Risk‐taking and the evolution of mechanisms for rapid escape from predators

Flight initiation distance (FID) is the distance at which an individual animal takes flight when approached by a human. This behavioural measure of risk‐taking reflects the risk of being captured by real predators, and it correlates with a range of life history traits, as expected if flight distance optimizes risk of predation. Given that FID provides information on risk of predation, we should expect that physiological and morphological mechanisms that facilitate flight and escape predict interspecific variation in flight distance. Haematocrit is a measure of packed red blood cell volume and as such indicates the oxygen transport ability and hence the flight muscle contracting reaction of an individual. Therefore, we predicted that species with short flight distances, that allow close proximity between a potential prey individual and a predator, would have high haematocrit. Furthermore, we predicted that species with large wing areas and hence relatively low costs of flight and species with large aspect ratios and hence high manoeuvrability would have evolved long flight speed. Consistent with these predictions, we found in a sample of 63 species of birds that species with long flight distances for their body size had low levels of haematocrit and large wing areas and aspect ratios. These findings provide evidence consistent with the evolution of risk‐taking behaviour being underpinned by physiological and morphological mechanisms that facilitate escape from predators and add to our understanding of predator–prey coevolution.     

Transition between moult and migration in a long-distance migratory passerine: organ flexibility in the African wintering area

Phenotypic flexibility of organs in migratory birds has been documented for a variety of species of different genera during the migratory period. However, very little is known about phenotypic mass changes of organs with respect to other events within the annual cycle. This seems particularly interesting when birds face different physiological challenges in quick succession. We investigated mass changes of 13 organs from garden warblers (Sylvia borin) during the transition from moult to migration. These long-distance migratory birds perform a complete moult within their wintering area just shortly before the onset of spring migration. Birds were sampled in three successive stages according to their moult status: group I consisted of birds with growing primary or secondary wing feathers, group II consisted of birds with completed wing moult but with still moulting body feathers, and group III consisted of birds that had completed wing moult and body moult. Size-corrected flight muscle, kidney mass, and pancreas mass differed significantly among the three groups. Flight muscle was heaviest in birds that were about to leave their wintering area (group III) compared with birds still in body moult (group II). Kidney and pancreas showed a pattern similar to each other, with the heaviest mass occurring in birds with moulting wing feathers (group I) and significantly reduced mass in birds that had completed wing moult (group II) or both wing and body moult (group III). Mass reductions of kidney and pancreas during the transition from moult to migration are considered to be related to the demands of moult, while increased flight muscle may be due to moult, migration, or both. Phenotypic mass changes of organs in birds occur during their migration, but they also occur during the transition between other phases of the annual cycle such as moult and migration and are not restricted to the flight muscle.     

Morphological adaptation of the digestive tract in relation to feeding ecology of raptors

The study examines some aspects of gross morphology in Falconiformes and Strigiformes. It is hypothesized that, in predatory birds, hunting strategy might influence the relative size of skeletal musculature and length of the digestive tract. Falconiform species were categorized as either 'attackers' or 'searchers' depending on the degree to which active, powered pursuit is required for prey capture. Attacking species feed predominantly on avian prey, requiring extreme agility, speed and acceleration for prey capture. Searchers feed largely on relatively slow-moving mammals and carrion. Comparisons between species of attackers and searchers showed that the former had heavier pectoral muscle mass, larger areas for flight muscle attachment and higher linearized wing loadings. Strigiformes had a pectoral muscle mass only half the size of that of attacking Falconiformes and had a correspondingly smaller sternum area. A skeletal body-size measure was determined to enable calculation of intestine length independent of body-size and shape differences. Attacking species have a small intestine which is 20–30% shorter than would be predicted on the basis of body-size and 50% shorter than found in searchers of equivalent body-size. Strigiformes that locate prey by active flight also have intestinal tracts shorter than expected. The likely effects of intestine length on digestive efficiency and food utilization are discussed and it is suggested that, in predatory birds, some species have evolved alimentary tracts that are shorter than necessary for maximum digestive efficiency in order to enhance prey capture.     

Cross sectional geometry of the forelimb skeleton and flight mode in pelecaniform birds

Avian wing elements have been shown to experience both dorsoventral bending and torsional loads during flapping flight. However, not all birds use continuous flapping as a primary flight strategy. The pelecaniforms exhibit extraordinary diversity in flight mode, utilizing flapping, flap‐gliding, and soaring. Here we (1) characterize the cross‐sectional geometry of the three main wing bone (humerus, ulna, carpometacarpus), (2) use elements of beam theory to estimate resistance to loading, and (3) examine patterns of variation in hypothesized loading resistance relative to flight and diving mode in 16 species of pelecaniform birds. Patterns emerge that are common to all species, as well as some characteristics that are flight‐ and diving‐mode specific. In all birds examined, the distal most wing segment (carpometacarpus) is the most elliptical (relatively high I_max/I_min) at mid‐shaft, suggesting a shape optimized to resist bending loads in a dorsoventral direction. As primary flight feathers attach at an oblique angle relative to the long axis of the carpometacarpus, they are likely responsible for inducing bending of this element during flight. Moreover, among flight modes examined the flapping group (cormorants) exhibits more elliptical humeri and carpometacarpi than other flight modes, perhaps pertaining to the higher frequency of bending loads in these elements. The soaring birds (pelicans and gannets) exhibit wing elements with near‐circular cross‐sections and higher polar moments of area than in the flap and flap‐gliding birds, suggesting shapes optimized to offer increased resistance to torsional loads. This analysis of cross‐sectional geometry has enhanced our interpretation of how the wing elements are being loaded and ultimately how they are being used during normal activities. J. Morphol., 2011. © 2011 Wiley‐Liss,Inc.     

Flight speeds among bird species: allometric and phylogenetic effects

Flight speed is expected to increase with mass and wing loading among flying animals and aircraft for fundamental aerodynamic reasons. Assuming geometrical and dynamical similarity, cruising flight speed is predicted to vary as (body mass)^1/6 and (wing loading)^1/2 among bird species. To test these scaling rules and the general importance of mass and wing loading for bird flight speeds, we used tracking radar to measure flapping flight speeds of individuals or flocks of migrating birds visually identified to species as well as their altitude and winds at the altitudes where the birds were flying. Equivalent airspeeds (airspeeds corrected to sea level air density, U_e) of 138 species, ranging 0.01–10 kg in mass, were analysed in relation to biometry and phylogeny. Scaling exponents in relation to mass and wing loading were significantly smaller than predicted (about 0.12 and 0.32, respectively, with similar results for analyses based on species and independent phylogenetic contrasts). These low scaling exponents may be the result of evolutionary restrictions on bird flight-speed range, counteracting too slow flight speeds among species with low wing loading and too fast speeds among species with high wing loading. This compression of speed range is partly attained through geometric differences, with aspect ratio showing a positive relationship with body mass and wing loading, but additional factors are required to fully explain the small scaling exponent of U_e in relation to wing loading. Furthermore, mass and wing loading accounted for only a limited proportion of the variation in U_e. Phylogeny was a powerful factor, in combination with wing loading, to account for the variation in U_e. These results demonstrate that functional flight adaptations and constraints associated with different evolutionary lineages have an important influence on cruising flapping flight speed that goes beyond the general aerodynamic scaling effects of mass and wing loading.     

Relationships between morphological parameters in birds with different flying habits

1. Data on morphological and physiological parameters from 346 species of birds were collected from diverse sources. 2. The observed relationships among some pairs of variables showed differences between the five flight styles into which the studied birds were classified. 3. The characteristic kind of flight for each species is related to four easily obtainable non-invasive parameters: body weight (BW), wing area (WA), wing span (WS) and boyd length (BL). 4. Wing-loading index (BW2/3/WA) gives the most effective variable to describe the flying habits of any species.     

Forelimb skeletal morphology and flight mode evolution in pelecaniform birds

The total length and mid-shaft diameters of wing elements of 50 species of pelecaniform birds were examined to investigate how forelimb skeletal morphology varies with body size and flight mode within this group. Pelecaniforms were assigned to flight mode categories based on primary habitual behaviors (soar, flap–glide, continuous flap). Allometric and discriminant function analyses were conducted on wing element variables in both historical (using independent contrasts) and ahistorical contexts. Results of this study indicate that when phylogenetic relationships are taken into account, only the length of the ulna scales with positive allometry, whereas all other variables exhibit isometry. These results differ from the ahistorical allometric analysis. Discriminant function analysis (DFA) significantly separated the flight mode groups (Wilk's λ=0.002, p<0.00001), with only six individuals from two species (out of n=284) misclassified. Results of historical canonical variates analysis supported the ahistorical DFA and identified two carpometacarpal (CMC) variables as important for separating the flight mode groups: dorsoventral CMC diameter and total CMC length. The carpometacarpus is that portion of the forelimb skeleton that serves as the attachment point for the primary flight feathers, and thus, that portion of the airfoil surface that mediates detailed flight control. Its morphology, more than any other element, reflects differences in flight mode in pelecaniforms. Results of this study indicate that, in pelecaniforms, wing bones generally exhibit isometry (with the exception of the ulna) and do possess specific morphologies reflective of the demands associated with different types of aerial locomotor specialization.     

SOARING BEHAVIOUR AND PERFORMANCE OF SOME EAST AFRICAN BIRDS, OBSERVED FROM A MOTOR-GLIDER

Various species of soaring birds were studied by following them in a motor-glider, mainly over the Serengeti National Park, Tanzania. The characteristics of thermal convection in the study area are described in general terms. The two vulture species of the genus Gyps live by scavenging among the herds of migratory ungulates, especially Wildebeest. They are not territorial, and gather in large numbers on kills. When raising young they may be obliged by game movements to forage at long distances from their nests. Their cross-country performance is adequate for a foraging radius of over 100 km in dry-season conditions. Their ability to compete with Spotted Hyaenas is thought to depend partly on this factor and partly on an advantage in arriving early at kills. These two species appear to find food more by watching other vultures than by searching for it directly. The Lappet-faced and White-headed Vultures are thought to be sedentary, and to depend on thorough searching of a fixed foraging territory, rather than on following migratory game. They have lower wing loadings than the Gyps vultures, and were not seen cross-country flying. They never gather in large numbers. The Hooded Vulture is a solitary nester, but it does fly across country, and does gather at kills. Vultures soar individually, and seem to be good at exploiting such phenomena as thermal streets. They do not travel in flocks. Tawny and Martial Eagles react positively to the glider, and are suspected of regarding it as potential prey. White Storks migrate between Europe and Africa, and also travel about within East Africa, by thermal soaring. They soar in flocks, and unlike vultures rely on co-ordinated social behaviour to locate thermals. In choosing their route, they often fail to react to obvious weather signs. They enter cumulus clouds from the bottom when thermalling, but probably do not climb far above cloudbase. Marabou Storks soar individually, but also sometimes travel in flocks. When doing so, they show less lateral spreading than White Storks, which reduces the effectiveness of the flock as a thermal-finding unit; on the other hand, they do seem to react to visible weather signs, like vultures or glider pilots. White Pelicans, which travel by thermal soaring between different lakes in the Rift Valley, show the most highly co-ordinated social soaring behaviour. Unlike White Storks, they fly in formation even when circling. Storks and pelicans showed more signs of alarm when approached by the glider than did the vultures or birds of prey. This could be due to their being preyed upon in flight, for instance by Martial Eagles. The basis of conventional thermal cross-country flying is outlined, and it is explained why the high wing loadings of the Gyps vultures are appropriate to their peripatetic habits. A method of thermal soaring without circling is discussed, and shown to be more readily feasible for small than for large birds. Some differences in soaring techniques between birds and glider pilots are interpreted in the light of this calculation. A case in which Black Kites apparently used this technique to soar in random turbulence is described. The cross-country speed attainable by thermal soaring should be similar to the cruising speed under power in both large and small birds. Rough calculations of the energy costs suggest that a large bird (White Stork) should reduce its fuel consumption by a factor of 23 by soaring rather than flying under power, whereas this factor would be only 2–4 for a small bird (Bonelli's Warbler). Other reasons why thermal soaring is an advantageous means of travel for large but not for small birds are also indicated.     

Flight threshold, wing muscle histolysis, and alary polymorphism: correlated traits for dispersal tendency in the Gerridae

ABSTRACT. 1. This paper tests the hypothesis that selection for dispersal ability within a species influences not only the occurrence and extent of wing reduction but also the tendency or ability of the macropterous individuals to fly.
2. Flight thresholds of four species of waterstriders (Hemiptera; Gerridae) were assessed using a tethered flight technique. The species tested varied from monomorphic macropterous ( Limnoporus dissortis Drake and Harris), through seasonally polymorphic ( Gerris comatus Drake and Hottes and G. buenoi Kirkaldy), to primarily apterous ( G.remigis Say).
3. Condition of the indirect, mesothoracic flight muscles, and presence or absence of mature or developing eggs (for females) were determined by dissection of all individuals immediately following flight testing. Only individuals with normal muscles were included in the analysis of flight thresholds.
4. Comparisons among species revealed that average flight threshold and extent of flight muscle histolysis were negatively associated with the proportion of macropterous individuals. Wing reduction was also associated with significant seasonal variation in flight threshold, particularly among females.
5. These results support our initial hypothesis, and further indicate that, within the Gerridae, dispersal tendency depends not only on the proportion of macropters but also on the dispersal capability of the macropterous individuals.     

The gliding speed of migrating birds: slow and safe or fast and risky?

Aerodynamic theory postulates that gliding airspeed, a major flight performance component for soaring avian migrants, scales with bird size and wing morphology. We tested this prediction, and the role of gliding altitude and soaring conditions, using atmospheric simulations and radar tracks of 1346 birds from 12 species. Gliding airspeed did not scale with bird size and wing morphology, and unexpectedly converged to a narrow range. To explain this discrepancy, we propose that soaring‐gliding birds adjust their gliding airspeed according to the risk of grounding or switching to costly flapping flight. Introducing the Risk Aversion Flight Index (RAFI, the ratio of actual to theoretical risk‐averse gliding airspeed), we found that inter‐ and intraspecific variation in RAFI positively correlated with wing loading, and negatively correlated with convective thermal conditions and gliding altitude, respectively. We propose that risk‐sensitive behaviour modulates the evolution (morphology) and ecology (response to environmental conditions) of bird soaring flight.     

Morphology, Velocity, and Intermittent Flight in Birds

Body size, pectoralis composition, aspect ratio of the wing,and forward speed affect the use of intermittent flight in birds.During intermittent non-flapping phases, birds extend theirwings and glide or flex their wings and bound. The pectoralismuscle is active during glides but not during bounds; activityin other primary flight muscles is variable. Mechanical power,altitude, and velocity vary among wingbeats in flapping phases;associated with this variation are changes in neuromuscularrecruitment, wingbeat frequency, amplitude, and gait. Speciesof intermediate body mass (35–158 g) tend to flap-glideat slower speeds and flap-bound at faster speeds, regardlessof the aspect ratio of their wings. Such behavior may reducemechanical power output relative to continuous flapping. Smallerspecies (<20 g) with wings of low aspect ratio may flap-boundat all speeds, yet existing models do not predict an aerodynamicadvantage for the flight style at slow speeds. The behaviorof these species appears to be due to wing shape rather thanpectoralis physiology. As body size increases among species,percent time spent flapping increases, and birds much largerthan 300 g do not flap-bound. This pattern may be explainedby adverse scaling of mass-specific power or lift per unit poweroutput available from flight muscles. The size limit for theability to bound intermittently may be offset somewhat by thescaling of pectoralis composition. The percentage of time spentflapping during intermittent flight also varies according toflight speed.     

Wing size but not wing shape is related to migratory behavior in a soaring bird

Both wing size and wing shape affect the flight abilities of birds. Intra and inter‐specific studies have revealed a pattern where high aspect ratio and low wing loading favour migratory behaviour. This, however, have not been studied in soaring migrants. We assessed the relationship between the wing size and shape and the characteristics of the migratory habits of the turkey vulture Cathartes aura, an obligate soaring migrant. We compared wing size and shape with migration strategy among three fully migratory, one partially migratory and one non‐migratory (resident) population distributed across the American continent. We calculated the aspect ratio and wing loading using wing tracings to characterize the wing morphology. We used satellite‐tracking data from the migratory populations to calculate distance, duration, speed and altitude during migration. Wing loading, but not aspect ratio, differed among the populations, segregating the resident population from the completely migratory ones. Unlike what has been reported in species using flapping flight during migration, the migratory flight parameters of turkey vultures were not related to the aspect ratio. By contrast, wing loading was related to most flight parameters. Birds with lower wing loading flew farther, faster, and higher during their longer journeys. Our results suggest that wing morphology in this soaring species enables lower‐cost flight, through low wing‐loading, and that differences in the relative sizes of wings may increase extra savings during migration. The possibility that wing shape is influenced by foraging as well as migratory flight is discussed. We conclude that flight efficiency may be improved through different morphological adaptations in birds with different flight mechanisms.     

Comparing aerodynamic efficiency in birds and bats suggests better flight performance in birds

Flight is one of the energetically most costly activities in the animal kingdom, suggesting that natural selection should work to optimize flight performance. The similar size and flight speed of birds and bats may therefore suggest convergent aerodynamic performance; alternatively, flight performance could be restricted by phylogenetic constraints. We test which of these scenarios fit to two measures of aerodynamic flight efficiency in two passerine bird species and two New World leaf-nosed bat species. Using time-resolved particle image velocimetry measurements of the wake of the animals flying in a wind tunnel, we derived the span efficiency, a metric for the efficiency of generating lift, and the lift-to-drag ratio, a metric for mechanical energetic flight efficiency. We show that the birds significantly outperform the bats in both metrics, which we ascribe to variation in aerodynamic function of body and wing upstroke: Bird bodies generated relatively more lift than bat bodies, resulting in a more uniform spanwise lift distribution and higher span efficiency. A likely explanation would be that the bat ears and nose leaf, associated with echolocation, disturb the flow over the body. During the upstroke, the birds retract their wings to make them aerodynamically inactive, while the membranous bat wings generate thrust and negative lift. Despite the differences in performance, the wake morphology of both birds and bats resemble the optimal wake for their respective lift-to-drag ratio regimes. This suggests that evolution has optimized performance relative to the respective conditions of birds and bats, but that maximum performance is possibly limited by phylogenetic constraints. Although ecological differences between birds and bats are subjected to many conspiring variables, the different aerodynamic flight efficiency for the bird and bat species studied here may help explain why birds typically fly faster, migrate more frequently and migrate longer distances than bats.     

On the ftight capabilities and distribution of the giant Miocene bird Argentavis magnificens (Teratornithidae)

Argentavis magnificens , the largest known flying bird, had a wingspan of over 6 m with a mass of 80 kg. Its enormous size suggests that it was not a powerful flapper. The wing shape is inferred as more like that of large extant birds that soar relatively slowly on thermals over land than of large pelagic birds that soar over water. Its high wing loading would have allowed it to fly in moderate to strong winds that must have been prohibitive for the largest known contemporary thermal soarers. The high wing loading would have been ill-suited to flight under poor thermal conditions, but it would have been useful in slope-soaring on uprising air current against hillsides. We propose that Argentavis had a large home range that included a nesting area in the mountains of western and northwestern Argentina, and a feeding area in the Pampas.     

Changes in diet and morphology of Finnish goshawks from 1960s to 1990s

We studied the morphology of the goshawk in northern Finland by measuring skin and skeletal characters of 258 museum specimens dated between 1961 and 1997. We predicted a decrease in the size of male goshawks from the 1960s because availability of their main prey, grouse, has decreased since then and grouse have been replaced in the diet by smaller prey during the breeding season. Based on the assumption that winter is the most critical period for females, we predicted that female size should have increased because their winter diet consisted of more and more mountain hare, which is a prey generally larger than grouse. Analyses revealed that male size has indeed decreased since the 1960s, while adult females have increased in size. Our data suggest that these morphological shifts were the result of selective pressures due to changes in diet. We also found changes in the (size-independent) shape of the hawks. Relative wing and tail lengths of adult hawks became longer between 1980 and 1990 compared with the 1960–1970 period, while relative juvenile wing and tail lengths tended to decrease. As a result of these morphological changes size dimorphism between the sexes increased from the 1960s to the 1990s. Received: 18 January 1999 / Accepted: 14 July 1999     

Gliding flight in the American Kestrel (Falco sparverius): An electromyographic study

Electromyographic (EMG) activity was studied in American Kestrels (Falco sparverius) gliding in a windtunnel tilted to 8 degrees below the horizontal. Muscle activity was observed in Mm. biceps brachii, triceps humeralis, supracoracoideus, and pectoralis, and was absent in M. deltoideus major and M. thoracobrachialis (region of M. pectoralis). These active muscles are believed to function in holding the wing protracted and extended during gliding flight. Quantification of the EMG signals showed a lower level of activity during gliding than during flapping flight, supporting the idea that gliding is a metabolically less expensive form of locomotion than flapping flight. Comparison with the pectoralis musculature of specialized gliding and soaring birds suggests that the deep layer of the pectoralis is indeed used during gliding flight and that the slow tonic fibers found in soaring birds such as vultures represents a specialization for endurant gliding. It is hypothesized that these slow fibers should be present in the wing muscles that these birds use for wing protraction and extension, in addition to the deep layer of the pectoralis. © 1993 Wiley-Liss, Inc.     

GENETIC CORRELATIONS AMONG TRAITS DETERMINING MIGRATORY TENDENCY IN THE SAND CRICKET,GRYLLUS FIRMUS

Migration by flight is an important component of the life cycles of most insects. The probability that a given insect will migrate by flight is influenced by many factors, most notably the presence or absence of fully-developed wings and functional flight musculature. Considerable variation has also been reported in the flight propensity of fully-winged individuals with functional flight musculature. We test the hypothesis that these components of migratory tendency are genetically correlated in a wing-dimorhic cricket, Gryllus firmus. Flight propensity and condition of the dorsal longitudinal flight muscles (DLM) are examined in fully-winged (LW) crickets from lines selected for increasing and for decreasing %LW, as well as from unselected control lines. Increased %LW is found to be associated with increased flight propensity among individuals with intact DLM, and with retention of functional DLM. The opposite is true for lines selected for decreased %LW. These results indicate both phenotypic and genetic correlations among behavioral, physiological, and morphological traits determining migratory tendency. We propose that these correlations may result from the multifunctional role of juvenile hormone, which has been reported to influence wing development, flight muscle development and degeneration, and flight propensity. Finally, we discuss the potential influence of genetic correlations for migratory traits on the evolution and maintenance of migratory polymorphisms in insects.     

Impact injuries and probability of survival in a large semiurban endemic pigeon in New Zealand, Hemiphaga novaeseelandiae

The New Zealand Pigeon or kereru (Hemiphaga novaeseelandiae) frequently collides with windows and vehicles. In this study of 146 kereru collected from 1996 to 2009, we used 118 radiographs and 91 necropsies to determine skeletal and soft tissue injuries. Vehicle collisions resulted in more damage to the extremities (wing and femur), whereas collisions with windows resulted in trauma to the head, fractures/dislocations of the coracoids and clavicles, and ruptured internal organs. Soft tissue injuries included damage to the flight muscles and heart ruptures caused by fractured coracoid bones, as well as extensive bruising of pectoral muscles and hemorrhaging of the lungs. Rehabilitation time was not related to number of skeletal injuries sustained, nor was the time until death for those that did not survive. In general, kereru with greater numbers of injuries were less likely to survive rehabilitation. Flight speed and force calculations suggest that a 570-g kereru would collide with 3-70 times the force of smaller birds (5-180 g); this may explain the discrepancies between the injuries characterized here and those reported for North American passerines. The differences in injuries sustained from collisions with windows and cars can be used to inform rehabilitators about the possible nature of injuries if the source of impact is known.     

A comparative study of the mechanics of the pectoralis muscle of the red‐tailed hawk and the barred owl

A comparison of the isometric forces and levers of the pectoralis muscle in red‐tailed hawks (Buteo jamaicensis) and barred owls (Strix varia) was done to identify differences that may correlate with their different flight styles. The pectoralis consists of two heads, the anterior m. sternobrachialis (SB) and the posterior m. thoracobrachialis (TB). These are joined at an intramuscular tendon and are supplied by separate primary nerve branches. As in other birds, the two heads have distinct fiber orientations in red‐tailed hawks and barred owls. SB's fiber orientation (posterolateral and mediolateral from origin to insertion) provides pronation and protraction of the humerus during adduction. Electromyographic studies in pigeons show that it is active in early downstroke and during level flight. TB is more active during take‐off and landing in pigeons. The anterolateral orientation (from origin to insertion) of its fibers provides a retractive component to humeral adduction used to control the wing during landing. In our study, the maximum isometric force produced by the combined pectoralis heads did not differ significantly between the hawk and owl, however, the forces were distributed differently between the two muscle heads. In the owl, SB and TB were capable of producing equal amounts of force, but in the hawk, SB produced significantly less force than did TB. This may reflect the need for a large TB to control landing in both birds during prey‐strike, with the owl maintaining both protractive (using SB) and retractive (using TB) abilities. Pronation and protraction may be less important in the flight behavior of the hawk, but its prey‐strike behavior may require the maintenance of a substantial TB for braking and controlled stalling, as it initiates strike behavior. J. Morphol. 2012. © 2011 Wiley Periodicals, Inc.     

Central projections of the wing afferents in the hawkmoth, Agrius convolvuli

Flight behaviors in various insect species are closely correlated with their mechanical and neuronal properties. Compared to locusts and flies which have been intensively studied, moths have “intermediate” properties in terms of the neurogenic muscle activations, power generation by indirect muscles, and two-winged-insect-like flapping behavior. Despite these unique characteristics, little is known about the neuronal mechanisms of flight control in moths. We investigated projections of the wing mechanosensory afferents in the central nervous system (CNS) of the hawkmoth, Agrius convolvuli, because the mechanosensory proprioceptive feedback has an essential role for flight control and would be presumably optimized for insect species. We conducted anterograde staining of nine afferent nerves from the fore- and hindwings. All of these afferents projected into the prothoracic, mesothoracic and metathoracic ganglia (TG1, 2 and 3) and had ascending fibers to the head ganglia. Prominent projection areas in the TG1–3 and suboesophageal ganglion (SOG) were common between the forewing, hindwing and contralateral forewing afferents, suggesting that information from different wings are converged at multiple levels presumably for coordinating wing flapping. On the other hand, differences of projections between the fore- and hindwing afferents were observed especially in projection areas of the tegulae in the TG1 and contralateral projections of the anterior forewing nerve in the TGs and SOG, which would reflect functional differences between corresponding mechanoreceptors on each wing. Afferents comprising groups of the campaniform sensilla at the wing bases had prominent ascending pathways to the SOG, resembling the head–neck motor system for gaze control in flies. Double staining of the wing afferents and flight or neck motoneurons also indicated potential connectivity between them. Our results suggest multiple roles of the wing proprioceptive feedback for flight and provide the anatomical basis for further understanding of neuronal mechanisms of the flight system in moths.