Stereoscopic artificial compound eyes for spatiotemporal perception in three-dimensional space.

Arthropods' eyes are effective biological vision systems for object tracking and wide field of view because of their structural uniqueness; however, unlike mammalian eyes, they can hardly acquire the depth information of a static object because of their monocular cues. Therefore, most arthropods rely on motion parallax to track the object in three-dimensional (3D) space. Uniquely, the praying mantis (Mantodea) uses both compound structured eyes and a form of stereopsis and is capable of achieving object recognition in 3D space. Here, by mimicking the vision system of the praying mantis using stereoscopically coupled artificial compound eyes, we demonstrated spatiotemporal object sensing and tracking in 3D space with a wide field of view. Furthermore, to achieve a fast response with minimal latency, data storage/transportation, and power consumption, we processed the visual information at the edge of the system using a synaptic device and a federated split learning algorithm. The designed and fabricated stereoscopic artificial compound eye provides energy-efficient and accurate spatiotemporal object sensing and optical flow tracking. It exhibits a root mean square error of 0.3 centimeter, consuming only approximately 4 millijoules for sensing and tracking. These results are more than 400 times lower than conventional complementary metal-oxide semiconductor-based imaging systems. Our biomimetic imager shows the potential of integrating nature's unique design using hardware and software codesigned technology toward capabilities of edge computing and sensing.

Modulation of prey capture kinematics in relation to prey distance helps predict success.

Predators are not perfect, as some of their prey capture attempts result in failure. Successful attempts may be partly due to predators modulating their capture kinematics in relation to variation in the visual cues of the prey to increase the probability of success. In praying mantises, which have been suggested to possess stereoscopic vision, variation in prey distance has been shown to elicit variation in the probability of an attempt. However, it remains to be examined whether variation in prey distance results in mantises modulating their attempt to successfully capture prey. The goals of this study were to examine these relationships using the praying mantis system. Using 11 adult female Sphodromantis lineola, we recorded 192 prey capture attempts at 1000 Hz with two cameras to examine the 3D kinematics of successful and unsuccessful prey capture attempts. Using a combination of principal component analysis (PCA) and logistic regression, our results show that as prey distance increases, mantises adjust through greater and faster expansion of the forelegs and body (PC1), which significantly predicts capture success. However, PC1 only explains 22% of the variation in all prey capture attempts, suggesting that the other components may be related to additional aspects of the prey. Our results suggest that the distances at which mantises prefer to attempt to capture prey may be the result of their greater probability of successfully capturing the prey. These results highlight the range of motions mantises use when attempting to capture prey, suggesting flexibility in their prey capture attempts in relation to prey position.

Diurnal predators in dim light: the ability of mantids to prey for supper.

Many insects rely heavily on visual cues in foraging and other life activities. Mantids are insect predators that usually ambush prey. The sophisticated visual system of mantids allows them to spot, track, and strike at prey with high accuracy. Mantids are categorized as diurnal animals in most cases, while our field observations suggested that they were active in foraging both day and night. Therefore, we hypothesize that predation in dim light is possible for mantids, while mantids are unable to capture prey in complete darkness. In this study, we experimentally examined whether different light conditions could affect the predation success and efficiency of mantid nymphs and adults, Hierodula chinensis Werner (Mantodea: Mantidae), through behavioral observations. Individual mantids were placed in individual chambers in complete darkness, simulated moonlight (0.1 lux), or simulated dusk (50 lux) conditions and were allowed to forage for prey items for 10 min. Our observations showed no evidence that H. chinensis could capture any prey in complete deprivation of light. The proportion of nymphs with successful predation in simulated moonlight was 50% higher than that in complete darkness and 45.83% lower than that in simulated dusk. The proportion of adults with successful predation in simulated moonlight was 42.11% higher than that in complete darkness and 57.89% lower than that in simulated dusk. Overall, the results provide new insights into the behavioral ecology of diurnal predators at night, with potential association with moonlight, starlight, and light pollution.

Extrinsic and intrinsic musculature of the raptorial forelegs in Mantodea (Insecta) in the light of functionality and sexual dimorphism.

Prehensile raptorial forelegs are prey capturing and grasping devices, best known for praying mantises (Mantodea) within insects. They show strong morphological and behavioral adaptations toward a lifestyle as generalist arthropod predators. In the past, few species of Mantodea were investigated, concerning morphological variability of the raptorial forelegs. Especially the knowledge of foreleg anatomy in the light of functional and comparative morphology is scarce. Our comparative approach is based on the, for arthropods very common, "female-biased sexual size dimorphism" (SSD) that occurs in almost every Mantodea species. Within Mantodea, this SSD is likely leading to a shift of the exploited ecological niche between male and female individuals due to changes in, for example, the possible prey size; which might be reflected in the chosen ecomorphs. In this context, we analyzed the musculature of the raptorial forelegs of female and male specimens in five different species with varying SSD, using high-resolution microcomputed tomography and dissection. We were able to confirm the presence of 15 extrinsic and 15 intrinsic muscles-including one previously undescribed muscle present in all species. Thus, presenting a detailed description and illustrative three-dimensional anatomical visualization of the musculature in Mantodea. Interestingly, almost no observable differences were found, neither between species, nor between the sexes. Furthermore, we homologized all described muscles, due to their attachment points, to the comprehensive nomenclature established by Friedrich and Beutel (2008), discussed potential functionality of the muscles and possible homologies to the neuropteran Mantispa styriaca (Büsse et al., 2021) and the newly introduced leg nomenclature by Aibekova et al. (2022). By elucidating the anatomy, particularly in the context of functionality and SSD, our results complement previous knowledge of the raptorial forelegs, and facilitate a better understanding of the underlying biomechanical system of the predatory strike, and ultimately, a future comparison to other insect taxa.

Behavioral Comparison in Males of Two Praying Mantis Species of the Same Genus, Hierodula patellifera and H. chinensis (Mantodea: Mantidae: Hierodulinae) in Japan, in Response to the Conspecific or Allospecific Species of Calling Females and Females' Headspace Crude Extract.

For many years, only one species of praying mantis in the genus Hierodula, Hierodula patellifera Serville, had been recorded in Japan. In recent years, however, Hierodula chinensis Werner, a larger species than H. patellifera Serville, has been discovered in Japan, and observations and collections in Japan have increased rapidly. There are reports that in some areas, H. patellifera became locally extinct due to the invasion of H. chinensis. Since females of H. patellifera attract conspecific males by volatile with characteristic calling behavior, a sex pheromone-mediated reproductive interference may exist between the two species. Both males of H. patellifera and males of H. chinensis were strongly attracted to conspecific females and crude headspace extract from conspecific females, while they were not attracted to females of allospecific species or crude headspace extract from allospecific females. These results indicate that sex pheromone-mediated reproductive interference may not exist between H. patellifera and H. chinensis.

The Role of Central Complex Neurons in Prey Detection and Tracking in the Freely Moving Praying Mantis (Tenodera sinensis).

Complex tasks like hunting moving prey in an unpredictable environment require high levels of motor and sensory integration. An animal needs to detect and track suitable prey objects, measure their distance and orientation relative to its own position, and finally produce the correct motor output to approach and capture the prey. In the insect brain, the central complex (CX) is one target area where integration is likely to take place. In this study, we performed extracellular multi-unit recordings on the CX of freely hunting praying mantises (Tenodera sinensis). Initially, we recorded the neural activity of freely moving mantises as they hunted live prey. The recordings showed activity in cells that either reflected the mantis's own movements or the actions of a prey individual, which the mantises focused on. In the latter case, the activity increased as the prey moved and decreased when it stopped. Interestingly, cells ignored the movement of the other prey than the one to which the mantis attended. To obtain quantitative data, we generated simulated prey targets presented on an LCD screen positioned below the clear floor of the arena. The simulated target oscillated back and forth at various angles and distances. We identified populations of cells whose activity patterns were strongly linked to the appearance, movement, and relative position of the virtual prey. We refer to these as sensory responses. We also found cells whose activity preceded orientation movement toward the prey. We call these motor responses. Some cells showed both sensory and motor properties. Stimulation through tetrodes in some of the preparations could also generate similar movements. These results suggest the crucial importance of the CX to prey-capture behavior in predatory insects like the praying mantis and, hence, further emphasize its role in behaviorally and ecologically relevant contexts.

Context-dependent effects on attack and defense behaviors in the praying mantis Tenodera sinensis.

Most behavior needs to strike a balance between the competing needs to find food and protect an animal from predators. The factors that influence this balance and the resulting behavior are not well understood in many animals. Here, we examined these influences in the praying mantis Tenodera sinensis by presenting perching individuals with alternating sinusoidally moving prey-like stimuli and rapidly expanding looming stimuli then scoring their behavior on a defensive-aggressive scale. In this way, we tested the hypothesis that such behaviors are highly context dependent. Specifically, we found that defensive responses, which are normally very consistent, are decreased in magnitude if the animal has just performed an aggressive response to the previous sinusoid. A thrash behavior not normally seen with looming alone was often seen following aggression. In thrashing, the animal tries to push the looming stimulus away. Thrashing almost exclusively followed aggressive responses to the sinusoid stimulus. Moreover, aggression levels were found to shift from low to high and back to low as adult animals aged and, in general, female mantises were more aggressive than males. Finally, the specific nature of the mid-life spike in aggressive behaviors differed according to whether the animals were lab raised or caught in the wild. Lab-raised animals showed roughly equal amounts of increased attention to the stimulus and very aggressive strike behaviors, whereas wild-caught animals tended to either ignore the stimulus or react very aggressively with strikes. Therefore, our hypothesis regarding context-dependent effects was supported, with all four factors influencing the behaviors that were studied.

A computational model of stereoscopic prey capture in praying mantises.

We present a simple model which can account for the stereoscopic sensitivity of praying mantis predatory strikes. The model consists of a single "disparity sensor": a binocular neuron sensitive to stereoscopic disparity and thus to distance from the animal. The model is based closely on the known behavioural and neurophysiological properties of mantis stereopsis. The monocular inputs to the neuron reflect temporal change and are insensitive to contrast sign, making the sensor insensitive to interocular correlation. The monocular receptive fields have a excitatory centre and inhibitory surround, making them tuned to size. The disparity sensor combines inputs from the two eyes linearly, applies a threshold and then an exponent output nonlinearity. The activity of the sensor represents the model mantis's instantaneous probability of striking. We integrate this over the stimulus duration to obtain the expected number of strikes in response to moving targets with different stereoscopic disparity, size and vertical disparity. We optimised the parameters of the model so as to bring its predictions into agreement with our empirical data on mean strike rate as a function of stimulus size and disparity. The model proves capable of reproducing the relatively broad tuning to size and narrow tuning to stereoscopic disparity seen in mantis striking behaviour. Although the model has only a single centre-surround receptive field in each eye, it displays qualitatively the same interaction between size and disparity as we observed in real mantids: the preferred size increases as simulated prey distance increases beyond the preferred distance. We show that this occurs because of a stereoscopic "false match" between the leading edge of the stimulus in one eye and its trailing edge in the other; further work will be required to find whether such false matches occur in real mantises. Importantly, the model also displays realistic responses to stimuli with vertical disparity and to pairs of identical stimuli offering a "ghost match", despite not being fitted to these data. This is the first image-computable model of insect stereopsis, and reproduces key features of both neurophysiology and striking behaviour.

Internal state effects on behavioral shifts in freely behaving praying mantises (Tenodera sinensis).

How we interact with our environment largely depends on both the external cues presented by our surroundings and the internal state from within. Internal states are the ever-changing physiological conditions that communicate the immediate survival needs and motivate the animal to behaviorally fulfill them. Satiety level constitutes such a state, and therefore has a dynamic influence on the output behaviors of an animal. In predatory insects like the praying mantis, hunting tactics, grooming, and mating have been shown to change hierarchical organization of behaviors depending on satiety. Here, we analyze behavior sequences of freely hunting praying mantises (Tenodera sinensis) to explore potential differences in sequential patterning of behavior as a correlate of satiety. First, our data supports previous work that showed starved praying mantises were not just more often attentive to prey, but also more often attentive to further prey. This was indicated by the increased time fraction spent in attentive bouts such as prey monitoring, head turns (to track prey), translations (closing the distance to the prey), and more strike attempts. With increasing satiety, praying mantises showed reduced time in these behaviors and exhibited them primarily towards close-proximity prey. Furthermore, our data demonstrates that during states of starvation, the praying mantis exhibits a stereotyped pattern of behavior that is highly motivated by prey capture. As satiety increased, the sequenced behaviors became more variable, indicating a shift away from the necessity of prey capture to more fluid presentations of behavior assembly.

Predation by avian predators may have initiated the evolution of myrmecomorph spiders.

Myrmecomorphy is a strategy utilized by a variety of species, among which spiders are the most common. It is supposed that myrmecomorphy tends to be selected by predator avoidance of preying on ants rather than by blind ant workers. To date, this hypothesis has been tested mainly on invertebrate predators (mantises and spiders). We are the first to test whether an imperfect myrmecomorph spider (Phrurolithus festivus) gains protection against avian predators (wild adult great tits-Parus major) through its appearance. In a set of preferential trials, we showed that the ant model and the myrmecomorph spider are equally well protected against attack, though the attacked myrmecomorphs are usually eaten. This suggests that the mimicry of the myrmecomorph spiders is effective against avian predators and works in a Batesian manner. In this study, we have provided evidence toward the evolution of myrmecomorphy in response to selective pressure elicited by visually-oriented predators like birds.

Enhanced polarotaxis can explain water-entry behaviour of mantids infected with nematomorph parasites.

A wide range of parasites manipulate the behaviours of their hosts in order to complete their life cycle1. Alteration of phototaxis is thought to be involved in host manipulation in many cases2,3. However, very little is known about what features of the light (intensity, spectrum, polarization) alter behaviour. Here we report that arboreal mantids (Hierodula patellifera) infected by nematomorph parasites (Chordodes sp.) are attracted to horizontally polarized light, which could induce the mantids to enter water, where the parasites can then emerge and reproduce. In a two-choice test, infected mantids were attracted to horizontally but not vertically polarized light. Uninfected mantids were not attracted to either. In a field experiment, 14 infected mantids entered a deep pool, where the water surface strongly reflected horizontally polarized light. By contrast, only two mantids entered a shallow pool, where the surface reflection had higher light intensity but weaker polarization. To our knowledge, this is the first study demonstrating that a manipulative parasite can take advantage of its hosts' ability to perceive polarized light stimuli to alter host behaviour. VIDEO ABSTRACT.

Aldehyde-specific responses of olfactory sensory neurons in the praying mantis.

Although praying mantises rely mainly on vision for predatory behaviours, olfaction also plays a critical role in feeding and mating behaviours. However, the receptive processes underlying olfactory signals remain unclear. Here, we identified olfactory sensory neurons (OSNs) that are highly tuned to detect aldehydes in the mantis Tenodera aridifolia. In extracellular recordings from OSNs in basiconic sensilla on the antennae, we observed three different spike shapes, indicating that at least three OSNs are housed in a single basiconic sensillum. Unexpectedly, one of the three OSNs exhibited strong excitatory responses to a set of aldehydes. Based on the similarities of the response spectra to 15 different aldehydes, the aldehyde-specific OSNs were classified into three classes: B, S, and M. Class B broadly responded to most aldehydes used as stimulants; class S responded to short-chain aldehydes (C3-C7); and class M responded to middle-length chain aldehydes (C6-C9). Thus, aldehyde molecules can be finely discriminated based on the activity patterns of a population of OSNs. Because many insects emit aldehydes for pheromonal communication, mantises might use aldehydes as olfactory cues for locating prey habitat.

The evolution of startle displays: a case study in praying mantises.

Anti-predator defences are typically regarded as relatively static signals that conceal prey or advertise their unprofitability. However, startle displays are complex performances that deter or confuse predators and can include a spectacular array of movements, colours and sounds. Yet, we do not fully understand the mechanisms by which they function, their evolutionary correlates, or the conditions under which they are performed and evolve. Here, we present, to our knowledge, the first phylogenetically controlled comparative analyses of startle displays including behavioural data, using praying mantises as a model system. We included 58 species that provide a good representation of mantis diversity and estimated the strength of phylogenetic signal in the presence and complexity of displays. We also tested hypotheses on potential evolutionary correlates, including primary defences and body size. We found that startle displays and morphological traits were phylogenetically conserved, whereas behavioural traits were highly labile. Surprisingly, body size was not correlated with display presence or complexity in phylogenetically controlled analyses. Species-rich clades were more likely to exhibit displays, suggesting that startle displays were probably involved in lineage diversification. We suggest that to further elucidate the conditions under which startle displays evolve, future work should include quantitative descriptions of multiple display components, habitat type, and predator communities. Understanding the evolution of startle displays is critical to our overall understanding of the theory behind predator-prey dynamics.

Mantis Shrimp Navigate Home Using Celestial and Idiothetic Path Integration.

Path integration is a robust mechanism that many animals employ to return to specific locations, typically their homes, during navigation. This efficient navigational strategy has never been demonstrated in a fully aquatic animal, where sensory cues used for orientation may differ dramatically from those available above the water's surface. Here, we report that the mantis shrimp, Neogonodactylus oerstedii, uses path integration informed by a hierarchical reliance on the sun, overhead polarization patterns, and idiothetic (internal) orientation cues to return home when foraging, making them the first fully aquatic path-integrating animals yet discovered. We show that mantis shrimp rely on navigational strategies closely resembling those used by insect navigators, opening a new avenue for the investigation of the neural basis of navigation behaviors and the evolution of these strategies in arthropods and potentially other animals as well. VIDEO ABSTRACT.

Evolutionary diversification in the raptorial forelegs of Mantodea: Relations to body size and depth perception.

Limb proportions have evolved among animals to meet functional demands among diverse environments. Studies from terrestrial, vertebrate locomotion have demonstrated that variation in limb proportions have adaptively evolved so animals can perform in a given environment. Most of the research on limb proportion evolution is among vertebrates and terrestrial locomotion, with little information on limb segment evolution in invertebrates or for other functional roles. For example, among invertebrates, multisegmented raptorial forelimbs have evolved multiple times independently to capture prey, but there is little information on the adaptive evolution and diversity of these limbs. Furthermore, as feeding performance is influenced by the sensory system, few studies have examined the coevolution of sensory-motor systems. Using mantises (Mantodea) I examined forelimb diversification among 97 species with a combination of methods, including ternary plots for morphospace visualization, phylogenetically informed allometric relationships, and comparison of evolutionary rates of diversification. Furthermore, using head width as a proxy for depth perception, I examined the correlated evolution of foreleg diversity with depth perception. The results show that among the three segments of the foreleg, the tibia is the smallest, most diverse, and has the highest rate of evolution after body size corrections. Furthermore, while all foreleg segments were related to head width, head width explained the most variation in tibial length compared with other foreleg segments. The results suggest a potential adaptive functional role of tibia length related to the displacement or force produced in this mechanical lever. Furthermore, results from this study support distinct ecomorphs of mantises, as several independent evolutions to grass mimicry evolve similar morphologies. RESEARCH HIGHLIGHT: This study demonstrates interspecific variation among segments of an invertebrate raptorial foreleg. Among Mantodea species the tibia is the most diverse and is related to a proxy for depth perception, while the other segments had strong relationships with body size. This suggests an adaptive, functional role of the tibia during prey capture.

Binocular responsiveness of projection neurons of the praying mantis optic lobe in the frontal visual field.

Praying mantids are the only insects proven to have stereoscopic vision (stereopsis): the ability to perceive depth from the slightly shifted images seen by the two eyes. Recently, the first neurons likely to be involved in mantis stereopsis were described and a speculative neuronal circuit suggested. Here we further investigate classes of neurons in the lobula complex of the praying mantis brain and their tuning to stereoscopically-defined depth. We used sharp electrode recordings with tracer injections to identify visual projection neurons with input in the optic lobe and output in the central brain. In order to measure binocular response fields of the cells the animals watched a vertical bar stimulus in a 3D insect cinema during recordings. We describe the binocular tuning of 19 neurons projecting from the lobula complex and the medulla to central brain areas. The majority of neurons (12/19) were binocular and had receptive fields for both eyes that overlapped in the frontal region. Thus, these neurons could be involved in mantis stereopsis. We also find that neurons preferring different contrast polarity (bright vs dark) tend to be segregated in the mantis lobula complex, reminiscent of the segregation for small targets and widefield motion in mantids and other insects.

A New Species of Praying Mantis from Peru Reveals Impaling as a Novel Hunting Strategy in Mantodea (Thespidae: Thespini).

A new species of lichen-mimicking praying mantis, Carrikerella simpira n. sp., is described from Tingo María region in Peru. The new species differs from its congeners in having reduced tergal lobes, a relatively sinuous pronotum, and it is found in the highland tropical rainforest of the Central Andes. Behavioral observations conducted on captive individuals revealed that juveniles and adults hunt by impaling prey using modified foretibial structures. Anatomical examinations of the incumbent trophic structures revealed functional adaptations for prey impaling in the foretibiae, primarily consisting of prominent, forwardly oriented, barbed spines. We provide an overall description of this novel hunting behavior in Mantodea and hypothesize on its evolutionary origin and adaptive significance for the Thespidae.

Predatory behavior changes with satiety or increased insulin levels in the praying mantis (Tenodera sinensis).

At any given moment, behavior is controlled by a combination of external stimuli and an animal's internal state. As physiological conditions change, vastly different behaviors might result from the same stimuli. For example, the motivation to hunt and hunting strategy are influenced by satiety. Here, we describe how sensory responsiveness and motor activity of a praying mantis (Tenodera sinensis) change as the insect feeds, leading to an altered hunting strategy. We further show that these changes can be induced by injection of insulin, which likely functions as a metabotropic indicator. Praying mantises directed their attention toward real and simulated prey less often as they fed and became sated. The range of distance and azimuth at which prey was detected decreased as did pursuit of prey, while opportunistic close-range attacks persisted. Together, these sensorimotor changes are indicative of a behavioral paradigm shift from 'pursuit' to 'ambush'. A similar effect was induced in starved praying mantises injected with 0.05 ml of 200 µg ml-1 bovine insulin. These experiments showed that insulin injection into the circulating hemolymph is sufficient to decrease prey orientation as well as in prey-directed locomotor behaviors (tracking and pursuit). The effects of prey consumption and insulin injection were similarly dose dependent. These results suggest that insulin is a signal of internal, physiological conditions that can modify responses to external stimuli. A change in hunting strategy thus results from coordinated effects of a neurohormone on a set of independent sensorimotor processes and the overall activity level of the animal.

The behavioral repertoire of Drosophila melanogaster in the presence of two predator species that differ in hunting mode.

The fruit fly, Drosophila melanogaster, has proven to be an excellent model organism for genetic, genomic and neurobiological studies. However, relatively little is known about the natural history of D. melanogaster. In particular, neither the natural predators faced by wild populations of D. melanogaster, nor the anti-predatory behaviors they may employ to escape and avoid their enemies have been documented. Here we observe and describe the influence of two predators that differ in their mode of hunting: zebra jumping spiders, Salticus scenicus (active hunters) and Chinese praying mantids, Tenodera sinensis (ambush predators) on the behavioral repertoire of Drosophila melanogaster. We documented three particularly interesting behaviors: abdominal lifting, stopping, and retreat-which were performed at higher frequency by D. melanogaster in the presence of predators. While mantids had only a modest influence on the locomotory activity of D. melanogaster, we observed a significant increase in the overall activity of D. melanogaster in the presence of jumping spiders. Finally, we observed considerable among-individual behavioral variation in response to both predators.

A neuronal correlate of insect stereopsis.

A puzzle for neuroscience-and robotics-is how insects achieve surprisingly complex behaviours with such tiny brains. One example is depth perception via binocular stereopsis in the praying mantis, a predatory insect. Praying mantids use stereopsis, the computation of distances from disparities between the two retinal images, to trigger a raptorial strike of their forelegs when prey is within reach. The neuronal basis of this ability is entirely unknown. Here we show the first evidence that individual neurons in the praying mantis brain are tuned to specific disparities and eccentricities, and thus locations in 3D-space. Like disparity-tuned cortical cells in vertebrates, the responses of these mantis neurons are consistent with linear summation of binocular inputs followed by an output nonlinearity. Our study not only proves the existence of disparity sensitive neurons in an insect brain, it also reveals feedback connections hitherto undiscovered in any animal species.