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Biomechanics of the Fibrillar Adhesive System in Insects James Michael

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Biomechanics of the Fibrillar Adhesive System in Insects James Michael Biomechanics of the Fibrillar Adhesive System in Insects James Michael Rex Bullock Biomechanics of the Fibrillar Adhesive System in Insects James Michael Rex Bullock Clare College Supervised by Dr Walter Federle This dissertation is submitted for the degree of Doctor of Philosophy Cambridge 2010 James M. R. Bullock, Biomechanics of the fibrillar adhesive system in insects University of Cambridge, 2010 DECLARATION This dissertation is submitted for the degree of Doctor of Philosophy. It is the result of my own work and includes nothing which is the outcome of work done in collaboration except where specifically indicated in the text and acknowledgements. It is not substantially the same as any previous material submitted for a degree at any other University. This thesis totals 151 pages (including bibliography and appendices) and does not exceed the prescribed word limit. Cambridge, 30 th September 2010 James Bullock iii ACKNOWLEDGEMENTS To my supervisor, Walter Federle, an enormous debt is owed. His help and guidance have been more than critical to the success of all that is contained within this thesis and his constant supply of ideas and inspiration have made him one of the best supervisors one could have, regardless of the field of research. Uncountable thanks are due to all current and honorary members of the Cambridge Insect Biomechanics workgroups. It has been an immense privilege to have studied and worked with you; Ulrike Bauer, Holger Bohn, Christofer Clemente, Kristien de Clercq, Jan- Henning Dirks, Patrick Drechsler, Thomas Endlein, Nanna Evers, Jamie Gundry, David Labonte, Li Ming-he, Karin Moll, Sean Ng, Anne Peattie, Gregory Sutton, Filip Szufnarowski, Dan Thornham, Kerstin Tüchert and Yanjia Gao. Many thanks go to Clare College and the Department of Zoology, who have both provided me with an exceptionally creative and friendly environment within which to live and work. In particular Sue Goodbody and Linda Wheatley deserve much credit. Thanks to my advisors, Simon Laughlin and Ullrich Steiner, to my examiners, Jon Barnes and Simon Maddrell, and to the other members of the Department of Zoology that I have worked with during the course of my PhD, including Malcolm Burrows, Charlie Ellington, Felix Evers and Heather Whitney. Additionally I would like to thank the members of the Cambridge Engineering Department (Mechanics, Materials and Design Division), Nanoscience Centre and Multi Imaging Centre for technical help concerning several areas of this work. Importantly thanks must go to Christofer Clemente, Saul Dominguez, Patrick Drechsler, Andreas Eckart, Thomas Endlein, Nanna Evers and Filip Szufnarowski for the initial and continued development of the LabVIEW motor control programmes and force feedback set-up. I would specifically like to express my deep gratitude to Christofer Clemente and Thomas Endlein for their continual guidance, advice and help with many of the technical and scientific aspects of this work. Thanks to Dan Thornham and all at the Telamba Homestay in Brunei Darussalam for the indispensable guidance and incredible hospitality I received during my time spent working in the field. v This thesis was funded by research grants from the UK Biotechnology and Biological Sciences Research Council and the Cambridge Isaac Newton Trust. Additional funding was received from Clare College and the Cambridge Philosophical Society. And to my family, Michael Bullock, Felicity Bullock, Charlie Bullock and Payel Das, who have given me constant love and support, everything else is owed. vi ABSTRACT Biomechanics of the fibrillar adhesive system in insects - James Michael Rex Bullock Many animals are able to scale smooth surfaces using adhesive structures on their feet. These organs are either soft pads with a relatively smooth surface or dense arrays of microscopic adhesive hairs with both designs having independently evolved in diverse taxa of arthropods and vertebrates. Biological adhesive pads out- perform conventional adhesives in many respects, making them important models for biomimetics. Hairy pads have attracted particular attention, because it has become feasible to fabricate similar synthetic microstructures. Nevertheless, the detailed performance and functional properties have not been characterised for any natural fibrillar adhesive system, and many fundamental aspects are still not understood. The aim of this thesis was therefore to investigate the fibrillar adhesive system of leaf beetles as a model. To investigate the functional implications of hairy pad design, the attachment performance between hairy pads of the leaf beetle Gastrophysa viridula and smooth pads of stick insects ( Carausius morosus ) was compared. Adhesive and frictional stresses were found to be similar in smooth and hairy pads, inconsistent with contact splitting theory, which predicts higher adhesive stresses for fibrillar adhesives. Hairy pads showed a greater direction- dependence of friction forces than smooth pads, confirming the importance of the asymmetric design of individual setae for effortless detachment. Experiments with contaminating particles also showed that hairy pads removed contamination more rapidly and efficiently than smooth pads. Self-cleaning ability had not been previously documented for adhesive organs of insects. To investigate to what extent the hairy system is able to compensate for surface roughness, whole-body attachment forces were measured for varying roughness levels. Attachment was reduced for all length scales of surface roughness, but in particular for asperity sizes smaller than the diameter of individual seta tips. Leaf beetles possess adhesive pads on three tarsal segments, which vary in setal morphology. However, the functional implications of this variation are unknown. The mechanical and adhesive properties of individual pads were therefore tested and their use during climbing observed. Proximal pads were shown to be stiffer than distal pads, conferring stability during pushing. In contrast, the softer distal pads allowed better attachment to rough surfaces. Hence the morphological variation is explained by an effective division of labour between the pads. To investigate an vii extreme example of pushing in a hairy system, pad use was studied during jumping in flea beetles. The pushing forces needed during take-off were exclusively produced by the proximal pads, again confirming the division of labour. To characterise the effects of different hair morphologies and to understand how individual setae contribute to array and whole-animal performance, single hair forces were measured using a glass capillary cantilever. Male- specific discoidal hairs were shown to be both stiffer and more adhesive than pointed and spatula-tipped setae, likely affecting overall pad stability and attachment. This thesis has shown that hairy pads are similar to smooth pads in the magnitude of adhesive stress supported yet outperform them in detachability and self-cleaning. It was also demonstrated that there are considerable differences in design and performance even within setal arrays of the same insect, indicating the limitations of general models of fibrillar adhesion and underlining the importance of specialised adaptations. viii PUBLICATIONS Some of the ideas and figures presented in this thesis have previously appeared in the following publications: Journal Papers Bullock, J. M. R., Drechsler, P. and Federle, W. (2008). Comparison of smooth and hairy attachment pads in insects: friction, adhesion and mechanisms for direction-dependence. Journal of Experimental Biology 211, 3333-3343. Bullock, J. M. R. and Federle, W. (2009). Division of labour and sex differences between fibrillar, tarsal adhesive pads in beetles: effective elastic modulus and attachment performance. Journal of Experimental Biology 212, 1876-1888. Clemente C. J., Bullock J. M. R., Beale A. and Federle W. (2009). Evidence for self-cleaning in fluid-based smooth and hairy adhesive systems of insects. Journal of Experimental Biology 213, 635-642. Bullock, J. M. R. and Federle, W. (2010). The effect of surface roughness on claw and adhesive hair performance in the dock beetle Gastrophysa viridula. Insect science in press. Abstracts Bullock, J. M. R. and Federle, W. (2008). Friction forces in the hairy adhesive pads of beetles. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 150, 90-91. Society for Experimental Biology, 6-10 th July, Marseille, France. Bullock, J. M. R. and Federle, W. (2008). Comparison of Attachment Performance in the Hairy and Smooth Adhesive Pads of Insects. Annual Meeting & Exhibition Final Program and Abstracts. Society for Integrative and Comparative Biology, 3-7th January, Boston, MA, USA. Bullock, J. M. R. and Federle, W. (2009). Why have more than one pad per leg? Determining the mechanical and adhesive properties of hairy attachment pads in beetles. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 153, 130. Society for Experimental Biology, 28 th June – 1 st July, Glasgow, Scotland. ix Clemente, C. J., Beale, A., Bullock, J. M. R. and Federle, W. (2009). Evidence for self-cleaning in fluid-based smooth and hairy adhesive systems of insects. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 153, 123. Society for Experimental Biology, 28 th June – 1 st July, Glasgow, Scotland. Bullock, J. M. R., Clemente, C. J. and Federle, W. (2010). Pushing and pulling: beetles use different tarsal pads to walk and climb.
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