Structure-Function Relationships in the Water-Use Strategies and Ecological Diversity of the Bromeliaceae

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Structure-Function Relationships in the Water-Use Strategies and Ecological Diversity of the Bromeliaceae Structure-function relationships in the water-use strategies and ecological diversity of the Bromeliaceae Jamie Oliver Males Clare College, University of Cambridge Date of submission: 5th May 2017 This dissertation is submitted for the degree of Doctor of Philosophy Structure-function relationships in the water-use strategies and ecological diversity of the Bromeliaceae Jamie Oliver Males Summary The Bromeliaceae is one of the largest and most ecologically diverse angiosperm families in the Neotropics. In recent years, this family has begun to emerge as a model system for the study of plant evolutionary ecology and physiology, and major advances have been made in understanding the factors involved in episodes of rapid diversification and adaptive radiation in specific bromeliad lineages. However, despite a long tradition of ecophysiological research on the Bromeliaceae, an integrative, evolutionarily-contextualised synthesis of the links between anatomical) physiological, and ecological aspects of bromeliad biology has hitherto been lacking. The overarching aim of this research project was therefore to use new quantitative data representing a wide range of bromeliad taxonomic and functional groups to elucidate how variation in leaf traits connected by structure- function relationships influences ecological differentiation among bromeliad taxa. Special emphasis was placed on hydraulic and water relations traits because of fast-paced contemporary developments in these fields. The methodologies employed included an assessment of the diversity of bromeliad hydrological habitat occupancy, quantification of key anatomical and physiological traits and their correlations, investigation of the links between vascular and extra-xylary anatomy and hydraulic efficiency and vulnerability, quantification of stomatal sensitivity to leaf-air vapour pressure deficit and stomatal kinetics, and a case study of trait-mediated niche segregation among congeneric epiphytic bromeliad species on the Caribbean island of Trinidad. The results highlight how divergences in a range of continuous and categorical anatomical traits underpin differences in physiological capacities and sensitivities, which in turn determine environmental relations and ecological distinctiveness. This research project therefore provides critical insights into the mechanistic basis of evolutionary diversification in a highly ecologically important family. It also represents the most comprehensive analysis of the significance of trait variation for ecological differentiation across any major radiation of herbaceous angiosperms. 1 Contents Declaration p. 5 Acknowledgements p. 6 Summary p. 7 1. General Introduction p. 8 2. Hydrological habitat position and range in terrestrial bromeliads p. 25 3. Integration of hydraulic and anatomical traits in the leaf economics of the Bromeliaceae p. 48 4. Structure-function relationships in bromeliad leaf hydraulics p. 87 5. Variation and ecological significance of stomatal sensitivity to vapour pressure deficit in the Bromeliaceae p. 119 6. Trait-mediated environmental niche differentiation in Trinidadian Aechmea bromeliads p. 146 7. General Discussion p. 194 Bibliography p. 212 Appendices p. 247 2 List of Figures • Fig. 1.1.1 p. 9 • Fig. 1.2.1 p. 23 • Fig. 2.3.1 p. 31 • Fig. 2.3.2 p. 35 • Fig. 2.4.1 p. 43 • Fig. 3.2.1 p. 53 • Fig. 3.3.1 p. 59 • Fig. 3.3.2 p. 60 • Fig. 3.3.3 p. 61 • Fig. 3.3.4 p. 62 • Fig. 3.3.5 p. 65 • Fig. 3.3.6 p. 67 • Fig. 3.3.7 p. 70 • Fig. 3.3.8 p. 73 • Fig. 3.3.9 p. 76 • Fig. 3.3.10 p. 78 • Fig. 3.4.1 p. 79 • Fig. 4A.3.1 p. 91 • Fig. 4A.3.2 p. 93 • Fig. 4A.3.3 p. 94 • Fig. 4A.3.4 p. 95 • Fig. 4A.3.5 p. 96 • Fig. 4B.3.1 p. 102 • Fig. 4B.3.2 p. 106 • Fig. 5.3.1 p. 124 • Fig. 5.3.2 p. 125 • Fig. 5.3.3 p. 126 • Fig. 5.3.4 p. 127 • Fig. 5.3.5 p. 127 • Fig. 5.3.6 p. 128 • Fig. 5.3.7 p. 129 • Fig. 5.3.8 p. 130 • Fig. 5.3.9 p. 131 • Fig. 5.3.10 p. 132 • Fig. 5.3.11 p. 133 • Fig. 5.3.12 p. 134 • Fig. 5.3.13 p. 135 • Fig. 5.3.14 p. 137 • Fig. 6.1.1 p. 147 • Fig. 6.1.2 p. 148 3 • Fig. 6.1.3 p. 149 • Fig. 6.1.4 p. 150 • Fig. 6.1.5 p. 154 • Fig. 6.3.1 p. 163 • Fig. 6.3.2 p. 168 • Fig. 6.3.3 p. 169 • Fig. 6.3.4 p. 171 • Fig. 6.3.5 p. 172 • Fig. 6.3.6 p. 175 • Fig. 6.3.7 p. 179 • Fig. 6.3.8 p. 182 • Fig. 7.2.1 p. 197 • Fig. 7.2.2 p. 210 4 List of Tables • Table 1.1.1 p. 11 • Table 2.2.1 p. 28 • Table 2.3.1 p. 34 • Table 3.2.1 p. 58 • Table 3.3.1 p. 64 • Table 3.3.2 p. 68 • Table 3.3.3 p. 71 • Table 3.3.4 p. 74 • Table 4A.3.3 p. 98 • Table 4B.2.1 p. 103 • Table 4B.3.1 p. 105 • Table 4B.3.2 p. 108 • Table 5.3.1 p. 138 • Table 6.1.1 p. 152 • Table 6.2.1 p. 160 • Table 6.3.1 p. 164 • Table 6.3.2 p. 167 • Table 6.3.3 p. 174 • Table 6.3.4 p. 177 • Table 6.3.5 p. 177 • Table 6.3.6 p. 178 • Table 6.3.7 p. 180 • Table 6.3.8 p. 181 • Table 7.2.1 p. 200 5 Declaration This dissertation is the result of my own work and includes nothing which is the outcome of work done in collaboration except as declared in the Preface and specified in the text. It is not substantially the same as any that I have submitted, or, is being concurrently submitted for a degree or diploma or other qualification at the University of Cambridge or any other University or similar institution except as declared in the Preface and specified in the text. I further state that no substantial part of my dissertation has already been submitted, or, is being concurrently submitted for any such degree, diploma or other qualification at the University of Cambridge or any other University or similar institution except as declared in the Preface and specified in the text. It does not exceed the prescribed word limit for the relevant Degree Committee. Jamie Males May 2017 6 Acknowledgements I would like to thank all members of the Physiological Ecology group at the Department of Plant Sciences for their support throughout my time at Cambridge. In particular, Moritz Meyer and Jessica Royles have provided a great deal of help in both practice and theory. I am grateful to Brent Helliker for his help in setting up apparatus for hydraulic measurements. Sourcing living material for characterisation was made possible through the assistance of Pete Michna and Alex Summers at Cambridge University Botanic Garden, Marcelo Sellaro at Royal Botanic Gardens Kew and Pete Brownless at Royal Botanic Gardens Edinburgh, and through the award of the Harry Luther International Bromeliad Scholarship from the Bromeliad Society International. I would like to thank Bruce Holst for all his help in securing this award and arranging my visit to Marie Selby Botanical Gardens. The fieldwork carried out in Trinidad would not have been possible without the time and resources invested in it by the staff of the National Herbarium of Trinidad and Tobago at the University of the West Indies. I am especially grateful to Yasmin Baksh-Comeau for her role in helping to organise all aspects of the fieldwork and the export of living material to the UK. Aline Horwath, Jared Griffiths, Brent Helliker, Shane Ballah, Shahada Paltoo, and Shivani Ramsubhag proved themselves to be excellent bromeliad hunters during various trips. Dan Jaggernauth’s knowledge of the trails and flora of the Northern Range was invaluable. I reserve special thanks for my supervisor, Howard Griffiths, for his enthusiasm, support, and tireless exertions in the field. 7 Summary The Bromeliaceae is one of the largest and most ecologically diverse angiosperm families in the Neotropics. In recent years, this family has begun to emerge as a model system for the study of plant evolutionary ecology and physiology, and major advances have been made in understanding the factors involved in episodes of rapid diversification and adaptive radiation in specific bromeliad lineages. However, despite a long tradition of ecophysiological research on the Bromeliaceae, an integrative, evolutionarily-contextualised synthesis of the links between anatomical) physiological, and ecological aspects of bromeliad biology has hitherto been lacking. The overarching aim of this research project was therefore to use new quantitative data representing a wide range of bromeliad taxonomic and functional groups to elucidate how variation in leaf traits connected by structure- function relationships influences ecological differentiation among bromeliad taxa. Special emphasis was placed on hydraulic and water relations traits because of fast-paced contemporary developments in these fields. The methodologies employed included an assessment of the diversity of bromeliad hydrological habitat occupancy, quantification of key anatomical and physiological traits and their correlations, investigation of the links between vascular and extra-xylary anatomy and hydraulic efficiency and vulnerability, quantification of stomatal sensitivity to leaf-air vapour pressure deficit and stomatal kinetics, and a case study of trait-mediated niche segregation among congeneric epiphytic bromeliad species on the Caribbean island of Trinidad. The results highlight how divergences in a range of continuous and categorical anatomical traits underpin differences in physiological capacities and sensitivities, which in turn determine environmental relations and ecological distinctiveness. This research project therefore provides critical insights into the mechanistic basis of evolutionary diversification in a highly ecologically important family.
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