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Why Are Passerine Eggshells Spotted? Using Calcium

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Why Are Passerine Eggshells Spotted? Using Calcium WHY ARE PASSERINE EGGSHELLS SPOTTED? USING CALCIUM SUPPLEMENTATION AS A TOOL TO EXPLORE EGGSHELL PIGMENTATION by Kaat Brulez A thesis submitted to The University of Birmingham For the degree of DOCTOR OF PHILOSOPHY School of Biosciences College of Life and Environmental Sciences The University of Birmingham July 2013 University of Birmingham Research Archive e-theses repository This unpublished thesis/dissertation is copyright of the author and/or third parties. The intellectual property rights of the author or third parties in respect of this work are as defined by The Copyright Designs and Patents Act 1988 or as modified by any successor legislation. Any use made of information contained in this thesis/dissertation must be in accordance with that legislation and must be properly acknowledged. Further distribution or reproduction in any format is prohibited without the permission of the copyright holder. ABSTRACT The eggshells of many avian species are spotted in appearance but the functional significance of such maculation is poorly understood. Protoporphyrin, responsible for brownish-red colouring on eggshells, is postulated to reinforce the structural integrity of eggshells under conditions when dietary calcium (Ca) is scarce. Within the context of this hypothesis, this thesis documents the use of Ca supplementation of two common British passerine species, blue (Cyanistes caeruleus ) and great tits ( Parus major ), to explore the relationships between eggshell Ca and protoporphyrin content and visible pigment spotting. It further assesses the diversity of avian eggshell coloration using museum eggshells of 73 British passerine species. Despite low soil Ca availability, females were not necessarily Ca-limited but Ca-supplements may still influence eggshell traits and breeding behaviour, possibly by providing females with more time to invest in other activities. The importance of quantifying eggshell pigment concentrations directly, rather than using a proxy, is highlighted. Finally, this thesis shows that passerine eggshell pigment concentrations are highly phylogenetically conserved, thereby encouraging future studies testing key hypotheses to compare eggshell pigmentation of closely related species. This phylogenetic association may be essential to explain the functional significance of eggshell coloration of avian species. ACKNOWLEDGEMENTS My research was funded through a Natural Environmental Research Council (NERC) through studentship NE/H52502X/1. Nestboxes and Ca supplements were kindly provided by CJ Wildlife Ltd. First, and most importantly, I would like to thank my supervisors Jim Reynolds, Phill Cassey and Andy Gosler for their continued support and encouragement. I am further indebted to the predecessors of Team Tit, namely Tim Harrison, Jen Smith, and Simone Webber, for having set-up a well organised and functional field site and methods. I am especially grateful to Simone Webber and Camille Duval for endless conversations on all things related and unrelated to tit ecology and eggshell coloration. Without these people, this thesis would not have been possible. Professionally, many people have been involved in this project. I particularly wish to thank Ivan Mikšík for processing hundreds of eggshell samples for pigment analysis and for being excited with each set of results. I am grateful to Alan Meeson, George Lovell and Jolyon Troscianko for taking time out of their own research to write scripts helping me to quantify eggshell size, coloration and maculation. I also wish to thank Chris Cooney for his help with the phylogenetic analyses. I am further indebted to Steve Portugal and Golo Maurer for introducing me to all the lab techniques and for the stimulating discussions. This study was made considerably easier due to the help of a large number of volunteers including my parents, Pam Holmes and those of the Worcestershire Wildlife Trust. I especially thank Mervyn and Rose Needham for their continuous encouragement throughout the four years of the study. I am extremely grateful to the members of Birmingham University Ringing Group, particularly Michael Barstow, Phil Ireland, Leigh and Tony Kelly, Andrew and Karen Moss, and Dan and Jane Potter for their help within and outside of the field seasons. Finally, thanks are also due to the many blue tits and great tits involved in this study. Without them this would not have been possible. I am sorry for having taken so many of your eggs. AUTHOR’S DECLARATIONS All of the chapters in this thesis were written by Kaat Brulez (KB) with comments and editing from Phill Cassey (PC), Andy G. Gosler (AGG) and S. Jim Reynolds (SJR). Further contributions for each chapter are detailed below. Chapter Two KB, PC and SJR conceived and designed the experiment. KB and Simone L. Webber (SLW) performed the fieldwork. KB and Ivan Mikšík (IM) performed the lab work. KB and PC analysed the data. All authors provided editorial advice. Chapter Three KB conceived and designed the experiment. KB and SLW performed the fieldwork. KB and IM performed the lab work. KB and Alan Meeson (AM) collected the colour data. KB analysed the data. Chapter Four KB, PC and SJR conceived and designed the experiment. KB and SLW performed the fieldwork. KB and IM performed the lab work. KB and AM collected the colour data. AGG visually scored the eggs. KB analysed the data. All authors provided editorial advice. A version of this chapter has been accepted in The Journal of Avian Biology . Chapter Five KB conceived and designed the experiment. KB and SLW performed the fieldwork. KB and IM performed the lab work. KB analysed the data. Chapter Six KB and PC conceived and designed the experiment. KB and IM performed the lab work. Steven J. Portugal (SJP) and Golo Maurer (GM) collected the species-specific data. GM photographed the eggs. P. George Lovell (PGL) collected the colour data. KB, PC and Chris Cooney (CC) analysed the data. TABLE OF CONTENTS CHAPTER ONE: GENERAL INTRODUCTION 1.1 The avian eggshell ................................................................................................................ 2 1.2 A synthesis of hypotheses for eggshell coloration .................................................................. 4 1.2.1 Aposematism .............................................................................................................. 5 1.2.2 Thermoregulation and gas conductance ....................................................................... 6 1.2.3 Crypsis ........................................................................................................................ 8 1.2.4 Egg recognition/brood parasitism ................................................................................ 9 1.2.5 The SSEC hypothesis ................................................................................................ 11 1.2.6 Structural-function hypothesis ................................................................................... 12 1.2.7 Alternative hypotheses .............................................................................................. 13 1.2.8 Gaps in our knowledge .............................................................................................. 13 1.3 Hypotheses explaining pigmentation of great tit and blue tit eggs ........................................ 13 1.4 Thesis objectives and structure ............................................................................................ 16 CHAPTER TWO: CALCIUM SUPPLEMENTATION DOES NOT INFLUENCE EGGSHELL PIGMENTATION IN CAVITY-NESTING BIRDS 2.1 Abstract .............................................................................................................................. 20 2.2 Introduction ........................................................................................................................ 21 2.3 Materials and methods ........................................................................................................ 23 2.3.1 Study site .................................................................................................................. 23 2.3.2 Field methods ............................................................................................................ 25 2.3.3 Egg sampling ............................................................................................................ 26 2.3.4 Pigment analysis ....................................................................................................... 28 2.3.5 Statistical analysis ..................................................................................................... 29 2.4 Results ................................................................................................................................ 30 2.4.1 Variation in thickness across the eggshell .................................................................. 31 2.4.2 Variation in eggshell thickness .................................................................................. 32 2.4.3 Relationship between eggshell thickness, maculation and pigment concentration ..................................................................................................................... 35 2.5 Discussion ........................................................................................................................... 36 2.5.1 Variation in thickness across the eggshell .................................................................. 36 2.5.2 Causes of variation in eggshell thickness
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