The Ecology of Root Disease Fungi in Missouri Forests
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THE ECOLOGY OF ROOT DISEASE FUNGI IN MISSOURI FORESTS _______________________________________ A Dissertation presented to the Faculty of the Office of Graduate Studies at the University of Missouri-Columbia _______________________________________________________ In Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy _____________________________________________________ by CHRISTOPHER A. LEE Dr. Rose-Marie Muzika, Dissertation Supervisor MAY 2016 The undersigned, appointed by the dean of the Graduate School, have examined the dissertation entitled THE ECOLOGY OF ROOT DISEASE FUNGI IN MISSOURI FORESTS presented by Christopher A. Lee, a candidate for the degree of doctor of philosophy, and hereby certify that, in their opinion, it is worthy of acceptance. Rose-Marie Muzika, PhD James English, PhD John Kabrick, PhD Ricardo Holdo, PhD ii ACKNOWLEDGEMENTS Many people gave generously of their time and expertise to help bring these studies to completion. I deeply appreciate their assistance. First among these are my advisor, Rose-Marie Muzika, and my graduate committee: Jim English, Rico Holdo, and John Kabrick. Johann Bruhn and Sharon Reed were also crucial to the development of the skills and the provision of information needed for these projects. I also thank everyone else at the University of Missouri and other institutions who shared their time, energy, and resources with me. These folks include the following: Debbie Allen Andres Rodrigues Peyton Bennett Jim Schoelz Sharon Burnham Mike Stambaugh Laura Conners Glen Stanosz Dan Dey Christine Steinwand Michelle Dobrowolski Susan Taylor Dave Haenke Nathan Weber Mark Hannink Lizzie Wright Jered Hayes Simeon Wright Kevin Hosman Yu Zhang Jason Hubbart LAD Foundation Chad King Mark Twain National Forest Joe Marschall Missouri Dept of Conservation Scott McWilliams Alford Forest Jeanne Mihail University of Missouri Life Sciences Lee Miller Program & Fellowship Tex Nall USDA Forest Service Northern Stephen Pallardy Research Station Patty Quackenbush University of Missouri Research Bob Rives Council iii TABLE OF CONTENTS ACKNOWLEDGEMENTS ................................................................................................ ii LIST OF ILLUSTRATIONS ............................................................................................. iv LIST OF TABLES ............................................................................................................. vi Chapter 1. GENERAL INTRODUCTION .................................................................................1 2. DISTRIBUTION OF HETEROBASIDION IRREGULARE IN MISSOURI PINE- OAK FORESTS .................................................................................................11 3. PATTERNS OF ARMILLARIA GALLICA OCCURRENCE AND ITS RELATIONSHIP TO TREE MORTALITY IN A CENTRAL MISSOURI HARDWOOD FOREST ....................................................................................41 4. OAK STUMP-SPROUT VIGOR AND ARMILLARIA INFECTION AFTER CLEARCUTTING .............................................................................................81 APPENDICES A. LIST OF TREE SPECIES ON STUDY PLOTS AT BASKETT RESEARCH AND EDUCATION AREA .............................................................................120 B. PLANT SENESCENCE FOR ECOLOGISTS: PRECISION IN CONCEPT, SCALE, AND TERMINOLOGY ....................................................................122 C. TREE ARCHITECTURE AS A PREDICTOR OF GROWTH AND MORTALITY AFTER AN EPISODE OF RED OAK DECLINE IN THE OZARK HIGHLANDS OF MISSOURI, USA ................................................140 VITA ................................................................................................................................179 iv LIST OF ILLUSTRATIONS Chapter 2 Figure Page 1. Missouri survey sites for Heterobasidion irregulare ...............................................32 2. Photos of example surveyed landscapes ..................................................................33 3. Shortleaf pine distribution in two example Missouri landscapes .............................34 4. Heterobasidion irregulare signs detected at Missouri survey sites .........................35 5. Plot of summed distances between cfu deposition rate at each pine-disk spore trap and all stumps within the plot (Clearwater 2 site) ...............................................36 Chapter 3 Figure Page 1. Mean diameters (cm) of live and dead tree stems by plot age ..................................74 2. Examples of fungi found on Cornus florida baits after one year of burial ...............75 3. Single most highly supported mortality models for individual plots with Akaike weights indicating level of support .....................................................................76 4. Correlograms displaying spatial autocorrelation of logistic regression residuals in 5- m distance classes for plot B4 ...........................................................................77 Chapter 4 Figure Page 1. Comparison of numbers of living sprouts between Armillaria-infected (positive) and uninfected (negative) stumps in 2012 ...............................................................114 2. Numbers of living sprouts on stumps in 2006 by parent tree diameter at breast height (dbh) (measured one year earlier) ..........................................................115 3. Relationship between numbers of sprouts and dominant sprout dbh in 2012 ......... 116 v 4. Relationship between change in size of largest sproutless gap around stump circumference ................................................................................................. 117 5. Examples of Armillaria signs and symptoms observed on oak stumps in Missouri clearcuts ...........................................................................................................118 vi LIST OF TABLES Chapter 2 Table Page 1. List of sites surveyed with basic characteristics ........................................................37 2. Candidate models to explain pathogen detection probability (i.e., likelihood of pathogen presence) ............................................................................................39 3. Candidate models to explain spore deposition rate within plots...............................40 Chapter 3 Table Page 1. Mean characteristics of estimated predictor variables by plot age ............................78 2. Average stand density parameters and fungal detections in plots .............................79 3. Single most highly supported mortality models for individual plots with Akaike weights indicating level of support .....................................................................80 Chapter 4 Table Page 1. Armillaria species recovered at study site one year after clearcutting ....................119 1 General Introduction Roots are essential to tree life and yet only dimly understood; they are a huge part of every tree’s mass and yet almost impossible to explore. Tree climbers can now map in their wholeness the intricacies of giant, ancient tree crowns 350 feet above the ground, but the seasonal turnover of fine root networks on those same trees must still be inferred from partial observation and sampling. The same climbers are fetching and photographing examples of a high-rise ecosystem we had no idea existed twenty years ago, including entire expanses of well-developed soil and “terrestrial” animal species living their life cycles in the tree crowns; meanwhile, we have cataloged only a tiny part of the species from all the kingdoms of life that live in and near those trees’ roots. Roots and the soil surrounding them compose milieux that are resistant to study because, like the interiors of trees, they are in some sense sealed systems, so that disturbing them breaks their continuity—but also because they are rich in numbers of individuals and diversity of species. Both helped and hindered by the other species that share the soil with them, roots serve a myriad of essential functions for trees. They hold trees in the ground. They forage for water deep in the soil profile as well as horizontally through the upper layers of the forest floor, competing with the root networks of neighboring trees for this important resource just as stems and crowns help the tree compete for sunlight. Likewise, they gather scarce mineral nutrients from the soil territories they claim. Roots can stay alive when the tree stem dies, producing adventitious shoots that develop into new tree crowns, providing the tree with continuity through many cycles of forest disturbance and development and affording some tree species a longevity that we cannot estimate with 2 much precision. While performing all these functions, roots at the same time offer an incredibly large and exposed surface area to resident soil organisms, some of which, like mycorrhizas, integrate themselves into the life of roots in mutualistic symbiosis, while others take advantage of root physiology and the peculiarities of root developmental processes to enter the tree and begin the process of colonizing the living and dead tissue within it. The latter organisms cause root diseases. Organisms from many kingdoms of life cause these diseases, including viruses, bacteria, fungi, nematodes, vertebrate animals, other plants, and many miscellaneous organisms such as oomycetes and other protists (Agrios 2005). Many of these disease-causing organisms have important and long-lasting impacts on Missouri tree species. One