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Cause and Impacts of the Early Season Collapse of Lilium Grayi (Gray’S Lily), on Roan Mountain, TN/ NC Russell J

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Cause and Impacts of the Early Season Collapse of Lilium Grayi (Gray’S Lily), on Roan Mountain, TN/ NC Russell J East Tennessee State University Digital Commons @ East Tennessee State University Electronic Theses and Dissertations Student Works 8-2013 Cause and Impacts of the Early Season Collapse of Lilium grayi (Gray’s lily), on Roan Mountain, TN/ NC Russell J. Ingram East Tennessee State University Follow this and additional works at: https://dc.etsu.edu/etd Part of the Botany Commons, Plant Pathology Commons, and the Population Biology Commons Recommended Citation Ingram, Russell J., "Cause and Impacts of the Early Season Collapse of Lilium grayi (Gray’s lily), on Roan Mountain, TN/NC" (2013). Electronic Theses and Dissertations. Paper 1190. https://dc.etsu.edu/etd/1190 This Thesis - Open Access is brought to you for free and open access by the Student Works at Digital Commons @ East Tennessee State University. It has been accepted for inclusion in Electronic Theses and Dissertations by an authorized administrator of Digital Commons @ East Tennessee State University. For more information, please contact [email protected]. Cause and Impacts of the Early Season Collapse of Lilium grayi (Gray’s lily), on Roan Mountain, TN/NC ____________________________ A thesis Presented to the faculty of the Department of Biological Sciences East Tennessee State University In partial fulfillment of the requirements for the degree Master of Science in Biology ____________________________ by Russell Jackson Ingram August 2013 ____________________________ Foster Levy, Ph.D.- Chair Jamey Donaldson, M.S. Aruna Kilaru, Ph.D. Timothy McDowell, Ph.D. Alan Windham, Ph.D. Keywords: Pseudocercosporella inconspicua, Lilium grayi, Gray’s lily, epidemiology, natural populations, spatial patterns, disease association, lily leaf spot ABSTRACT Cause and Impacts of the Early Season Collapse of Lilium grayi (Gray’s lily), on Roan Mountain, TN/NC by Russell Jackson Ingram A population of the rare Southern Appalachian endemic species Lilium grayi, (Gray’s lily) Roan Mountain, TN/NC was monitored for 2 years to determine the cause and impact of an early season collapse. High concentrations of the Lilium spp. host-specific fungal phytopathogen, Pseudocercosporella inconspicua (G. Winter) U. Braun were associated with 19/20 symptomatic and 0/30 asymptomatic plants. Strength of the association between pathogen and disease and the replication of disease symptoms in 4/4 healthy hosts showed that P. inconspicua was the causal agent of the disease referred to as lily leaf spot. Disease had a severe impact on the population with 59% of mature and 98% of adolescent plants undergoing early senescence. Only 32% of mature plants produced capsules and they were frequently diseased. A recurring spatiotemporal pattern typical of an infectious disease suggested that the lily leaf spot disease is capable of causing sequential annual epidemics of unknown long-term consequences to the stability of the host population. 2 Copyright 2013 by Russell J. Ingram All Right Reserved 3 DEDICATION This Thesis is Dedicated To: The memory of my father, Robert Jackson Ingram Jr., I hope I have made you proud. To my grandmother, Minette Cass Hatcher, whose unwavering love was the light by which I walked for so many years. Words cannot express how grateful I am. To my grandfather, Jack Bell Hatcher, whose passion for horticulture helped me find the path to happiness. You may not know it but you are the example by which I follow. To my mother, Elizabeth Sue Ingram, who taught me to strive for greatness. You taught me to never settle and most importantly, to never give up. 4 ACKNOWLEDGEMENTS I would like offer my sincerest gratitude to my advisor Dr. Foster Levy. Your passion for learning and commitment to science will continue to inspire my efforts for years to come. “The mediocre teacher tells. The good teacher explains. The superior teacher demonstrates. The great teacher inspires.” ― William Arthur Ward I would like to offer my deepest thanks to my undergraduate advisor and friend, Dr. Stacy Bennetts. You believed in me before I could. I would like to offer my deepest thanks to my undergraduate professor and friend, Dr. Donna Wear. “The journey of a thousand miles begins with a single step.” ― Lao Tzu Thank you for helping me to take that first step. I would like to acknowledge the work of committee member, Jamey Donaldson. Your years of research conducted on Roan Mountain were the impetus for this research. Thank you for sharing your wealth of botanical and ecological experience and I wish you many more happy years on Roan. I would also like to thank Dr. Alan Windham and Dr. Mark Windham for their generosity and guidance. Without their expertise in the field of plant pathology, much of this research would not have been possible. 5 TABLE OF CONTENTS Page ABSTRACT……………………………………………………………………………… 2 LIST OF TABLES………………………………………………………………………... 11 LIST OF FIGURES………………………………………………………………………. 14 Chapter 1. INTRODUCTION………………………………………………………………... 16 History of the Early Season Collapse of Lilium grayi on Roan Mountain TN/NC 16 Determination of the Causes of Plant Disease…………………………………... 24 Fungal Disease in Natural Populations………………………………………...... 30 Factors Affecting Disease Outbreak in Natural Plant Populations…………….... 33 Disease Assessment: Factors Affecting the Severity of Disease in Plant Hosts... 35 Factors Affecting the Impact of Disease in Natural Plant Populations…………. 37 Statement of Purpose…………………………………………………………..... 39 2. METHODS………………………………………………………………………... 40 Symptomatology of the Early Season Collapse of Lilium grayi……………….... 40 Diagnosis of the Candidate Pathogen, Pseudocercopsorella inconspicua…….... 45 Cultivation of the Host, Lilium grayi, Gray’s Lily…………………………….... 46 Culture of the Pathogen, Mycosphaerella martagonis, (Anamorph: Pseudocercosporella inconspicua)………………………………… 46 Isolation of the Fungal Pathogen, Pseudocercosporella inconspicua, from Diseased Host Tissue……………………………………………………………. 47 6 Chapter Page Viral Testing of Diseased Lilium grayi……………………………………......... 49 Measuring Background Levels of Pseudocercosporella inconspicua Conidia: Conidial Baseline Study……………………………………………………….... 50 Association of the Pathogen, Pseudocercosporella inconspicua, with the Symptoms of the Early Season Collapse of Lilium grayi..................................... 51 Reproducing the Symptoms of the Early Season Collapse: Inoculation of Healthy Hosts within the Field…………………………………………………. 53 Investigation of the Impacts of the Early Season Collapse on Nonreproductively Mature Lilies……………………………………………… 54 Investigation of the Impacts of the Early Season Collapse on Reproductively Mature Lilies…………………………………………………... 57 Investigation of the Impact of Pseudocercosporella inconspicua on Seed Viability of Lilium grayi………………………………………………………... 61 3. RESULTS……………………………………………………………………………... 64 Diagnosis of the Candidate Pathogen, Pseudocercosporella inconspicua……... 64 Isolation of the Fungal Pathogen, Pseudocercosporella inconspicua, from Diseased Host Tissue…………………………………………………………… 64 Viral Testing of Diseased Lilium grayi……………………………………….... 65 Measuring Background Levels of Pseudocercosporella inconspicua Conidia: Conidial Baseline Study……………………………………………………….. 65 Association of the Pathogen, Pseudocercosporella inconspicua, with the Symptoms of the Early Season Collapse of Lilium grayi …………………….. 66 7 Chapter Page Reproducing the Symptoms of the Early Season Collapse: Inoculation of Healthy Hosts within the Field……………………………….... 68 Investigation of the Impacts of the Early Season Collapse on Nonreproductively Mature Lilies…………………………………………….... 70 Investigation of the Impacts of the Early Season Collapse on Reproductively Mature Lilies…………………………………………………... 77 Investigation of the Impact of Pseudocercosporella inconspicua on Seed Viability of Lilium grayi……………………………………………………….. 96 4. DISCUSSION………………………………………………………………………... 98 Determination of the Causal Organism of the Early Season Collapse of Lilium grayi...................................................................................................... 98 Epidemiology of the Lily Leaf Spot Disease...................................................... 103 Impact of Disease on Host Survivorship............................................................. 109 Impact of Disease on Host Reproduction........................................................... 110 Impact of Disease on Host Recruitment............................................................. 112 Conclusions……………………………………………………………………. 113 REFERENCES………………………………………………………………………….. 115 APPENDICES…………………………………………………………………………... 123 Appendix A: Results of the Correlation Analysis of Lily Morphological Traits, Capsule Production, Browsed Status, Reproductive Damage by Disease, and Plant Location………………………………………………………………….. 123 8 Chapter Page Appendix B: Results of the Correlation Analysis of Disease Severity, Browsed Status, Reproductive Damage by Disease, Capsule Production, and Plant Location (x-coordinate)………………………………………………………… 124 Appendix C: Reproductively Mature Gray’s Lily Demographic and Disease Severity Data Collected During 2011………………………………………….. 125 Appendix D: Reproductively Mature Gray’s Lily Demographic and Disease Severity Data Collected During 2012………………………………………….. 129 Appendix E: Nonreproductively Mature Lily Demographic and Disease Severity Data Collected in 2011………………………………………………... 134 Appendix F: Nonreproductively Mature Lily Demographic and Disease Severity Data Collected in 2012………………………………………………... 138 Appendix G: Morphological Diagnosis of P. inconspicua: Measurements of
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