SNMP1 is critical for sensitive detection of the desert locust aromatic courtship inhibition pheromone phenylacetonitrile.

BACKGROUND: Accurate detection of pheromones is crucial for chemical communication and reproduction in insects. In holometabolous flies and moths, the sensory neuron membrane protein 1 (SNMP1) is essential for detecting long-chain aliphatic pheromones by olfactory neurons. However, its function in hemimetabolous insects and its role for detecting pheromones of a different chemical nature remain elusive. Therefore, we investigated the relevance of SNMP1 for pheromone detection in a hemimetabolous insect pest of considerable economic importance, the desert locust Schistocerca gregaria, which moreover employs the aromatic pheromone phenylacetonitrile (PAN) to govern reproductive behaviors. RESULTS: Employing CRISPR/Cas-mediated gene editing, a mutant locust line lacking functional SNMP1 was established. In electroantennography experiments and single sensillum recordings, we found significantly decreased electrical responses to PAN in SNMP1-deficient (SNMP1-/-) locusts. Moreover, calcium imaging in the antennal lobe of the brain revealed a substantially reduced activation of projection neurons in SNMP1-/- individuals upon exposure to PAN, indicating that the diminished antennal responsiveness to PAN in mutants affects pheromone-evoked neuronal activity in the brain. Furthermore, in behavioral experiments, PAN-induced effects on pairing and mate choice were altered in SNMP1-/- locusts. CONCLUSIONS: Our findings emphasize the importance of SNMP1 for chemical communication in a hemimetabolous insect pest. Moreover, they show that SNMP1 plays a crucial role in pheromone detection that goes beyond long-chain aliphatic substances and includes aromatic compounds controlling reproductive behaviors.

Synergistic olfactory processing for social plasticity in desert locusts.

Desert locust plagues threaten the food security of millions. Central to their formation is crowding-induced plasticity, with social phenotypes changing from cryptic (solitarious) to swarming (gregarious). Here, we elucidate the implications of this transition on foraging decisions and corresponding neural circuits. We use behavioral experiments and Bayesian modeling to decompose the multi-modal facets of foraging, revealing olfactory social cues as critical. To this end, we investigate how corresponding odors are encoded in the locust olfactory system using in-vivo calcium imaging. We discover crowding-dependent synergistic interactions between food-related and social odors distributed across stable combinatorial response maps. The observed synergy was specific to the gregarious phase and manifested in distinct odor response motifs. Our results suggest a crowding-induced modulation of the locust olfactory system that enhances food detection in swarms. Overall, we demonstrate how linking sensory adaptations to behaviorally relevant tasks can improve our understanding of social modulation in non-model organisms.

Asymmetry between the dorsal and ventral digging valves of the female locust: function and mechanics.

BACKGROUND: The female locust is equipped with unique digging tools, namely two pairs of valves-a dorsal and a ventral-utilized for excavating an underground hole in which she lays her eggs. This apparatus ensures that the eggs are protected from potential predators and provides optimal conditions for successful hatching. The dorsal and the ventral valves are assigned distinct roles in the digging process. Specifically, the ventral valves primarily function as anchors during propagation, while the dorsal valves displace soil and shape the underground tunnel. RESULTS: In this study, we investigated the noticeable asymmetry and distinct shapes of the valves, using a geometrical model and a finite element method. Our analysis revealed that although the two pairs of valves share morphological similarities, they exhibit different 3D characteristics in terms of absolute size and structure. We introduced a structural characteristic, the skew of the valve cross-section, to quantify the differences between the two pairs of valves. Our findings indicate that these structural variations do not significantly contribute to the valves' load-bearing capabilities under external forces. CONCLUSIONS: The evolutionary development of the form of the female locust digging valves is more aligned with fitting their respective functions rather than solely responding to biomechanical support needs. By understanding the intricate features of these locust valves, and using our geometrical model, valuable insights can be obtained for creating more efficient and specialized tools for various digging applications.

Toxic tasting: how capuchin monkeys avoid grasshoppers' chemical defenses.

Platyrrhines consume many species of arthropods in the order Orthoptera. Some species of orthopterans can produce chemical defenses that render them toxic or unpalatable and thus act as predator deterrents. These species include the stick grasshoppers (family Proscopiidae), which are widely distributed in the Caatinga biome in northeastern Brazil, which comprises part of the distribution of capuchin monkeys. Capuchin monkeys are omnivores and consume a wide variety of foods, including unpleasant-tasting, potentially toxic items, which they need to learn how to process. We describe the processing of stick grasshoppers (Stiphra sp.) by wild capuchin monkeys (Sapajus libidinosus) that live in Serra da Capivara National Park, Brazil, and compare how individuals of different age classes handle these potentially toxic food items. S. libidinosus predominantly avoided consuming the digestive tract, which contains toxic compounds, when feeding on stick grasshoppers. Immatures took longer than adults to process the stick grasshoppers, indicating that capuchins need to learn how to process the toxic digestive tract of these prey to avoid consuming it.

Risk of migration: not all gregarious locust nymphs reach appropriate refuges.

Sedentary animals choose appropriate refuges against predators, while migratory ones may not necessarily do so. In ectotherms, refuge selection is critical during low temperatures, because they cannot actively evade predators. To understand how migratory ectotherms alter their defensive behaviors depending on refuge quality in cold temperatures, we evaluated migratory gregarious desert locust nymphs (Schistocerca gregaria) in the Sahara Desert, where daily thermal constraints occur. We recorded how roosting plant type (bush/shrub) and its height influenced two alternative defense behaviors (dropping/stationary) during cold mornings, in response to an approaching simulated ground predator. Most locusts in bushes dropped within the bush and hid irrespective of their height, whereas those roosting > 2 m height in shrubs remained stationary. These defenses are effective and match with refuge plant types because dynamic locomotion is not required. When nymphs roosted on shrubs < 1.5-m height, which was an unsafe position, nearly half showed both defensive behaviors, indicating that escaping decisions become ambiguous when the refuges are inappropriate. These results suggest that locusts display flexible defensive behaviors when finding appropriate refuges and selecting refuge before daily thermal limitations occur could be critical for migratory ectotherms, which is a risk associated with migration.

Target for lipid-to-carbohydrate intake minimizes cost of growth.

Many theoretical treatments of foraging use energy as currency, with carbohydrates and lipids considered interchangeable as energy sources. However, herbivores must often synthesize lipids from carbohydrates since they are in short supply in plants, theoretically increasing the cost of growth. We tested whether a generalist insect herbivore (Locusta migratoria) can improve its growth efficiency by consuming lipids, and whether these locusts have a preferred caloric intake ratio of carbohydrate to lipid (C : L). Locusts fed pairs of isocaloric, isoprotein diets differing in C and L consistently selected a 2C : 1L target. Locusts reared on isocaloric, isoprotein 3C : 0L diets attained similar final body masses and lipid contents to locusts fed the 2C : 1L diet, but they ate more and had a ~12% higher metabolic rate, indicating an energetic cost for lipogenesis. These results demonstrate that some animals can selectively regulate carbohydrate-to-lipid intake and that consumption of dietary lipids can improve growth efficiency.

Theoretical principles explain the structure of the insect head direction circuit.

To navigate their environment, insects need to keep track of their orientation. Previous work has shown that insects encode their head direction as a sinusoidal activity pattern around a ring of neurons arranged in an eight-column structure. However, it is unclear whether this sinusoidal encoding of head direction is just an evolutionary coincidence or if it offers a particular functional advantage. To address this question, we establish the basic mathematical requirements for direction encoding and show that it can be performed by many circuits, all with different activity patterns. Among these activity patterns, we prove that the sinusoidal one is the most noise-resilient, but only when coupled with a sinusoidal connectivity pattern between the encoding neurons. We compare this predicted optimal connectivity pattern with anatomical data from the head direction circuits of the locust and the fruit fly, finding that our theory agrees with experimental evidence. Furthermore, we demonstrate that our predicted circuit can emerge using Hebbian plasticity, implying that the neural connectivity does not need to be explicitly encoded in the genetic program of the insect but rather can emerge during development. Finally, we illustrate that in our theory, the consistent presence of the eight-column organisation of head direction circuits across multiple insect species is not a chance artefact but instead can be explained by basic evolutionary principles.

Insects, including fruit flies and locusts, move throughout their environment to find food, interact with each other or escape danger. To navigate their surroundings, insects need to be able to keep track of their orientation. This tracking is achieved through visual cues and integrating information about their movements whilst flying so they know which direction their head is facing. The set of neurons responsible for relaying information about the direction of the head (also known as heading) are connected together in a ring made up of eight columns of cells. Previous studies showed that the level of activity across this ring of neurons resembles a sinusoid shape: a smooth curve with one peak which encodes the animal's heading. Neurons downstream from this eight-column ring, which relay velocity information, also display this sinusoidal pattern of activation. Aceituno, Dall'Osto and Pisokas wanted to understand whether this sinusoidal pattern was an evolutionary coincidence, or whether it offers a particular advantage to insects. To answer this question, they established the mathematical criteria required for neurons in the eight-column ring to encode information about the heading of the animal. This revealed that these conditions can be satisfied by many different patterns of activation, not just the sinusoidal shape. However, Aceituno, Dall'Osto and Pisokas show that the sinusoidal shape is the most resilient to variations in neuronal activity which may impact the encoded information. Further experiments revealed that this resilience only occurred if neurons in the circuit were connected together in a certain pattern. Aceituno, Dall'Osto and Pisokas then compared this circuit with experimental data from locusts and fruit flies and found that both insects exhibit the predicted connection pattern. They also discovered that animals do not have to be born with this neuronal connection pattern, but can develop it during their lifetime. These findings provide fresh insights into how insects relay information about the direction of their head as they fly. They suggest that the structure of the neuronal circuit responsible for encoding head direction was not formed by chance but instead arose due to the evolutionary benefits it provided.

Study on the prediction method of grasshopper occurrence risk in Inner Mongolia based on the maximum entropy model during the growing period.

Grasshoppers represent a significant biological challenge in Inner Mongolia's grasslands, severely affecting the region's animal husbandry. Thus, dynamic monitoring of grasshopper infestation risk is crucial for sustainable livestock farming. This study employed the Maxent model, along with remote sensing data, to forecast Oedaleus decorus asiaticus occurrence during the growing season, using grasshopper suitability habitats as a base. The Maxent model's predictive accuracy was high, with an AUC of 0.966. The most influential environmental variables for grasshopper distribution were suitable habitat data (34.27%), the temperature-vegetation dryness index during the spawning period (18.81%), and various other meteorological and vegetation factors. The risk index model was applied to calculate the grasshopper distribution across different risk levels for the years 2019-2022. The data indicated that the level 1 risk area primarily spans central, eastern, and southwestern Inner Mongolia. By examining the variable weights, the primary drivers of risk level fluctuation from 2019 to 2022 were identified as accumulated precipitation and land surface temperature anomalies during the overwintering period. This study offers valuable insights for future O. decorus asiaticus monitoring in Inner Mongolia.

Recent advances in insect vision in a 3D world: looming stimuli and escape behaviour.

Detecting looming motion directly towards the insect is vital to its survival. Looming detection in two insects, flies and locusts, is described and contrasted. Pathways using looming detectors to trigger action and their topographical layout in the brain is explored in relation to facilitating behavioural selection. Similar visual stimuli, such as looming motion, are processed by nearby glomeruli in the brain. Insect-inspired looming motion detectors are combined to detect and avoid collision in different scenarios by robots, vehicles and unmanned aerial vehicle (UAV)s.

A neural m6A pathway regulates behavioral aggregation in migratory locusts.

RNA N6-methyladenosine (m6A), as the most abundant modification of messenger RNA, can modulate insect behaviors, but its specific roles in aggregation behaviors remain unexplored. Here, we conducted a comprehensive molecular and physiological characterization of the individual components of the methyltransferase and demethylase in the migratory locust Locusta migratoria. Our results demonstrated that METTL3, METTL14 and ALKBH5 were dominantly expressed in the brain and exhibited remarkable responses to crowding or isolation. The individual knockdown of methyltransferases (i.e., METTL3 and METTL14) promoted locust movement and conspecific attraction, whereas ALKBH5 knockdown induced a behavioral shift toward the solitary phase. Furthermore, global transcriptome profiles revealed that m6A modification could regulate the orchestration of gene expression to fine tune the behavioral aggregation of locusts. In summary, our in vivo characterization of the m6A functions in migratory locusts clearly demonstrated the crucial roles of the m6A pathway in effectively modulating aggregation behaviors.

Linking shape conspicuous asymmetry with shape covariation patterns and performance in the insect head and mandibles.

Bilateral symmetry is widespread across animals, yet, among bilaterians, many cases of conspicuous asymmetries evolved. This means that bilaterally homologous structures on the left and right sides display divergent phenotypes. The evolution of such divergent phenotypes between otherwise similarly shaped structures can be thought to be favored by modularity, but this has rarely been studied in the context of left-right differences. Here, we provide an empirical example, using geometric morphometrics to assess patterns of asymmetry and covariation between landmark partitions in a grasshopper with conspicuously asymmetric mandibles. Our morphometric data confirm the presence of strictly directional conspicuous asymmetry in the mandibles and surrounding structures. Covariance patterns and tests hint at a strong integration between mandibles despite their divergent morphologies, and variational modularity with the head capsule. While mandibles have been selected to achieve a key-and-lock morphology by having interlocking shapes, the developmental modularity required to achieve this seems to be overwritten by developmental and/or functional integration, allowing the precise matching required for feeding. The consequent conflicting covariation patterns are reminiscent of the palimpsest model. Finally, the degree of directional asymmetry appears to be under selection, although we find no relationship between bite force and mandible shape or asymmetry.

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.