Morphology of powerful suction organs from blepharicerid larvae living in raging torrents

Abstract

Background Suction organs provide powerful yet dynamic attachments for many aquatic animals, including octopus, squid, remora, and clingfish. While the functional morphology of suction organs from some cephalopods and fishes has been investigated in detail, there are only few studies on such attachment devices in insects. Here we characterise the morphology and ultrastructure of the suction attachment organs of net-winged midge larvae (genus Liponeura; Diptera: Blephariceridae) – aquatic insects that live on rocks in rapid alpine waterways where flow speeds can reach 3 m s− 1 – using scanning electron microscopy, confocal laser scanning microscopy, and X-ray computed micro-tomography (micro-CT). Furthermore, we study the function of these organs in vivo using interference reflection microscopy. Results We identified structural adaptations important for the function of the suction attachment organs in L. cinerascens and L. cordata. First, a dense array of spine-like microtrichia covering each suction disc comes into contact with the substrate upon attachment, analogous to hairy structures on suction organs from octopus, clingfish, and remora fish. These spine-like microtrichia may contribute to the seal and provide increased shear force resistance in high-drag environments. Second, specialised rim microtrichia at the suction disc periphery were found to form a continuous ring in close contact and may serve as a seal on a variety of surfaces. Third, a V-shaped cut on the suction disc (“V-notch“) is actively opened via two cuticular apodemes inserting on its flanks. The apodemes are attached to dedicated V-notch opening muscles, thereby providing a unique detachment mechanism. The complex cuticular design of the suction organs, along with specialised muscles that attach to them, allows blepharicerid larvae to generate powerful attachments which can withstand strong hydrodynamic forces and quickly detach for locomotion. Conclusion The suction organs from Liponeura are underwater attachment devices specialised for resisting extremely fast flows. Structural adaptations from these suction organs could translate into future bioinspired attachment systems that perform well on a wide range of surfaces.

Evolutionary optimization of an anatomical suction cup: Lip collagen content and its correlation with flow and substrate in Neotropical suckermouth catfishes (Loricarioidei)

“…Opening and closing of these channels is controlled via manipulation of the maxilla itself, to which the maxillary barbel is attached, with the barbel being integrated into the oral disk (Geerinckx, Brunain, et al, 2007). A similar channel‐like structure was recently described in the suction cups of blepharicerid fly larvae (Kang, Johnston, van de Kamp, Faragó, & Federle, 2019), suggesting such channels make an important contribution to the optimal performance of anatomical suction cups more generally. Additional comparative studies would help identify how these structures are optimized for performance in the widely divergent habitats occupied by various evolutionary lineages.…”

Extreme suction attachment performance from specialised insects living in mountain streams (Diptera: Blephariceridae)

“…The ventral disc surface of H. lugubris is covered in a dense array of microtrichia (Figures 1c & 3). The suction disc sealing rim, which seals the disc for suction attachment, closely resembles that of L. cinerascens [10] and comprises a dense array of upright rim microtrichia ( Figure 1c). This is different to L. cordata, which has a distinct rim made up of a single row of flat rim microtrichia [10].…”

“…The suction disc contacts the surface for attachment, and the piston and underlying piston muscles (Figure 1c & d) actively lower the pressure inside the suction chamber. Two apodemes attaching to the V-notch in H. lugubris mediate its muscle-controlled opening for rapid detachment of the suction organ ( Figure 1e; see also [10]).…”

“…Using its suction organs, the larva can locomote relatively quickly and possibly over long distances: blepharicerid larvae migrate from one stone to another to find the swiftest regions of the stream [5,6]. Once development is complete, the winged adult emerges from its pupa, floats to the water surface, and immediately flies away to mate and lay eggs to begin the cycle anew [7,8] The remarkable morphology of blepharicerid suction organs is well-described [6,[9][10][11]. The organ superficially resembles a synthetic piston-pump, with a suction disc that interacts with the surface and creates a seal, a central piston and powerful piston muscles to manipulate the pressure, and a suction chamber with a thick cuticular wall to withstand low pressures during attachments.…”

“…There are spinelike microstructures called microtrichia on the suction disc that contact glass surfaces and may increase resistance to shear forces. In addition, a dedicated detachment system allows the larva to rapidly detach its suction organ during locomotion [10].…”