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Evolution of hyperflexible joints in sticky prey capture appendages of harvestmen (Arachnida, )

Article in Organisms Diversity & Evolution · April 2016 Impact Factor: 2.89 · DOI: 10.1007/s13127-016-0278-2

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Jonas O. Wolff Jochen Martens Macquarie University Johannes Gutenberg-Universität Mainz

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Axel Schönhofer Stanislav Gorb Johannes Gutenberg-Universität Mainz Christian-Albrechts-Universität zu Kiel

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ORIGINAL ARTICLE

Evolution of hyperflexible joints in sticky prey capture appendages of harvestmen (Arachnida, Opiliones)

Jonas O. Wolff1 & Jochen Martens2 & Axel L. Schönhofer2 & Stanislav N. Gorb1

Received: 23 October 2015 /Accepted: 27 March 2016 # Gesellschaft für Biologische Systematik 2016

Abstract The rigid leg segments of are flexibly efficiency of the pedipalp as a means of prey capture, because connected by joints, which usually consist of two ball-and- in springtails detachable scales limit the action of the sticky bowl hinges, permitting a uniaxial pivoting up to 140°. secretion of pedipalpal setae. Here, we report the occurrence of hyperflexible joints (range of movements = 160–200°) in the pedipalps (second pair of Keywords Prey capture . Adhesion . Predator-prey appendages) of some harvestmen ( and interaction . Biomechanics . Torsion . Kinematics . ), representing some of the most flexible leg Arachnida . Soil communities joints among arthropods. Hyperflexion is achieved by a reduc- tion of hinges and a strong constriction of the joint region. We demonstrate that hyperflexion occurs during prey capture and Introduction is used to clamp appendages of the prey, in addition to attach- ment by glue secreted by specialized setae. By means of high- The coevolution of predator and prey frequently leads to an speed video recordings, we found that in the Sabaconidae the increase in speed and efficacy of means of prey capture or tibiotarsal joint of the pedipalp can flex extremely rapidly defense (Dawkins and Krebs 1979;Vermeij1994;Abrams (<5 ms), limiting prey escape. This is the fastest reported 2000). In predators, there are numerous exam- predatory strike in and caused both by leverage ples of limb modifications that enhance the ability to over- and a click mechanism. By comparative analysis of different whelm and/or secure prey, including raptorial clamps (e.g., related taxa, we retraced joint evolution and found that mantids and amblypygids) (Ass 1973;Weygoldt2000), hyperflexion has independently evolved in Sabaconidae and capture baskets (e.g., dragonflies and asilids) (Gorb Nemastomatidae, with totally different joint kinematics. We 1999), sticky pads (e.g., solifuges) (Willemart et al. hypothesize that (rapid) hyperflexion evolved to enhance the 2011), snap-traps (trap-jaw ants) (Gronenberg et al. 1993), harpoons (mantis shrimps) (Murphy and Patek 2012), smashing clubs (mantis shrimps) (Patek and Electronic supplementary material The online version of this article Caldwell 2005), or even hydraulic pistols (snapping (doi:10.1007/s13127-016-0278-2) contains supplementary material, shrimps) (Versluis et al. 2000). The fastest movements which is available to authorized users. are enabled by a click mechanism, in which a high amount of energy is accumulated by the elastic deformation of a * Jonas O. Wolff [email protected] cuticular structure, which is suddenly released by a de- arresting or buckling mechanism. Such mechanisms have evolved both in predators like trap-jaw ants, which close 1 Functional Morphology and Biomechanics, Zoological Institute, Kiel their mandibles in less than 1 millisecond (Gronenberg University, Am Botanischen Garten 9, D-24118 Kiel, Germany et al. 1993), and in arthropods that are frequent targets of 2 Department of Evolutionary Biology, Institute of Zoology, Johannes predation, like springtails (Collembola) being capable of Gutenberg University Mainz, Joh.-von-Müller-Weg 6, catapulting rescue jumps with a take-off speed of 1.4 m/s D-55128 Mainz, Germany (Christian 1978). Springtails are, besides mites, a J.O. Wolff et al. ubiquitous and dominant part of soil arthropod communi- Material and methods ties and an important food source for arthropod predators (Hopkin 1997). Their catapult mechanism has been hy- Anatomical studies and phylogenetic analysis pothesized to be a result of an evolutionary Barms race^ between them and their predators (Hopkin 1997). For ex- Material ample, some ground beetles have evolved an antennal cap- ture basket that closes faster than the springtail can take off For anatomical studies, we used conserved material held in the (Bauer and Völlenkle 1976; Bauer 1982; Hintzpeter and private collections of the authors (f (females), m (males), juv Bauer 1986). However, speed is not only determined by (juveniles)): Caddidae: Caddo agilis BANKS 1892, Macon Co., the mechanism of movement generation, but also the time NC, USA, 2012, f, m; Acropsopilionidae: Acropsopilio of reaction, dependent on neuronal signal transmission. neozealandiae FORSTER 1948, South-Island, New Zealand, Thus, another predatory trick is the usage of sticky secre- 1990, f; Ischyropsalididae: Ischyropsalis luteipes SIMON tions, since these act directly on the prey without the ne- 1872, Cataluña, , 2009, f, m, juv; Taracidae: cessity of a sensory feedback (Betz and Kölsch 2004). Hesperonemastoma modestum BANKS 1894, CA, USA, Viscid glue can be found in springtail hunting rove beetles 2011, f, m, juv; Sabaconidae: Sabacon simoni DRESCO 1952, (Bauer and Pfeiffer 1991; Schomann et al. 2008), mites Alpes-Maritimes, France, 2008, f, m, juv; : (Alberti 1973, 2010), harvestmen (Wolff et al. 2014, Dicranolasma pauper DAHL 1903, Trentino-Alto, , 2014, 2016), and carnivorous plants (Verbeek and Boasson f, juv; Nemastomatidae: HERMANN 1993). However, the efficacy of glue is decreased by de- 1804, Mainz, Germany, 2014, f, m. tachable scales that help the springtail freeing from the glue trap (Bauer and Pfeiffer 1991; Wolff et al. 2014). Such scales evolved multiple times among springtails, in- Light microscopy (LM) dicating their role in defense from glue-using predators (Zhang et al. 2014). Light microscopical images of and their pedipalps In a previous study, we observed that the harvestman were made with a multifocus stereo microscope (Leica Mitostoma chrysomelas (Nemastomatidae) uses two M205 A, Leica Microsystems GmbH, Wetzlar, Germany) counter-strategies to reduce prey loss (Wolff et al. 2014). (1) equipped with a camera (Leica DFC420). The patello-tibial It stretches its legs to prevent ground contact and therefore joint and the tibiotarsal joint were studied in detail using dif- generation of opposing forces by the prey. (2) It highly flexes ferent illumination techniques. To understand the kinematics its tarsus against the tibia and thereby occasionally clamps of the joints, different specimens were studied that had their appendages of the prey in between. The latter must be based tibia and/or tarsus in a differently retracted/expanded state. on a more complex modification of the tibiotarsal joint, since arthropod leg joints usually do not exceed a range of motion (ROM) higher than 140° (extremes e.g., 120° in the femur- Scanning electron microscopy (SEM) patellar joint of spider walking legs (Parry and Brown 1959); 140° in the tibiotarsal joint in the raptorial legs of mantids Pedipalps were removed using fine forceps and dehydrated in (Corrette 1990)). In order to retrace the evolution of a series of increasing ethanol concentrations (80, 90, 100 and hyperflexibility (ROM > 160°), we comparatively studied 100 % on a molecular sieve), followed by critical point dry- the functional joint morphology in different representatives ing. Samples were glued on stubs using a carbon-rich double- of related harvestmen families, all of which are ground- sided adhesive tape. In some samples, the patella, tibia, and dwellers. The pedipalps of the monogeneric family tarsus were slightly pulled apart to uncover joint structures. Sabaconidae were of particular interest, since previous au- Specimens were sputter-coated with 10 nm Au-Pd and stud- thors remarked that the tarsus can be highly flexed against ied with a Hitachi S 4800 scanning electron microscope the tibia (Simon 1879; Shear 1975; Juberthie et al. 1981). In (Hitachi Ltd., Tokyo, ) at an acceleration voltage of fixative-preserved specimens of Sabaconidae, we often found 3.0 kV. the tibia and tarsus bent and twisted in an unusual manner. Glue secreting setae of M. chrysomelas before and after Previous authors wondered about the function of the uniquely being in contact with springtail cuticle were visualized by shaped pedipalps and setae in this family, but never observed Cryo-SEM. For that purpose, fresh specimens were attached their use during prey capture (Shear 1975, 1986;Juberthie to a sample holder using Tissue-Tek® compound, shock fro- et al. 1981). To reveal biological and mechanical functions zen in liquid nitrogen, directly sputtered with 10 nm Au-Pd of hyperflexible pedipalps, we studied the prey capture be- using the Gatan ALTO-2500 cryo system (Gatan Inc., havior of M. chrysomelas and Sabacon simoni by means of Abingdon, UK), and viewed in the SEM with the stage cooled high-speed video recordings. up to −120 °C (for details see Wolff et al. 2014). Evolution of hyperflexible joints in sticky prey capture appendages of harvestmen (Arachnida, Opiliones)

Microcomputed tomography (μCT) with dental wax (Polyvinylsiloxane) containing humid fil- ter paper and different species and sizes of living collem- Further anatomical observations on the distal pedipalp were bolans collected on the campus of Kiel University. Prey made on female S. simoni, by means of μCT. We used two capture events were filmed with a high-speed video cam- different specimens of which one had the tarsus in an extended era (Fastcam SA 1.1, Photron Inc., San Diego, CA, USA), and one in a flexed condition. Specimens were initially stored in equipped with a macro lens, and using frame rates of 70 % ethanol and dehydrated in a series of increasing ethanol 500–1000 fps. To obtain such frame rates at sufficient concentrations and critical-point dried. Dried samples were magnification, an additional light source (Storz Techno glued onto plastic pipette tips with cyanacrylate glue and Light 217, Karl Storz GmbH & Co. KG, Tuttlingen, scanned with a SkyScan 1172 HR micro-CT (Bruker microCT, Germany) was applied for illumination of the scenes. Kontich, Belgium) with an acceleration voltage of 40 kV and a voxel size of 1 μm. 3D images were reconstructed using the NRecon 1.6.6 software and processed with Amira 6.0.0. Results

Reconstruction of joint kinematics Comparative anatomy of patella-tibial (p-t) and tibiotarsal (t-t) joints of pedipalps The range of motion (ROM) of the joints was estimated based on the comparison of specimens fixed with different states of The results of our comparative studies are schematically illus- flexion/extension and manual movement of the segments by trated in Fig. 1. The Caddidae and Acropsopilionidae have fine preparation needles. To evaluate if these observations are previously been hypothesized to represent an ancient habitus comparable with natural movements, macro-photographs of of harvestmen belonging to the Palpatores clade, whereas the the species taken in their natural environments were taken as Caddidae are the sister group of all representatives of the references and in S. simoni and M. chrysomelas additionally infraorder Eupnoi and the Acropsopilionidae of the high-speed videographic recordings (see below). The ROM (Groh and Giribet 2014). Both C. agilis and was set in relation to the relative segment width at its proximal A. neozealandiae show bicondylar joints with a planar pivot joint (width divided by the maximal width of the segment), the axis. The hinges are composed of a ball-like or spur-like struc- reciprocal defines the degree of segment constriction. ture in the proximal cuticular brim of the distal segment fitting into a bowl-like structure in the distal cuticular brim of the Phylogenetic mapping proximal segment. The hinge structures are heavily sclero- tized, indicated by a dark, tanned cuticle. In both species, there Characters were mapped onto a compiled tree based on is no constriction at the joint site, but the proximal part of both Schönhofer (2013), and Groh and Giribet (2014). To trace tibia and tarsus is their thickest part (except in the tarsus of the character evolution of the joint ROM, we performed A. neozealandiae, which is slightly inflated in the median Ancestral State Reconstruction in Mesquite 3.04 (Maddison part). In C. agilis, the pivot plane is rotated, such that the tibia and Maddison 2015) using Parsimony. performs a lateral movement (adduction/abduction instead of flexion/extension). This is a typical character in the Eupnoi Behavioral observation and high-speed videography (Shultz 2000). The range of motion (ROM) is below 90° in (HSV) both joints in both species. The basal joint morphology and function in Animals A. neozealandia can be regarded as an ancestral state in the dyspnoid lineage. There is a trend of joint constriction Living individuals of M. chrysomelas were collected be- and correlated increased flexibility that reached their ex- tween July and November 2013 and March and April tremes in the Sabaconidae (here S. simoni)and 2014 in the southern suburban area of Kiel, northern Nemastomatidae (here M. chrysomelas). In I. luteipes (sis- Germany and in rural areas near Mainz, South-Western ter lineage to H. modestum and S. simoni)andD. pauper Germany. Living juveniles of S. simoni were collected (sister lineage to M. chrysomelas), the degree of joint during a field trip in the south-western in August– constriction is low and the ROM is below 90°. September 2014. The animals were collected by hand H. modestum showsanintermediatestepwithajointcon- (turning logs and stones). Harvestmen were kept in plastic striction of 1.9-fold and a ROM of 120° in the p-t-joint, tubes with humid tissues under cool conditions (10– and respectively 2.8-fold and 160° in the t-t-joint. In 15 °C) and starved for at least 1 week. For observations S. simoni, the degree of joint constriction is above 3- of prey capture, the animals were placed in an arena fold and the ROM is up to 200°. This is because the joint 24 × 32 × 15 mm made from cover slides glued together has a modified mono-condylar hinge, which allows not J.O. Wolff et al.

Fig. 1 Evolution of distal pedipalpal joints in harvestmen. Phylogenetic tree based on Schönhofer (2013) and Groh and Giribet (2014). The right schematic images of the joints between patella, tibia, and tarsus. Numbers below give the relative width of the joint (width of segment at the joint divided by highest width of the segment) and the range of movement (ROM). (Superscript number one) Reconstruction of ancestral states of ROM of the tibiotarsal joint with Mesquite V 3.04; (Superscript number 2) character traces of glandular setae following Wolff et al. (2016); Single asterisk in the p-t-joint of C. agilis, the pivot axis is tilted such that adduction-abduction movement is performed instead of flexion-extension (typical for Eupnoi); Double asterisks in the p-t- and t-t-joints of S. simoni are not uniaxial but perform rotational movements in addition to flexion-extension movements (number represents full range of movement)

only pivoting but also rotating (twisting) movements in a Observation of hyperflexion during prey capture controlled direction. In the t-t-joint, the proximal part of the tarsal stalk is split into two sclerites, which work in a We observed and high-speed-video recorded 12 prey cap- click and arresting mechanism (see below). In ture events by 8 juvenile Sabacon simoni on entomobryid M. chrysomelas, the p-t-joint has a degree of joint con- springtails, of which 11 were successful (in the remaining strictionof1.5andaROMof160°.Thetarsuscanper- case the prey was lost due to its large size). The harvest- form hyperflexion with a ROM of 185°, related to a men primarily caught springtails of one half to equivalent higher degree of joint constriction (=3.1). In contrast to to their own body length, but in one case a springtail of S. simoni, both joints have kept their bicondylar condition twice its own body length was successfully overwhelmed. and rotational/lateral movement is limited. In most cases, the harvestmen actively searched for prey. Evolution of hyperflexible joints in sticky prey capture appendages of harvestmen (Arachnida, Opiliones)

When doing so, they used the second leg pair as feelers (Fig. 2b,c,e). The flexion movement of the tarsus was andheldthepedipalpsforwardswithtibiaeflexed(such very quick (3–5ms,Fig.2f–i) and usually led to at least that their concave sides faced forwards) and tarsi extend- one appendage of the springtail being clamped between ed (Fig. 2a, d). The pedipalps were slightly tapped on the the tibia and tarsus. Simultaneously, the tibiae performed ground alternately. When the pedipalp touched a spring- a quick torsional movement inwards, such that the prey tail (usually at the frontally held side of tibia or tarsus), was pulled between the pedipalps and in the reach of the the harvestmen immediately reacted by flexion of the chelicerae (Fig. 2i). The prey was then pulled closely tarsus against the tibia and by elevation of the body towards the body and grasped with the chelicerae.

Fig. 2 Joint hyperflexion during prey capture of S. simoni and M. f–g lateral view, h frontal view. i Prey grasping by quick rotational chrysomelas. Prey items are marked by an asterisk. a–i S. simoni. j–p. movement of the tibia, moving the prey towards the chelicerae, lateral M. chrysomelas. a, j Active search for prey; tarsi are extended, lateral view. n Extended tibia, flexed tarsus. A detached piece of a prey view. b, k Body posture after the catch of a springtail. Legs are stretched appendage is clamped in between tibia and tarsus (arrowhead). o Cryo- to prevent ground contact of the prey; tarsi are flexed, and the prey is SEM image of pedipalpal glandular setae with distal glue droplet. p Same secured between both pedipalps. c, l Clamping of prey legs between tibiae after contact with a springtail. The droplets are contaminated with and flexed tarsi, frontal view. d, m Detail of pedipalp with extended tibia detached setae of the springtail. Abbreviations: pa patella, pe pedipalp, and tarsus, lateral view. e Flexed tibia and tarsus. f–h Rapid tarsal flexion, ta tarsus, ti tibia J.O. Wolff et al.

With M. chrysomelas we recorded 38 prey capture Discussion events (of 18 harvestmen and including different species and sizes of springtails), half of which were successful Evolutionary trends in the range of movements (prey was eaten) (for details see Wolff et al. 2014). Tarsal of pedipalpal joints hyperflexion usually occurs after prey contact (Fig. 2k-n). Often, the harvestmen directly picked up the springtail Among Dyspnoi, there is an evolutionary trend to a stalk-like from the ground by flexing the tarsus thereby clamping constriction of tibial and tarsal basis leading to increased range appendages of the prey between tibia and tarsus. In one of movement of their joints. The highest expression case, the grip was so strong that a clamped leg detached of this character was found in the Sabaconidae and when the prey attempted to struggle free (Fig. 2n). With a Nemastomatidae. We found that both S. simoni and duration of 10–20 ms, tarsal flexion is slower in M. chrysomelas solely use their pedipalps during prey grasp- M. chrysomelas than in S. simoni. After contact with ing. Their pedipalps are covered in setae that produce a sticky entomobryomorph springtails, the glandular setae of the substance, which helps to arrest the prey (Wolff et al. 2014). pedipalp (Fig. 2o) are usually highly contaminated with However, several lineages of epigaeic collembolans have scale- and bristle-like setae of the prey (Fig. 2p). evolved broad, flattened setae (Bscales^) that densely cover both body and appendages and easily detach (Zhang et al. 2014). These contaminate the sticky setae (see Fig. 2p), which Morphology and kinematics of the distal pedipalpal joints leads to significant prey loss (Wolff et al. 2014). Since the in Sabacon sticky setae are synapomorphic to all Palpatores (Wolff et al. 2016), the constriction and hyperflexibility of joints in the The pedipalp of S. simoni exhibits a unique shape of the tibia pedipalps of Nemastomatidae and Sabaconidae have evolved and tarsus and their articulating joints. Both segments are in a second step. We assume that this might be an adaptation to highly inflated and contain strong flexor muscles. The proxi- enhance the prey capture success. This might be part of an mal pieces near the basal joint are shrunk to thin stalks Barms-race^-like evolutionary dynamics between springtails (Fig. 3a: tis, tas). The tibia is bent ventrally and can be twisted and springtail hunters. Although multiple taxa are involved by 180°, such that the concave side is facing dorsally (see (conflicting with the concept of coevolution), the mechanisms Fig. 1). In resting harvestmen, the tibia is usually in this state of prey capture (usage of glue in different springtail hunters) together with 90° flexion. The single hinge of the p-t-joint is and defense (scales in different lineages of springtails) are composed of a ball-like structure in the interior of the patellar similar and thus can be presumed to have high selective ef- brim and a bowl-like structure at the tip of the proximally fects. Springtail fossils show that some lineages had already narrowing tibial stalk. evolved scales (i.e., Tomoceridae) in , while others The tarsus is of a globular shape and fits perfectly in the had not (Oncopoduridae) (Christiansen and Pike 2002). In concave depression of the tibia (Fig. 3b). The depression is amber from the Cretaceous, a species of Nemastomatidae free of glandular setae (Fig. 3a), which prevents any has also been found, showing strikingly similar pedipalps interlocking with the tarsal setae. The t-t-joint is highly flex- and glandular setae than the recent ones (Giribet and Dunlop ible due to wide membranous parts. There are two sclerites 2005). Phylogenetic analysis revealed that Sabaconidae split embedded in the joint membrane, a pro-lateral square-like from the Taracidae and diversified into some major lineages in one (plsc), at which the flexor muscle attaches, and a dorsal, the early Cretaceous (Schönhofer et al. 2013). Fossils of a pin-like one (dsc) that is connected to the tarsal stalk and Sabacon are known from Baltic amber (Palaeogene: Eocene) interacts with a complex protuberance of the tibial brim showing the typical stalked, concave and inflated tibiae (Fig. 3c–i: tsp). In the flexed and the extended position, the (Dunlop 2006), leading to the assumption that these were tip of the dorsal sclerite is placed in different positions. In the already capable of hyperflexion. Hence, the proposed evolu- extended state, its tip is locked between a massive (tsp-I) and tionary scenario is possible. a hook-like (tsp-II) protuberances of the tibia (Fig. 3d, g: po-1). The pro-lateral sclerite is clearly visible. In the flexed Function of the hyperflexible t-t-joints in Sabacon state, the ventral sclerite is placed into a pocket of the tibial and Mitostoma brim beneath the protuberance (Fig. 3f, i: po-3). The pro- lateral sclerite is retracted into the tibia in this state. The We found that hyperflexion is not homologous in Sabaconidae pedipalps in most animals of the investigated material were and Nemastomatidae and that the tarsal flexion in both fami- fixed in one of these positions, but in some cases the tarsus lies uses different mechanisms, leading to the difference in the was partly flexed, showing an intermediate position with the speed of motion. The comparison of the joint configuration at tip of the dorsal sclerite placed in the spoon-like third tibial different steps of tarsal flexion found in the ethanol preserved protuberance (tsp-III) (Fig. 3e, h:po-2). material allows us to draw a conclusion on its working Evolution of hyperflexible joints in sticky prey capture appendages of harvestmen (Arachnida, Opiliones)

Fig. 3 Functional morphology of the tibiotarsal joint in the Sabacon visualization of the joint in the respective state. The yellow lines illustrate pedipalp. a,b Tibia and tarsus of the pedipalp of a female S. simoni, the tendons of the tarsus flexor muscle (ta-fm); the thin black lines ventral view (remark: the ventral site is facing frontally/dorsally in rest indicate how the pro-lateral sclerite (plsc) is mechanically connected to due to the peculiarity of the p-t-joint). a Extended state of t-t-joint. Note the tarsus. d, g Tarsus fully extended, dsc locked in position 1. e, h.Tarsus the tibial depression, in which setae are lacking. b Flexed state of t-t-joint. partly flexed, with dsc between positions 1 and 3. f, i Tarsus fully flexed, The tarsus fits perfectly in the seta-free tibial depression. Note that the with dsc in position 3 and plsc totally retracted and concealed by the tarsal tarsus has rotated sideways. c Fine structure of the t-t-joint visualized by stalk. Abbreviations: dsc dorsal sclerite (pin-like), gs glue secreting SEM, pro-lateral view. The arthrodial membrane is fractured for a better glandular seta (plumose seta), plsc pro-lateral sclerite, po1–3 positions view on sclerotized structures. Hence, the dorsal sclerite (dsc) is not in a of the needle-like dorsal sclerite during different states of tarsal flexion, normal position. Note the distinct tibial spurs (tsc). d–f Different states of jme joint membrane, ta tarsus, ta-fm tarsus flexor muscle, tas tarsal stalk the t-t-joint found in ethanol-preserved material, pro-lateral view, (proximal constriction of the tarsus), ti tibia, tsp tibial spurs (numbered arrowheads mark positions of the pin-like tip of the dsc; g–i schematic I–III) mechanism. In Sabacon, the speed of tarsal flexion is presum- Once released, the dorsal sclerite probably slides along the ably caused by a click mechanism. Such mechanisms work by rounded tsp-III into the brim pocket (Fig. 3f, i: po-3). Since an elastic deformation of a temporary arrested cuticular struc- the muscle is attached on the pro-lateral sclerite (plsc) next to ture, which stores elastic energy generated by the muscle con- the sole hinge, its contraction leads to a simultaneous twisting traction. The sudden energy release leads to a movement that movement of the tarsus (Fig. 3a-b, g-i). In arachnids, leg ex- is quicker than the muscle contraction. In Sabacon, the dorsal tension is usually driven by the internal hemolymph pressure. sclerite is presumably suddenly released from its locked In the Sabacon t-t-joint, the hemolymph pressure may inflate position-1 (Fig. 3d, g: po-1) during flexion of the tarsus. the retracted pro-lateral arthrodial membranes, when the J.O. Wolff et al. flexor muscle relaxes. This leads to the tarsus extending and References twisting back and a return of the dorsal sclerite into position-1. 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Proceedings of the Royal Society of London. Series B: Biological Author contributions J.O.W. and J.M conceived and designed the Sciences, 266(1418), 525–535. study. A.L.S. and J.M. assembled the material and literature. J.O.W. per- Groh, S., & Giribet, G. (2014). Polyphyly of Caddoidea, reinstatement of formed the experiments and analyzed the data. J.O.W. wrote the paper, the family Acropsopilionidae in Dyspnoi, and a revised classifica- and all the other authors equally contributed in the revision. tion system of Palpatores (Arachnida, Opiliones). Cladistics, 31, 277–290. Funding This work was supported by the German National Merit Gronenberg, W. (1995). The fast mandible strike in the trap-jaw ant Foundation (Studienstiftung des Deutschen Volkes) to J.O.W. and by Odontomachus. Journal of Comparative Physiology A, 176(3), German Science Foundation (Deutsche Forschungsgemeinschaft, DFG) 399–408. (μCT Großgeräteantrag) to S.N.G. J.M. thanks the Feldbausch Gronenberg, W. (1996). Fast actions in small animals: springs and click Foundation and Wagner Foundation, both at Fachbereich Biologie of mechanisms. Journal of Comparative Physiology A, 178(6), 727–734. Johannes Gutenberg University Mainz, for the annual research and travel Gronenberg, W., Tautz, J., & Hölldobler, B. (1993). Fast trap jaws and giant grants. neurons in the ant Odontomachus. Science, 262(5133), 561–563. Evolution of hyperflexible joints in sticky prey capture appendages of harvestmen (Arachnida, Opiliones)

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