Crawford, Niall Alexander (2016) The biomechanics of tree frog adhesion under challenging conditions. PhD thesis http://theses.gla.ac.uk/7102/ Copyright and moral rights for this thesis are retained by the author A copy can be downloaded for personal non-commercial research or study, without prior permission or charge This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the Author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the Author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given. Glasgow Theses Service http://theses.gla.ac.uk/ [email protected] The Biomechanics of tree frog adhesion under challenging conditions Niall Alexander Crawford (MRes) This thesis is submitted for the degree of Doctor of Philosophy February 2016 Centre for Cell Engineering College of Medical, Veterinary and Life Sciences 2 Abstract Tree frogs have evolved specialised toe pads which allow them to efficiently climb vertical surfaces. The toe pad stick by using ‘wet adhesion’ – a combination of forces produced by a thin layer of fluid between the pad and the surface which provide temporary adhesion to allow quick attachment and detachment for climbing. Most studies on tree frogs have been based on their adhesive capabilities on surfaces which are flat, clean and dry (usually glass). However, climbing tree frogs in the wild will come across a variety of surfaces which could affect their adhesive abilities. This PhD investigated whether tree frog adhesion is affected by various ‘challenging’ surfaces, which reflect conditions that tree frogs may encounter whilst climbing. These include rough surfaces, wet conditions, surfaces with loose particulate and hydrophobic surfaces. Experiments were predominantly conducted using a force transducer to measure adhesive and frictional forces of single toe pads, as well as whole animal attachment experiments involving a rotating tilting board. The toe pads of tree frogs were shown to possess a self-cleaning mechanism, whereby the pads will remove contaminants (and subsequently recover adhesive forces) through repeated use, thanks to shear movements of the pad and the presence of pad fluid which aids contaminant deposition. To investigate how torrent frogs (frogs which inhabit waterfalls) can adhere to rough and flooded surfaces, the performance of torrent frogs species Staurois guttatus was compared to a tree frog species (Rhacophorus pardalis). Torrent frogs could produce higher adhesive forces than tree frogs with their toe pads, and possess a specialised toe pad morphology (directional fluid channels on the pad periphery) which may contribute to better performance in flooded conditions. Torrent frogs utilise large areas of ventral skin to stay attached on overhanging surfaces, while tree frogs display a reduction in contact area resulting in a failure to stay attached. This combination of ability and behaviour 3 will help torrent frogs to stay attached on the rough and flooded surfaces that make up their waterfall habitat. On rough surfaces, tree frogs showed improved (compared to smooth surface performance) performance on smaller scale roughness (asperity size <10 µm), and poorer performance on the larger scale roughnesses tested (30 – 425 µm). Interference reflection microscopy (IRM) revealed that larger asperities result in pad fluid being unable to fill the larger gaps of such surfaces, which was confirmed by adding water to rough surfaces to improve attachment performance. The soft pad does however aid in conforming to some rough surfaces, which could account for the better performance on the smaller scale roughness. Many plant surfaces exhibit hydrophobic properties, and so the adhesive performance of tree frogs on hydrophobic surfaces was compared to that on hydrophilic surfaces. It was found that the toe pads could produce similar adhesive and frictional forces on both surfaces. The pad fluids contact angles were then measured on hydrophobic surfaces using IRM, where droplets of pad fluid formed lower contact angles (and are therefore exhibiting higher wettability) than water. Though the exact composition of pad fluid is unknown, some form of surfactant must be present which aids wetting of surfaces (either a surface modification or detergent present in the fluid) to allow wet adhesion to occur - goniometer experiments of water on dried footprints on hydrophobic surfaces confirmed this. The ability to stick in a variety of conditions could provide inspiration for ‘smart’ adhesives, which mimic the adaptable adhesion of tree frog toe pads. 4 Table of Contents 1. General Introduction ......................................................................... 12 1.1 Advantages to climbing .................................................................... 13 1.2 Climbing with adhesive pads ............................................................. 13 1.2.1 Dry adhesion ........................................................................... 15 1.2.2 Wet adhesion .......................................................................... 18 1.2.3 Adhesion in insects and spiders ..................................................... 21 1.2.4 Adhesion in tree frogs ................................................................ 23 1.3 Challenges for adhesive pads ............................................................. 26 1.3.1 Fast, effortless detachment ......................................................... 27 1.3.2 Self-cleaning properties of adhesive pads ......................................... 29 1.3.3 Sticking under wet conditions ....................................................... 30 1.3.4 Adhesion to rough surfaces .......................................................... 31 1.4 Bioinspiration ............................................................................... 34 1.5 Aims of this thesis .......................................................................... 36 2. General Materials and Methods ............................................................. 37 2.1 Introduction – adhesion measuring techniques ........................................ 38 2.1.1 Whole animal force measurement techniques .................................... 38 2.1.2 Smaller scale force measurements ................................................. 39 2.2 Materials and methods .................................................................... 41 2.2.1 Frog species and care ................................................................ 41 2.2.2 Whole animal experimentation methods .......................................... 42 2.2.3 Single toe pad experimentation methods ......................................... 45 2.3 Conclusions .................................................................................. 48 3. Evidence of self-cleaning in the adhesive toe pads of tree frogs .................... 49 3.1 Introduction ................................................................................. 50 3.2 Materials and methods .................................................................... 52 3.2.1 Study animals .......................................................................... 52 3.2.2 Contamination ......................................................................... 52 3.2.3 Force measurements ................................................................. 53 3.2.4 Statistics ................................................................................ 55 3.3 Results ....................................................................................... 56 3.3.1 Single toe pad force recovery ....................................................... 56 3.3.2 Contact area and bead deposition .................................................. 58 3.4 Discussion ................................................................................... 61 3.4.1 Occurrence of self-cleaning ......................................................... 61 3.4.2 Mechanisms of self-cleaning in tree frogs ......................................... 64 5 3.4.3 Comparisons with other animals .................................................... 65 3.4.4 Biomimetic implications ............................................................. 66 4. The attachment abilities of torrent frogs on rough and wet surfaces .............. 68 4.1 Introduction ................................................................................. 69 4.2 Materials and methods .................................................................... 71 4.2.1 Experiments from 2010 study ....................................................... 71 4.2.2 Study animals and location .......................................................... 73 4.2.3 Force measurements ................................................................. 75 4.2.4 Morphology investigation using SEM ................................................ 76 4.2.5 Statistics ............................................................................... 76 4.3 Results ....................................................................................... 77 4.3.1 Force measurements of toe pads, belly and thigh skin .......................... 77 4.3.2 Skin morphology ....................................................................... 79 4.4 Discussion ..................................................................................