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Leeds Thesis Template Muscle mechanics and hydrodynamics of jet propulsion swimming in marine invertebrates Thomas Robert Neil Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds Faculty of Biological Sciences School of Biomedical Sciences July 2016 - ii - Intellectual property rights The candidate confirms that the work submitted is his own and that appropriate credit has been given where reference has been made to the work of others. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. © 2016 The University of Leeds and Thomas Robert Neil - iii - Declaration The work carried out in this thesis was supported by several individuals. Dr Graham Askew assisted in the collection of all the data gathered in chapter two. Marion Kaufmann instrumented the animals and collected the majority of the in vivo power output measurements of the king scallops. Dr David Ellerby provided laboratory space and equipment at Wellesley College for the collection of the bay scallop data. Dr Richard Marsh assisted with the instrumenting and swimming of the bay scallops. Dr Graham Askew assisted with muscle preparations, equipment set up and analysis in chapter three. Dr Graham Askew assisted in data analysis and the implementation of equations in chapters four, five and six. - iv - Acknowledgements First and foremost I would like to thank Dr Graham Askew for giving me this great opportunity to study in his laboratory and provide invaluable guidance throughout my PhD. I have learnt a great deal under his supervision and the work we have done together has been both interesting and a great deal of fun. I would like to thank Dr Richard Marsh and Dr David Ellerby for their assistance with data collection at Wellesley college. In particular I would like to give thanks to Rich and his wife Judy for putting Graham and I up for three weeks and taking very good care of us! Thank you to all my lab mates past and present, I’m glad you came along for the ride and made this whole process an enjoyable one, I will forever have fond memories of lunch time crosswords, sporcle and gun fights. Thank you to Yazi for making our time in Leeds special and putting up with me this whole time, unfortunately I’m not going to stop talking about the sea any time soon. I would also like to thank my family for all their support despite never really understanding what it was I was doing. Finally, thanks go to the EPSRC for funding this research and making this whole project possible. - v - Abstract Locomotion amongst animals is widespread and diverse. Movement is of fundamental biological importance to animals, enabling them to forage, migrate, pursue prey and mate. Animals have evolved a great range of locomotor mechanisms that span huge size ranges and diversity across the animal kingdom, yet several common principles underlie most of these mechanisms, the understanding of which can help explain why certain biological locomotor systems have evolved for particular environments. Constraints on an animal’s morphological traits are bought about by body size, meaning that several aspects of locomotor performance are found to vary with body mass. Burst performance plays a crucial role in many animals lives, with the ability to accelerate and manoeuvre quickly often being essential for survival. The power available from the muscles during this type of locomotion is generally thought to decrease with increasing body size, with cycle frequency predicted to limit maximal muscle mass-specific performance. Muscle mass-specific power was measured in vivo in scallops covering a 96-fold range in body mass. Power was measured using sonomicrometry crystals to measure muscle length changes during swimming whilst pressure was simultaneously monitored within the mantle cavity. The scaling of the contractile characteristics of the adductor muscles of scallops was investigated to determine what affect the intrinsic properties of the muscle have on the scaling of muscle power output. Muscle fibre bundles were dissected and attached to a force transducer to measure force and muscle length change. Muscles were electrically stimulated via platinum plate electrodes. The scaling of twitch kinetics and the force velocity relationship were characterised in vitro. Jet propulsion via pulsed jets have been shown to be able to produce more thrust per unit of ejected fluid then an equivalent steady jet. The benefit is bought about through the production of isolated vortex rings, which entrain additional ambient - vi - fluid into the wake. There are numerous biological swimmers that use jet propulsion as their primary form of locomotion, however, their ability to be able to use vortex rings to enhance their propulsive performance has only been investigated in a few systems. Jet wake structure and swimming performance were quantified in three animals that swim by jet propulsion; scallops, Nautilus and jellyfish. The properties of the wakes were characterised using particle image velocimetry to measure the wake structure of the jets that were produced. Muscle mass-specific power output was found to decrease with increasing size in scallops. Frequency decreased with increasing size, muscle stress was found to be approximately constant whilst muscle strain decreased with increasing size in king scallops. The scaling exponents for muscle power were greater than those of the scaling of cycle frequency, suggesting that cycle frequency is not the sole determinant of the scaling of muscle power output. Muscle power output measured in vitro was also found to decrease with increasing body mass, but scaled with an exponent greater than that measured in vivo. The Vmax of the muscles decreased with increasing size, but did not scale in the same way as cycle frequency, suggesting that the intrinsic contractile properties of the muscle were not the sole determinant of cycle frequency in scallops. King scallops and Nautilus were found to produce two distinct jet modes, one in which isolated vortex rings were produced (Jet mode 1) and one which consisted of a leading vortex ring followed by a trailing jet of fluid (Jet mode 2). No differences were found in jet mode and the thrust produced from the jet, although enhanced thrust was found in king scallops producing jets at formation numbers of ~4. The wake structure of Rhizostomeae jellyfish revealed that they propel themselves via and interaction of two vortex rings that are produced as they swim. They were also - vii - found to manipulate the formation of a vortex ring that is formed as they swim, manoeuvring it to within their sub-umbrella cavity, providing them with an additional boost during swimming. - viii - Table of Contents Intellectual property rights ................................................................................. ii Declaration ........................................................................................................ iii Acknowledgements ........................................................................................... iv Abstract .............................................................................................................. v Table of Contents .............................................................................................. viii List of Tables ..................................................................................................... xiii List of Figures .................................................................................................... xiv Chapter 1 General Introduction ........................................................................... 1 1.1 Muscle function during locomotion ............................................................. 1 1.1.1 Quantifying in vitro muscle characteristics ...................................... 2 1.1.2 Isometric muscle performance ........................................................ 2 1.1.3 The force velocity relationship ......................................................... 3 1.1.4 In vivo muscle mechanical performance ......................................... 4 1.1.5 The Work Loop Technique ............................................................... 5 1.2 The scaling of muscle power output ............................................................ 7 1.2.1 Theoretical approaches to the scaling of maximum muscle power output ................................................................................... 7 1.2.2 Experimental studies ........................................................................ 8 1.2.3 The scaling of frequency and mass-specific work ............................ 9 1.2.4 Scaling of maximum power output determined using the work loop technique ...................................................................... 10 1.2.5 Whole animal approaches to the scaling of maximum muscle power output ................................................................................. 11 1.3 Aquatic Locomotion ................................................................................... 12 1.3.1 Visualising the flow: particle image velocimetry ........................... 13 1.3.2 Hydrodynamic efficiency ................................................................ 14 1.3.3 Jets as a means of propulsion ........................................................ 15 1.3.4 Optimal Vortex Formation ............................................................
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