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Carnivorous Plant Responses to Resource Availability Carnivorous plant responses to resource availability: environmental interactions, morphology and biochemistry Christopher R. Hatcher A doctoral thesis submitted in partial fulfilment of requirements for the award of Doctor of Philosophy of Loughborough University November 2019 © by Christopher R. Hatcher (2019) Abstract Understanding how organisms respond to resources available in the environment is a fundamental goal of ecology. Resource availability controls ecological processes at all levels of organisation, from molecular characteristics of individuals to community and biosphere. Climate change and other anthropogenically driven factors are altering environmental resource availability, and likely affects ecology at all levels of organisation. It is critical, therefore, to understand the ecological impact of environmental variation at a range of spatial and temporal scales. Consequently, I bring physiological, ecological, biochemical and evolutionary research together to determine how plants respond to resource availability. In this thesis I have measured the effects of resource availability on phenotypic plasticity, intraspecific trait variation and metabolic responses of carnivorous sundew plants. Carnivorous plants are interesting model systems for a range of evolutionary and ecological questions because of their specific adaptations to attaining nutrients. They can, therefore, provide interesting perspectives on existing questions, in this case trait-environment interactions, plant strategies and plant responses to predicted future environmental scenarios. In a manipulative experiment, I measured the phenotypic plasticity of naturally shaded Drosera rotundifolia in response to disturbance mediated changes in light availability over successive growing seasons. Following selective disturbance, D. rotundifolia became more carnivorous by increasing the number of trichomes and trichome density. These plants derived more N from prey and flowered earlier. This suggests that D. rotundifolia extend their fundamental niche in part due to phenotypic plasticity into environments that are shaded and are, for non- carnivorous plants, high in stress and disturbance—untenable environments according to universal adaptive theory. In an observational study on peatlands across Europe, I investigated how habitat heterogeneity and climate-driven changes in nutrient availability impact on D. i rotundifolia trait variability. I found that patterns of hydrology and light are consistent across peatlands. But, climate driven N accumulation alters the expression of carnivory which can reverse expected patterns of trait expression. These findings have implications for predicting the ecological impacts of climate change, as patterns of precipitation and evaporation may have different consequences depending on specific local topology and climate norms and can have significant impacts at small spatial scales, to the extent that entire habitats may be lost. I conducted a research review to determine the role of secondary plant metabolites in carnivory. This identified similar patterns of metabolite production among closely- and distantly-related carnivorous taxa, which suggests that secondary metabolites are important for plants to facilitate carnivory. The review supports the hypothesis that secondary plant metabolites are drivers of plant diversification and evolution of plants into new environments. In a laboratory experiment using Drosera capensis, I measured the metabolic response of trap tissue to simulated prey capture, using an omics approach. There was a substantial response to simulated prey capture. More compounds were up-regulated following prey capture than expected (over 30 times more than currently identified across all carnivorous species). In addition, changes in several metabolites suggested that their function is different to that previously reported. The findings of this thesis highlight substantial phenotypic plasticity and intraspecific trait variation as a means for plants to cope with environmental resource availability and variability. Furthermore, it is clear that climate interacts with processes of nutrient availability, hydrology, and subsequent vegetation patterns which means that accurate predictions of species responses to climate change must be highly contextualised to local environments. The findings of this thesis also suggest that secondary metabolites may hold a significant role in the response and survival of plants to changing environments as they have the propensity for plants to adapt at a rate faster than mutation. ii Acknowledgements I would like to extend my thanks to my primary supervisor, Dr Jon Millett, I thank you for your continued professional support and advice, and your belief in me when I first approached you as a PhD candidate. I thank you for your support in this thesis and also in my development as a scientist. To my second supervisor, Dr Dave Ryves, I thank you for your feedback. To Prof Paul Wood, I thank you for your support throughout my PhD–not just as my internal assessor, but for the day-to-day support you provide to myself, other postgraduates and undergraduates studying at Loughborough University. To Prof Adam Hart, I thank you for directing my passion for the natural world into research and your perpetual source of inspiration and aspiration as an academic. I thank the technical support at Loughborough University, in particular Richard Harland. You are always willing and in good spirit to help and without you, aspects of this project would have been considerably more difficult to complete. I give my gratitude to Ulf Sommer, Dr Liam Heaney & Prof Duncan Cameron for advice on metabolomic analyses. Thanks to Angus Davidson for assistance with the drawings for the evolutionary tree. I thank Dr Oliver Preedy for access to the pXRF for tissue analysis and I thank the South West Carnivorous Plants nursery for supplying Drosera capensis for Chapter 5. To my wife, Mrs Sarah Hatcher, I thank you for your unyielding encouragement and tolerance of me. To my parents, Mr Leslie Hatcher and Mrs Jacqueline Hatcher, thank you for your continued support over the years which have made me the person I am today. iii Funding This PhD was funded by a Loughborough University PhD studentship. Stable isotope analysis in Chapters 2 & 3 was funded by the UK Natural Environment Research Council (NERC), through funding to the Life Sciences Mass Spectrometry Facility (LSMSF). Fieldwork was supported in Chapter 3 by Transnational Access funding provided through the European Union H2020 programme as part of the Long-Term Ecosystem Research in Europe (eLTER) project, and by a separate grant from the International Peatland Society. Metabolomic analysis, in Chapter 5, was funded by a NERC grant at the NERC Biomolecular Analysis Facility (NBAF) in Birmingham. Publication At the time of thesis submission, a version of Chapter 4 has been accepted for publication in Annals of Botany. C.R. Hatcher, D.B. Ryves, J. Millett (in press) The function of secondary plant metabolites in plant carnivory. Annals of Botany iv Table of Contents Abstract ................................................................................................................................ i Acknowledgements ........................................................................................................ iii Funding ............................................................................................................................. iv Publication ........................................................................................................................ iv List of tables ....................................................................................................................... x List of figures ................................................................................................................. xiii Preface................................................................................................................................. 1 Chapter 1 Introduction ..................................................................................................... 3 1.1 Carnivorous plants ................................................................................................... 9 1.2 Responses of carnivorous plants to resource availability ................................... 16 1.2.1 Mineral nutrition and responses to nutrient availability ............................. 16 1.2.2 Responses to light ............................................................................................ 20 1.2.3 Responses to water availability ...................................................................... 22 1.3 Secondary metabolites and carnivorous plants ................................................... 25 1.4 Habitats ................................................................................................................... 28 1.5 Plant responses to climate...................................................................................... 31 1.6 Research questions ................................................................................................. 33 1.7 Thesis structure ....................................................................................................... 34 Chapter 2 Phenotypic plasticity in the carnivorous habit of the round-leaved sundew, Drosera rotundifolia, to disturbance ............................................................. 36 v 2.1 Introduction
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