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Visual Constraints Upon Avian Behaviour

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Visual Constraints Upon Avian Behaviour Visual constraints upon avian behaviour Alexandra Louise Pollard September 2009 Thesis submitted for the degree of Doctor of Philosophy, Cardiff School of Biosciences, Cardiff University UMI Number: U585391 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. Dissertation Publishing UMI U585391 Published by ProQuest LLC 2013. Copyright in the Dissertation held by the Author. Microform Edition © ProQuest LLC. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code. ProQuest LLC 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106-1346 Declarations DECLARATION This work has not previously been accepted in substance for any degree and is not concurrently submitted in candidature for any degree. Signed ............ "...............(candidate) Date ... 2 d . f c k i ............ STATEMENT 1 This thesis is being submitted in partial fulfillment of the requirements for the degree of PhD. j j Signed (candidate) Date ........ ................................... STATEMENT 2 This thesis is the result of my own independent work/investigation, except where otherwise stated. Qfther sources are acknowledged by explicit references. Signed ^rrfT. ........................................ (candidate) Date STATEMENT 3 I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loan, and for the title and summary to be made available to outside organisations. _____ - Signed ..............................(candidate) Date Acknowledgements Throughout the course of my PhD studies I have received support and advice from many people, to whom I am indebted. Firstly I would like to thank my supervisors Rob Thomas, Peter Ferns and Kate Buchanan for their advice and guidance on the project and thesis. I am grateful to my advisor Jon Erichsen for his contributions to the project and the use of his microscope. I would like to thank Dave Kelly and Nicola Marples for their valuable insights and ideas on my project. I would not have been able to complete my studies without the fieldwork assistance and help with observations by Katherine Booth Jones, Heather Coats, James Chen, Peter Jenkins, Soski Nagano, Matt Postles, Lucy Rowse and Frances Thistlethwaite. I would also like to thank the following: The Tamplin family, Forestry Commission, Tower of London, EMRIC, Natural History Museum (London and Tring), Turbary Owl Sanctuary (Whitestake), Naturalis (Leiden), A Rocha Portugal, Ed Drewitt, Peter Howlett, Nicola Goodship, Claire Bale, James Orpwood, Wendy Fernandes, Gabi Juma, Renata Medeiros, Viola Ross-Smith and Loys Richards-Hobbs, and the rest of the office past and present for providing friendship and tea. These acknowledgments would not be complete without expressing my gratitude to my mum and dad, and Chris who provided support, love and motivation. I am especially grateful to Emily for providing perspective. Summary The aim of my PhD research was to investigate how avian behaviours may be constrained by eye design and visual capabilities. As great diversity exists across bird species in the design of the visual system, I utilised this variation to examine and explain the links between vision and behaviour. Several methods were employed in order to gain ocular information from species: including measuring eye size, retinal image brightness and retinal topographic analysis. I applied and developed these methods in studies ranging from a microscopic scale analysis of retinal structure, to studies comparing whole eye size and morphology, to gain an insight into how the timing of different behaviours may be constrained by visual capability, and how artificially modified visual constraints can lead to behavioural plasticity. Specifically, I compared the visual ability of extant diurnally and nocturnally active avian species with that ofArchaeopteryx , finding that this early bird was likely to have been diurnal in the timing of its activity. Following on from this, I found that eye size, controlling for body mass, is an important predictor in the timing of onset of dawn song for species around the world. This relationship is stronger in circumstances when twilight length is longer. This study also revealed how species richness may affect the timing of behaviours, suggesting that tropical birds are able to partition their dawn choruses to reduce masking of acoustic signals. When the presence of artificial lighting modifies the visual constraints at twilight and night, I found that European robins Erithacus rubecula correspondingly modified their singing, foraging and mass regulation behaviour. Overall, my research highlights the great diversity of avian visual adaptations, and emphasises that understanding the differences between them is intrinsic to appreciating the way in which behaviour is constrained by visual ability. Table of contents Title page i Declaration ii Acknowledgments iii Summary iv Table of contents v Chapter 1 An introduction to avian vision and sensory ecology Introduction 1 Evolution of the eye 2 Eye size and function 6 The refractive eye 12 Supporting and protecting the eye 24 Processing light information - the retina and neural centres 31 Optical specialisations for underwater vision in diving birds 53 Avian vision in context: Sensory Hierarchies 56 Conclusion 61 Chapter 2 Methods of assessing avian eye design Abstract 62 Introduction 63 Measuring eye size and eye morphology 64 Measurements using ultrasound 68 Measurements using magnetic resonance imaging 72 Estimating maximum retinal image brightness 75 Case study - Was Archaeopteryx diurnal or nocturnal? 80 Refinement of the calculation of retinal image brightness 82 Constituent eye structures: Measuring retinal design 91 Testing the methodology - a case study: Do nocturnal species have 93 higher retinal image brightness estimates than diurnal species and can any inference be made on the activity patterns ofArchaeopteryx litho graphical Introduction 93 Methods 95 Results 96 Discussion 99 Chapter 3 How does a night-migrating bird differ in its visual ability when compared to a diumally active species? Abstract 102 Introduction 103 Hypotheses 112 Methods 113 Results 119 Discussion 123 Chapter 4 Visual constraints on the timing of onset of dawn song around the world Abstract 126 Introduction 127 vi Methods 137 Results A: Testing for Phylogenetic Autocorrelation 149 B: The relationship between visual ability and the onset of dawn song 152 C: Variation with distance from the equator in the slope of the 167 relationship between eye size and the onset of dawn song D: Variation with twilight length in the slope of the relationship 172 between eye size and the onset of dawn song E: Variation in the onset of dawn song start time 176 F: Are estimates of retinal image brightness better than eye size 180 measures in predicting the timing of the onset of dawn song? Discussion The relationship between visual ability and the onset of dawn song 191 Variation in the slope of the eye vs. song relationship with distance 194 from the equator and with twilight length Comparing eye size and maximum retinal image brightness as 197 predictors of the timing of the onset of dawn song Chapter 5 Effects of artificial lighting on the behaviour of European robins Abstract 201 Introduction 202 Methods A. Study of free-living robins 206 B: Study of aviary-held birds 210 Results A. Study of free-living robins 217 B: Study of aviary-held birds 226 Discussion 235 Chapter 6 Conclusions 242 References 249 Appendices 306 viii Chapter 1 An introduction to avian vision and sensory ecology The purpose of my study is to examine variation in eye design among birds, and determine how this variation is related to variation in behaviour and ecology. Birds have remarkably large eyes for animals of their body mass, reflecting the central role of vision in guiding their behaviour (Tansley and Erichsen, 1985). Bennett and Thery (2007) describe birds as “visually guided creatures with extraordinary eyes; indeed, they have perhaps the most richly endowed visual system of any vertebrate.” Birds have extremely varied eye designs, which have been studied in detail for a considerable time (see for example Ramon y Cajal’s 1889 study on avian retinal morphology). The wealth of available literature addresses many aspects of avian eye design. In this first chapter, I introduce key areas of animal spatial vision in general, and avian vision in particular, that are relevant to understanding the links between visual adaptations and the behaviour and ecology of birds. I discuss the evolution, structure and function of the avian eye, and give examples of visual constraints on bird behaviour in different circumstances. Following on from this first chapter, the thesis progresses with increasing ocular magnitude, beginning at methodologies employed in my studies (Chapter 2), with a case study using extant birds’ eye designs to predict the timing of Archaeopteryx behaviours and food type. I then provide details of a study comparing retinal design in the European storm petrel and the European starling (Chapter 3). I then examine the complex relationships between overall eye size and the timing of onset of dawn song in species from around the world in Chapter 4, and then investigate
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