may play a large role in kinematic adjustments. Comparing the revolution frequency of the feeder to measurements of free flight yaws reveals that feeder tracking, even at one revolution every two seconds, is well below the maximum yaw capacity of the hummingbirds.
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