Earliest evidence of avian primary feather moult.

Feather moulting is a crucial process in the avian life cycle, which evolved to maintain plumage functionality. However, moulting involves both energetic and functional costs. During moulting, plumage function temporarily decreases between the shedding of old feathers and the full growth of new ones. In flying taxa, a gradual and sequential replacement of flight feathers evolved to maintain aerodynamic capabilities during the moulting period. Little is known about the moult strategies of non-avian pennaraptoran dinosaurs and stem birds, before the emergence of crown lineage. Here, we report on two Early Cretaceous pygostylian birds from the Yixian Formation (125 mya), probably referable to Confuciusornithiformes, exhibiting morphological characteristics that suggest a gradual and sequential moult of wing flight feathers. Short primary feathers interpreted as immature are symmetrically present on both wings, as is typical among extant flying birds. Our survey of the enormous collection of the Tianyu Museum confirms previous findings that evidence of active moult in non-neornithine pennaraptorans is rare and likely indicates a moult cycle greater than one year. Documenting moult in Mesozoic feathered dinosaurs is critical for understanding their ecology, locomotor ability and the evolution of this important life-history process in birds.

The small hive beetle's capacity to disperse over long distances by flight.

The spread of invasive species often follows a jump-dispersal pattern. While jumps are typically fostered by humans, local dispersal can occur due to the specific traits of a species, which are often poorly understood. This holds true for small hive beetles (Aethina tumida), which are parasites of social bee colonies native to sub-Saharan Africa. They have become a widespread invasive species. In 2017, a mark-release-recapture experiment was conducted in six replicates (A-F) using laboratory reared, dye-fed adults (N = 15,690). Honey bee colonies were used to attract flying small hive beetles at fixed spatial intervals from a central release point. Small hive beetles were recaptured (N = 770) at a maximum distance of 3.2 km after 24 h and 12 km after 1 week. Most small hive beetles were collected closest to the release point at 0 m (76%, replicate A) and 50 m (52%, replicates B to F). Temperature and wind deviation had significant effects on dispersal, with more small hive beetles being recaptured when temperatures were high (GLMM: slope = 0.99, SE = 0.17, Z = 5.72, P < 0.001) and confirming the role of wind for odour modulated dispersal of flying insects (GLMM: slope = - 0.39, SE = 0.14, Z = - 2.90, P = 0.004). Our findings show that the small hive beetles is capable of long-distance flights, and highlights the need to understand species specific traits to be considered for monitoring and mitigation efforts regarding invasive alien species.

Bottom-up butterfly model with thorax-pitch control and wing-pitch flexibility.

The diversity in butterfly morphology has attracted many people around the world since ancient times. Despite morphological diversity, the wing and body kinematics of butterflies have several common features. In the present study, we constructed a bottom-up butterfly model, whose morphology and kinematics are simplified while preserving the important features of butterflies. The present bottom-up butterfly model is composed of two trapezoidal wings and a rod-shaped body with a thorax and abdomen. Its wings are flapped downward in the downstroke and backward in the upstroke by changing the geometric angle of attack (AOA). The geometric AOA is determined by the thorax-pitch and wing-pitch angles. The thorax-pitch angle is actively controlled by abdominal undulation, and the wing-pitch angle is passively determined because of a rotary spring representing the basalar and subalar muscles connecting the wings and thorax. We investigated the effectiveness of abdominal undulation for thorax-pitch control and how wing-pitch flexibility affects aerodynamic-force generation and thorax-pitch control, through numerical simulations using the immersed boundary-lattice Boltzmann method. As a result, the thorax-pitch angle perfectly follows the desired angle through abdominal undulation. In addition, there is an optimal wing-pitch flexibility that maximizes the flying speed in both the forward and upward directions, but the effect of wing-pitch flexibility on thorax-pitch control is not significant. Finally, we compared the flight behavior of the present bottom-up butterfly model with that of an actual butterfly. It was found that the present model does not reproduce reasonable body kinematics but can provide reasonable aerodynamics in butterfly flights.

Altering developmental oxygen exposure influences thermoregulation and flight performance of Manduca sexta.

Endothermic, flying insects are capable of some of the highest recorded metabolic rates. This high aerobic demand is made possible by the insect's tracheal system, which supplies the flight muscles with oxygen. Many studies focus on metabolic responses to acute changes in oxygen to test the limits of the insect flight metabolic system, with some flying insects exhibiting oxygen limitation in flight metabolism. These acute studies do not account for possible changes induced by developmental phenotypic plasticity in response to chronic changes in oxygen levels. The endothermic moth Manduca sexta is a model organism that is easy to raise and exhibits a high thorax temperature during flight (∼40°C). In this study, we examined the effects of developmental oxygen exposure during the larval, pupal and adult stages on the adult moth's aerobic performance. We measured flight critical oxygen partial pressure (Pcrit-), thorax temperature and thermoregulating metabolic rate to understand the extent of developmental plasticity as well as effects of developmental oxygen levels on endothermic capacity. We found that developing in hypoxia (10% oxygen) decreased thermoregulating thorax temperature when compared with moths raised in normoxia or hyperoxia (30% oxygen), when moths were warming up in atmospheres with 21-30% oxygen. In addition, moths raised in hypoxia had lower critical oxygen levels when flying. These results suggest that chronic developmental exposure to hypoxia affects the adult metabolic phenotype and potentially has implications for thermoregulatory and flight behavior.

A trans-oceanic flight of over 4,200 km by painted lady butterflies.

The extent of aerial flows of insects circulating around the planet and their impact on ecosystems and biogeography remain enigmatic because of methodological challenges. Here we report a transatlantic crossing by Vanessa cardui butterflies spanning at least 4200 km, from West Africa to South America (French Guiana) and lasting between 5 and 8 days. Even more, we infer a likely natal origin for these individuals in Western Europe, and the journey Europe-Africa-South America could expand to 7000 km or more. This discovery was possible through an integrative approach, including coastal field surveys, wind trajectory modelling, genomics, pollen metabarcoding, ecological niche modelling, and multi-isotope geolocation of natal origins. The overall journey, which was energetically feasible only if assisted by winds, is among the longest documented for individual insects, and potentially the first verified transatlantic crossing. Our findings suggest that we may be underestimating transoceanic dispersal in insects and highlight the importance of aerial highways connecting continents by trade winds.

Universal wing- and fin-beat frequency scaling.

We derive an equation that applies for the wing-beat frequency of flying animals and to the fin-stroke frequency of diving animals like penguins and whales. The equation states that the wing/fin-beat frequency is proportional to the square root of the animal's mass divided by the wing area. Data for birds, insects, bats, and even a robotic bird-supplemented by data for whales and penguins that must swim to stay submerged-show that the constant of proportionality is to a good approximation the same across all species; thus the equation is universal. The wing/fin-beat frequency equation is derived by dimensional analysis, which is a standard method of reasoning in physics. We finally demonstrate that a mathematically even simpler expression without the animal mass does not apply.

Metabolic Rate Suppression and Maintenance of Flight Muscle Metabolic Capacity during Diapause in Bumble Bee (Bombus impatiens) Queens.

AbstractThe common eastern bumble bee (Bombus impatiens) queens endure cold winter months by entering a diapause state. During this overwintering period, these animals use stored energy reserves while maintaining a low metabolic rate. This study investigates changes in the metabolic rate of bumble bee queens during diapause-like laboratory conditions and the potential reorganization of the flight muscle metabolic properties during this period. We first confirmed the hypometabolic state of queens during diapause in the laboratory, which lowered their resting metabolic rate to less than 5% of normal resting values. Body mass decreased during diapause, body composition changed where carbohydrates decreased initially, and later protein declined, with a similar trend for lipid content. Using cellular respirometry, we determined the capacity of the flight muscle cells of bumble bee queens to use various metabolic fuels and whether this capacity changes during the progression of diapause to favor stored lipid-derived substrates. Queens showed a low capacity to oxidize the amino acid proline, compared with workers, and their capacity to oxidize all metabolic substrates did not change during a 4-mo diapause period in the laboratory. We also show no detectable ability to oxidize fatty acid by flight muscle mitochondria in this species. The metabolic properties of flight muscle tissue were further characterized using metabolic enzyme activity profiles showing little change during diapause, indicating that profound metabolic suppression is induced without major changes in muscle metabolic phenotypes. Overall, B. impatiens queens undergo diapause while maintaining flight muscle capacity under the conditions used.

Insect ecology: Tracking migratory butterflies through pollen.

Painted ladies are well-known migratory butterflies, but confirmation of the details of their swarming flights through Europe has evaded scientists until now. It was their role as pollinators, carrying pollen grains on their flights, that helped unlock the secrets of their migrations.

The respiratory system influences flight mechanics in soaring birds.

The subpectoral diverticulum (SPD) is an extension of the respiratory system in birds that is located between the primary muscles responsible for flapping the wing1,2. Here we survey the pulmonary apparatus in 68 avian species, and show that the SPD was present in virtually all of the soaring taxa investigated but absent in non-soarers. We find that this structure evolved independently with soaring flight at least seven times, which indicates that the diverticulum might have a functional and adaptive relationship with this flight style. Using the soaring hawks Buteo jamaicensis and Buteo swainsoni as models, we show that the SPD is not integral for ventilation, that an inflated SPD can increase the moment arm of cranial parts of the pectoralis, and that pectoralis muscle fascicles are significantly shorter in soaring hawks than in non-soaring birds. This coupling of an SPD-mediated increase in pectoralis leverage with force-specialized muscle architecture produces a pneumatic system that is adapted for the isometric contractile conditions expected in soaring flight. The discovery of a mechanical role for the respiratory system in avian locomotion underscores the functional complexity and heterogeneity of this organ system, and suggests that pulmonary diverticula are likely to have other undiscovered secondary functions. These data provide a mechanistic explanation for the repeated appearance of the SPD in soaring lineages and show that the respiratory system can be co-opted to provide biomechanical solutions to the challenges of flight and thereby influence the evolution of avian volancy.

The most remarkable migrants-systematic analysis of the Western European insect flyway at a Pyrenean mountain pass.

In autumn 1950 David and Elizabeth Lack chanced upon a huge migration of insects and birds flying through the Pyrenean Pass of Bujaruelo, from France into Spain, later describing the spectacle as combining both grandeur and novelty. The intervening years have seen many changes to land use and climate, posing the question as to the current status of this migratory phenomenon. In addition, a lack of quantitative data has prevented insights into the ecological impact of this mass insect migration and the factors that may influence it. To address this, we revisited the site in autumn over a 4 year period and systematically monitored abundance and species composition of diurnal insect migrants. We estimate an annual mean of 17.1 million day-flying insect migrants from five orders (Diptera, Hymenoptera, Hemiptera, Lepidoptera and Odonata) moving south, with observations of southward 'mass migration' events associated with warmer temperatures, the presence of a headwind, sunlight, low windspeed and low rainfall. Diptera dominated the migratory assemblage, and annual numbers varied by more than fourfold. Numbers at this single site hint at the likely billions of insects crossing the entire Pyrenean mountain range each year, and we highlight the importance of this route for seasonal insect migrants.

Asynchronous haltere input drives specific wing and head movements in Drosophila.

Halteres are multifunctional mechanosensory organs unique to the true flies (Diptera). A set of reduced hindwings, the halteres beat at the same frequency as the lift-generating forewings and sense inertial forces via mechanosensory campaniform sensilla. Though haltere ablation makes stable flight impossible, the specific role of wing-synchronous input has not been established. Using small iron filings attached to the halteres of tethered flies and an alternating electromagnetic field, we experimentally decoupled the wings and halteres of flying Drosophila and observed the resulting changes in wingbeat amplitude and head orientation. We find that asynchronous haltere input results in fast amplitude changes in the wing (hitches), but does not appreciably move the head. In multi-modal experiments, we find that wing and gaze optomotor responses are disrupted differently by asynchronous input. These effects of wing-asynchronous haltere input suggest that specific sensory information is necessary for maintaining wing amplitude stability and adaptive gaze control.

Perception of motion salience shapes the emergence of collective motions.

Despite the profound implications of self-organization in animal groups for collective behaviors, understanding the fundamental principles and applying them to swarm robotics remains incomplete. Here we propose a heuristic measure of perception of motion salience (MS) to quantify relative motion changes of neighbors from first-person view. Leveraging three large bird-flocking datasets, we explore how this perception of MS relates to the structure of leader-follower (LF) relations, and further perform an individual-level correlation analysis between past perception of MS and future change rate of velocity consensus. We observe prevalence of the positive correlations in real flocks, which demonstrates that individuals will accelerate the convergence of velocity with neighbors who have higher MS. This empirical finding motivates us to introduce the concept of adaptive MS-based (AMS) interaction in swarm model. Finally, we implement AMS in a swarm of ~102 miniature robots. Swarm experiments show the significant advantage of AMS in enhancing self-organization of the swarm for smooth evacuations from confined environments.

Seasonal patterns and processes of migration in a long-distance migratory bird: energy or time minimization?

Optimal migration theory prescribes adaptive strategies of energy, time or mortality minimization. To test alternative hypotheses of energy- and time-minimization migration we used multisensory data loggers that record time-resolved flight activity and light for positioning by geolocation in a long-distance migratory shorebird, the little ringed plover, Charadrius dubius. We could reject the hypothesis of energy minimization based on a relationship between stopover duration and subsequent flight time as predicted for a time minimizer. We found seasonally diverging slopes between stopover and flight durations in relation to the progress (time) of migration, which follows a time-minimizing policy if resource gradients along the migration route increase in autumn and decrease in spring. Total flight duration did not differ significantly between autumn and spring migration, although spring migration was 6% shorter. Overall duration of autumn migration was longer than that in spring, mainly owing to a mid-migration stop in most birds, when they likely initiated moult. Overall migration speed was significantly different between autumn and spring. Migratory flights often occurred as runs of two to seven nocturnal flights on adjacent days, which may be countering a time-minimization strategy. Other factors may influence a preference for nocturnal migration, such as avoiding flight in turbulent conditions, heat stress and diurnal predators.

How touch helps hummingbirds hover.

Georgina Mills discusses new research looking at how hummingbirds use somatosensation to adjust their flight.

Disturbance of hibernating bats due to researchers entering caves to conduct hibernacula surveys.

Estimating population changes of bats is important for their conservation. Population estimates of hibernating bats are often calculated by researchers entering hibernacula to count bats; however, the disturbance caused by these surveys can cause bats to arouse unnaturally, fly, and lose body mass. We conducted 17 hibernacula surveys in 9 caves from 2013 to 2018 and used acoustic detectors to document cave-exiting bats the night following our surveys. We predicted that cave-exiting flights (i.e., bats flying out and then back into caves) of Townsend's big-eared bats (Corynorhinus townsendii) and western small-footed myotis (Myotis ciliolabrum) would be higher the night following hibernacula surveys than on nights following no surveys. Those two species, however, did not fly out of caves more than predicted the night following 82% of surveys. Nonetheless, the activity of bats flying out of caves following surveys was related to a disturbance factor (i.e., number of researchers × total time in a cave). We produced a parsimonious model for predicting the probability of Townsend's big-eared bats flying out of caves as a function of disturbance factor and ambient temperature. That model can be used to help biologists plan for the number of researchers, and the length of time those individuals are in a cave to minimize disturbing bats.

Flow sensing on dragonfly wings.

One feature of animal wings is their embedded mechanosensory system that can support flight control. Insect wings are particularly interesting as they are highly deformable yet the actuation is limited to the wing base. It is established that strain sensors on insect wings can directly mediate reflexive control; however, little is known about airflow sensing by insect wings. What information can flow sensors capture and how can flow sensing benefit flight control? Here, we use the dragonfly (Sympetrum striolatum) as a model to explore the function of wing sensory bristles in the context of flight control. Combining our detailed anatomical reconstructions of both the sensor microstructures and wing architecture, we used computational fluid dynamics simulations to ask the following questions. (1) Are there strategic locations on wings that sample flow for estimating aerodynamically relevant parameters such as the local effective angle of attack? (2) Is the sensory bristle distribution on dragonfly wings optimal for flow sensing? (3) What is the aerodynamic effect of microstructures found near the sensory bristles on dragonfly wings? We discuss the benefits of flow sensing for flexible wings and how the evolved sensor placement affects information encoding.

It pays to follow the leader: Metabolic cost of flight is lower for trailing birds in small groups.

Many bird species commonly aggregate in flocks for reasons ranging from predator defense to navigation. Available evidence suggests that certain types of flocks-the V and echelon formations of large birds-may provide a benefit that reduces the aerodynamic cost of flight, whereas cluster flocks typical of smaller birds may increase flight costs. However, metabolic flight costs have not been directly measured in any of these group flight contexts [Zhang and Lauder, J. Exp. Biol. 226, jeb245617 (2023)]. Here, we measured the energetic benefits of flight in small groups of two or three birds and the requirements for realizing those benefits, using metabolic energy expenditure and flight position measurements from European Starlings flying in a wind tunnel. The starlings continuously varied their relative position during flights but adopted a V formation motif on average, with a modal spanwise and streamwise spacing of [0.81, 0.91] wingspans. As measured via CO2 production, flight costs for follower birds were significantly reduced compared to their individual solo flight benchmarks. However, followers with more positional variability with respect to leaders did less well, even increasing their costs above solo flight. Thus, we directly demonstrate energetic costs and benefits for group flight followers in an experimental context amenable to further investigation of the underlying aerodynamics, wake interactions, and bird characteristics that produce these metabolic effects.

Moth resonant mechanics are tuned to wingbeat frequency and energetic demands.

An insect's wingbeat frequency is a critical determinant of its flight performance and varies by multiple orders of magnitude across Insecta. Despite potential energetic benefits for an insect that matches its wingbeat frequency to its resonant frequency, recent work has shown that moths may operate off their resonant peak. We hypothesized that across species, wingbeat frequency scales with resonance frequency to maintain favourable energetics, but with an offset in species that use frequency modulation as a means of flight control. The moth superfamily Bombycoidea is ideal for testing this hypothesis because their wingbeat frequencies vary across species by an order of magnitude, despite similar morphology and actuation. We used materials testing, high-speed videography and a model of resonant aerodynamics to determine how components of an insect's flight apparatus (stiffness, wing inertia, muscle strain and aerodynamics) vary with wingbeat frequency. We find that the resonant frequency of a moth correlates with wingbeat frequency, but resonance curve shape (described by the Weis-Fogh number) and peak location vary within the clade in a way that corresponds to frequency-dependent biomechanical demands. Our results demonstrate that a suite of adaptations in muscle, exoskeleton and wing drive variation in resonant mechanics, reflecting potential constraints on matching wingbeat and resonant frequencies.

Erratum: Modified Fear Conditioning for Inducing Flight Behaviors in Mice.

This corrects the article 10.3791/66266.