Obstacle negotiation in female desert locust oviposition digging.

The female locust lays its eggs deep within soft substrate to protect them from predators and provide optimal conditions for successful development and hatching. During oviposition digging, the female's abdomen is pooled and extends into the ground, guided by a dedicated excavation mechanism at its tip, comprising two pairs of specialized digging valves. Little is known about how these active valves negotiate the various obstacles encountered on their path. In this study, female locusts oviposited their eggs in specialized sand-filled tubes with pre-inserted 3D-printed plastic obstacles. The subterranean route taken by the abdomen and digging valves upon encountering the obstacles was investigated, characterized, and compared to that in control tubes without obstacles. Data were obtained by way of visual inspection, by utilizing cone beam computed tomography scans in high-definition mode, and by making paraffin casts of the oviposition burrows (after egg hatching). We demonstrate, for the first time, the subterranean navigation ability of the female locust's excavation mechanism and its ability to circumvent obstacles during oviposition. Finally, we discuss the role of active sensory-motor mechanisms versus the passive embodied function of the valves, central control, and decision-making.

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.

Locust behavior and city topology: A biodynamic approach for assessing urban flows.

A city's economic growth and the inhabitants' wellbeing are highly affected by its topology and connecting networks, which, in turn, influence movement and flows in the city. Flow relates to how a city is developed, organized, managed, and built. The analysis of flow in cities is challenging but essential. In this study, the fields of urban design and animal science are combined, and a new approach for exploring the relationships between urban topology and physical flow is developed. Specifically, we establish an interdisciplinary methodology to evaluate mobility performance in various urban settings, utilizing experimental observations of the dynamic behavior of natural-biological agents, i.e., locusts, within physical city models. Our novel approach enriches the currently available toolbox by using living organisms as indicators for flow in physical city models. Our findings improve our understanding of the intricate flow interactions in urban settings.

When night becomes day: Artificial light at night alters insect behavior under semi-natural conditions.

Light is the most important Zeitgeber for temporal synchronization in nature. Artificial light at night (ALAN) disrupts the natural light-dark rhythmicity and thus negatively affects animal behavior. However, to date, ALAN research has been mostly conducted under laboratory conditions in this context. Here, we used the field cricket, Gryllus bimaculatus, to investigate the effect of ALAN on insect behavior under semi-natural conditions, i.e., under shaded natural lighting conditions, natural temperature and soundscape. Male crickets were placed individually in outdoor enclosures and exposed to ALAN conditions ranging from <0.01 to 1500 lx intensity. The crickets' stridulation behavior was recorded for 14 consecutive days and nights and their daily activity patterns were analysed. ALAN impaired the crickets' stridulation rhythm, evoking a change in the crickets' naturally synchronized daily activity period. This was manifested by a light-intensity-dependent increase in the proportion of insects demonstrating an intrinsic circadian rhythm (free-run behavior). This also resulted in a change in the population's median activity cycle period. These ALAN-induced effects occurred despite the crickets' exposure to almost natural conditions. Our findings provide further validity to our previous studies on ALAN conducted under lab conditions and establish the deleterious impacts of ALAN on animal behavioral patterns. TEASER: Artificial light at night alters cricket behavior and desynchronizes their stridulation even under near-natural conditions.

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.

Crickets in the spotlight: exploring the impact of light on circadian behavior.

Crickets serve as a well-established model organism in biological research spanning various fields, such as behavior, physiology, neurobiology, and ecology. Cricket circadian behavior was first reported over a century ago and prompted a wealth of studies delving into their chronobiology. Circadian rhythms have been described in relation to fundamental cricket behaviors, encompassing stridulation and locomotion, but also in hormonal secretion and gene expression. Here we review how changes in illumination patterns and light intensity differentially impact the different cricket behaviors as well as circadian gene expression. We further describe the cricket's circadian pacemaker. Ample anatomical manipulations support the location of a major circadian pacemaker in the cricket optic lobes and another in the central brain, possibly interconnected via signaling of the neuropeptide PDF. The cricket circadian machinery comprises a molecular cascade based on two major transcriptional/translational negative feedback loops, deviating somewhat from the canonical model of Drosophila and emphasizing the significance of exploring alternative models. Finally, the nocturnal nature of crickets has provided a unique avenue for investigating the repercussions of artificial light at night on cricket behavior and ecology, underscoring the critical role played by natural light cycles in synchronizing cricket behaviors and populations, further supporting the use of the cricket model in the study of the effects of light on insects. Some gaps in our knowledge and challenges for future studies are discussed.

Vision-based collective motion: A locust-inspired reductionist model.

Naturally occurring collective motion is a fascinating phenomenon in which swarming individuals aggregate and coordinate their motion. Many theoretical models of swarming assume idealized, perfect perceptual capabilities, and ignore the underlying perception processes, particularly for agents relying on visual perception. Specifically, biological vision in many swarming animals, such as locusts, utilizes monocular non-stereoscopic vision, which prevents perfect acquisition of distances and velocities. Moreover, swarming peers can visually occlude each other, further introducing estimation errors. In this study, we explore necessary conditions for the emergence of ordered collective motion under restricted conditions, using non-stereoscopic, monocular vision. We present a model of vision-based collective motion for locust-like agents: elongated shape, omni-directional visual sensor parallel to the horizontal plane, and lacking stereoscopic depth perception. The model addresses (i) the non-stereoscopic estimation of distance and velocity, (ii) the presence of occlusions in the visual field. We consider and compare three strategies that an agent may use to interpret partially-occluded visual information at the cost of the computational complexity required for the visual perception processes. Computer-simulated experiments conducted in various geometrical environments (toroidal, corridor, and ring-shaped arenas) demonstrate that the models can result in an ordered or near-ordered state. At the same time, they differ in the rate at which order is achieved. Moreover, the results are sensitive to the elongation of the agents. Experiments in geometrically constrained environments reveal differences between the models and elucidate possible tradeoffs in using them to control swarming agents. These suggest avenues for further study in biology and robotics.

The hybrid bio-robotic swarm as a powerful tool for collective motion research: a perspective.

Swarming or collective motion is ubiquitous in natural systems, and instrumental in many technological applications. Accordingly, research interest in this phenomenon is crossing discipline boundaries. A common major question is that of the intricate interactions between the individual, the group, and the environment. There are, however, major gaps in our understanding of swarming systems, very often due to the theoretical difficulty of relating embodied properties to the physical agents-individual animals or robots. Recently, there has been much progress in exploiting the complementary nature of the two disciplines: biology and robotics. This, unfortunately, is still uncommon in swarm research. Specifically, there are very few examples of joint research programs that investigate multiple biological and synthetic agents concomitantly. Here we present a novel research tool, enabling a unique, tightly integrated, bio-inspired, and robot-assisted study of major questions in swarm collective motion. Utilizing a quintessential model of collective behavior-locust nymphs and our recently developed Nymbots (locust-inspired robots)-we focus on fundamental questions and gaps in the scientific understanding of swarms, providing novel interdisciplinary insights and sharing ideas disciplines. The Nymbot-Locust bio-hybrid swarm enables the investigation of biology hypotheses that would be otherwise difficult, or even impossible to test, and to discover technological insights that might otherwise remain hidden from view.

Exposure to a nocturnal light pulse simultaneously and differentially affects stridulation and locomotion behaviors in crickets.

It is crucial for living organisms to be in synchrony with their environment and to anticipate circadian and annual changes. The circadian clock is responsible for entraining organisms' activity to the day-night rhythmicity. Artificial light at night (ALAN) was shown to obstruct the natural light cycle, leading to desynchronized behavioral patterns. Our knowledge of the mechanisms behind these adverse effects of ALAN, however, is far from complete. Here we monitored the stridulation and locomotion behavior of male field crickets (Gryllus bimaculatus), raised under light:dark conditions, before, during, and after exposure to a nocturnal 3-h pulse of different ALAN intensities. The experimental insects were then placed under a constant light regime (of different intensities); their behavior was continuously monitored; and the period of their daily activity rhythms was calculated. The light pulse treatment induced a simultaneous negative (suppressing stridulation) and positive (inducing locomotion) effect, manifested in significant changes in the average level of the specific activity on the night of the pulse compared to the preceding and the following nights. The transition to constant light conditions led to significant changes in the period of the circadian rhythms. Both effects were light-intensity-dependent, indicating the importance of dark nights for both individual and population synchronization.

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.

The biomechanics of ultra-stretchable nerves.

When digging in the ground during egg laying the female locust extends her abdomen to 2-3 times of its original length. How the abdominal nervous system accommodates such extreme elongation remains unknown. We characterized and quantified the system's biomechanical response using controlled ex vivo elongation and force measurements. The microstructure of the nerves was studied using histology and high-resolution confocal microscopy. Although the nervous system of sexually mature females demonstrated fully reversible hyper-extensibility of up to 275%, the elongation observed in premature females and males was much more limited. The unique extension dynamics of the different groups were captured by their very different force-displacement curves. Confocal microscopy suggested that elongation is not owing to undulations of the nervous system structure. Thus, the exceptional resistance to deformation and rupture presents the female locust abdominal nervous system as a valuable model for understanding the functionality and pathology related to nerve extension and reversible elongation.

Transcriptional Response of Circadian Clock Genes to an 'Artificial Light at Night' Pulse in the Cricket Gryllus bimaculatus.

Light is the major signal entraining the circadian clock that regulates physiological and behavioral rhythms in most organisms, including insects. Artificial light at night (ALAN) disrupts the natural light-dark cycle and negatively impacts animals at various levels. We simulated ALAN using dim light stimuli and tested their impact on gene expression in the cricket Gryllus bimaculatus, a model of insect physiology and chronobiology. At night, adult light-dark-regime-raised crickets were exposed for 30 min to a light pulse of 2-40 lx. The relative expression of five circadian-clock-associated genes was compared using qPCR. A dim ALAN pulse elicited tissue-dependent differential expression in some of these genes. The strongest effect was observed in the brain and in the optic lobe, the cricket's circadian pacemaker. The expression of opsin-Long Wave (opLW) was upregulated, as well as cryptochrome1-2 (cry) and period (per). Our findings demonstrate that even a dim ALAN exposure may affect insects at the molecular level, underscoring the impact of ALAN on the circadian clock system.

The biomechanics of the locust ovipositor valves: a unique digging apparatus.

The female locust has a unique mechanism for digging in order to deposit its eggs deep in the ground. It uses two pairs of sclerotized valves to displace the granular matter, while extending its abdomen as it propagates underground. This ensures optimal conditions for the eggs to incubate and provides them with protection from predators. Here, the direction-dependent biomechanics of the locust's major, dorsal digging valves are quantified and analysed under forces in the physiological range and beyond, considering the hydration level as well as the females' sexual maturation state. Our findings reveal that the responses of the valves to compression forces in the digging and propagation directions change upon sexual maturation to follow their function and depend on environmental conditions. In addition, mature females, which lay eggs, have stiffer valves, up to approximately 19 times the stiffness of the pre-mature locusts. The valves are stiffer in the major working direction, corresponding to soil shuffling and compression, compared with the direction of propagation. Hydration of the valves reduces their stiffness but increases their resilience against failure. These findings provide mechanical and materials guidelines for the design of novel non-drilling burrowing tools, including three-dimensionally printed anisotropic materials based on composites.

Microbiome-related aspects of locust density-dependent phase transition.

Locust plagues are a notorious, ancient phenomenon. These swarming pests tend to aggregate and perform long migrations, decimating cultivated fields along their path. When population density is low, however, the locusts will express a cryptic, solitary, non-aggregating phenotype that is not considered a pest. Although the transition from the solitary to the gregarious phase has been well studied, associated shifts in the locust's microbiome have yet to be addressed. Here, using 16S rRNA amplicon sequencing, we compared the bacterial composition of solitary desert locusts before and after a phase transition. Our findings revealed that the microbiome is altered during the phase transition, and that a major aspect of this change is the acquisition of Weissella (Firmicutes). Our findings led us to hypothesize that the locust microbiome plays a role in inducing aggregation behaviour, contributing to the formation and maintenance of a swarm. Employing a mathematical model, we demonstrate the potential evolutionary advantage of inducing aggregation under different conditions; specifically, when the aggregation-inducing microbe exhibits a relatively high horizontal transmission rate. This is the first report of a previously unknown and important aspect of locust phase transition, demonstrating that the phase shift includes a shift in the gut and integument bacterial composition.

Lifelong exposure to artificial light at night impacts stridulation and locomotion activity patterns in the cricket Gryllus bimaculatus.

Living organisms experience a worldwide continuous increase in artificial light at night (ALAN), negatively affecting their behaviour. The field cricket, an established model in physiology and behaviour, can provide insights into the effect of ALAN on insect behaviour. The stridulation and locomotion patterns of adult male crickets reared under different lifelong ALAN intensities were monitored simultaneously for five consecutive days in custom-made anechoic chambers. Daily activity periods and acrophases were compared between the experimental groups. Control crickets exhibited a robust rhythm, stridulating at night and demonstrating locomotor activity during the day. By contrast, ALAN affected both the relative level and timing of the crickets' nocturnal and diurnal activity. ALAN induced free-running patterns, manifested in significant changes in the median and variance of the activity periods, and even arrhythmic behaviour. The magnitude of disruption was light intensity dependent, revealing an increase in the difference between the activity periods calculated for stridulation and locomotion in the same individual. This finding may indicate the existence of two peripheral clocks. Our results demonstrate that ecologically relevant ALAN intensities affect crickets' behavioural patterns, and may lead to decoupling of locomotion and stridulation behaviours at the individual level, and to loss of synchronization at the population level.

The social brain of 'non-eusocial' insects.

Decisions are seldom entirely devoid of social influence. Even in organisms that have traditionally been considered non-social, the social environment plays an important role in mediating behavior. Here we review the current knowledge regarding the neural basis of social behaviors in non-eusocial insects, with a particular focus on fruit flies, cockroaches and locusts. Each are shown to offer valuable, and complementary, insights into how social behavior is mediated at the neural level. The presented studies demonstrate that social cues, which are integrated in primary sensory areas, exert a considerable influence on behavior. Further studies with these models, and others, will provide important insights into the diversity of social behaviors, and into the way that these are encoded in dedicated brain and neuronal structures.

Collective motion as a distinct behavioral state of the individual.

The collective motion of swarms depends on adaptations at the individual level. We explored these and their effects on swarm formation and maintenance in locusts. The walking kinematics of individual insects were monitored under laboratory settings, before, as well as during collective motion in a group, and again after separation from the group. It was found that taking part in collective motion induced in the individual unique behavioral kinematics, suggesting the existence of a distinct behavioral mode that we term a "collective-motion-state." This state, characterized by behavioral adaptation to the social context, is long lasting, not induced by crowding per se, but only by experiencing collective motion. Utilizing computational models, we show that this adaptability increases the robustness of the swarm. Overall, our findings suggest that collective motion is not only an emergent property of the group but also depends on a behavioral mode, rooted in endogenous mechanisms of the individual.

The maternal foam plug constitutes a reservoir for the desert locust's bacterial symbionts.

A hallmark of the desert locust's ancient and deserved reputation as a devastating agricultural pest is that of the long-distance, multi-generational migration of locust swarms to new habitats. The bacterial symbionts that reside within the locust gut comprise a key aspect of its biology, augmenting its immunity and having also been reported to be involved in the swarming phenomenon through the emission of attractant volatiles. However, it is still unclear whether and how these beneficial symbionts are transmitted vertically from parent to offspring. Using comparative 16S rRNA amplicon sequencing and direct experiments with engineered bacteria, we provide evidence for vertical transmission of locust gut bacteria. The females may perform this activity by way of inoculation of the egg-pod's foam plug, through which the larvae pass upon hatching. Furthermore, analysis of the composition of the foam revealed chitin to be its major component, along with immunity-related proteins such as lysozyme, which could be responsible for the inhibition of some bacteria in the foam while allowing other, more beneficial, strains to proliferate. Our findings reveal a potential vector for the transgenerational transmission of symbionts in locusts, which contributes to the locust swarm's ability to invade and survive in new territories.