Functional principles of steerable multi‐element probes in insects

• Published in: Biological reviews of the Cambridge Philosophical Society 2019-04, Vol.94 (2), p.555-574
• Main Authors: Cerkvenik, Uroš, Dodou, Dimitra, van Leeuwen, Johan L., Gussekloo, Sander W. S.
• Format: Article
• Language: English
• Subjects: Aquatic insects; Biological evolution; Buckling; buckling avoidance; Culicidae; Deformation mechanisms; Drilling; Egg laying; Exploration; Food; Food sources; hemipterans; Insects; Kinematics; Larvae; Material properties; Mechanical properties; Morphology; Mosquitoes; Mouthparts; multi-element probes; Navigation behavior; Original; parasitic wasps; Physical characteristics; Piercing; Probes; Saliva; Sliding; spatial probing; Steering; Substrates; Taxa
• ISSN: 1464-7931; 1469-185X
• DOI: 10.1111/brv.12467

ABSTRACT 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 slen