Wing Hinge Research Articles

Temperature dependence and response characteristics of the isolated wing hinge stretch receptor in the locust

1. A preparation is described by which the wing hinge stretch receptor (SR) ofLocusta migratoria is mechanically isolated so that it can be subjected to stretch stimuli while avoiding interference with wing hinge mechanics. 2. Using this approach and sinusoidal stretches of different amplitudes the SR can be stimulated up to a definite saturation frequency. The discharge frequency at a given stretch and the saturation frequency both depend dramatically on ambient temperature. High instantaneous frequencies (up to 650 Hz, as found in flying locusts) were only obtained at a high temperature of 32 °C. 3. The instantaneous spike frequency of the SR in response to short stretches (within the time range of wing beat period) reflects exactly the amount of the stretch and not its rate of change. Thus, the SR is a receptor signalling the momentary position of the sclerites to which it is attached.

Structure and innervation of the third axillary muscle of Manduca relative to its role in turning flight.

The morphology, ultrastructure, innervation and physiology of the third axillary muscle in Manduca sexta were examined to investigate the role of this muscle in flight. The muscle consists of three parts: the upper bundle, which originates on the episternum, and the middle and lower bundles, which originate on the epimeron; all three parts insert on the tip of a projection from the third axillary sclerite. The middle bundle is composed of tonic fibres, and is innervated by a single slow axon, while the other two bundles consist of intermediate fibres and are each innervated by a single fast axon. The shape and position of the third axillary sclerite within the wing hinge are such that its primary function appears to be remotion of the wing. The length of the third axillary muscle determines the amount of remotion, independency of the degree of elevation or depression of the wing and independently of the amount of remotion of the contralateral wing. Electrophysiological recordings from the three parts of the muscle during tethered flight indicate that they may each function independently of each other and in different ways. The tonic (middle) bundle is capable of maintaining tension to hold the wings in the folded position at rest and is active when the wings are folded at the end of flight. The intermediate (upper and lower) bundles are activated phasically with impulses that may occur with various relationships to the timing of activation of a direct depressor, the subalar, or of several of the elevators. The findings are consistent with the hypothesis that the third axillary muscles on both sides are important in determining the asymmetric degrees of remotion observed in turning flight.

The Central Nervous Organization of the Motor Neurones to a Steering Muscle In Locusts

ABSTRACT The pleuroaxillary or pleuroalar muscles of the locust (M85, Ml 14) are located in the meso- and metathoracic segments only. Each extends from the posterior face of the pleural ridge and runs dorsally and obliquely, inserting on the third axillary sclerite of the wing hinge. Each muscle consists of two distinct parts, a and b (Fig. 1). Each pleuroaxillary muscle is innervated by two motor neurones which give rise to a small and a large muscle potential in electromyogram recordings (Fig. 6E). The cell body of each neurone lies posteriorly in the ganglion and the axon runs out in nerve 4 (Figs 3–6). The two motor neurones of a particular muscle share many common morphological features (Figs 3–6). There is also clear segmental homology between the motor neurones supplying the meso- and metathoracic muscles (Fig. 3). Serial transverse sections of the motor neurones show that their arborization is confined mainly to a dorsal region of the neuropile. Some of the collaterals encompass, and terminate in, dorsal longitudinal tracts. Branching extends far anteriorly. Posteriorly, one secondary neurite runs ventrally (Figs 7, 8). A few secondary and tertiary neurites of the metathoracic pleuroaxillary motor neurones terminate within the neuropile of the first abdominal neuromere (Figs 6, 8). Additional features which distinguish these neurones from other flight motor neurones are discussed.

Apparent genetic complexity generated by developmental thresholds: the apterous locus in Drosophila melanogaster.

Mutations at the apterous (ap) locus in Drosophila melanogaster give rise to three distinct phenotypes: aberrant wings, female sterility and precocious adult death. The wing phenotype includes five types of abnormality: blistering, deficiencies, duplications, high-order repetitions and transformation of structures. The mildest phenotype is seen with homozygous apblt animals which have either normal or slightly blistered wings. Most alleles produce, in the homozygote, a deficient wing in which part or all of the wing margin and wing blade is missing, but wing hinge and notum regions are normal. Animals hemizygous for each of 20 ap alleles, as well as apID/apXa heterozygotes, show duplication of parts of the notum associated with complete wing deficiency. Animals heterozygous for apc and the other tested ap alleles show repetitions of parts of the anterior wing margin, an engrailed-like transformation of posterior wing margin into anterior margin or both. Both apblt and apc show similar phenotypes in homozygotes and hemizygotes, yet both produce a less extreme phenotype than that of the other hemizygotes, suggesting that neither mutation causes loss of the entire ap+ function. The 15 alleles that cause precocious death and female sterility occur in six complementation groups based on complementation for these phenotypes. This supports the previous conclusion that the effects of apterous mutations on the wing do not correlate with their effects on viability and fertility. We propose an explanation for the effects of apterous mutations on the wing in which quantitative reductions in the activity of gene product give rise to qualitatively different phenotypes because of different threshold requirements of the ap+ function for critical events in wing disc development.

Isolation and characterization of temperature-sensitivelethal (2) giant larva alleles : I. Mutagenesis and larval pathology.

EMS induced temperature-sensitivelethal (2) giant larva, 1(2)gl, alleles were isolated by screening against a knownl(2)gl allele. Analysis of the lethal phase of thel(2)gl ts-deficiency heterozygotes demonstrated: (1) the majority of thel(2)gl tslarvae survive to late third instar, (2) at 29°C the majority of thel(2)gl tslarvae failed to pupate and only rarely did they differentiate adult cuticular structures, (3) at 15°C the majority of the larvae pupated and frequently differentiated adult cuticular structures. Examination of the imaginal discs ofl(2)gl tslarvae reared at 29°C revealed the presence of morphologically abnormal wing, haltere and leg imaginal discs. No morphologically abnormal discs were found in thel(2)gl tslarvae reared at 15°C. Studies on both the histology and the developmental capacity of the morphologically normal and abnormall(2)gl tsdiscs were performed. The morphologically normal discs are histologically normal and produce a full complement of adult cuticular structures. However, the morphologically abnormal discs contained both regions that maintained the normal monolayer epithelium and regions that had lost the normal tissue architecture. The implants obtained when the morphologically abnormal discs are injected into metamorphosing larvae contained only a limited number of the normal complement of adult structures and usually only structures found in the ventral wing hinge region were recovered. In addition, the "metamorphosed" morphologically abnormal discs contained undifferentiated tissue that gave rise to transplantable neoplasms when cultured in adults. The results of the studies on the pathology of thel(2)gl tslarvae are discussed with respect to the role of thel(2)gl tsfunction during normal development, the autonomy of the neoplastic development of thel(2)gl tstissues, and similarities between neoplastic development inDrosophila and mammals.

Occurrence of Resilin in Elastic Structures in the Food-Pump of Reduviid Bugs

ABSTRACT Resilin is a naturally occurring rubber. It is extremely efficient, returning almost all the energy stored during its deformation. Resilin was first described by Weis-Fogh (1960), who with Andersen (Andersen & Weis-Fogh, 1964) produced an extensive review covering the identification, physical and chemical properties of the substance. Andersen & Weis-Fogh set out five diagnostic characters for resilin and reported five sites of resilin occurrence: the wing hinge in all insects studied, includingSchistocerca gregaria and Periplaneta americana; tendons in Aeshna cyanea and Calliphora ery-throcephala; the hindleg spring of various fleas; the abdominal spring of Oryctes sp. and Melolontha sp.; and the clypeolabral spring of Schistocerca gregaria. This communication reports the occurrence of resilin in the food-pump of Reduviid bugs and discusses its functional significance.

Differentiation of an identified sensory neuron (SR) and associated structures (CTO) in grasshopper embryos.

The differentiation of an identified sensory neuron, the grasshopper wing hinge Stretch Receptor (SR), is examined throughout embryogenesis. The morphological features of the SR axon, as it finds its path from the peripheral cell body to the CNS, and the timing of this peripheral growth were determined by intracellular injection of Lucifer yellow. The course of growth of the SR axon within the CNS and the sequence of formation of the identified branches in its characteristic central arborization were investigated by silver intensification of cobalt-stained axons. In addition, intracellular recording from the cell body of SR was used to determine the onset of electrical excitability and the characteristics of the somal action potential. A brief account of the differentiation of the closely associated wing hinge Chordotonal Organ is also given. During differentiation, the cell bodies of SR and the first wing hinge Chordotonal Organ neuron (CTN1) extended processes and migrate posteriorly along a peripheral epithelial ridge. The cell bodies migrate up to 150 micrometers with a group of undifferentiated cells to a specific site at the posterior edge of the segment. As the SR and CTN1 cell bodies migrate, their trailing axons stretch across the epithelial ridge. These axons from the medial body wall nerve (1D2) that the axons of subsequent sensory neurons follow.

High-frequency discharge of the locust wing hinge stretch receptor during flight

High-frequency discharge of the locust wing hinge stretch receptor during flight

Acquisition of differentiative capacity in imaginal wing discs of Drosophila melanogaster

The wing discs from larvae undergoing the moult from 1st to 2nd instar are able to differentiate some parts of the adult wing when forced to undergo a premature metamorphosis. The first structures which differentiate are parts of the wing hinge and the wing blade. As development proceeds and older discs are forced through metamorphosis, the capacity to differentiate moves out both proximally and distally until gradually all of the derivatives of a mature wing disc are formed. Individual structures often differentiate from young discs in an incomplete form and pattern elements, such as bristles or sensilla, are added as older discs are tested.

Origin and evolution of insect wings and their relation to metamorphosis, as documented by the fossil record.

In contemporary entomology the morphological characters of insects are not always treated according to their phylogenetic rank. Fossil evidence often gives clues for different interpretations. All primitive Paleozoic pterygote nymphs are now known to have had articulated, freely movable wings reinforced by tubular veins. This suggests that the wings of early Pterygota were engaged in flapping movements, that the immobilized, fixed, veinless wing pads of Recent nymphs have resulted from a later adaptation affecting only juveniles, and that the paranotal theory of wing origin is not valid. The wings of Paleozoic nymphs were curved backwards in Paleoptera and were flexed backwards at will in Neoptera, in both to reduce resistance during forward movement. Therefore, the fixed oblique-backwards position of wing pads in all modern nymphs is secondary and is not homologous in Paleoptera and Neoptera. Primitive Paleozoic nymphs had articulated and movable prothoracic wings which became in some modern insects transformed into prothoracic lobes and shields. The nine pairs of abdominal gillplates of Paleozoic mayfly nymphs have a venation pattern, position, and development comparable to that in thoracic wings, to which they are serially homologous. Vestigial equivalents of wings and legs were present in the abdomen of all primitive Paleoptera and primitive Neoptera. The ontogenetic development of Paleozoic nymphs was confluent, with many nymphal and subimaginal instars, and the metamorphic instar was missing. The metamorphic instar originated by the merging together of several instars of old nymphs; it occurred in most orders only after the Paleozoic, separately and in parallel in all modern major lineages (at least twice in Paleoptera, in Ephemeroptera and Odonata; separately in hemipteroid, blattoid, orthopteroid, and plecopteroid lineages of exopterygote Neoptera; and once only in Endopterygota). Endopterygota evolved from ametabolous, not from hemimetabolous, exopterygote Neoptera. The full primitive wing venation consists of six symmetrical pairs of veins; in each pair, the first branch is always convex and the second always concave; therefore costa, subcosta, radius, media, cubitus, and anal are all primitively composed of two separate branches. Each pair arises from a single veinal base formed from a sclerotized blood sinus. In the most primitive wings the circulatory system was as follows: the costa did not encircle the wing, the axillary cord was missing, and the blood pulsed in and out of each of the six primary, convex-concave vein pair systems through the six basal blood sinuses. This type of circulation is found as an archaic feature in modern mayflies. Wing corrugation first appeared in preflight wings, and hence is considered primitive for early (paleopterous) Pterygota. Somewhat leveled corrugation of the central wing veins is primitive for Neoptera. Leveled corrugation in some modern Ephemeroptera, as well as accentuated corrugation in higher Neoptera, are both derived characters. The wing tracheation of Recent Ephemeroptera is not fully homologous to that of other insects and represents a more primitive, segmental stage of tracheal system. Morphology of an ancient articular region in Palaeodictyoptera shows that the primitive pterygote wing hinge in its simplest form was straight and composed of two separate but adjoining morphological units: the tergal, formed by the tegula and axillaries; and the alar, formed by six sclerotized blood sinuses, the basivenales. The tergal sclerites were derived from the tergum as follows: the lateral part of the tergum became incised into five lobes; the prealare, suralare, median lobe, postmedian lobe and posterior notal wing process. From the tips of these lobes, five slanted tergal sclerites separated along the deep paranotal sulcus: the tegula, first axillary, second axillary, median sclerite, and third axillary. Primitively, all pteralia were arranged in two parallel series on both sides of the hinge. In Paleoptera, the series stayed more or less straight; in Neoptera, the series became V-shaped. Pteralia in Paleoptera and Neoptera have been homologized on the basis of the fossil record. A differential diagnosis between Paleoptera and Neoptera is given. Fossil evidence indicates that the major steps in evolution, which led to the origin first of Pterygota, then of Neoptera and Endopterygota, were triggered by the origin and the diversification of flight apparatus. It is believed here that all above mentioned major events in pterygote evolution occurred first in the immature stages.

Proprioceptive input on the locust flight motor revealed by muscle stimulation

1. The locust is suspended in the laminar air stream of an open jet wind tunnel. During flight the 1st basalar muscle of the hindwing (M127) or of the forewing (M97) is stimulated every 6th or 8th wing beat with a single electric pulse triggered by simultaneously recorded action potentials of another downstroke muscle. The exact time relationship of the stimulus relative to the wing beat cycle is varied systematically (Fig. 1). 2. In response to the electric stimulus the time of occurrence of other downstroke muscles changes slightly depending on the phase of the stimulus respective to the wing beat period. Stimulation of M127 (hindwing) leads to the following results: all recorded muscles react qualitatively in the same manner. If the stimulus occurs during the downstroke phase (first half of wing beat period) up to 3 subsequent wing beat intervals in the direct downstroke muscles are slightly elongated (Fig. 2). If the stimulus occurs during the upstroke phase the next following interval is decreased and the subsequent interval slightly increased (Fig. 3). 3. If the stimulated muscle is cut near its apodeme at the wing hinge region the influence of the stimulus on the other muscles vanishes (Fig. 6). Thus, the effect depends on the mechanical action of the stimulated muscle on the wing hinge. Therefore, the possibility is excluded that the antidromic spike evoked in the motor axon of the stimulated muscle is responsible for the described reactions. 4. The latency between the stimulus and the next influenced muscle action potential may be as short as 20 ms (Fig. 7). 5. Stimulation of the forewing 1st basalar muscle shows reactions which are different from animal to animal. In contrast to the “hindwing stimulation” different muscles may react differently to a particular stimulus (Fig. 8). 6. The general conclusion which can be drawn is that the sensory equipment of the wing and wing hinge region monitors wing movement quite specifically and exerts subtle influences on motor elements of the flight system.

Efferent system of the lateral ocellus in the dragonfly: Its relationships with the ocellar afferent units, the compound eyes, and the wing sensory system

1. The activity of lateral ocellar nerve fibres of the dragonfly was studied with special reference to the activity of efferent fibres. 2. Afferent and efferent impulses were recorded from the distal and proximal cut-ends of the ocellar nerve using suction electrodes. The lateral ocellar nerve was found to contain, at least, two kinds of afferent (one large and the other small) and three kinds of efferent (one large and the others small) fibres (Fig. 7). 3. The large efferent fibre was activated by illumination of the compound eyes, and also during wingbeat (Figs. 4, 5, and 6). 4. In the intact ocellar nerve, the large afferent fibre was also activated during wing-beat, but the evoked discharge was inhibited by illumination (Fig. 2). The result suggests an excitatory pathway from the efferent fibre to the large afferent within the distal synaptic region of the ocellar nerve. 5. The impulse activities of wing sensory nerves were recorded relative to the position and movement of the wings (Fig. 10). 6. Electric stimulation of a wing sensory nerve produced bursting discharges in efferent fibres in both ipsi- and contra-lateral ocellar nerves (Fig. 11). It is probable that the efferent fibres are excited by input from sense organs in the wing's hinges.

Development of cuticular patterns in the legs of a cell lethal mutant ofDrosophila melanogaster.

The development of cuticular patterns in the legs ofDrosophila melanogaster was studied in the temperature-sensitive cell autonomous lethal mutant1 (1)ts726 by treating animals with heat pulses of two days' duration at different developmental stages, in order to find out whether or not models which account for regulation of imaginal discs in the late third instar also hold for earlier developmental periods. Eight kinds of phenotypes were found, each of which occurred only after heat pulses that started at particular time: (1) complete and incomplete mirror image duplications of mesothoracic legs: early second instar; (2) homoeotic transformation to wing hinge in mesothoracic legs: early second instar; (3) prothoracic leg fusions: early second instar; (4) hypertrophied sex combs: early third instar; (5) outgrowths: early third instar; (6) sex comb teeth on second tarsal segment: early third instar; (7) reversed bristle polarity in intersegmental membrane gaps: early third instar; (8) deleted individual bristles: middle of third instar. These phenotypes were compared with patterns predicted by two models that have been devised to account for regeneration data: the polar coordinate model, and the gradient-of-morphogenetic-potential model. Some of the data (especially the finding of circumferentially incomplete partial duplicates) are more readily predicted by the polar coordinate model, although neither model can be ruled out. Phenotypes (6) and (7) can be accounted for by postulating a tandemly repeated positional signal corresponding to tarsal segmentation. The homoeotic transformation may be due to a transdetermination event occurring in situ during regulative growth following cell death. Since deletion of individual sex comb teeth leads to altered sex comb rotation, it is suggested that adjacent sex comb tooth cells interact during rotation.

The locust wing hinge stretch receptors. I. Primary sensory neurones with enormous central arborizations

In locusts a single-celled stretch receptor (SR) neurone at the base of each wing monitors wing elevation and contributes to the control of the flight motor output. The central projections of these neurones are very complex but consistent in detail in the three species studied (Chortoicetes, Locusta and Schistocerca). The hindwing SR projects to the second and third thoracic ganglia, the forewing SR to the first, second and third thoracic ganglia. Both send fine axons into the abdominal connective. Within the ganglia each SR forms an extensive arborization, entirely ipsilateral and mainly in the dorsal neuropile, divided into medial, mediolateral, and lateral branches. The projections of the two ipsilateral SR neurones overlap almost completely in the second and third ganglia. There are recurrent loops between branches of a single neurone both within and between ganglia. Light microscope analysis shows apparent contacts between the SR aneurones and flight motor neurones and other wing sensory afferents, as well as long interneurones, other motor neurones and two types of multiaxonal neurones of unknown function. There are three groups of contacts between each SR and a flight motor neurone: laterally on the main branches, medially with the terminal twigs; and in the anterior dorso-medial glomerulus, where the inter ganglionic recurrent branch also terminates. All contacts are ipsilateral except for those with the contralateral branches of the dorsal longitudinal muscle motor neurones. We suggest that the SR neurones are multifunctional. Differential information transfer could result both from the spatial distribution of synaptic connections with the motor neurones and from filtering caused by low safety factors at branch junctions. Information in the lateral branching could be used for general excitation and control of firing frequency of the motor neurones; that in the medial branch for wing control and co-ordination.

The locust wing hinge stretch receptors. II. Variation, alternative pathways and "mistakes" in the central arborizations.

The central arborizations of the stretch receptor (SR) neurones are very consistent from one individual to another. Superimposition of normalized neurones from eight individuals of Locusta show very little variation even in the detailed branching pattern. There is, however, a commonly found alternative course for the main medial branch in the metathoracic ganglion. Rare, radical departures from the normal branching pattern are termed "mistakes." Only three have been found, all in the forewing SR projection, one with an extra branch and two with missing branches. Terminals of twigs in the alternative region of the medial branch occupy consistent positions in the neuropile, although these are reached by different routes. Mistakes have terminals in areas normally containing SR endings. Both these findings suggest that there may be labelled sites in the neuropile which the growing tips of the SR neurones seek out.

The jumping mechanism of Xenopsylla cheopis. III. Execution of the jump and activity.

The flea's hind legs are the chief source of jumping power, but in species which execute large jumps, take-off is accelerated by elastic energy released from a resilin pad (homologous with the wing hinge ligaments of flying insects) situated in the pleural arch. A central click mechanism, operated by a rapid twitch of the trochanteral depressor (the starter muscle), synchronizes the separate sources of energy which power the jump. Ciné photos confirm the morphological evidence that the flea takes off from the trochanters, not the tarsi. The loss of wings, associated with lateral compression of the body and the shortening of the pleural ridge (which thus lowers the position of the pleural arch) together with modifications of the direct and indirect flight muscles, are some of the main morphological features associated with the change from a flying to a saltatorial mode of progression. The flea's take-off basically resembles that of other Panorpoid insects (Diptera, Mecoptera, etc.). The release of elastic energy from the pleural arch is a system by which the force used to move the wings of flying insects is rapidly fed back into the legs and adds power to the jump.

Localization of primordia within the dorsal mesothoracic disc of drosophila.

AbstractDistal regions or “marginal ridge” areas of the dorsal mesothoracic disc of mature Drosophila larvae, not previously included in fate maps, were marked by microcauterization in situ. Structures assumed to have primordia in the distal half of the disc (mesopleura, pteropleura, arch, ventral scutellum, ventral wing hinge and wing proper) are either missing, deficient, or damaged among adults surviving the operation. In contrast, neither the dorsal wing hinge nor mesonotum, which are known to have primordia in the proximal half of the disc, are similarly affected.The pattern of distribution of deformities in surviving adults indicates that (a) the anlage of the mesopleural sclerite is located in the distal edge portion or “marginal ridge” of the disc, (b) anlagen of pteropleura, arch and ventral scutellum may also be tentatively assigned to this location, (c) there are significantly high associations between deformities affecting the pteropleura and the ventral wing hinge, and (d) the anlage of the deep phragma of the postnotum may be more closely related to the first abdominal tergite than to the dorsal mesothoracic disc.The distal localization of pleural, arch, and ventral scutellar anlagen corresponds to the physical separation from mesonotal anlagen predicted from an earlier statistical analysis of genetic mosaics; i.e., these presumptive sclerites are separated from the mesonotal anlagen by the anlagen of the wing in the “pouch” area of the disc.The new information has been incorporated into a hypothetical fate map of the disc, which includes anlagen plans suggested by previous authors.

A Stretch Reflex Controlling Wingbeat Frequency in Grasshoppers

ABSTRACT The stretch receptors of the wing hinge of the locust Schistocerca fire once or twice at the top of the wingstroke during normal flight. Removal of the four stretch receptors results in a decrease of the wingstroke frequency to about one-half normal. Interference with the normal timing of the stretch-receptor input (mechanically or by electrical stimulation) does not affect the normal wingstroke frequency. With respect to this sensory source the centrally generated motor output pattern is independent of input phase. The results are discussed briefly in relation to the question of central v. peripheral control of locomotion.

Biology and physics of locust flight IV. Notes on sensory mechanisms in locust flight

The wing stroke of locusts is remarkably constant and independent of external conditions. Is this rigid rhythmicity due to a rhythmicity of the central nervous system or is it determined by peripheral factors? The flight behaviour of the desert locust ( Schistocera gregaria ) was studied under various experimental conditions in order to find which external factors can initiate, maintain or alter the wing movements, excluding reactions which depend upon higher nervous centres. The ‘tarsal reflex’ and the response seen when the aerodynamic sense organ on the head is stimulated (Weis-Fogh 1949, 1950) were reinvestigated in order to relate them to two hitherto unknown reactions: the maintenance of flapping when the wings are exposed to wind and the regulation of the lift when the body angle ( = angle of pitch) is changed during forward flight. Both depend on receptors whose nature is still unknown. Inhibition . As in most other insects, the flight of a locust cannot be started when the legs, or only part of one leg, have contact with a rigid body; flight stops when such contact is regained. Amputation of the legs abolishes these reactions, showing that some leg proprioceptors inhibit flight. Initiation . A suspended locust can be induced to fly in three ways. (1) By application of a sufficiently strong stimulus which normally provokes escape reactions; the flight lasts only a few seconds. Adaptation is generally quick. (2) By sudden removal of the support for the legs (‘ tarsal reflex’ although not confined to the tarsi). The flight lasts 5 s on average, corresponding to one hundred wing strokes. There is practically no adaptation. (3) By blowing upon the wind-sensitive hairs on the head. The wind must exceed 2 m/s, but its direction is of little importance. Since the static bending has no effect, the adequate stimulus seems to be minute vibrations of the hairs. The flight lasts as long as the wind blows and the hairs are therefore also involved in the maintenance of flight. When the locust has stopped, the legs begin to flutter, and eventually remain still, but normally flight is not resumed unless one of the above stimuli is applied. Maintenance . Two receptor systems are involved. (1) The wind-sensitive hairs on the head. In a wind they emit impulses irrespectively of whether the locust has any chance of flapping its wings or not. ‘Wind on the head’ is therefore an extrinsic flight stimulus. The flight posture is never complete. (2) A hitherto unknown receptor system in the pterothorax which was studied in insects whose supra-oesophageal ganglia were cauterized (‘decerebrate’). It maintains the movements when the wings oscillate in a wind but cannot initiate them; the adequate stimulus is the rhythmically changing wind pressure on the wings. ‘Wind on the wings’ is therefore an intrinsic flight stimulus. When the average lift exceeds half the body weight, flight continues in complete flight posture but stops when the lift approaches zero. The experiments indicate that the stimulation ceases when the lift becomes negative during the upstroke . The receptors are unknown; it is suggested that they are situated at the wing hinge. The locust does not adapt to either of these stimuli and invariably stops a few seconds after they have ceased. Control of lift . The locust tends to keep the lift constant during a given performance. This observation, together with the constancy of most stroke parameters, made it possible to investigate the mechanism involved. The method was to make the insect fly steadily against a horizontal wind and then alter the inclination to the wind (= the body angle) at regular intervals. The data permitted an estimate of the mean change in wing twisting Δθ. Δθ increased (wings pronated) by 15 ± 3° when the body angle was increased from 0 to 15°. This is the main factor in the control of lift. The discussion shows that this presupposes a system of lift-sensitive receptors (probably campaniform sensilla at the wing hinge). If present in other insects, the homoeostatic character of the wing stroke of Drosophila (Chadwick 1953) may therefore be caused by a nervous mechanism and need not be a consequence of the energetics of flight. Central rhythm . It is concluded that the central nervous system ( does not initiate flight rhythm de novo ; ( b ) does neither determine the stroke frequency nor the strength of the contractions of the controller-depressor muscles; ( c ) may control the phasing of the contractions, although a simpler hypothesis is advanced; ( d ) may control the indirect flight muscles but only as far as to produce stimuli of constant (maximum?) strength.

Biology and physics of locust flight. I. Basic principles in insect flight. A critical review

Natural flapping flight is a complicated type of locomotion; it involves a large number of parameters and demands a higher rate of energy consumption than any other known achievement within the animal kingdom. The extensive literature provides a diffuse and sometimes misleading picture of the mechanics and energetics of flight. The purpose of this critical review is twofold; first, an attempt is made to reveal how far contemporary knowledge has advanced towards a quantitative understanding of the basic physical events which result in flight; secondly, the conceptual analysis and the conclusions arrived at serve as a general introduction to a detailed experimental study of the flight performance of the desert locust ( Schistocerca gregaria Forskal). The results of this study will be published as a series of mutually dependent papers which are referred to as parts, the present being part I; their content is indicated by the general title ‘Biology and physics of locust flight’. The abstracts at the end of the major sections can be read as a continuum and independent of the remaining text. Most qualitative principles in insect flight are fairly well understood, although some authors have claimed that the observed movements did not permit flight according to ordinary aerodynamic principles. The data upon which these calculations are based were, however, found to be inadequate. In general, if one attempts to interpret the observed performance in quantitative terms, a conceptual analysis of the necessary knowledge shows that both the conditions for observation and the measured parameters must be defined more rigorously than has hitherto been the case. A theoretical treatment, partly based upon the experimental evidence in the succeeding parts, reveals that the energy account of a wing stroke comprises at least three independent terms, namely,an aerodynamic term due to the wind forces on the wings, an inertial term due to the acceleration of the wing mass, and an elastic term caused by the elastic deformations of the thorax. Finally, extra-muscular damping within the thorax may be involved but it does not seem to be important compared with the other quantities. The mechanical energy and the forces which the muscles must provide can be estimated by the torque about the wing hinge to which these terms give rise. However, in order to summate the torque contributions their detailed variations during the stroke must be known, and since all of them are extremely sensitive to alterations in the stroke cycle, no existing theory can deal with the energetics of the flight as a whole. One is therefore forced to investigate the wing stroke empirically. An experimental study must take place under rigorously controlled aerodynamic and biological conditions and must include the simultaneous variation in time and space of a considerable number of kinematic and dynamic parameters whose nature is briefly outlined. However, an experimental approach would be much hampered if one had to take unusual aerodynamic (inertal) forces into account. Fortunately, an analysis of existing aerodynamic theories on flapping flight reveals that there is little to be said against and much in favour of considering natural flight as being based upon conventional aerodynamic principles, even in the case of small insects like mosquitoes. At least, unconventional aerodynamics need not be assumed in order quantitatively to explain observed performances, although some authors (cf. Osborne 1951) have reached the opposite conclusion. The assumptions made in the most complete theories (Holst & Küchemann 1941 ; Walker 1925 , 1927 ; Osborne 1951) are discussed in detail and the basic equations have been homogenized to fit the rest of the text. Various theoretical deductions considered of general interest are tabulated (e.g. influence of distance from fulcrum, induced wind) and the theories are tested by inserting values from insect types whose performances are best known. The calculations also gave the order of magnitude of the power necessary to overcome the aerodynamic forces ( = aerodynamic power). This external power certainly claims a considerable fraction of the total metabolic rate. A short review (§6) of the regulation of flight also emphasizes the importance of considering both aerodynamic, inertial and elastic terms as significant simultaneous factors in the energy account and thus in the regulation of the power output; the special mechanisms concerned with the stability in flight fall outside the scope of the paper, however, and will be discussed in part IV .