Paolo S. Segre

A fundamental avian wing-stroke provides a new perspective on the evolution of flight

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 (Fig. 1). 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°, when referenced to gravity, that directs aerodynamic forces about 40° above horizontal, permitting a 180° 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.

Precocial development of locomotor performance in a ground-dwelling bird (Alectoris chukar): negotiating a three-dimensional terrestrial environment.

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.

How Baleen Whales Feed: The Biomechanics of Engulfment and Filtration.

Baleen whales are gigantic obligate filter feeders that exploit aggregations of small-bodied prey in littoral, epipelagic, and mesopelagic ecosystems. At the extreme of maximum body size observed among mammals, baleen whales exhibit a unique combination of high overall energetic demands and low mass-specific metabolic rates. As a result, most baleen whale species have evolved filter-feeding mechanisms and foraging strategies that take advantage of seasonally abundant yet patchily and ephemerally distributed prey resources. New methodologies consisting of multi-sensor tags, active acoustic prey mapping, and hydrodynamic modeling have revolutionized our ability to study the physiology and ecology of baleen whale feeding mechanisms. Here, we review the current state of the field by exploring several hypotheses that aim to explain how baleen whales feed. Despite significant advances, major questions remain about the processes that underlie these extreme feeding mechanisms, which enabled the evolution of the largest animals of all time.

Burst muscle performance predicts the speed, acceleration, and turning performance of Anna’s hummingbirds

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 Annas 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

Hummingbirds control turning velocity using body orientation and turning radius using asymmetrical wingbeat kinematics

Turning in flight requires reorientation of force, which birds, bats and insects accomplish either by shifting body position and total force in concert or by using left–right asymmetries in wingbeat kinematics. Although both mechanisms have been observed in multiple species, it is currently unknown how each is used to control changes in trajectory. We addressed this problem by measuring body and wingbeat kinematics as hummingbirds tracked a revolving feeder, and estimating aerodynamic forces using a quasi-steady model. During arcing turns, hummingbirds symmetrically banked the stroke plane of both wings, and the body, into turns, supporting a body-dependent mechanism. However, several wingbeat asymmetries were present during turning, including a higher and flatter outer wingtip path and a lower more deviated inner wingtip path. A quasi-steady analysis of arcing turns performed with different trajectories revealed that changes in radius were associated with asymmetrical kinematics and forces, and changes in velocity were associated with symmetrical kinematics and forces. Collectively, our results indicate that both body-dependent and -independent force orientation mechanisms are available to hummingbirds, and that these kinematic strategies are used to meet the separate aerodynamic challenges posed by changes in velocity and turning radius.

Hydrodynamic properties of fin whale flippers predict maximum rolling performance

ABSTRACT Maneuverability is one of the most important and least understood aspects of animal locomotion. The hydrofoil-like flippers of cetaceans are thought to function as control surfaces that effect maneuvers, but quantitative tests of this hypothesis have been lacking. Here, we constructed a simple hydrodynamic model to predict the longitudinal-axis roll performance of fin whales, and we tested its predictions against kinematic data recorded by on-board movement sensors from 27 free-swimming fin whales. We found that for a given swimming speed and roll excursion, the roll velocity of fin whales calculated from our field data agrees well with that predicted by our hydrodynamic model. Although fluke and body torsion may further influence performance, our results indicate that lift generated by the flippers is sufficient to drive most of the longitudinal-axis rolls used by fin whales for feeding and maneuvering. Summary: A simple hydrodynamic model predicts fin whale rolling performance.

Characterizing Chilean blue whale vocalizations with DTAGs: a test of using tag accelerometers for caller identification

ABSTRACT Vocal behavior of blue whales (Balaenoptera musculus) in the Gulf of Corcovado, Chile, was analysed using both audio and accelerometer data from digital acoustic recording tags (DTAGs). Over the course of three austral summers (2014, 2015 and 2016), seventeen tags were deployed, yielding 124 h of data. We report the occurrence of Southeast Pacific type 2 (SEP2) calls, which exhibit peak frequencies, durations and timing consistent with previous recordings made using towed and moored hydrophones. We also describe tonal downswept (D) calls, which have not been previously described for this population. As being able to accurately assign vocalizations to individual whales is fundamental for studying communication and for estimating population densities from call rates, we further examine the feasibility of using high-resolution DTAG accelerometers to identify low-frequency calls produced by tagged blue whales. We cross-correlated acoustic signals with simultaneous tri-axial accelerometer readings in order to analyse the phase match as well as the amplitude of accelerometer signals associated with low-frequency calls, which provides a quantitative method of determining if a call is associated with a detectable acceleration signal. Our results suggest that vocalizations from nearby individuals are also capable of registering accelerometer signals in the tagged whales DTAG record. We cross-correlate acceleration vectors between calls to explore the possibility of using signature acceleration patterns associated with sounds produced within the tagged whale as a new method of identifying which accelerometer-detectable calls originate from the tagged animal. Summary: Characterization of the Chilean blue whale vocal repertoire and a modified method of using DTAG accelerometers to identify calling blue whales.

The biomechanical origin of extreme wing allometry in hummingbirds

Flying animals of different masses vary widely in body proportions, but the functional implications of this variation are often unclear. We address this ambiguity by developing an integrative allometric approach, which we apply here to hummingbirds to examine how the physical environment, wing morphology and stroke kinematics have contributed to the evolution of their highly specialised flight. Surprisingly, hummingbirds maintain constant wing velocity despite an order of magnitude variation in body weight; increased weight is supported solely through disproportionate increases in wing area. Conversely, wing velocity increases with body weight within species, compensating for lower relative wing area in larger individuals. By comparing inter- and intraspecific allometries, we find that the extreme wing area allometry of hummingbirds is likely an adaptation to maintain constant burst flight capacity and induced power requirements with increasing weight. Selection for relatively large wings simultaneously maximises aerial performance and minimises flight costs, which are essential elements of humming bird life history.Hummingbirds are known to defy the predicted scaling relationships between body and wing size. Here, Skandalis et al. develop a ‘force allometry’ framework to show that, regardless of wing size, hummingbird species have the same wing velocity during flight.

Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds

Animals living in and interacting with natural environments must monitor and respond to changing conditions and unpredictable situations. Using information from multiple sensory systems allows them to modify their behavior in response to their dynamic environment but also creates the challenge of integrating different, and potentially contradictory, sources of information for behavior control. Understanding how multiple information streams are integrated to produce flexible and reliable behavior is key to understanding how behavior is controlled in natural settings. Natural settings are rarely still, which challenges animals that require precise body position control, like hummingbirds, which hover while feeding from flowers. Tactile feedback, available only once the hummingbird is docked at the flower, could provide additional information to help maintain its position at the flower. To investigate the role of tactile information for hovering control during feeding, we first asked whether hummingbirds physically interact with a feeder once docked. We quantified physical interactions between docked hummingbirds and a feeder placed in front of a stationary background pattern. Force sensors on the feeder measured a complex time course of loading that reflects the wingbeat frequency and bill movement of feeding hummingbirds, and suggests that they sometimes push against the feeder with their bill. Next, we asked whether the measured tactile interactions were used by feeding hummingbirds to maintain position relative to the feeder. We created two experimental scenarios—one in which the feeder was stationary and the visual background moved and the other where the feeder moved laterally in front of a white background. When the visual background pattern moved, docked hummingbirds pushed significantly harder in the direction of horizontal visual motion. When the feeder moved, and the background was stationary, hummingbirds generated aerodynamic force in the opposite direction of the feeder motion. These results suggest that docked hummingbirds are using visual information about the environment to maintain body position and orientation, and not actively tracking the motion of the feeder. The absence of flower tracking behavior in hummingbirds contrasts with the behavior of hawkmoths, and provides evidence that they rely primarily on the visual background rather than flower-based cues while feeding.

A hydrodynamically active flipper-stroke in humpback whales

A central paradigm of aquatic locomotion is that cetaceans use fluke strokes to power their swimming while relying on lift and torque generated by the flippers to perform maneuvers such as rolls, pitch changes and turns [1]. Compared to other cetaceans, humpback whales (Megaptera novaeangliae) have disproportionately large flippers with added structural features to aid in hydrodynamic performance [2,3]. Humpbacks use acrobatic lunging maneuvers to attack dense aggregations of krill or small fish, and their large flippers are thought to increase their maneuverability and thus their ability to capture prey. Immediately before opening their mouths, humpbacks will often rapidly move their flippers, and it has been hypothesized that this movement is used to corral prey [4,5] or to generate an upward pitching moment to counteract the torque caused by rapid water engulfment [6]. Here, we demonstrate an additional function for the rapid flipper movement during lunge feeding: the flippers are flapped using a complex, hydrodynamically active stroke to generate lift and increase propulsive thrust. We estimate that humpback flipper-strokes are capable of producing large forward oriented forces, which may be used to enhance lunge feeding performance. This behavior is the first observation of a lift-generating flipper-stroke for propulsion cetaceans and provides an additional function for the uniquely shaped humpback whale flipper.