Collision avoidance and a looming sensitive neuron: size matters but biggest is not necessarily best

Locusts possess visual neurons that can be uniquely identified in each locust and that respond selectively to looming stimuli, giving the animal a warning of impending collision. It has been suggested that one such neuron, the lobula giant movement detector (LGMD), issues this warning by generating a peak in its response that occurs ca. 25 ms after a looming object reaches a subtense of 17 degrees on the eye. This peak is proposed to be a trigger for escape behaviour. We use both modelling and electrophysiological techniques to show that this early peak in LGMD response is not the 'essential functional variable' used naturally by the locust to trigger escape, but rather results from the unnaturally large stimulus used in the previous experimental work. The natural predators of Locusta in Africa, where the locust evolved, are small birds such as the fiscal shrike Lanius collaris humeralis and the carmine bee-eater Merops nubicus, with pectoral diameters of 40-45 mm (measurements from museum specimens). Locusta in flight are less than 100 mm wing tip to wing tip. When a locust views small approaching objects, the response of the LGMD continues to increase throughout the object's approach and the locust is able to trigger escape behaviours without the LGMD response peaking prior to collision.     

The contribution of surface waxes to pre-penetration growth of an entomopathogenic fungus on host cuticle

A locust wing bioassay, that allowed an entomopathogenic fungus to be removed from host cuticle before penetration, was used to investigate the role of surface lipids and waxes in pre-penetration growth of the specific locust pathogen Metarhizium anisopliae var. acridum. SEM and atomic force electron microscopy showed the impact of the fungus on the architecture of the cuticle surface. Although the fungus can germinate on authentic alkanes as the sole carbon source, only low levels of germination occurred on crude, non-polar wing cuticle extracts, containing a mixture of long-chain n-alkanes and other waxes (identified in particular by gas chromatography and mass spectroscopy). The fungus removed a large proportion of non-polar and polar components during pre-penetration growth on the wing. Polar crude extracts from Schistocerca gregaria hindwings, which contained fatty acids, fatty acid esters, glucose, amino acids and peptides, were strong promoters of germination, and poor germination was observed on a locust hindwing from which the extract had been taken. Thus simple polar compounds, also present on the surface, may be required to stimulate germination before the fungus can make use of a complex mixture of non-polar lipids.     

Role of wing pronation in evasive steering of locusts

Evasive steering is crucial for flying in a crowded environment such as a locust swarm. We investigated how flying locusts alter wing-flapping symmetry in response to a looming object approaching from the side. Desert locusts (Schistocerca gregaria) were tethered to a rotatable shaft that allowed them to initiate a banked turn. A visual stimulus of an expending disk on one side of the locust was used to evoke steering while recording the change in wingbeat kinematics and electromyography (EMG) of metathoracic wing depressors. Locusts responded to the looming object by rolling to the contralateral direction. During turning, EMG of hindwing depressors showed an omission of one action potential in the subalar depressor (M129) of the hindwing inside the turn. This omission was associated with increased pronation of the same wing, reducing its angle-of-attack during the downstroke. The link between spike-omission in M129 and wing pronation was verified by stimulating the hindwing depressor muscles with an artificial motor pattern that included the misfire of M129. These results suggest that hindwing pronation is instrumental in rotating the body to the side opposite of the approaching threat. Turning away from the threat would be highly adaptive for collision avoidance when flying in dense swarms.     

Wing dimorphism in the migratory locust,Locusta migratoria: differentiation of wing morph and phase polyphenism

A short‐winged morph was recently discovered in the migratory locust, Locusta migratoria. It is different from the normal, long‐winged morph not only in forewing length but also in hind femur length, displaying a dimorphism. To understand the significance of this dimorphism, other morphological characters were compared between the two morphs, and the time of differentiation of wing‐pad length was investigated. Wing weights were heavier in the long‐winged morph than in the short‐winged morph. This result showed that the short‐winged morph is not formed by a failure of wing expansion. No obvious morph‐specific differences were observed in wing venation, but wing allometry studies indicated that the distal areas of the fore‐ and hindwings were disproportionally reduced in the short‐winged morph compared to the long‐winged morph. The morphological differentiation of the wing pad between the two morphs was observed at the penultimate nymphal stage. The flight muscle was well developed in the two morphs, and no sign of flight muscle histolysis was detected in either morph after adult emergence. An analysis of adult body dimensions suggested that the density‐dependent phase shifts known for the long‐winged morph of this locust were also exhibited by the short‐winged morph, demonstrating that these shifts are not specific to the migratory long‐winged morph.     

Wing kinematics during natural leaping in the mantids Mantis religiosa and Iris oratoria

High-speed flash photography was used to analyse wing movements of Mantis religiosa and Iris oratoria at the moment of take-off during natural leaping. Wing kinematics are compared with those of the similarly designed locust wing. Iris oratoria showed strong coupling between leg extensor and wing depressor muscle activity immediately prior to take-off, with a possible enhancement of jump momentum. A 'clap and peel' was observed in the hind wings of both species during the first downstroke. Supination in the mantid forewing is accomplished by a backward rotation of the whole of the main wing plate about the claval furrow. Both fore- and hind wings show pronounced ventral flexure at the lower point of stroke reversal. Camber was developed in the hind wing during the upstroke as well as the downstroke. Possible roles of the claval furrow and transverse flexion in protecting the forewing base against torsional forces generated at stroke reversal are discussed.     

应用荧光染色法检测寄主昆虫体表病原真菌孢子及其附着孢

采用蝗虫翅膀作为侵染组织,探讨了荧光染色剂Calcofluor White M2R在观测寄主体表绿僵菌孢子及其附着孢形成中的应用。结果表明,在荧光显微镜下,清晰可见蝗虫翅膀上发蓝色荧光的绿僵菌孢子、芽管及附着孢,而蝗虫翅膀未被染色,避免了干扰观察目标物。该方法可以准确观察病原真菌孢子在昆虫体表组织的萌发及附着孢形成。     

Veins improve fracture toughness of insect wings

During the lifetime of a flying insect, its wings are subjected to mechanical forces and deformations for millions of cycles. Defects in the micrometre thin membranes or veins may reduce the insect’s flight performance. How do insects prevent crack related material failure in their wings and what role does the characteristic vein pattern play? Fracture toughness is a parameter, which characterises a material’s resistance to crack propagation. Our results show that, compared to other body parts, the hind wing membrane of the migratory locust S. gregaria itself is not exceptionally tough (1.04±0.25 MPa√m). However, the cross veins increase the wing’s toughness by 50% by acting as barriers to crack propagation. Using fracture mechanics, we show that the morphological spacing of most wing veins matches the critical crack length of the material (1132 µm). This finding directly demonstrates how the biomechanical properties and the morphology of locust wings are functionally correlated in locusts, providing a mechanically ‘optimal’ solution with high toughness and low weight. The vein pattern found in insect wings thus might inspire the design of more durable and lightweight artificial ‘venous’ wings for micro-air-vehicles. Using the vein spacing as indicator, our approach might also provide a basis to estimate the wing properties of endangered or extinct insect species.     

Flight motor patterns recorded in surgically isolated sections of the ventral nerve cord ofLocusta migratoria

Summary In the locust,Locusta migratoria, the pairs of connectives between the three thoracic ganglia and in the neck were transected in all possible combinations. Each of these preparations was tested for the production of rhythmic flight motor activity, with sensory input from the wing receptors intact and after deafferentation. The motor activity elicited in these preparations was characterized by intracellular recordings from motoneurons and electromyographic analyses.The motor patterns observed in locusts with either the neck or the pro-mesothoracic connectives severed (Figs. 2, 3, and 4) were very similar to the flight motor pattern produced by animals with intact connectives. The activity recorded in mesothoracic flight motoneurons of locusts with either only the meso-metathoracic connectives cut or both the meso-metathoracic and the neck connectives transected were similar to each other. Rhythmic motor activity could be observed in these preparations only as long as sensory feedback from the wing receptors was intact. These patterns were significantly different from the intact motor pattern (Figs. 5, 6, and 7). Similar results were obtained when the mesothoracic ganglion was isolated from the other two thoracic ganglia, although the oscillations produced under these conditions were weak (Fig. 8 upper). In the isolated metathorax no rhythmic flight motor activity could be recorded (Fig. 8 lower), even when wing afferents were intact.Considering the differences between the motor patterns observed in the various preparations these results suggest that the ganglia of the locust ventral nerve cord do not contain segmental, homologous flight oscillators which are coupled to produce the intact flight rhythm. Instead they support the idea that the functional flight oscillator network is distributed throughout the thoracic ganglia (Robertson and Pearson 1984). The results also provide further evidence that sensory feedback from the wing sense organs is necessary for establishing the correct motor pattern in the intact animal (Wendler 1974, 1983; Pearson 1985; Wolf and Pearson 1987 a).Abbreviations CPG central pattern generator - EMG electromyogram     

The expansion of Schistocerca gregaria at the imaginal ecdysis: The mechanical properties of the cuticle and the internal pressure

(1) At the imaginal ecdysis of Schistocerca, the cuticle is viscoelastic rather than elastic. (2) The cuticle becomes softer just before emergence. It is suggested that this is due to an ‘eclosion hormone’. The softening permits the extrication of the appendages and an increase in the size of the locust. (3) The stiffness of the cuticle increases transiently at the end of emergence. (4) In the later part of wing expansion, the cuticle becomes elastic and its stiffness again increases. (5) Maximum pressures are recorded about 10 min into emergence, and pressures in the gut are greater than those in the tracheal system. (6) From these results it is concluded that the expansion of the wings initially depends on the high haemolymph pressure and low stiffness. Only in the last 15 min of wing expansion do the processes involved in autonomous expansion become important.     

Peculiarities of ultrastructural organization of the metathoracic ganglion in the locustLocusta migratoria larva

In electron microscopic study of structural organization of the thoracic ganglion of the locust larva of the 1st age (1–2 days after hatching), the data on the structure of motoneurons of the 1st nerve, basal and motor neuropil of the larva were obtained. The effector elements of the larval locust CNS are formed rather early and have the structural plan similar to that in adult insects. However, in the larval motoneurons innervating the flight muscles (longitudinal dorsal muscles, wing depressors) the clearly seen features of immaturity of these nervous elements are revealed. Study of the larval ganglion neuropil has shown that the basal neuropil is morphologically formed sufficiently completely as early as in larvae of the first days after hatching. There are shown longitudinal contacts between axons of the ventral neuropil zone, the presence of axons forming theen-passant contacts as well as the synapses with a heterogeneous set of vesicles in the presynaptic area. The presence of the great number of granular vesicles in the basal neuropil of the locust larva may indicate an important role of catecholamines in the early development of the nervous system in the locust larva.     

Proprioceptive activity of the wing-hinge stretch receptor in Manduca sexta and other atympanate moths: a study of the noctuoid moth ear B cell homologue

A multiterminal neurone, recently identified at the wing-hinge of the atympanate moth Manduca sexta, is shown to respond as a proprioceptor monitoring elevatory movements of the hind wing. Extracellular recordings from the individual receptor axon confirm this cell to be the source of the spontaneous and regular discharge observed in previous recordings of peripheral nerve 3N1b1. When the wing is raised, this tonic discharge rate increases proportionally with the angle of elevation. When the wing is displaced sinusoidally at a low frequency, the receptor discharge is modulated throughout the wing beat, increasing steadily to a maximum at the top of the upstroke, then slowly decreasing to a minimum at the bottom of the downstroke. At higher wing-beat frequencies, a phasic burst of activity occurs near the top of the upstroke, followed by a silent period during the down-stroke. Video-microscopic observations of the wing-hinge during active, stationary flight suggest that the receptor is stimulated by the stretching of its peripheral attachment, the subalar membrane. Stretch receptor sensitivity to wing movement is demonstrated in representatives of 4 lepidopteran families, suggesting that the proprioceptive response is widespread among the Lepidoptera. The functional role of the wing-hinge receptor, and its proposed homologous relationship to both the B cell of the noctuoid moth ear, and the locust wing-hinge stretch receptor are discussed.Abbreviations CO chordotonal organ - EGAA Enhanced Graphics Acquisition and Analysis System - HP hair plate - 3N1b1 tympanal nerve - SR stretch receptor     

Synchronization of wing beat cycle of the desert locust, Schistocerca gregaria, by periodic light flashes

Studies on the generation of rhythmic motor patterns have shown that peripheral sensory input may contribute substantially to the rhythm generating network. A prominent example is the wing beat frequency of desert locusts, which can be entrained to rhythmic mechanosensory input, but also to the frequency of periodic light flashes. To further analyze the entrainment by light, tethered flying locusts were presented with periodic light flashes, while the position of the forewing was filmed. We show that entrainment of wing beat occurs both in the UV and green range of light. Animals maintained a characteristic phase relationship to the light stimulus with the most elevated wing position occurring at the end of the dark phase. Speed and time course of entrainment varied greatly and ranged from the duration of a single wing beat cycle to several seconds. To identify the visual system mediating entrainment, synchronization to UV light was tested after cutting the optic stalks to the optic lobes/compound eyes or the ocellar nerves. The results show that light entrainment of the locust flight pattern is largely and perhaps exclusively mediated via the fast ocellar pathway and may have a role to stabilize flight with respect to the horizon.     

Structural-functional peculiarities of the wing apparatus of insects that do not have and do have the maneuvering flight

The work considers character of behavior in flight and discusses peculiarities of structural-functional organization of the wing apparatus of two representatives of insects—the migratory Asian locust Locusta migratoria (a low-maneuvering insect) and the dragonfly-darner Aeshna sp. (an insect able to perform complex maneuvers in air). The main principles underlying the insect wing apparatus activity are considered and the mechanisms allowing the dragonflies to perform complex maneuvers in the flight are analyzed in detail.     

Locust flight initiation: a comparison of normal and artificial release

Flight initiation was analysed in the migratory locust, Locusta migratoria L. using conventional and high‐speed video systems. Flight was initiated by three methods: normal jump, free fall and controlled catapult. Parameters evaluated were time from release to wing‐opening, body angle, speed, height gain, wing‐opening, initial wing‐beat frequency. Fastest wing‐opening occurred following a normal jump. A catapult device allowed manipulation of the launching parameters: speed and angles at launching. It appeared that in an artificially catapulted start there was a minimum speed (v > 0.75 m/s) required to initiate flight. However, under free‐fall conditions a mean speed of v = 0.6 m/s at wing‐opening was observed. When the different parameters of the controlled catapult start were equal to those for normal jump then the time to wing‐opening was found to be extended for the catapult launch. However, other parameters were not affected, occasionally even a ‘kick in air’ was observed. The catapult launches indicated that within about three wing‐beat cycles the animals showed active flight, with positive lift and constant or increasing speed, compared to a ballistic trajectory. Our results indicate that a controlled catapult device will prove useful to the study of sensory and central processes underlying free flight initiation.     

The 3′,5′-adenosine-monophosphate system during the larval-adult moulting cycle in the migratory locust,Locusta migratoria

During the larval-adult moulting cycle of the migratory locust the concentration of 3′,5′-AMP and the activities of adenylate cyclase, phosphodiesterase, protein kinase, and phosphorylase a and b were measured in wing pads and wings, and in the integument of the abdomen. In the wing pads the maximum of adenylate cyclase activity precedes the increase in 3′,5′-AMP concentration as well as the binding capacity and the 3′,5′-AMP-dependent activation of the protein kinase. Around ecdysis adenylate cyclase activity shows a minimum, but increases later. 3′,5′-AMP concentration and the nucleotide dependent protein kinase activity are decreasing in the adult locust. The protein kinase activity in absence of 3′,5′-AMP (independent protein kinase plus basal activity of dependent protein kinase) shows the highest activities in the four day old last instar and in the one day old adult. Phosphodiesterase activity stays rather constant during the instar stage but rises after ecdysis. Phosphorylase a and b increase their activities just around ecdysis. In the integument of the abdomen essentially the same pattern of concentration and activity changes can be detected, with the exception that extreme decreases during adult life do not take place.     

The interaction of positive and negative sensory feedback loops in dynamic regulation of a motor pattern

In many rhythmic behaviors, phasic sensory feedback modifies the motor pattern. This modification is assumed to depend on feedback sign (positive vs. negative). While on a phenomenological level feedback sign is well defined, many sensory pathways also process antagonistic, and possibly contradictory, sensory information. We here model the locust flight pattern generator and proprioceptive feedback provided by the tegula wing receptor to test the functional significance of sensory pathways processing antagonistic information. We demonstrate that the tegula provides delayed positive feedback via interneuron 301, while all other pathways provide negative feedback. Contradictory to previous assumptions, the increase of wing beat frequency when the tegula is activated during flight is due to the positive feedback. By use of an abstract model we reveal that the regulation of motor pattern frequency by sensory feedback critically depends on the interaction of positive and negative feedback, and thus on the weighting of antagonistic pathways.     

Change of Activity of Locomotor Centers of the Locust Locusta migratoria under Effect of Increased Gravitation

The work studies effects of elevated gravitation on activity of locomotor centers in the locust Locusta migratoria L. Under effect of the increased gravity field the excitation of the motor centers that provide activity of the locus wing apparatus was shown to decrease. Analysis of the data obtained has allowed us concluding that the higher CNS centers (subesophageal ganglion) produce at least two types of excitatory (stimulatory) effects on segmental centers, one of the types affecting motor centers in the rest state, the other, in the active state. We believe that it is the impulses of the second type that are inhibited under effect of the increased radial acceleration on the organism. There is every reason to think that an important role in these processes is played by peculiar structures of the supraesophageal ganglion protocerebrum: mushroom bodies and the central complex that regulates activity of the locust segmental centers both directly and indirectly via the subesophageal ganglion.     

Estimation of climatic favourable areas for locust outbreaks in Spain: integrating species' presence records and spatial information on outbreaks

For millennia, locust swarms have recurrently devastated crop productivity across continents. In much of Europe, locust outbreaks have been considerably reduced by human pressure in recent decades, but important foci of outbreaks still exist in Spain. Distribution models are often used to derive spatial hypotheses and risk maps. Because insufficient information is available to include the extreme plasticity of the solitary and gregarious phases of locusts in large‐scale spatial models, we modelled the distribution either of Acrididae species or of outbreaks per se. Confirmed occurrences of Dociostaurus, Calliptamus and Chorthippus species were obtained from a field survey complemented by museum collection data and the published literature. The locations of confirmed or potential outbreaks covering two time periods of 20 years each were obtained from the literature and from Spanish autonomous community reports. Models were built with one topographic and eleven climatic predictors. We evaluated the ability of different models to predict outbreak recurrence and found that models based on Moroccan locust data or outbreak occurrence data performed the best. We generated a predictive map of the climatic favourability for locust outbreaks in Spain and found that the major foci of locust swarms were encompassed by those areas categorized by the models as areas of highest risk. Predictive maps of outbreak favourability can facilitate the more sustainable use of insecticides and more efficient integrated pest management.     

Reflex activation of locust flight motoneurones by proprioceptors responsive to muscle contractions

 This report investigates the reflex activation of locust flight motoneurones following their spiking activity. As shown elsewhere, an electrical stimulus applied to a flight muscle produces multiple waves of delayed excitation in wing elevator and depressor motoneurones. Nerve ablation experiments show that this response is initiated by the mechanical movement of the stimulated muscle, and not the antidromic spike evoked in the motoneurone. The delayed excitation still occurs in the absence of inputs from the wing receptor systems, and also when all other sources of afferent feedback are abolished, excepting thoracic nerve 2. Following complete deafferentation, spikes in flight motoneurones had no influence on other flight motoneurones. Numerous afferents in the purely sensory nerve 2 are excited by flight muscle contractions. The responses are consistent for repeated contractions of the same muscle, but differ when other muscles are stimulated. During tethered flight, changes in the activation of single flight muscles are reflected in changes of the nerve 2 discharge pattern. Electrical stimulation of this nerve causes delayed excitation of flight motoneurones, and can initiate flight activity. It is suggested that internal proprioceptors, such as those associated with nerve 2, will contribute to shaping the final motor output for flight behaviour. Accepted: 24 April 1996     

Morphological and behavioural characteristics of a gynandromorph of the desert locust, Schistocerca gregaria

Abstract.  Morphological and behavioural characteristics are investigated for a gynandromorph of the desert locust, Schistocerca gregaria , appearing under isolated rearing conditions in the laboratory. It has both male and female external reproductive organs bilaterally. The body size and dimensions are similar to a normal male. Morphometric traits (fore wing length/maximum head width ratio and fore wing length/hind femur length ratio) of the gynandromorph are typical for the values of solitarious locusts. When the gynandromorph is placed into an arena holding ten sexually mature gregarious females, it shows a distinct male behaviour: it jumps on a female and tries to mate with her. When kept together with males, males recognize this gynandromorph as a female because some of them try to mount, although no successful copulation is observed. The results suggest that the gynandromorph might have had a female-specific pheromone. Dissection reveals that the gynandromorph has no testis but abnormal ovaries containing vitellogenic oocytes. These observations indicate that the gynandromorph obtained has a mixture of male and female morphological characteristics and behaves like a male but is recognized as a female by conspecific males.