Gluing the ‘unwettable’: soil-dwelling harvestmen use viscoelastic fluids for capturing springtails

Abstract

Gluing can be a highly efficient mechanism of prey capture, as it should require less complex sensory-muscular feedback. Whereas it is well known in insects, this mechanism is much less studied in arachnids, except spiders. Soil-dwelling harvestmen (Opiliones, Nemastomatidae) bear drumstick-like glandular hairs (clavate setae) at their pedipalps, which were previously hypothesized to be sticky and used in prey capture. However, clear evidence for this was lacking to date. Using high-speed videography, we found that the harvestman Mitostoma chrysomelas was able to capture fast-moving springtails (Collembola) just by a slight touch of the pedipalp. Adhesion of single clavate setae increased proportionally with pulloff velocity, from 1 μN at 1 μm s −1 up to 7 μN at 1 mm s −1 , which corresponds to the typical weight of springtails. Stretched glue droplets exhibited characteristics of a viscoelastic fluid forming beadson-a-string morphology over time, similar to spider capture threads and the sticky tentacles of carnivorous plants. These analogies indicate that viscoelasticity is a highly efficient mechanism for prey capture, as it holds stronger the faster the struggling prey moves. Cryo-scanning electron microscopy of snap-frozen harvestmen with glued springtails revealed that the gluey secretions have a high affinity to wet the microstructured cuticle of collembolans, which was previously reported to be barely wettable for both polar and non-polar liquids. Glue droplets can be contaminated with the detached scaly setae of collembolans, which may represent a counter-adaptation against entrapment by the glue, similar to the scaly surfaces of Lepidoptera and Trichoptera (Insecta) facilitating escape from spider webs.

The evolution of pedipalps and glandular hairs as predatory devices in harvestmen (Arachnida, Opiliones)

“…Scales have independently evolved multiple times amongst springtails and may cover the whole body, including legs and furca (Zhang et al ., ). They detach easily, enabling the animal to escape when glued (Bauer & Pfeiffer, ; Wolff et al ., ). Springtail scales were frequently found on the small soil‐dwelling Caddo agilis (Caddidae; Fig.…”

“…In some cases the springtails were able to escape by shedding their scale‐like setae [see Wolff et al . () for more details, statistics, and discussion of predator‐prey interaction and counter‐adaptations of springtails]. Sabacon spp.…”

“…Scanning electron micrographs ( SEM s). A, cryo‐ SEM image of collembolan setae adhering to clavate setae of Mitostoma chrysomelas (Nemastomatidae) after touching the pedipalp with an entomobryomorph springtail (see Wolff et al ., ; for details of experimental procedure). B, scale‐like collembolan setae (arrowheads) between plumose setae, as frequently found in conserved material of Caddo agilis (Caddidae).…”

“…Scavenging, and even kleptoparasitism, has indeed been demonstrated to be part of the foraging strategy in certain harvestmen (Bristowe, ; Sabino & Gnaspini, ; Morse, ; Wijnhoven, ). However, they are also able to grasp and overcome highly mobile prey, such as collembolans, lepidopterans, hymenopterans, and dipterans, using the front legs, pedipalps, and chelicerae (Rühm, ; Frank, ; Bristowe, ; Immel, ; Phillipson, ; Gruber, ; Santos & Gnaspini, ; Wolff et al ., ).…”

“…These exhibit a complex ultrastructure that supports the secretion and retention of a glue droplet (Rimsky‐Korsakow, ; Wachmann, ). This secretion shows good wetting and viscoelastic properties and is used to capture small arthropods such as springtails (Wolff et al ., ). Dense fields of branching setae (so‐called plumose setae or ‘bottle‐brush’ setae) also occur in other dyspnoid harvestmen, such as Sabaconidae and Taracidae, and in many Eupnoi (Gruber, ; Lopez, Emerit & Rambla, ; Shear, ; Giribet et al ., ; Wijnhoven, ).…”