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Ecological and Evolutionary Consequences Of View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by D-Scholarship@Pitt ECOLOGICAL AND EVOLUTIONARY CONSEQUENCES OF PLANT GROWTH ON SERPENTINE SOIL: EFFECTS OF SOIL METALS ON PLANT MORPHOLOGY, METAL ACCUMULATION, PLANT-POLLINATOR INTERACTIONS, AND POLLEN- PISTIL INTERACTIONS by George A. Meindl BS, Humboldt State University, 2007 MA, Humboldt State University, 2009 Submitted to the Graduate Faculty of the Kenneth P. Dietrich School of Arts and Sciences in partial fulfillment of the requirements for the degree of Doctor of Philosophy, Biological Sciences University of Pittsburgh 2014 UNIVERSITY OF PITTSBURGH KENNETH P. DIETRICH SCHOOL OF ARTS AND SCIENCES This dissertation was presented by George A. Meindl It was defended on November 3, 2014 and approved by Dr. Daniel Bain, Dept. of Geology and Planetary Science, University of Pittsburgh Dr. Walter Carson, Dept. of Biological Sciences, University of Pittsburgh Dr. Susan Kalisz, Dept. of Biological Sciences, University of Pittsburgh Dr. Rick Relyea, Dept. of Biological Sciences, University of Pittsburgh Dissertation Advisor: Dr. Tia-Lynn Ashman, Dept. of Biological Sciences, University of Pittsburgh ii Copyright © by George A. Meindl 2014 iii ECOLOGICAL AND EVOLUTIONARY CONSEQUENCES OF PPLANTLANT GROWTH ON SERPENTINE SOIL: EFFECTS OF SOIL METALS ON PLANT MORPHOLOGY, METAL ACCUMULATION, PLANT-POLLINATOR INTERACTIONS, AND POLLEN-PISTIL INTERACTIONS George A. Meindl, PhD University of Pittsburgh, 2014 Edaphic factors are a strong selective force in shaping both plant species distributions and the diversification of many lineages. Specifically, adaptation to novel soil environments can result in species-level changes in floral morphology, phenology, or chemistry, each of which may affect plant reproduction. However, whether floral chemical changes alter plant reproduction following colonization of novel soils is poorly described. In this work, I investigate the effects of soil chemistry on plant chemistry, plant-animal interactions, and pollen-pistil interactions using serpentine-adapted plant species to help determine the effects of the soil chemical environment on plant reproduction and reproductive isolation. I show that (1) plants accumulate soil metals into vegetative and reproductive organs, as well as into pollen and nectar, (2) floral metal accumulation deters generalist pollinators and filters natural pollinator communities, and (3) floral metal accumulation alters pollen grain germination. These findings have important implications for plant reproduction on metal-rich soils. For example, my research has identified two novel mechanisms through which serpentine soil chemistry may foster reproductive isolation between species or populations growing in disparate soil environments. First, floral metal accumulation may result in pollinator filtering. Specifically, closely related plant species occurring in sympatry that differ in floral metal accumulation may become reproductively isolated through reduced pollinator sharing. Second, floral metal accumulation may provide a iv mechanism through which gene flow is reduced between serpentine and non-serpentine populations by altering pollen germination and pollen-pistil compatibility. I found that elevated metal concentrations in the pistils of maternal plants limits pollen tube growth towards ovules in non-adapted species. Furthermore, my results suggest that using metal hyperaccumulating plants in phytoremediation should be considered with caution. While I found that generalist pollinators exhibited decreased visitation to Ni-enriched flowers, they still visited these flowers, and therefore likely ingested a potentially toxic resource. If bioaccumulation of heavy metals occurs in plant-pollinator systems near metal-contaminated soils, pollinator populations may become threatened. This study highlights the influence of the soil environment on plant ecological interactions and plant evolution, and elucidates the role of the edaphic factor on plant reproduction. v TABLE OF CONTENTS PREFACE ............................................................................................................................... XXII 1.0 INTRODUCTION................................................................................................................ 1 2.0 EDAPHIC FACTORS AND PLANT-INSECT INTERACTIONS: DIRECT AND INDIRECT EFFECTS OF SERPENTINE SOIL ON FLORIVORES AND POLLINATORS ........................................................................................................................... 7 2.1 INTRODUCTION ....................................................................................................... 7 2.2 METHODS ................................................................................................................. 10 2.2.1 Study System .................................................................................................. 10 2.2.2 Study Sites ....................................................................................................... 11 2.2.3 Abiotic and Biotic Interactions in Natural Populations ............................. 12 2.2.3.1 Floral display/flower chemistry ......................................................... 12 2.2.3.2 Pollinators ............................................................................................ 13 2.2.3.3 Florivores ............................................................................................. 14 2.2.4 Abiotic and Biotic Interactions for Experimental Plants ........................... 15 2.2.4.1 Floral display/flower chemistry ......................................................... 15 2.2.4.2 Pollinators ............................................................................................ 16 2.2.4.3 Florivores ............................................................................................. 17 2.3 RESULTS ................................................................................................................... 18 vi 2.3.1 Abiotic and Biotic Interactions in Natural Populations ............................. 18 2.3.1.1 Floral display/flower chemistry ......................................................... 18 2.3.1.2 Pollinators ............................................................................................ 18 2.3.1.3 Florivores ............................................................................................. 19 2.3.2 Abiotic and Biotic Interactions for Experimental Plants ........................... 19 2.3.2.1 Floral display/flower chemistry ......................................................... 19 2.3.2.2 Pollinators ............................................................................................ 20 2.3.2.3 Florivores ............................................................................................. 20 2.4 DISCUSSION ............................................................................................................. 21 3.0 NICKEL ACCUMULATION IN LEAVES, FLORAL ORGANS AND REWARDS VARIES BY SERPENTINE SOIL AFFINITY ....................................................................... 42 3.1 INTRODUCTION ..................................................................................................... 42 3.2 METHODS ................................................................................................................. 45 3.2.1 Study system ................................................................................................... 45 3.2.2 Experimental design ...................................................................................... 46 3.2.3 Organ/reward collection and chemical analysis .......................................... 47 3.2.4 Statistical analysis .......................................................................................... 48 3.3 RESULTS ................................................................................................................... 49 3.4 DISCUSSION ............................................................................................................. 50 3.5 CONCLUSIONS ........................................................................................................ 55 4.0 VARIATION IN NICKEL ACCUMULATION IN LEAVES, REPRODUCTIVE ORGANS AND FLORAL REWARDS IN TWO HYPERACCUMULATING BRASSICACEAE SPECIES...................................................................................................... 60 vii 4.1 INTRODUCTION ..................................................................................................... 60 4.2 MATERIALS AND METHODS .............................................................................. 63 4.2.1 Study system ................................................................................................... 63 4.2.2 Experimental design ...................................................................................... 64 4.2.3 Organ/reward collection and chemical analysis .......................................... 65 4.2.4 Statistical analysis .......................................................................................... 66 4.3 RESULTS ................................................................................................................... 67 4.4 DISCUSSION ............................................................................................................. 68 5.0 THE EFFECTS OF ALUMINUM AND NICKEL IN NECTAR ON THE FORAGING BEHAVIOR
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