Muscle function in avian flight: achieving power and control

Flapping flight places strenuous requirements on the physiological performance of an animal. Bird flight muscles, particularly at smaller body sizes, generally contract at high frequencies and do substantial work in order to produce the aerodynamic power needed to support the animal's weight in the air and to overcome drag. This is in contrast to terrestrial locomotion, which offers mechanisms for minimizing energy losses associated with body movement combined with elastic energy savings to reduce the skeletal muscles' work requirements. Muscles also produce substantial power during swimming, but this is mainly to overcome body drag rather than to support the animal's weight. Here, I review the function and architecture of key flight muscles related to how these muscles contribute to producing the power required for flapping flight, how the muscles are recruited to control wing motion and how they are used in manoeuvring. An emergent property of the primary flight muscles, consistent with their need to produce considerable work by moving the wings through large excursions during each wing stroke, is that the pectoralis and supracoracoideus muscles shorten over a large fraction of their resting fibre length (33-42%). Both muscles are activated while being lengthened or undergoing nearly isometric force development, enhancing the work they perform during subsequent shortening. Two smaller muscles, the triceps and biceps, operate over a smaller range of contractile strains (12-23%), reflecting their role in controlling wing shape through elbow flexion and extension. Remarkably, pigeons adjust their wing stroke plane mainly via changes in whole-body pitch during take-off and landing, relative to level flight, allowing their wing muscles to operate with little change in activation timing, strain magnitude and pattern.     

The Control of Mechanical Power in Insect Flight

SYNOPSIS. The cost of locomotion is rarely constant, but rathervaries as an animal changes speed and direction. Ultimately,the locomotory muscles of an animal must compensate for thesechanging requirements by varying the amount of mechanical powerthat they produce. In this paper, we consider the mechanismsby which the mechanical power generated by the asynchronousflight muscles of the fruit fly, Drosophila melanogaster, isregulated to match the changing requirements during flight controlbehaviors. Our data come from individual flies flown in a flightarena under conditions in which stroke kinematics, total metaboliccost, and flight force are simultaneously measured. In orderto increase force production, flies must increase wing beatfrequency and wing stroke amplitude. Theory predicts that thesekinematics changes should result in a roughly cubic increasein the mechanical power requirements for flight. However, themechanical energy generated by muscle should increase only linearlywith stroke amplitude and frequency. This discrepancy impliesthat flight muscles must either recruit myofibrils or increaseactivation in order to generate sufficient mechanical powerto sustain elevated force production. By comparing respirometricallymeasured total metabolic power with kinematically estimatedmechanical power, we have calculated that the stress in theflight muscles of Drosophila must increase by 50% to accommodatea doubling of flight force. Electrophysiological evidence suggeststhat this change in stress may be accomplished by an increasedneural drive to the asynchronous muscles, which in turn mayact to recruit additional cross bridges through an increasein cytosolic calcium.     

Distributed power and control actuation in the thoracic mechanics of a robotic insect

Recent advances in the understanding of biological flight have inspired roboticists to create flapping-wing vehicles on the scale of insects and small birds. While our understanding of the wing kinematics, flight musculature and neuromotor control systems of insects has expanded, in practice it has proven quite difficult to construct an at-scale mechanical device capable of similar flight performance. One of the key challenges is the development of an effective and efficient transmission mechanism to control wing motions. Here we present multiple insect-scale robotic thorax designs capable of producing asymmetric wing kinematics similar to those observed in nature and utilized by dipteran insects to maneuver. Inspired by the thoracic mechanics of dipteran insects, which entail a morphological separation of power and control muscles, these designs show that such distributed actuation can also modulate wing motion in a robotic design.     

Linking demographic and food‐web models to understand management trade‐offs

Alternatives in ecosystem‐based management often differ with respect to trade‐offs between ecosystem values. Ecosystem or food‐web models and demographic models are typically employed to evaluate alternatives, but the approaches are rarely integrated to uncover conflicts between values. We applied multistate models to a capture–recapture dataset on common guillemots Uria aalge breeding in the Baltic Sea to identify factors influencing survival. The estimated relationships were employed together with Ecopath‐with‐Ecosim food‐web model simulations to project guillemot survival under six future scenarios incorporating climate change. The scenarios were based on management alternatives for eutrophication and cod fisheries, issues considered top priority for regional management, but without known direct effects on the guillemot population. Our demographic models identified prey quantity (abundance and biomass of sprat Sprattus sprattus) as the main factor influencing guillemot survival. Most scenarios resulted in projections of increased survival, in the near (2016–2040) and distant (2060–2085) future. However, in the scenario of reduced nutrient input and precautionary cod fishing, guillemot survival was projected to be lower in both future periods due to lower sprat stocks. Matrix population models suggested a substantial decline of the guillemot population in the near future, 24% per 10 years, and a smaller reduction, 1.1% per 10 years, in the distant future. To date, many stakeholders and Baltic Sea governments have supported reduced nutrient input and precautionary cod fishing and implementation is underway. Negative effects on nonfocal species have previously not been uncovered, but our results show that the scenario is likely to negatively impact the guillemot population. Linking model results allowed identifying trade‐offs associated with management alternatives. This information is critical to thorough evaluation by decision‐makers, but not easily obtained by food‐web models or demographic models in isolation. Appropriate datasets are often available, making it feasible to apply a linked approach for better‐informed decisions in ecosystem‐based management.     

The impact of urbanization on body size of Barn Swallows Hirundo rustica gutturalis

Urbanization implies a dramatic impact on ecosystems, which may lead to drastic phenotypic differences between urban and nonurban individuals. For instance, urbanization is associated with increased metabolic costs, which may constrain body size, but urbanization also leads to habitat fragmentation, which may favor increases in body mass when for instance it correlates with dispersal capacity. However, this apparent contradiction has rarely been studied. This is particularly evident in China where the urbanization process is currently occurring at an unprecedented scale. Moreover, no study has addressed this issue across large geographical areas encompassing locations in different climates. In this regard, Barn Swallows (Hirundo rustica) are a suitable model to study the impact of urbanization on wild animals because they are a widely distributed species tightly associated with humans. Here, we collected body mass and wing length data for 359 breeding individuals of Barn Swallow (H. r. gutturalis) from 128 sites showing different levels of urbanization around the whole China. Using a set of linear mixed‐effects models, we assessed how urbanization and geography influenced body size measured using body mass, wing length, and their regression residuals. Interestingly, we found that the impact of urbanization was sex‐dependent, negatively affecting males’ body mass, its regression residuals, and females’ wing length. We also found that northern and western individuals were larger, regarding both body mass and wing length, than southern and eastern individuals. Females were heavier than males, yet males had slightly longer wings than females. Overall, our results showed that body mass of males was particularly sensitive trait to urbanization, latitude, and longitude, while it only showed a weak response to latitude in females. Conversely, while wing length showed a similar geographical pattern, it was only affected by urbanization in the case of females. Further research is needed to determine whether these phenotypic differences are associated with negative effects of urbanization or potential selective advantages.     

QTL detection power of multi-parental RIL populations in Arabidopsis thaliana

A major goal of today's biology is to understand the genetic basis of quantitative traits. This can be achieved by statistical methods that evaluate the association between molecular marker variation and phenotypic variation in different types of mapping populations. The objective of this work was to evaluate the statistical power of quantitative trait loci (QTL) detection of various multi-parental mating designs, as well as to assess the reasons for the observed differences. Our study was based on an empirical data of 20 Arabidopsis thaliana accessions, which have been selected to capture the maximum genetic diversity. The examined mating designs differed strongly with respect to the statistical power to detect QTL. We observed the highest power to detect QTL for the diallel cross with random mating design. The results of our study suggested that performing sibling mating within subpopulations of joint-linkage mapping populations has the potential to considerably increase the power for QTL detection. Our results, however, revealed that using designs in which more than two parental alleles segregate in each subpopulation increases the power even more.     

Site-occupancy in relation to flight-morphology in caddisflies

1. The relationship between morphology and site‐occupancy provides opportunities to infer differences in dispersal and flight ability, but empirical data for aquatic insects is limited. 2. In this study, 17 species of caddisflies from 10 families were collected from springs, streams and lakes, and total body mass, relative thorax mass, relative wing area (wing loading), and the aspect ratio of the fore and hind wings (combined) were measured. 3. Partial least‐squares regression analysis of two independent distributional data sets produced significant models within which total body mass, relative thorax mass and wing loading were positively associated with site‐occupancy, whereas aspect ratio was negatively associated with site‐occupancy. 4. These results suggest that the faunal composition of streams is influenced by species dispersal abilities.     

Elastic joints in dermapteran hind wings: materials and wing folding

Representatives of Dermaptera probably have the most unusual hind wing venation and folding pattern among insects. Both correlate with unusual wing folding mechanics, in which folding is achieved from within the wing and unfolding is done by the cerci. In this account, the hind wings of the earwig Forficula auricularia were studied by means of bright field and fluorescence microscopy. Resilin, a rubber-like protein, was revealed in several, clearly defined patches. It occurs dorsally in the radiating veins, but ventrally in the intercalary vein. This distribution determines the folding direction, and resilin is the major driving mechanism for wing folding. Resilin stores elastic energy in broadened vein patches and along the folds. At the other locations, the mid-wing mechanism and central area, the primary function of resilin is suggested to be prevention of material failure. The arrangement of resilin patches is such that the wing cannot be unfolded from the thorax proper but must be unfolded by the cerci. In Dermaptera, the antagonistic movements of folding and unfolding are achieved in two different ways, resilin and cerci. To our knowledge this is unique.     

Butterfly wing patterns

This paper integrates genetical studies of variation in the wing patterns of Lepidoptera with experimental investigations of developmental mechanisms. Research on the tropical butterfly,Bicyclus anynana, is described. This work includes artificial selection of lines with different patterns of wing eyespots followed by grafting experiments on the lines to examine the phenotypic and genetic differences in terms of developmental mechanisms. The results are used to show how constraints on the evolution of this wing pattern may be related to the developmental organisation. The eyespot pattrn can be envisaged as a set of developmental homologues; a common developmental mechanism is associated with a quantitative genetic system involving high genetic correlations. However, individual genes which influence only subsets of the eyespots, thus uncoupling the interdependence of the eyespots, may be important in evolutionary change. The postulated evolutionary constraints are illustrated with respect to differences in wing pattern found among other species ofBicyclus.     

Of hummingbirds and helicopters: hovering costs, competitive ability, and foraging strategies

Wing morphology and flight kinematics profoundly influence foraging costs and the overall behavioral ecology of hummingbirds. By analogy with helicopters, previous energetic studies have applied the momentum theory of aircraft propellers to estimate hovering costs from wing disc loading (WDL), a parameter incorporating wingspan (or length) and body mass. Variation in WDL has been used to elucidate differences either among hummingbird species in nectar-foraging strategies (e.g., territoriality, traplining) and dominance relations or among gender-age categories within species. We first demonstrate that WDL, as typically calculated, is an unreliable predictor of hovering (induced power) costs; predictive power is increased when calculations use wing length instead of wingspan and when actual wing stroke amplitudes are incorporated. We next evaluate the hypotheses that foraging strategy and competitive ability are functions of WDL, using our data in combination with those of published sources. Variation in hummingbird behavior cannot be easily classified using WDL and instead is correlated with a diversity of morphological and physiological traits. Evaluating selection pressures on hummingbird wings will require moving beyond wing and body mass measurements to include the assessment of the aerodynamic forces, power requirements, and power reserves of hovering, forward flight, and maneuvering. However, the WDL-helicopter dynamics model has been instrumental in calling attention to the importance of comparative wing morphology and related aerodynamics for understanding the behavioral ecology of hummingbirds.     

Comparative functional morphology of the wings of Diptera

Wings of representative species of the order Diptera were compared with a simple model structure in which corrugated spars diverge from a V-shaped leading edge spar. Both develop torsion and camber when subjected to aerodynamic loads, forming a propeller shape. Both the leading edge and the cubitus of flies' wings twist basally, allowing camber to be set up as the media hinges up or down at the arculus. Three different wing types were identified: stiff wings possessing two or three main spars; and wings capable of ventral flexion. In wings possessing only two spars, found mainly in the Nematocera, control of camber is achieved largely by the use of cross veins. Wing control and flight are generally imprecise. The third spar, found in most Brachycera, in the Syrphidae and in the Conopidae controls camber and helps support a broader wing. Finer control of camber is exerted by marginal cross veins, and these insects generally have precise, darting flight. Ventral flexion mechanisms are found in the Simuliidae, the Stratiomyiidae, and widely in the Schizophora. Control of ventral flexion, which occurs at the end of the downstroke, allows fast, unpredictable manoeuvres. Functional similarities indicate either phylogenetic relationship or convergence.     

Decline of an arctic top predator: synchrony in colony size fluctuations, risk of extinction and the subpolar gyre

Analysis of synchrony in population fluctuations is a central topic in ecology. It can help identify factors that regulate populations, and also the scales at which these factors exert their influence. Using long-term data from seven Brünnich’s guillemot colonies in Svalbard, Norway, we determined that year to year population fluctuations were synchronized in six of the seven colonies. The seventh colony was located farther away and in a different oceanographic system. Moreover, all seven colonies have declined significantly since the late 1990s following a very similar pattern. If the rate of population decline does not change, Brünnich’s guillemots in Svalbard have a high probability of becoming quasi-extinct within the next 50 years. The high synchrony between the different colonies could further increase this risk of extinction. Our results indicate that environmental forcing plays a role in the colony size fluctuation of Brünnich’s guillemot (i.e., a Moran effect). These fluctuations are well explained by changes in the subpolar gyre in the region where Brünnich’s guillemots overwinter. This subpolar gyre weakened in the mid-1990s, leading to a warming of the North Atlantic. Our study indicates that this basin-scale shift in the subpolar gyre is closely related to the decline in Brünnich’s guillemot in Svalbard. Our results suggest that the causal mechanism linking changes in oceanographic conditions in the North Atlantic and Brünnich’s guillemot population dynamics are likely mediated, at least partly, by changes in recruitment.     

Effect of flexural and torsional wing flexibility on lift generation in hoverfly flight

The effect of wing flexibility in hoverflies was investigated using an at-scale mechanical model. Unlike dynamically-scaled models, an at-scale model can include all phenomena related to motion and deformation of the wing during flapping. For this purpose, an at-scale polymer wing mimicking a hoverfly was fabricated using a custom micromolding process. The wing has venation and corrugation profiles which mimic those of a hoverfly wing and the measured flexural stiffness of the artificial wing is comparable to that of the natural wing. To emulate the torsional flexibility at the wing-body joint, a discrete flexure hinge was created. A range of flexure stiffnesses was chosen to match the torsional stiffness of pronation and supination in a hoverfly wing. The polymer wing was compared with a rigid, flat, carbon-fiber wing using a flapping mechanism driven by a piezoelectric actuator. Both wings exhibited passive rotation around the wing hinge; however, these rotations were reduced in the case of the compliant polymer wing due to chordwise deformations during flapping which caused a reduced effective angle of attack. Maximum lift was achieved when the stiffness of the hinge was similar to that of a hoverfly in both wing cases and the magnitude of measured lift is sufficient for hovering; the maximum lift achieved by the single polymer and carbon-fiber wings was 5.9?×?10(2)(?)μN and 6.9?×?10(2)(?)μN, respectively. These results suggest that hoverflies could exploit intrinsic compliances to generate desired motions of the wing and that, for the same flapping motions, a rigid wing could be more suitable for producing large lift.     

Studies in RF Power Communication,SAR, and Temperature Elevation in Wireless Implantable Neural Interfaces

Implantable neural interfaces are designed to provide a high spatial and temporal precision control signal implementing high degree of freedom real-time prosthetic systems. The development of a Radio Frequency (RF) wireless neural interface has the potential to expand the number of applications as well as extend the robustness and longevity compared to wired neural interfaces. However, it is well known that RF signal is absorbed by the body and can result in tissue heating. In this work, numerical studies with analytical validations are performed to provide an assessment of power, heating and specific absorption rate (SAR) associated with the wireless RF transmitting within the human head. The receiving antenna on the neural interface is designed with different geometries and modeled at a range of implanted depths within the brain in order to estimate the maximum receiving power without violating SAR and tissue temperature elevation safety regulations. Based on the size of the designed antenna, sets of frequencies between 1 GHz to 4 GHz have been investigated. As expected the simulations demonstrate that longer receiving antennas (dipole) and lower working frequencies result in greater power availability prior to violating SAR regulations. For a 15 mm dipole antenna operating at 1.24 GHz on the surface of the brain, 730 uW of power could be harvested at the Federal Communications Commission (FCC) SAR violation limit. At approximately 5 cm inside the head, this same antenna would receive 190 uW of power prior to violating SAR regulations. Finally, the 3-D bio-heat simulation results show that for all evaluated antennas and frequency combinations we reach FCC SAR limits well before 1 °C. It is clear that powering neural interfaces via RF is possible, but ultra-low power circuit designs combined with advanced simulation will be required to develop a functional antenna that meets all system requirements.     

Wing folding and free-flight kinematics in Coleoptera (Insecta): a comparative study

Relative movements of the main wing areas around the major flexion lines are compared during wing folding at rest, and during the supinatory phase of the flight cycle, which involves considerable wing deformation. Folding of the wing apex at rest is achieved by a combination of movements around the median flexion line (the main longitudinal flexion line), the principal transverse fold, and a variety of smaller, oblique 'tucking' folds. During flight, wing tip deformation is strongly influenced by elastic forces involved in the normal wing folding and unfolding processes. Those beetles possessing an inwardly sprung wing apex display partial folding at supination, associated with the temporary relaxation of the forces opposing spring recoil. These beetles also show enhanced mobility about the median flexion line which facilitates leading edge supination. The presence of the principal transverse fold may help to concentrate ventral flexure towards the wing tip. The wings of beetles possessing an outwardly-sprung apex are much less affected by the presence of the flexion lines associated with folding. In these cases, enhanced supination of the leading edge, in the face of an overall increase in wing membrane stiffness, may be related to the presence of the highly-sclerotized pterostigma.     

Wing‐beat characteristics of birds recorded with tracking radar and cine camera

This study presents wing‐beat frequency data measured mainly by radar, complemented by video and cinematic recordings, for 153 western Palaearctic and two African species. Data on a further 45 Palaearctic species from other sources are provided in an electronic appendix. For 41 species with passerine‐type flight, the duration of flapping and pausing phases is given. The graphical presentations of frequency ranges and wing‐beat patterns show within‐species variation and allow easy comparison between species, taxonomic groups and types of flight. Wing‐beat frequency is described by Pennycuick (J. Exp. Biol. 2001; 204: 3283–3294) as a function of body‐mass, wing‐span, wing‐area, gravity and air density; for birds with passerine‐type flight the power‐fraction has also to be considered. We tested Pennycuick’s general allometric model and estimated the coefficients based on our data. The general model explained a high proportion of variation in wing‐beat frequency and the coefficients differed only slightly from Pennycuick’s original values. Modelling continuous‐flapping flyers alone resulted in coefficients not different from those predicted (within 95% intervals). Doing so for passerine‐type birds resulted in a model with non‐significant contributions of body‐mass and wing‐span to the model. This was mainly due to the very high correlation between body‐mass, wing‐span and wing‐area, revealing similar relative scaling properties within this flight type. However, wing‐beat frequency increased less than expected with respect to power‐fraction, indicating that the drop in flight level during the non‐flapping phases, compensated by the factor (g/q)^0.5 in Pennycuick’s model, is smaller than presumed. This may be due to lift produced by the body during the bounding phase or by only partial folding of the wings.     

Aerodynamic performance of a hovering hawkmoth with flexible wings: a computational approach

Insect wings are deformable structures that change shape passively and dynamically owing to inertial and aerodynamic forces during flight. It is still unclear how the three-dimensional and passive change of wing kinematics owing to inherent wing flexibility contributes to unsteady aerodynamics and energetics in insect flapping flight. Here, we perform a systematic fluid-structure interaction based analysis on the aerodynamic performance of a hovering hawkmoth, Manduca, with an integrated computational model of a hovering insect with rigid and flexible wings. Aerodynamic performance of flapping wings with passive deformation or prescribed deformation is evaluated in terms of aerodynamic force, power and efficiency. Our results reveal that wing flexibility can increase downwash in wake and hence aerodynamic force: first, a dynamic wing bending is observed, which delays the breakdown of leading edge vortex near the wing tip, responsible for augmenting the aerodynamic force-production; second, a combination of the dynamic change of wing bending and twist favourably modifies the wing kinematics in the distal area, which leads to the aerodynamic force enhancement immediately before stroke reversal. Moreover, an increase in hovering efficiency of the flexible wing is achieved as a result of the wing twist. An extensive study of wing stiffness effect on aerodynamic performance is further conducted through a tuning of Young's modulus and thickness, indicating that insect wing structures may be optimized not only in terms of aerodynamic performance but also dependent on many factors, such as the wing strength, the circulation capability of wing veins and the control of wing movements.     

Discrete design of enzyme kinetic experiments

The usefulness of discrete designs in enzyme kinetics as an alternative to continuous designs is discussed in this paper, focusing on designs satisfying the D-optimality criterion. This study has been carried out using a program called DODID, specifically devised for this purpose, which is available by request to the authors. The results presented in this paper show that the relative efficiency of the D-optimal discrete designs with respect to the continuous ones increases rapidly when increasing the number of possible values for the control variables. Relative efficiencies higher than 0.98 are achieved when using 20 possible values for each variable. The power of the tools provided by the computational approach of this work is proved by the analysis made on the robustness of different designs for estimating the kinetic parameters when a wrong assumption on the error structure has been made. The robustness of the designs made assuming medium constant error (error variance proportional to the true response) is thus confirmed. A comparative study of several discriminating designs is also presented. The results obtained show that the designs produced by adding the optimal discrete designs corresponding to both candidate models plus the point where the weighted difference between the predicted values is maximum, is a good choice when designing an experiment for discrimination.     

Genetic variation for the positioning of wing veins in Drosophila melanogaster

SUMMARY To define the components of variation for wing shape in Drosophila in relation to what is known about the developmental control of wing patterning, we have characterized shape variation in the wings of 12 randomly chosen highly inbred lines. Despite large differences in wing size between males and females, and between flies reared at 18°C or 25°C, wing shape is remarkably unaffected by these variables and is highly line specific. The shape of each intervein region of the wing appears to be independently regulated at the genetic level, consistent with the role of secreted growth factors in establishing the locations of wing veins. Sex and temperature were found to have different effects on cell number in two intervein regions, with the result that wing shape is to a large extent independent of cell density. Dietary cholesterol was also shown to affect the breadth of the central intervein region, consistent with an effect on the strength of Hedgehog signaling during wing development. We conclude that wing shape is under tighter genetic control than wing size, and hypothesize that this control is achieved in large part by gene activity at the level of wing vein determination and differentiation.