Drilling into solid substrates with slender beam-like structures is a mechanical challenge, but is regularly done by female parasitic wasps. The wasp inserts her ovipositor into solid substrates to deposit eggs in hosts, and even seems capable of steering the ovipositor while drilling. The ovipositor generally consists of three longitudinally connected valves that can slide along each other. Alternative valve movements have been hypothesized to be involved in ovipositor damage avoidance and steering during drilling. However, none of the hypotheses have been tested in vivo. We used 3D and 2D motion analysis to quantify the probing behavior of the fruit-fly parasitoid Diachasmimorpha longicaudata (Braconidae) at the levels of the ovipositor and its individual valves. We show that the wasps can steer and curve their ovipositors in any direction relative to their body axis. In a soft substrate, the ovipositors can be inserted without reciprocal motion of the valves. In a stiff substrate, such motions were always observed. This is in agreement with the damage avoidance hypothesis of insertion, as they presumably limit the overall net pushing force. Steering can be achieved by varying the asymmetry of the distal part of the ovipositor by protracting one valve set with respect to the other. Tip asymmetry is enhanced by curving of ventral elements in the absence of an opposing force, possibly due to pretension. Our findings deepen the knowledge of the functioning and evolution of the ovipositor in hymenopterans and may help to improve man-made steerable probes.

Hemipterans, mosquitoes, and parasitic wasps probe in a variety of substrates to find hosts for their larvae or food sources. Probes capable of sensing and precise steering enable insects to navigate through solid substrates without visual information and to reach targets that are hidden deep inside the substrate. The probes belong to non‐related taxa and originate from abdominal structures (wasps) or mouthparts (hemipterans and mosquitoes), but nevertheless share several morphological characteristics. Although the transport function clearly differs (egg laying and acquisition of liquid food), the functional demands on the mechanical behaviour of the probe within the substrate tend to be similar. The probe needs to be thin to limit substrate deformation, and long, in order to attain substantial path lengths or depths. We linked the morphology across taxa to the different functional requirements, to provide insights into the biology of probing insects and the evolution of their probes.Current knowledge of insect probes is spread over many taxa, which offers the possibility to derive general characteristics of insect probing. Buckling during initial puncturing is limited by external support mechanisms. The probe itself consist of multiple (3–6) parts capable of sliding along one another. This multi‐part construction presumably enables advancement and precise three‐dimensional steering of the probe through the substrate with very low net external pushing forces, preventing buckling during substrate penetration. From a mechanical viewpoint, a minimum of three elements is required for 3D steering and volumetric exploration, as realised in the ovipositors of wasps. More elements, such as in six‐element probes of mosquitoes, may enhance friction in soft substrates. Alternatively, additional elements can have functions other than ‘drilling’, such as saliva injection in mosquitoes.Despite the gross similarities, probes show differences in their cross sections, tip morphologies, relative lengths of their elements, and the shape of their interconnections. The hypothesis is that the probe morphology is influenced by the substrate properties, which are mostly unknown. Correlating the observed diversity to substrate‐specific functional demands is therefore currently impossible.We conclude that a multipart probe with sliding elements is highly effective for volumetric substrate probing. Shared functional demands have led to an evolutionary convergence of slender multi‐element probes in disparate insect taxa. To fully understand 3D probing, it is necessary to study the sensory and material properties, as well as the detailed kinematics and dynamics of the various probes in relation to the nature of the selective pressure originating from the species‐specific substrates. Such knowledge will deepen our understanding of probing mechanisms and may support the development of slender, bio‐inspired probes.

Parasitic wasps use specialized needle‐like structures, ovipositors, to drill into substrates to reach hidden hosts. The external ovipositor (terebra) consists of three interconnected, sliding elements (valvulae), which are moved reciprocally during insertion. This presumably reduces the required pushing force on the terebra and limits the risk of damage whilst probing. Although this is an important mechanism, it is still not completely understood how the actuation of the valvulae is achieved, and it has only been studied with the ovipositor in rest position. Additionally, very little is known about the magnitude of the forces generated during probing. We used synchrotron X‐ray microtomography to reconstruct the actuation mechanism of the parasitic wasp Diachasmimorpha longicaudata (Braconidae) in four distinct phases of the probing cycle. We show that only the paired first valvulae of the terebra move independently, while the second valvula moves with the metasoma (‘abdomen’). The first valvula movements are initiated by rotation of one chitin plate (first valvifer) with respect to another such plate (second valvifer). This is achieved indirectly by muscles connecting the non‐rotating second valvifer and the abdominal ninth tergite. Contrary to previous reports, we found muscle fibres running inside the terebra, although their function remains unclear. The estimated maximal forces that can be exerted by the first valvulae are small (protraction 1.19 mN and retraction 0.874 mN), which reduces the risk of buckling, but are sufficient for successful probing. The small net forces of the valvulae on the substrate may still lead to buckling of the terebra; we show that the sheaths surrounding the valvulae prevent this by effectively increasing the diameter and second moment of area of the terebra. Our findings improve the comprehension of hymenopteran probing mechanisms, the function of the associated muscles, and the forces and damage‐limiting mechanism that are involved in drilling a slender terebra into a substrate.

Female field crickets use phonotaxis to locate males by their calling song. Male song production and female behavioural sensitivity form a pair of matched frequency filters, which inGryllus bimaculatusare tuned to a frequency of about 4.7 kHz. Directional sensitivity is supported by an elaborate system of acoustic tracheae, which make the ears function as pressure difference receivers. As a result, phase differences between left and right sound inputs are transformed into vibration amplitude differences. Here we critically tested the hypothesis that acoustic properties of internal transmissions play a major role in tuning directional sensitivity to the calling song frequency, by measuring tympanal vibrations as a function of sound direction and frequency. Rather than sharp frequency tuning of directional sensitivity corresponding to the calling song, we found broad frequency tuning, with optima shifted to higher frequencies. These findings agree with predictions from a vector summation model for combining external and internal sounds. We show that the model provides robust directional sensitivity that is, however, broadly tuned with an optimum well above the calling song frequency. We therefore advocate that additional filtering, e.g. at a higher (neuronal) level, significantly contributes to frequency tuning of directional sensitivity.

Many parasitic wasps use slender and steerable ovipositors to lay eggs in hosts hidden in substrates, but it is currently unknown how steering is achieved. The ovipositors generally consist of three longitudinally connected elements, one dorsal and two ventral valves that can slide along each other. For the parasitic wasp Diachasmimorpha longicaudata, it has been shown that protraction of the ventral valves causes incurving of the ventral valves towards the dorsal one, which results in a change in probing direction. We hypothesise that this shape change is due to differences in bending stiffness along the ovipositor. Alignment of the stiff tip of the dorsal valve with a more flexible ventral S-shaped region situated just behind the tip straightens this S-bend and results in upwards rotation of the ventral tip. We show that the S-shaped region of the ventral valves has a low bending stiffness because it contains soft materials such as resilin. In contrast, the large cross-sectional area of the dorsal valve tip area probably results in a high bending stiffness. Elsewhere, the dorsal valve is less stiff than the ventral valves. Our results support the hypothesis that the interaction between the stiff dorsal valve portion and the more flexible S-shaped region co-determine the configurational tip changes required for steering the ovipositor in any desired direction along curved paths in the substrate. This provides novel insights in the understanding of steering mechanisms of the hymenopteran ovipositor, and for the application in man-made probes.

Many insects can climb on smooth inverted substrates using adhesive hairy pads on their legs. The hair–surface contact is often mediated by minute volumes of liquid, which form capillary bridges in the contact zones and aid in adhesion. The liquid transport to the contact zones is poorly understood. We investigated the dynamics of liquid secretion in the dock beetleGastrophysa viridulaby quantifying the volume of the deposited liquid footprints during simulated walking experiments. The footprint volume increased with pad–surface contact time and was independent of the non-contact time. Furthermore, the footprint volume decreased to zero after reaching a threshold cumulative volume (approx. 30 fl) in successive steps. This suggests a limited reservoir with low liquid influx. We modelled our results as a fluidic resistive system and estimated the hydraulic resistance of a single attachment hair of the order of MPa · s/fl. The liquid secretion in beetle hairy pads is dominated by passive suction of the liquid during the contact phase. The high calculated resistance of the secretion pathway may originate from the nanosized channels in the hair cuticle. Such nanochannels presumably mediate the transport of cuticular lipids, which are chemically similar to the adhesive liquid.