Roles of muscle activities in foreleg movements during predatory strike of the mantis.

Foreleg trajectory in the mantis strike varies depending on prey distance. To examine how muscle activities affect foreleg trajectory, we recorded strike behaviours of the Chinese mantis with a high-speed camera and electromyograms of the foreleg trochanteral extensor and flexor. At the approach phase of the mantis strike, the prothorax-coxa (P-C) joint elevated and the femur-tibia (F-T) joint extended. At the sweep phase, the coxa-trochanter (C-T) joint rapidly extended, then, the F-T joint rapidly flexed to capture the prey. At capture initiation, the C-T joint extended more with greater prey distance. After cutting the tendon of the trochanteral flexor, the C-T joint extended similarly to that of the intact foreleg but did not flex after it reached its peak angle. After cutting the tendon of the trochanteral extensor, the C-T joint did not extend as much as that of the intact foreleg. During rapid extension of the C-T joint, a burst of spikes from the coxal trochanteral extensor was observed in electromyograms. Among several parameters, burst duration was the best predictor of C-T joint angular change during strike. Unexpectedly, trochanteral flexor activity was also observed during rapid extension of the C-T joint. These results indicated that the coxal trochanteral extensor mainly contributed to the rapid C-T extension during strike, but other muscles also contributed at the beginning of extension. The trochanteral flexor appeared to contribute to C-T flexion by countering the rapid extension.

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.

Three-dimensional atlas of thoracic ganglia in the praying mantis, Tenodera aridifolia.

The praying mantis is a good model for the study of motor control, especially for investigating the transformation from sensory signals into motor commands. In insects, thoracic ganglia (TG) play an important role in motor control. To understand the functional organization of TG, an atlas is useful. However, except for the fruitfly, no three-dimensional atlas of TG has not been reported for insects. In this study, we generated a three-dimensional atlas of prothoracic, mesothoracic, and metathoracic ganglia in the praying mantis (Tenodera aridifolia). First, we observed serial sections of the prothoracic ganglion stained with hematoxylin and eosin to identify longitudinal tracts and transverse commissures. We then visualized neuropil areas by immunostaining whole-mount TG with an anti-synapsin antibody. Before labeling each neuropil area, standardization using the iterative shape averaging method was applied to images to make neuropil contours distinct. Neuropil areas in TG were defined based on their shape and relative position to tracts and commissures. Finally, a three-dimensional atlas was reconstructed from standardized images of the TG. The standard TG are available at the Comparative Neuroscience Platform website (cns.neuroinf.jp/modules/xoonips/detail.php?item_id=11946) and can be used as a common reference map to combine the anatomical data obtained from different individuals.

Unraveling the functional organization of lobula complex in the mantis brain by identification of visual interneurons.

The praying mantis shows broad repertories of visually guided behaviors such as prey recognition and defense against collision. It is likely that neurons in the lobula complex (LOX), the third visual neuropil in the optic lobe, play significant roles in these behaviors. The LOX in the mantis brain consists of five neuropils: outer lobes 1 and 2 (OLO1 and OLO2); anterior lobe (ALO); dorsal lobe (DLO); and stalk lobe (SLO), and ALO comprise ventral and dorsal subunits, ALO-V and ALO-D. To understand the functional organization of LOX, intracellular electrodes were used for recording from and staining neurons in these neuropils of the mantis (Tenodera aridifolia). The neurons belonged to three categories based on their response properties and morphologies. First, tangential ALO-V neurons projecting to ventromedial neuropils (VMNP) (TAproM1 and 2), tangential DLO (or ALO-D) neurons projecting to VMNP (TDproM1 and 2), and tangential ALO-V centrifugal neurons (TAcen) all showed directional sensitivity and sustained excitation to gratings drifting in preferred direction (outward-downward, inward-upward, outward-upward, inward-downward, and inward, respectively). Second, tangential OLO neurons projecting to VMNP or ventrolateral neuropils (VLNP) (TOproM or TOproL), columnar OLO commissural neurons (COcom), and SLO commissural neurons (Scom) all showed strong excitation to 2°-8° moving squares but little excitations to drifting gratings. COcom and SLO neurons ramified in both left and right LOX. Last, the class of tangential ALO-V neurons projecting to VLNP (TAproL1, 2, and 3) responded best to looming circles and showed little excitation to receding, darkening, and lightening circles.

Aversive Learning in the Praying Mantis (Tenodera aridifolia), a Sit and Wait Predator.

Animals learn to associate sensory cues with the palatability of food in order to avoid bitterness in food (a common sign of toxicity). Associations are important for active foraging predators to avoid unpalatable prey and to invest energy in searching for palatable prey only. However, it has been suggested that sit-and-wait predators might rely on the opportunity that palatable prey approach them by chance: the most efficient strategy could be to catch every available prey and then decide whether to ingest them or not. In the present study, we investigated avoidance learning in a sit-and-wait predator, the praying mantis (Tenodera aridifolia). To examine the effects of conspicuousness and novelty of prey on avoidance learning, we used three different prey species: mealworms (novel prey), honeybees (novel prey with conspicuous signals) and crickets (familiar prey). We sequentially presented the prey species in pairs and made one of them artificially bitter. In the absence of bitterness, the mantises consumed bees and crickets more frequently than mealworms. When the prey were made bitter, the mantises still continued to attack bitter crickets as expected. However, they reduced their attacks on bitter mealworms more than on bitter bees. This contrasts with the fact that conspicuous signals (e.g. coloration in bees) facilitate avoidance learning in active foraging predators. Surprisingly, we found that the bitter bees were totally rejected after an attack whereas bitter mealworms were partially eaten (~35%). Our results highlight the fact that the mantises might maintain a selection pressure on bees, and perhaps on aposematic species in general.

Head Movements During Visual Orienting Toward Moving Prey in the Lizard Takydromus tachydromoides.

It is important to investigate visual orienting in reptiles to better understand the basic organization of the oculomotor system in vertebrates. However, quantitative analyses of visual orienting behavior in reptiles have rarely been conducted, except in chameleons. In the present study, we videorecorded the head and body movements of the lizard Takydromus tachydromoides during visual tracking of moving prey and analyzed them frame-by-frame. Before approaching prey, visual tracking mainly consisted of brief intermittent turns of the head (saccade). After the head saccades, the angular position of the prey relative to the lizard head was kept at 10-70° (laterally) in most cases, rather than at 0° (in front). In addition, the ratio of the amplitude of the head saccades to prey position was 0.2-0.3, which is much smaller than 1, suggesting that the head did not orient exactly toward the prey after most saccades. These results were observed under both white (homogeneous) and grating (structured) backgrounds. Possible functions of head saccades in the lizard are discussed.

Organization of the antennal lobes in the praying mantis (Tenodera aridifolia).

Olfaction in insects plays pivotal roles in searching for food and/or for sexual partners. Although many studies have focused on the olfactory processes of nonpredatory insect species, little is known about those in predatory insects. Here, we investigated the anatomical features of the primary olfactory center (antennal lobes) in an insect predator whose visual system is well developed, the praying mantis Tenodera aridifolia. Both sexes of T. aridifolia were found to possess 54 glomeruli, and each glomerulus was identified based on its location and size. Moreover, we found a sexual dimorphism in three glomeruli (macroglomeruli) located at the entrance of the antennal nerves, which are 15 times bigger in males than their homologs in females. We additionally deduced the target glomeruli of olfactory sensory neurons housed in cognate types of sensilla by degenerating the sensory afferents. The macroglomeruli received sensory inputs from grooved peg sensilla, which are present in a large number at the proximal part of the males' antennae. Furthermore, our findings suggest that glomeruli at the posteriodorsal part of the antennal lobes receive sensory information from putative hygro- and thermosensitive sensilla. The origins of projections connected to the protocerebrum are also discussed. J. Comp. Neurol. 525:1685-1706, 2017. © 2016 Wiley Periodicals, Inc.

Behavioural interactions between the lizard Takydromus tachydromoides and the praying mantis Tenodera aridifolia suggest reciprocal predation between them.

The Japanese lacertid lizard Takydromus tachydromoides and the praying mantis Tenodera aridifolia are sympatric generalist predators feeding on similar prey. To confirm reciprocal predation between them, we observed the behavioural interactions between the lizards and the mantises of different sizes in a laboratory condition. The lizards caught small mantises (from first to fifth instars), but sometimes escaped from large mantises (from sixth instar to adult). Large mantises occasionally showed catch responses to the lizards. The lizards sometimes caught the mantis without a tongue-flick response (sampling of chemical cues), and they sometimes did not catch the small mantises showing immobile or cryptic responses that prevent visual detection. These results suggested the primary role of vision on recognition of the mantis as a prey. The lizards spent a longer time to approach larger mantises. The time from orienting to catch was longer when the lizards showed tongue-flick responses. The lizard also spent a longer time before deciding to escape from the mantis than to catch it. Biological significance of these differences in timing was discussed.

Antennal development in the praying mantis (Tenodera aridifolia) highlights multitudinous processes in hemimetabolous insect species.

Insects possess antennae equipped with a large number of segments (flagellomeres) on which sensory organs (sensilla) are located. Hemimetabolous insects grow by molting until they reach adulthood. In these species, the sensory structures develop and mature during each stage of development; new flagellomeres are generated at each molt elongating the antennae, and new sensilla appear. The praying mantis (Tenodera aridifolia) is a hemimetabolous insect with 7 different instars before it reaches adulthood. Because their antennae are provided with an atypical sensillar distribution, we previously suggested that their antennae develop with a different mechanism to other hemimetaboulous insect species. In the present study, we measured the number, length and width of flagellomeres along the antennae in nymph and adult mantis Tenodera aridifolia. For this study, we developed a new and innovative methodology to reconstruct the antennal development based on the length of flagellomeres. We observed and confirmed that the antennae of mantises develop with the addition of new segments at two distinct sites. In addition, we constructed a complete database of the features of the flagellum for each stage of development. From our data, we found that sexual dimorphism appears from the 6 instar (larger number and wider flagellomeres in males) in accordance with the appearance of their genital apparatus. The antennal sexual dimorphism completes at adulthood with longer flagellomeres and the emergence of a huge number of grooved peg sensilla in males during the last molting, which suggests once again their function as sex-pheromone receptive sensilla.

Role of a looming-sensitive neuron in triggering the defense behavior of the praying mantis Tenodera aridifolia.

In responses to looming objects, the praying mantis shows a defense behavior, which consists of retracting forelegs under the prothorax. The role of a looming-sensitive neuron in triggering this behavior was investigated by simultaneously recording the activity and behavioral responses of the neuron. The mantis initiated the defense behavior earlier in response to larger and slower looming stimuli. The time remaining to collision at defense initiation was linearly correlated with the ratio of the half-size of an approaching object to its speed (l/|v|), suggesting that the defense behavior occurred a fixed delay after the stimuli had reached a fixed angular threshold. Furthermore, the results suggested that high-frequency spikes of the looming-sensitive neuron were involved in triggering the defense behavior: the distribution of maximum firing rate for trials with defense was shifted to larger rates compared with trials without defense; the firing rate of the neuron exceeded 150 Hz ∼100 ms before the defense initiation regardless of stimulus parameters; when a looming stimulus ceased approach prematurely, high-frequency spikes were removed, and the occurrence of defense was reduced.

The antennal sensilla of the praying mantis Tenodera aridifolia: a new flagellar partition based on the antennal macro-, micro- and ultrastructures.

In insects, the antenna consists of a scapus, a pedicellus, and a flagellum comprising many segments (flagellomeres). These segments possess many morphological types of sensory organs (sensilla) to process multimodal sensory information. We observed the sensilla on flagellomeres in praying mantis (Tenodera aridifolia) with both scanning and transmission electron microscopes. We classified the sensilla into six types: chaetic, campaniform, coelocapitular, basiconic, trichoid and grooved peg sensilla, and inferred their presumptive functions on the basis of their external and internal structures. In addition, based on their distribution, we newly divided the flagellum into 6 distinct parts. This new division leads to a better understanding about the sexual dimorphism and the antennal development in the mantises. The sexual difference in distribution of the grooved peg sensilla suggests that this type of sensilla may play a role in sex-pheromone detection in mantis, which is a rare case of double-walled sensilla mediating this function.

Antennal pointing at a looming object in the cricket Acheta domesticus.

Antennal pointing responses to approaching objects were observed in the house cricket Acheta domesticus. In response to a ball approaching from the lateral side, crickets oriented the antenna ipsilateral to the ball towards it. In response to a ball approaching from the front, crickets oriented both antennae forward. Response rates of antennal pointing were higher when the ball was approaching from the front than from behind. The antennal angle ipsilateral to the approaching ball was positively correlated with approaching angle of the ball. Obstructing the cricket's sight decreased the response rate of antennal pointing, suggesting that this response was elicited mainly by visual stimuli. Although the response rates of antennal pointing decreased when the object ceased its approach at a great distance from the cricket, antennal pointing appeared to be resistant to habituation and was not substantially affected by the velocity, size and trajectory of an approaching ball. When presented with computer-generated visual stimuli, crickets frequently showed the antennal pointing response to a darkening stimulus as well as looming and linearly-expanding stimuli. Drifting gratings rarely elicited the antennal pointing. These results suggest that luminance change is sufficient to elicit antennal pointing.

Defensive abdominal rotation patterns of tenebrionid beetle, Zophobas atratus, pupae.

Exarate pupae of the beetle Zophobas atratus Fab. (Coleoptera: Tenebrionidae) have free appendages (antenna, palp, leg, and elytron) that are highly sensitive to mechanical stimulation. A weak tactile stimulus applied to any appendage initiated a rapid rotation of abdominal segments. High-speed photography revealed that one cycle of defensive abdominal rotation was induced in an all-or-none fashion by bending single or multiple mechanosensory hairs on a leg or prodding the cuticular surface of appendages containing campaniform sensilla. The direction of the abdominal rotation completely depended on the side of stimulation; stimulation of a right appendage induced a right-handed rotation about the anterior-posterior axis of the pupal body and vice versa. The trajectories of the abdominal rotations had an ellipsoidal or pear-shaped pattern. Among the trajectory patterns of the rotations induced by stimulating different appendages, there were occasional significant differences in the horizontal (right-left) component of abdominal rotational movements. Simultaneous stimulation of right and left appendages often induced variable and complex patterns of abdominal movements, suggesting an interaction between sensory signals from different sides. When an abdominal rotation was induced in a freely lying pupa, the rotation usually made the pupa move away from or turn its dorsum toward the source of stimulation with the aid of the caudal processes (urogomphi), which served as a fulcrum for transmitting the power of the abdominal rotation to the movement or turning of the whole body. Pattern generation mechanisms for the abdominal rotation were discussed.

Defensive gin-trap closure response of tenebrionid beetle, Zophobas atratus, pupae.

Pupae of the beetle Zophobas atratus Fab. (Coleoptera: Tenebrionidae) have jaws called gin traps on the lateral margin of their jointed abdominal segments. When a weak tactile stimulation was applied to the intersegmental region between the two jaws of a gin trap in a resting pupa, the pupa rapidly closed and reopened single or multiple gin traps adjacent to the stimulated trap for 100200 ms. In response to a strong stimulation, a small or large rotation of the abdominal segments occurred after the rapid closure of the traps. Analyses of trajectory patterns of the last abdominal segment during the rotations revealed that the rotational responses were graded and highly variable with respect to the amplitudes of their horizontal and vertical components. The high variability of these rotational responses is in contrast with the low variability (or constancy) of abdominal rotations induced by the tactile stimulation of cephalic and thoracic appendages. Since the closed state of the gin traps lasts only for a fraction of a second, the response may mainly function to deliver a "painful" stimulus to an attacker rather than to cause serious damage.

Defence behaviours of the praying mantis Tenodera aridifolia in response to looming objects.

Defence responses to approaching objects were observed in the mantis Tenodera aridifolia. The mantis showed three kinds of behaviour, fixation, evasion and cryptic reaction. The cryptic reaction consisted of rapid retraction of the forelegs under the prothorax or rapid extending of the forelegs in the forward direction. Obstructing the mantis' sight decreased its response rates, suggesting that the visual stimuli generated by an approaching object elicited the cryptic reaction. The response rate of the cryptic reactions was highest for objects that approached on a direct collision course. Deviation in a horizontal direction from the direct collision course resulted in a reduced response. The response rate of the cryptic reaction increased as the approaching velocity of the object increased, and the rate decreased as the object ceased its approach at a greater distance from the mantis. These results suggest that the function of the observed cryptic reactions is defence against impending collisions. The possible role of the looming-sensitive neuron in the cryptic reaction is also discussed.

Coordinated movements of the head and body during orienting behaviour in the praying mantis Tenodera aridifolia.

The visual orienting behaviour towards prey in the free-moving mantis was investigated with a high-speed camera. The orienting behaviour consisted of head, prothorax, and abdomen rotations. Coordinated movements of these body parts in the horizontal plane were analysed frame-by-frame. Rotations of these body parts were initiated with no or slight (≤40 ms) differences in timing. The initiation timing of prothorax-abdomen rotation was affected by its initial angle before the onset of orienting. There were positive correlations in amplitude among head-prothorax, prothorax-abdomen, and abdomen rotations. The ratio of these rotations to total gaze rotation was affected by the initial prothorax-abdomen angle before the onset of orienting. Our data suggest that coordinated movements of the head, prothorax, and abdomen during orienting are ballistic events and are pre-determined according to visual and proprioceptive information before the onset of orienting.

A descending contralateral directionally selective movement detector in the praying mantis Tenodera aridifolia.

Extracellular recordings were made from a directionally selective neuron in the ventral nerve cord of mantises. The neuron's preferred direction of motion was forward and upward over the compound eye contralateral to its axon at the cervical connective. The neuron was sensitive to wide-field motion stimuli, resistant to habituation, and showed transient excitation in response to light ON and OFF stimuli. Its responses to drifting gratings depended on the temporal frequency and contrast of the stimulus. These results suggest that the neuron receives input from correlation-type motion detectors.

Responses of descending neurons to looming stimuli in the praying mantis Tenodera aridifolia.

Responses to visual stimuli of some neurons that descend the nerve cord from the brain were recorded extracellularly in the mantis Tenodera aridifolia. Most of the recorded neurons showed their largest responses to looming stimuli that simulated a black circle approaching towards the mantis. The neurons showed a transient excitatory response to a gradually darkening or receding circle. The neurons showed sustained excitation to the linearly expanding stimuli, but the spike frequency decreased rapidly. The responses of the neurons were affected by both the diameter and the speed of looming stimuli. Faster or smaller looming stimuli elicited a higher peak frequency. These responses were observed in both recordings from the connective between suboesophageal and prothoracic ganglia and the connective between prothoracic and mesothoracic ganglia. There was a one-to-one correspondence of spike firing between these two recordings with a fixed delay. The neurons had the receptive field on ipsilateral side to its axon at the cervical connective. These results suggest that there is a looming-sensitive descending neuron, with an axon projecting over prothoracic ganglion, in the mantis nervous system.

Preparing for escape: an examination of the role of the DCMD neuron in locust escape jumps.

Many animals begin to escape by moving away from a threat the instant it is detected. However, the escape jumps of locusts take several hundred milliseconds to produce and the locust must therefore be prepared for escape before the jumping movement can be triggered. In this study we investigate a locust's preparations to escape a looming stimulus and concurrent spiking activity in its pair of uniquely identifiable looming-detector neurons (the descending contralateral movement detectors; DCMDs). We find that hindleg flexion in preparation for a jump occurs at the same time as high frequency DCMD spikes. However, spikes in a DCMD are not necessary for triggering hindleg flexion, since this hindleg flexion still occurs when the connective containing a DCMD axon is severed or in response to stimuli that cause no high frequency DCMD spikes. Such severing of the connective containing a DCMD axon does, however, increase the variability in flexion timing. We therefore propose that the DCMD contributes to hindleg flexion in preparation for an escape jump, but that its activity affects only flexion timing and is not necessary for the occurrence of hindleg flexion.

Investigating saccade programming in the praying mantis Tenodera aridifolia using distracter interference paradigms.

To investigate the saccadic system in the mantis, I applied distracter interference paradigms. These involved presenting the mantis with a fixation target and one or several distracters supposed to affect saccades towards the target. When a single target was presented, a medium-sized target located in its lower visual field elicited higher rates of saccade response. This preference for target size and position was also observed when a target and a distracter were presented simultaneously. That is, the mantis chose and fixated the target rather than a distracter that was much smaller or larger than the target, or was located above the target. Furthermore, the mantis' preference was not affected by increasing the number of distracters. However, the presence of the distracter decreased the occurrence rate of saccade and increased the response time to saccade. I conclude that distracter interference paradigms are an effective way of investigating the visual processing underlying saccade generation in the mantis. Possible mechanisms of saccade generation in the mantis are discussed.