Dragonfly Locomotion: Ecology, Form and Function
Total Page：16
File Type：pdf, Size：1020Kb
Dragonfly locomotion: Ecology, form and function Zak Mitchell Submitted in accordance with the requirements for the degree of Doctor of philosophy The University of Leeds Faculty of Biological Sciences School of Biology June 2018 - ii - Intellectual property statements The candidate confirms that the work submitted is his/her/their 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. © 2018 The University of Leeds and Zak Mitchell - iii - Acknowledgements First and foremost I would like to thank my supervisor Dr. Christopher Hassall and co-supervisor Dr. Graham Askew, for endless encouragement, advice and assistance, in addition to giving me the opportunity to study in their laboratories. Without them and their guidance this work would not have been possible. Secondly I would like to thank my family for supporting me and all of my endeavours throughout my entire life, even though my brother is the only one that knows what most of the words in this document mean. Thank you to Julia Humes. Without her love and support this thesis would probably never have been finished, and my time at Leeds would have been nowhere near as amazing as it was. I would like to thank all the great people I have met in Leeds University, past and present, for keeping me sane the last four years and providing a fantastic atmosphere to work in. In particular thank you to Dr. Giovanna Villalobos for sharing the load of trying to keep thousands of dragonfly larvae alive – despite their efforts to the contrary. I would also like to thank all my friends in or out of Leeds, for putting up with me prattling on about dragonflies and lasers, countless hours of games and for telling me to get a real job no more once or twice a month. In particular thanks to Mr. William Farmer because he asked to be mentioned here (the reason for which I still don’t know). Finally thank you the Natural Environment Research Council (NERC) for funding this work. - iv - Abstract The Odonata is a charismatic insect order remarked for their flight ability. They are a useful model system for ecological and evolutionary processes, but in particular their strong and unique flight abilities make them a model taxon to study the biomechanics of flight. Movement is fundamental to a range of processes in biology, including population spatial dynamics. With increasingly urgent demands to understand and predict the impacts of climate change, uncovering the processes driving the movement of populations is paramount. Currently the macroecological patterns caused by climate change are reasonably well documented – particularly for the Odonata. However the mechanisms driving population movements are less clear. Despite considerable advances in our knowledge of the biomechanics of insect flight, little of this has been applied in an ecological context. This thesis aims to identify the gaps in our knowledge of macroecological processes and how biomechanical techniques can advance the field. I have set out a number of methods demonstrating how the biomechanics of flight in Odonata impacts ecological patterns. Range shifts are perhaps one of the best detailed impacts of climate change. At some level they must be driven by the movements of individuals, yet many studies have found little evidence to correlate flight ability and dispersal in insects. Using laboratory measures of flight performance I show that climate induced range shifts in the Odonata are limited by flight efficiency. This has important implications for conservation, as knowing how flight ability is able to restrict a species’ range shift will aid reserve design and future ecosystem predictions. The possible reason behind the lack of evidence linking flight ability and dispersal is the use of proxies for flight performance, and the assumptions of the relationship between these measures and actual flight performance. Indeed, in the literature there are a host of different often mutually exclusive assumptions regarding the role of morphology in shaping flight ability. I provide empirical evidence of how wing morphology affects flight performance, showing that a large proportion of assumptions made within the literature are not supported, or are only weakly - v - supported. This calls into question how prevalent the effects of flight performance on dispersal are, given the use of misleading assumptions. In many systems the state of adult organisms is strongly dependent on the experience of juveniles. For the Odonata, a number of mass and size carry-over effects exist between larva and adult forms, but whether locomotory performance is linked in this way is as of yet unknown. Here I show that there is no correlation between larval and adult locomotory performance, suggesting that muscle development mechanisms are different for larvae and adults. Except for existing mass and size effects, flight performance should not be strongly affected by larval conditions. Finally, various behaviours have the capacity to affect dispersal in a species. One of the behaviours recently empirically confirmed in the Odonata is that of reversible polarotaxis: initial repulsion from polarised light sources as immature adults and the attraction back to polarised light as mature adults. I predicted that reversible polarotaxis would help aid dispersal, repelling insects from natal habitats and encouraging them to find new ones. However, the individual-based model of dispersal that I developed shows that reversible polarotaxis is more important in speeding up the progression through life stages, reducing the time taken to reach feeding habitats and to return to breeding sites. Individuals without polarotaxis would experience higher mortality and lower rates of energy uptake (taking longer to find food) and also higher mortality rates taking longer to return to breeding sites (including lower reproductive success from potentially spending less time at breeding sites). All the work here is then synthesised to create a comprehensive description of Odonata flight morphology (form), its effects on flight performance (function) and the ecological patterns it generates (ecology). I demonstrate that biomechanics can provide important insights into ecological processes – in this case, that flight performance is an important limiting factor for range expansions, where other limitations are perhaps not present. In addition flight morphology is strongly linked with flight performance, suggesting that up to 74% of studies have used incorrect assumptions regarding the links between morphology and performance. - vi - Table of Contents Dragonfly locomotion: Ecology, form and function .................................................. i Intellectual property statements ............................................................................ ii Acknowledgements ............................................................................................... iii Abstract .................................................................................................................iv List of Tables .......................................................................................................... x List of Figures ........................................................................................................ xii List of abbreviations ........................................................................................... xviii Chapter 1 – Introduction: A review of dragonfly flight ecology ............................... 1 1.1 Abstract ................................................................................................................ 1 1.2 Introduction ......................................................................................................... 2 1.3 Flight Biomechanics ............................................................................................. 5 1.3.1 Insect flight .................................................................................................... 5 1.3.2 Odonata muscle physiology .......................................................................... 9 1.3.3 Odonata flight biomechanics ...................................................................... 10 1.4 The ecology of Odonata flight............................................................................ 13 1.5 Linking flight performance and dispersal .......................................................... 17 1.6 Thesis Outline..................................................................................................... 19 1.6.1 – Chapter 2 .................................................................................................. 20 1.6.2 – Chapter 3 .................................................................................................. 20 1.6.3 – Chapter 4 .................................................................................................. 20 1.6.4 – Chapter 5 .................................................................................................. 21 1.6.5 – Chapter 6 .................................................................................................. 21 1.7 Conclusion .......................................................................................................... 21 Chapter 2 – Comparative analysis of Odonata flight performance and associations