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Comparative Functional Morphology of Attachment Devices in Arachnida

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Comparative Functional Morphology of Attachment Devices in Arachnida Comparative functional morphology of attachment devices in Arachnida Vergleichende Funktionsmorphologie der Haftstrukturen bei Spinnentieren (Arthropoda: Arachnida) DISSERTATION zur Erlangung des akademischen Grades doctor rerum naturalium (Dr. rer. nat.) an der Mathematisch-Naturwissenschaftlichen Fakultät der Christian-Albrechts-Universität zu Kiel vorgelegt von Jonas Otto Wolff geboren am 20. September 1986 in Bergen auf Rügen Kiel, den 2. Juni 2015 Erster Gutachter: Prof. Stanislav N. Gorb _ Zweiter Gutachter: Dr. Dirk Brandis _ Tag der mündlichen Prüfung: 17. Juli 2015 _ Zum Druck genehmigt: 17. Juli 2015 _ gez. Prof. Dr. Wolfgang J. Duschl, Dekan Acknowledgements I owe Prof. Stanislav Gorb a great debt of gratitude. He taught me all skills to get a researcher and gave me all freedom to follow my ideas. I am very thankful for the opportunity to work in an active, fruitful and friendly research environment, with an interdisciplinary team and excellent laboratory equipment. I like to express my gratitude to Esther Appel, Joachim Oesert and Dr. Jan Michels for their kind and enthusiastic support on microscopy techniques. I thank Dr. Thomas Kleinteich and Dr. Jana Willkommen for their guidance on the µCt. For the fruitful discussions and numerous information on physical questions I like to thank Dr. Lars Heepe. I thank Dr. Clemens Schaber for his collaboration and great ideas on how to measure the adhesive forces of the tiny glue droplets of harvestmen. I thank Angela Veenendaal and Bettina Sattler for their kind help on administration issues. Especially I thank my students Ingo Grawe, Fabienne Frost, Marina Wirth and André Karstedt for their commitment and input of ideas. I thank all other present and former members of the ‗Functional Morphology and Biomechanics‘ group for their help and nice company, namely Dr. Philipp Bußhardt, Dr. Petra Ditsche, Dr. Elena Gorb, Dr. Alexander Kovalev, Dr. Constanze Grohmann, Dr. Yoko Matsumura, Dr. Henrik Peisker, Dr. Marlene Spinner, Dr. Wey-Lim Wong, Emre Kızılkan, Kai Deng, Hamed Rajabi, Theresa Gödel, Dennis Petersen, Philipp Hofmann and Mike Schindler. I like to express my gratitude to Siegfried Huber (Mühlhofen) for continuous support by supplying various arachnids both living and conserved, as well as great photographs. I thank Michael Seiter (Wien) for the fruitful collaboration and shared enthusiasm on whip-spiders. I am deeply grateful to Dr. Axel Schönhofer (Nackenheim) for his enthusiastic collaboration on harvestmen and the organization of a wonderful collection trip in the South-Western Alps. I thank Dr. Peter Jäger and Julia Altmann (Senckenberg Institute Frankfurt) and Dr. Peter Michalik (University of Greifswald) for the access to the arachnological collections and kind hospitality. I further thank Prof. Jochen Martens (Johannes Gutenberg University Mainz), Dr. Lucia Kuhn-Nentwig (University of Bern), Darrell Ubick (Californian Academy of Sciences), Prof. Jutta Schneider (University of Hamburg), Dr. Christopher Taylor (Curtin University Perth), Hay Wijnhoven (Nijmegen), Jürgen Guttenberger and Salvatore Canu (Usini) for providing animals or specimens. I thank Dr. Anja Klann (University of Greifswald), Prof. Glauco Machado and Solimary García (University of São Paulo) for their kind permission to cite the communication of their unpublished observations. Thanks to Melvyn Yeo, Arno Grabolle, Jörg Pageler, Hans-Jürgen Thorns, Jan van Duinen, Tobias Bellmann (on behalf of his deceased father Heiko Bellmann), Dr. Walter Pfliegler, Markus Gottlieb, Tobias Töpfer and Lennart Bendixen for their kind permission to use their great photographs. I like to thank the referees and the members of the examination board for taking the time. I am deeply grateful for the financial support of the German National Merit Foundation (Studienstiftung des Deutschen Volkes). This work would have not been possible without the ongoing support of my wife Lydia. Abstract Attachment is one of the major interactions between an organism and its environment. An enormous diversity of organs or secretory products has been evolved to enhance adhesion and friction with various substrates. The biological functions comprise maintenance of position, locomotion, prey capture, defence, reproduction or dispersal. There are numerous studies that deal with this issue in lizards, frogs, insects, barnacles, mussels and echinoderms, but the second largest class of arthropods, the Arachnida, are highly neglected. This work surveys the attachment organs and structures, and adhesive secretions occurring in this class and discusses the relationship between morphology and function, evolutionary trends, and biomimetic potential. The found diversity comprises interlocking and clamping devices (like claws, spines, hooks, pincer, locking piercer and raptorial legs), smooth and hairy adhesive pads, suckers, and hardening and viscid glue. Mechanical attachment is found in every arachnid order. The membrane based smooth adhesive pads occur in pseudoscorpions (Pseudoscorpiones), camel spiders (Solifugae), ticks (Ixodida and Holothyrida), mites (Opilioacarida, Mesostigmata, Sarcoptiformes and Trombidiformes), harvestmen nymphs (Opiliones), and prenymphs of scorpions (Scorpiones), whip spiders (Amblypygi) and whip scorpions (Thelyphonida). Hairy adhesive pads are found in spiders (Araneae), harvestmen (Opiliones), mites (Trombidiformes), and hooded tickspiders (Ricinulei). A unique micro-patterned adhesive pad (‗smooth‘ pad with spatulae) occurs in whip spiders (Amblypygi). Suckers are present in mites (Sarcoptiformes and Trombidiformes). Hardening glue is produced by spiders (Araneae), whip spiders (Amblypygi), whip scorpions (Thelyphonida), scorpions (Scorpiones), harvestmen (Opiliones), pseudoscorpions (Pseudoscorpiones), ticks (Ixodida), and mites (Mesostigmata, Sarcoptiformes and Trombidiformes). Viscid secretions for attachment purposes are produced by spiders (Araneae), harvestmen (Opiliones), and mites (Mesostigmata and Trombidiformes). The mechanical function and fine structure of selected attachment devices was studied, namely the arolia of whip spiders, whip scorpions, scorpions, pseudoscorpions and ticks, the tenent setae of some mites, the glandular setae and secretion of harvestmen, and the silken attachment discs of spiders. Further morphological examinations were performed on the scopulae of harvestmen and ricinuleids, the arolia of harvestmen and the secretions serving camouflage with soil particles in harvestmen and mites. Most structures and secretion properties have remarkable analogies among insects, lizards and tree frogs, which illustrate the optimal biological solutions for universal or specific attachment. This holds for the shape of claws, the spatulate or (rarer) mushroom-like shape of contact elements in adhesive hairs, the inner directed fibrillation of smooth adhesive pads, and the viscoelastic properties of prey capture adhesives. However, some of the described attachment devices are rather unique. In scorpion prenymphs the perhaps most simple type of an adhesive foot pad was found, represented by the non-sclerotized sac-like tip of the pretarsus that is hold in shape by the internal fluid pressure and can be invaginated by a muscle. An aroliar shape building a narrow, transverse contact has evolved in three different orders of arachnids. This structure presumably enhances the ability to switch quickly between a distribution and concentration of stress, which is of high importance for dynamic adhesion. In whip-spiders an arolium was found that exhibits hexagonal microstructures with spatulate tips, which have previously only known from hairy adhesive pads. These pads can generate a high adhesive strength, comparable to spiders and geckoes, even in the absence of fluids. The hexagonal order presumably permits a rapid drainage, enhancing the adhesion on wet surfaces, as known from tree frogs. The prehensile tarsi of harvestmen have dense pads of thin pointed setae, permitting a secure grip without the necessity of adhesive structures. The glandular setae of harvestmen exhibit special microstructures that arrest a droplet of viscid glue even at high pulling stresses. The silken attachment discs of spiders are secretory glue products with a unique hierarchical structure enhancing the flaw tolerance and attachment performance on anti-adhesive surfaces. The results may be of high relevance for our understanding of the function and evolution of attachment devices, as well as for the life history, behaviour, ecology and phylogeny of arachnids. The findings may also be a source of inspiration for biomimetic approaches and demonstrate that the high neglecting of arachnids in biomechanic research is unjustified. Kurzzusammenfassung Befestigung ist eine der wichtigsten Interaktionen zwischen einem Organismus und seiner Umwelt. Zu diesem Zweck entstand im Laufe der Evolution eine enorme Vielfalt an Klammer- und Haftorganen sowie klebrigen Sekreten. Ihre biologischen Funktionen umfassen Positions-Beibehaltung, Fortbewegung, Beutefang, Verteidigung, Reproduktion und Verbreitung. Zahlreiche Studien befassen sich mit dem Aufbau, der mechanischen Funktion und der stofflichen Zusammensetzung solcher Organe oder Sekrete bei Echsen, Fröschen, Insekten, Seepocken, Muscheln oder Stachelhäutern, aber die zweitgrößte Klasse der Gliederfüßer (Arthropoda), die Spinnentiere (Arachnida), sind bei dieser Forschung weitgehend ignoriert. Diese Arbeit gibt einen Überblick über Haftorgane, -strukturen, und -sekrete in dieser Tierklasse
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