Pausing to swarm: locust intermittent motion is instrumental for swarming-related visual processing.

Intermittent motion is prevalent in animal locomotion. Of special interest is the case of collective motion, in which social and environmental information must be processed in order to establish coordinated movement. We explored this nexus in locust, focusing on how intermittent motion interacts with swarming-related visual-based decision-making. Using a novel approach, we compared individual locust behaviour in response to continuously moving stimuli, with their response in semi-closed-loop conditions, in which the stimuli moved either in phase with the locust walking, or out of phase, i.e. only during the locust's pauses. Our findings clearly indicate the greater tendency of a locust to respond and 'join the swarming motion' when the visual stimuli were presented during its pauses. Hence, the current study strongly confirms previous indications of the dominant role of pauses in the collective motion-related decision-making of locusts. The presented insights contribute to a deeper general understanding of how intermittent motion contributes to group cohesion and coordination in animal swarms.

Effects of age and noise on tympanal displacement in the Desert Locust.

Insect cuticle is an evolutionary-malleable exoskeleton that has specialised for various functions. Insects that detect the pressure component of sound bear specialised sound-capturing tympani evolved from cuticular thinning. Whilst the outer layer of insect cuticle is composed of non-living chitin, its mechanical properties change during development and aging. Here, we measured the displacements of the tympanum of the desert Locust, Schistocerca gregaria, to understand biomechanical changes as a function of age and noise-exposure. We found that the stiffness of the tympanum decreases within 12 h of noise-exposure and increases as a function of age, independent of noise-exposure. Noise-induced changes were dynamic with an increased tympanum displacement to sound within 12 h post noise-exposure. Within 24 h, however, the tone-evoked displacement of the tympanum decreased below that of control Locusts. After 48 h, the tone-evoked displacement of the tympanum was not significantly different to Locusts not exposed to noise. Tympanal displacements reduced predictably with age and repeatably noise-exposed Locusts (every three days) did not differ from their non-noise-exposed counterparts. Changes in the biomechanics of the tympanum may explain an age-dependent decrease in auditory detection in tympanal insects.

Community change and population outbreak of grasshoppers driven by climate change.

The response of insects to climate changes in various aspects has been well-documented. However, there is a dearth of comprehensive review specifically focusing on the response and adaptation of grasshoppers, which are important primary consumers and pests in grassland and agricultural ecosystems. The coexistence of grasshopper species forms diverse communities and coherent groups in spatial-temporal scales. It makes them excellent models for studying the interplay of phenology, dispersal, trophic relationship, and population dynamics, all influenced by climate changes. Certain grasshopper species have adapted to climate change through mechanisms such as diapause. Here, we delve into grasshopper community changes, their adaptive strategies, and population outbreaks in response to climate change and land use. By serving as ecological indicators, grasshoppers offer valuable insights for monitoring climatic and environmental shifts. Last, this review puts forth several future directions for comprehending the population dynamics of insects in the context of climate change.

Control of high-speed jumps in muscle and spring actuated systems: a comparative study of take-off energetics in bush-crickets (Mecopoda elongata) and locusts (Schistocerca gregaria).

The Orthoptera are a diverse insect order well known for their locomotive capabilities. To jump, the bush-cricket uses a muscle actuated (MA) system in which leg extension is actuated by contraction of the femoral muscles of the hind legs. In comparison, the locust uses a latch mediated spring actuated (LaMSA) system, in which leg extension is actuated by the recoil of spring-like structure in the femur. The aim of this study was to describe the jumping kinematics of Mecopoda elongata (Tettigoniidae) and compare this to existing data in Schistocerca gregaria (Acrididae), to determine differences in control of rotation during take-off between similarly sized MA and LaMSA jumpers. 269 jumps from 67 individuals of M. elongata with masses from 0.014 g to 3.01 g were recorded with a high-speed camera setup. In M. elongata, linear velocity increased with mass0.18 and the angular velocity (pitch) decreased with mass-0.13. In S. gregaria, linear velocity is constant and angular velocity decreases with mass-0.24. Despite these differences in velocity scaling, the ratio of translational kinetic energy to rotational kinetic energy was similar for both species. On average, the energy distribution of M. elongata was distributed 98.8% to translational kinetic energy and 1.2% to rotational kinetic energy, whilst in S. gregaria it is 98.7% and 1.3%, respectively. This energy distribution was independent of size for both species. Despite having two different jump actuation mechanisms, the ratio of translational and rotational kinetic energy formed during take-off is fixed across these distantly related orthopterans.

4-Vinylanisole promotes conspecific interaction and acquisition of gregarious behavior in the migratory locust.

Chemical signals from conspecifics are essential in insect group formation and maintenance. Migratory locusts use the aggregation pheromone 4-vinylanisole (4VA), specifically released by gregarious locusts, to attract and recruit conspecific individuals, leading to the formation of large-scale swarms. However, how 4VA contributes to the transition from solitary phase to gregarious phase remains unclear. We investigated the occurrence of locust behavioral phase changes in the presence and absence of 4VA perception. The findings indicated that solitary locusts require crowding for 48 and 72 h to adopt partial and analogous gregarious behavior. However, exposure to increased concentrations of 4VA enabled solitary locusts to display behavioral changes within 24 h of crowding. Crowded solitary locusts with RNAi knockdown of Or35, the specific olfactory receptor for 4VA, failed to exhibit gregarious behaviors. Conversely, the knockdown of Or35 in gregarious locusts resulted in the appearance of solitary behavior. Additionally, a multi-individual behavioral assay system was developed to evaluate the interactions among locust individuals, and four behavioral parameters representing the inclination and conduct of social interactions were positively correlated with the process of crowding. Our data indicated that exposure to 4VA accelerated the behavioral transition from solitary phase to gregarious phase by enhancing the propensity toward proximity and body contact among conspecific individuals. These results highlight the crucial roles of 4VA in the behavioral phase transition of locusts. Furthermore, this study offers valuable insights into the mechanisms of behavioral plasticity that promote the formation of locust swarms and suggests the potential for 4VA application in locust control.

Convergent escape behaviour from distinct visual processing of impending collision in fish and grasshoppers.

In animal species ranging from invertebrate to mammals, visually guided escape behaviours have been studied using looming stimuli, the two-dimensional expanding projection on a screen of an object approaching on a collision course at constant speed. The peak firing rate or membrane potential of neurons responding to looming stimuli often tracks a fixed threshold angular size of the approaching stimulus that contributes to the triggering of escape behaviours. To study whether this result holds more generally, we designed stimuli that simulate acceleration or deceleration over the course of object approach on a collision course. Under these conditions, we found that the angular threshold conveyed by collision detecting neurons in grasshoppers was sensitive to acceleration whereas the triggering of escape behaviours was less so. In contrast, neurons in goldfish identified through the characteristic features of the escape behaviours they trigger, showed little sensitivity to acceleration. This closely mirrored a broader lack of sensitivity to acceleration of the goldfish escape behaviour. Thus, although the sensory coding of simulated colliding stimuli with non-zero acceleration probably differs in grasshoppers and goldfish, the triggering of escape behaviours converges towards similar characteristics. Approaching stimuli with non-zero acceleration may help refine our understanding of neural computations underlying escape behaviours in a broad range of animal species. KEY POINTS: A companion manuscript showed that two mathematical models of collision-detecting neurons in grasshoppers and goldfish make distinct predictions for the timing of their responses to simulated objects approaching on a collision course with non-zero acceleration. Testing these experimental predictions showed that grasshopper neurons are sensitive to acceleration while goldfish neurons are not, in agreement with the distinct models proposed previously in these species using constant velocity approaches. Grasshopper and goldfish escape behaviours occurred after the stimulus reached a fixed angular size insensitive to acceleration, suggesting further downstream processing in grasshopper motor circuits to match what was observed in goldfish. Thus, in spite of different sensory processing in the two species, escape behaviours converge towards similar solutions. The use of object acceleration during approach on a collision course may help better understand the neural computations implemented for collision avoidance in a broad range of species.

Organization of descending neurons in the brain of the desert locust.

In most animals, multiple external and internal signals are integrated by the brain, transformed and, finally, transmitted as commands to motor centers. In insects, the central complex is a motor control center in the brain, involved in decision-making and goal-directed navigation. In desert locusts, it encodes celestial cues in a compass-like fashion indicating a role in sky-compass navigation. While several descending brain neurons (DBNs) including two neurons transmitting sky compass signals have been identified in the locust, a complete analysis of DBNs and their relationship to the central complex is still lacking. As a basis for further studies, we used Neurobiotin tracer injections into a neck connective to map the organization of DBNs in the brain. Cell counts revealed a maximum of 324 bilateral pairs of DBNs with somata distributed in 14 ipsilateral and nine contralateral groups. These neurons invaded most brain neuropils, especially the posterior slope, posterior and ventro-lateral protocerebrum, the antennal mechanosensory and motor center, but less densely the lateral accessory lobes that are targeted by central-complex outputs. No arborizations were found in the central complex and only few processes in the mushroom body, antennal lobe, lobula, medulla, and superior protocerebrum. Double label experiments provide evidence for the presence of GABA, dopamine, tyramine, but not serotonin, in small sets of DBNs. The data show that some DBNs may be targeted directly by central-complex outputs, but many others are likely only indirectly influenced by central-complex networks, in addition to input from multiple other brain areas.

The chemical ecology of locust cannibalism.

An anticannibalistic signaling pathway offers a new understanding of locust swarm formation.

Integration of optic flow into the sky compass network in the brain of the desert locust.

Flexible orientation through any environment requires a sense of current relative heading that is updated based on self-motion. Global external cues originating from the sky or the earth's magnetic field and local cues provide a reference frame for the sense of direction. Locally, optic flow may inform about turning maneuvers, travel speed and covered distance. The central complex in the insect brain is associated with orientation behavior and largely acts as a navigation center. Visual information from global celestial cues and local landmarks are integrated in the central complex to form an internal representation of current heading. However, it is less clear how optic flow is integrated into the central-complex network. We recorded intracellularly from neurons in the locust central complex while presenting lateral grating patterns that simulated translational and rotational motion to identify these sites of integration. Certain types of central-complex neurons were sensitive to optic-flow stimulation independent of the type and direction of simulated motion. Columnar neurons innervating the noduli, paired central-complex substructures, were tuned to the direction of simulated horizontal turns. Modeling the connectivity of these neurons with a system of proposed compass neurons can account for rotation-direction specific shifts in the activity profile in the central complex corresponding to turn direction. Our model is similar but not identical to the mechanisms proposed for angular velocity integration in the navigation compass of the fly Drosophila.

Approaching object acceleration differentially affects the predictions of neuronal collision avoidance models.

The processing of visual information for collision avoidance has been investigated at the biophysical level in several model systems. In grasshoppers, the (so-called) [Formula: see text] model captures reasonably well the visual processing performed by an identified neuron called the lobular giant movement detector as it tracks approaching objects. Similar phenomenological models have been used to describe either the firing rate or the membrane potential of neurons responsible for visually guided collision avoidance in other animals. Specifically, in goldfish, the [Formula: see text] model has been proposed to describe the Mauthner cell, an identified neuron involved in startle escape responses. In the vinegar fly, a third model was developed for the giant fiber neuron, which triggers last resort escapes immediately before an impending collision. One key property of these models is their prediction that peak neuronal responses occur at a fixed delay after the simulated approaching object reaches a threshold angular size on the retina. This prediction is valid for simulated objects approaching at a constant speed. We tested whether it remains valid when approaching objects accelerate. After characterizing and comparing the models' responses to accelerating and constant speed stimuli, we find that the prediction holds true for the [Formula: see text] and the giant fiber model, but not for the [Formula: see text] model. These results suggest that acceleration in the approach trajectory of an object may help distinguish and further constrain the neuronal computations required for collision avoidance in grasshoppers, fish and vinegar flies.

Thermoregulatory behavior of lekking male desert locusts, Schistocerca gregaria, in the Sahara Desert.

Most terrestrial animals are constrained by extreme heat conditions such as midday desert environments, while a few terrestrial ectothermic insects are active in such ecological niches. Sexually mature males of the desert locust (Schistocerca gregaria) in the Sahara Desert remain on the open ground, despite the ground temperatures exceeding their lethal limit, to form leks and to mate incoming gravid females during the daytime. Lekking male locusts apparently suffer from extreme heat stress and greatly fluctuating thermal conditions. The present study examined the thermoregulatory strategies of the lekking male S. gregaria. Our field observations showed that lekking males changed their body orientation toward the sun depending on the temperature and time of day. In the relatively cool morning, males basked by orienting perpendicular to the sun's rays, maximizing the area of body surface exposed to the sun's rays. In contrast, around midday, when the ground surface temperature exceeded lethal high temperatures, some males tended to shelter inside the plants or remain in the shade. However, the remainder stayed on the ground, stilted (i.e., extending their legs to raise their bodies off the hot ground) and oriented parallel to the sun's rays, which minimized radiative heating. Measurements of body temperature throughout the hot middle period of the day confirmed that the stilting posture prevented overheating. Their critical lethal body temperature was as high as 54.7 °C. In this lekking system, gravid females enter male leks by flying. These incoming females usually landed on open ground, whereupon nearby males immediately approached, mounted, and mated the female, implying that males with greater heat-tolerance can increase mating chance. These results suggest that behavioral thermoregulation and physiologically high heat tolerance of male desert locusts allows them to endure extreme thermal conditions for lekking.

Neurons sensitive to non-celestial polarized light in the brain of the desert locust.

Owing to alignment of rhodopsin in microvillar photoreceptors, insects are sensitive to the oscillation plane of polarized light. This property is used by many species to navigate with respect to the polarization pattern of light from the blue sky. In addition, the polarization angle of light reflected from shiny surfaces such as bodies of water, animal skin, leaves, or other objects can enhance contrast and visibility. Whereas photoreceptors and central mechanisms involved in celestial polarization vision have been investigated in great detail, little is known about peripheral and central mechanisms of sensing the polarization angle of light reflected from objects and surfaces. Desert locusts, like other insects, use a polarization-dependent sky compass for navigation but are also sensitive to polarization angles from horizontal directions. In order to further analyze the processing of polarized light reflected from objects or water surfaces, we tested the sensitivity of brain interneurons to the angle of polarized blue light presented from ventral direction in locusts that had their dorsal eye regions painted black. Neurons encountered interconnect the optic lobes, invade the central body, or send descending axons to the ventral nerve cord but are not part of the polarization vision pathway involved in sky-compass coding.

Visual processing and collective motion-related decision-making in desert locusts.

Collectively moving groups of animals rely on the decision-making of locally interacting individuals in order to maintain swarm cohesion. However, the complex and noisy visual environment poses a major challenge to the extraction and processing of relevant information. We addressed this challenge by studying swarming-related decision-making in desert locust last-instar nymphs. Controlled visual stimuli, in the form of random dot kinematograms, were presented to tethered locust nymphs in a trackball set-up, while monitoring movement trajectory and walking parameters. In a complementary set of experiments, the neurophysiological basis of the observed behavioural responses was explored. Our results suggest that locusts use filtering and discrimination upon encountering multiple stimuli simultaneously. Specifically, we show that locusts are sensitive to differences in speed at the individual conspecific level, and to movement coherence at the group level, and may use these to filter out non-relevant stimuli. The locusts also discriminate and assign different weights to different stimuli, with an observed interactive effect of stimulus size, relative abundance and motion direction. Our findings provide insights into the cognitive abilities of locusts in the domain of decision-making and visual-based collective motion, and support locusts as a model for investigating sensory-motor integration and motion-related decision-making in the intricate swarm environment.

High carbohydrate consumption increases lipid storage and promotes migratory flight in locusts.

Migration allows animals to track favorable environments and avoid harmful conditions. However, migration is energetically costly, so migrating animals must prepare themselves by increasing their energy stores. Despite the importance of locust migratory swarms, we still understand little about the physiology of locust migration. During long-distance flight, locusts rely on lipid oxidation, despite the fact that lipids are relatively rare in their leaf-based diets. Therefore, locusts and other insect herbivores synthesize and store lipid from ingested carbohydrates, which are also important for initial flight. These data suggest that diets high in carbohydrate should increase lipid stores and the capacity for migratory flight in locusts. As predicted, locust lipid stores and flight performance increased with an increase in the relative carbohydrate content in their food. However, locust flight termination was not associated with complete lipid depletion. We propose potential testable mechanisms that might explain how macronutrient consumption can affect flight endurance.

Cytosolic and mitochondrial ribosomal proteins mediate the locust phase transition via divergence of translational profiles.

The phase transition from solitary to gregarious locusts is crucial in outbreaks of locust plague, which threaten agricultural yield and food security. Research on the regulatory mechanisms of phase transition in locusts has focused primarily on the transcriptional or posttranslational level. However, the translational regulation of phase transition is unexplored. Here, we show a phase-dependent pattern at the translation level, which exhibits different polysome profiles between gregarious and solitary locusts. The gregarious locusts exhibit significant increases in 60S and polyribosomes, while solitary locusts possess higher peaks of the monoribosome and a specific "halfmer." The polysome profiles, a molecular phenotype, respond to changes in population density. In gregarious locusts, ten genes involved in the cytosolic ribosome pathway exhibited increased translational efficiency (TE). In solitary locusts, five genes from the mitochondrial ribosome pathway displayed increased TE. The high expression of large ribosomal protein 7 at the translational level promotes accumulation of the free 60S ribosomal subunit in gregarious locusts, while solitary locusts employ mitochondrial small ribosomal protein 18c to induce the assembly of mitochondrial ribosomes, causing divergence of the translational profiles and behavioral transition. This study reveals the translational regulatory mechanism of locust phase transition, in which the locusts employ divergent ribosome pathways to cope with changes in population density.

Control of high-speed jumps: the rotation and energetics of the locust (Schistocerca gregaria).

Locusts (Schistocerca gregaria) jump using a latch mediated spring actuated system in the femur-tibia joint of their metathoracic legs. These jumps are exceptionally fast and display angular rotation immediately after take-off. In this study, we focus on the angular velocity, at take-off, of locusts ranging between 0.049 and 1.50 g to determine if and how rotation-rate scales with size. From 263 jumps recorded from 44 individuals, we found that angular velocity scales with mass-0.33, consistent with a hypothesis of locusts having a constant rotational kinetic energy density. Within the data from each locust, angular velocity increased proportionally with linear velocity, suggesting the two cannot be independently controlled and thus a fixed energy budget is formed at take-off. On average, the energy budget of a jump is distributed 98.7% to translational kinetic energy and gravitational potential energy, and 1.3% to rotational kinetic energy. The percentage of energy devoted to rotation was constant across all sizes of locusts and represents a very small proportion of the energy budget. This analysis suggests that smaller locusts find it harder to jump without body rotation.

A Robust Visual System for Looming Cue Detection Against Translating Motion.

Collision detection is critical for autonomous vehicles or robots to serve human society safely. Detecting looming objects robustly and timely plays an important role in collision avoidance systems. The locust lobula giant movement detector (LGMD1) is specifically selective to looming objects which are on a direct collision course. However, the existing LGMD1 models cannot distinguish a looming object from a near and fast translatory moving object, because the latter can evoke a large amount of excitation that can lead to false LGMD1 spikes. This article presents a new visual neural system model (LGMD1) that applies a neural competition mechanism within a framework of separated ON and OFF pathways to shut off the translating response. The competition-based approach responds vigorously to monotonous ON/OFF responses resulting from a looming object. However, it does not respond to paired ON-OFF responses that result from a translating object, thereby enhancing collision selectivity. Moreover, a complementary denoising mechanism ensures reliable collision detection. To verify the effectiveness of the model, we have conducted systematic comparative experiments on synthetic and real datasets. The results show that our method exhibits more accurate discrimination between looming and translational events-the looming motion can be correctly detected. It also demonstrates that the proposed model is more robust than comparative models.

The sky compass network in the brain of the desert locust.

Many arthropods and vertebrates use celestial signals such as the position of the sun during the day or stars at night as compass cues for spatial orientation. The neural network underlying sky compass coding in the brain has been studied in great detail in the desert locust Schistocerca gregaria. These insects perform long-range migrations in Northern Africa and the Middle East following seasonal changes in rainfall. Highly specialized photoreceptors in a dorsal rim area of their compound eyes are sensitive to the polarization of the sky, generated by scattered sunlight. These signals are combined with direct information on the sun position in the optic lobe and anterior optic tubercle and converge from both eyes in a midline crossing brain structure, the central complex. Here, head direction coding is achieved by a compass-like arrangement of columns signaling solar azimuth through a 360° range of space by combining direct brightness cues from the sun with polarization cues matching the polarization pattern of the sky. Other directional cues derived from wind direction and internal self-rotation input are likely integrated. Signals are transmitted as coherent steering commands to descending neurons for directional control of locomotion and flight.

Egg size-dependent embryonic development in the desert locust, Schistocerca gregaria.

Phenotypic plasticity in body size is a product of modification of the developmental pathway. Although hatchlings of the desert locust, Schistocerca gregaria, show egg size-dependent plasticity in body size, it remains unclear how embryogenesis during egg development regulates final embryonic body size. To determine the developmental pathway causing body size variation at hatching, we examined egg and embryonic development at the early, middle, and late egg developmental stages in S. gregaria by comparing small and large eggs. Crowd-reared females produced larger eggs than isolated-reared females. The daily egg developmental rate was similar between small and large eggs: eggs dramatically absorbed external water after days 3 to 7 and nearly doubled the initial egg weight at the late stage of day 12. Morphological measurements of eggs and embryos at different days after oviposition revealed that large eggs were longer than small eggs throughout developmental stages. However, embryo length was similar between small and large eggs at the early stage (anatrepsis). Embryos begin to absorb yolk into their bodies after blastokinesis. The size of large-egg embryos increased significantly from the middle stage (katatrepsis) due to absorption of more yolk than small eggs. Egg length and embryo length were conspicuously larger in large eggs than in small eggs on day 12 of late katatrepsis. These results suggest that egg size did not influence the egg developmental rate and initial embryo size. Large eggs had more yolk and space, resulting in larger final embryos than small eggs. The amount of yolk and size of eggshells during katatrepsis could play a key role in determining hatchling body size in S. gregaria.