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Armillaria in Massachusetts Forests: Ecology, Species Distribution, and Population Structure, with an Emphasis on Mixed Oak Forests

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Armillaria in Massachusetts Forests: Ecology, Species Distribution, and Population Structure, with an Emphasis on Mixed Oak Forests University of Massachusetts Amherst ScholarWorks@UMass Amherst Open Access Dissertations 5-13-2011 Armillaria in Massachusetts Forests: Ecology, Species Distribution, and Population Structure, with an Emphasis on Mixed Oak Forests Nicholas Justin Brazee University of Massachusetts Amherst, [email protected] Follow this and additional works at: https://scholarworks.umass.edu/open_access_dissertations Part of the Plant Sciences Commons Recommended Citation Brazee, Nicholas Justin, "Armillaria in Massachusetts Forests: Ecology, Species Distribution, and Population Structure, with an Emphasis on Mixed Oak Forests" (2011). Open Access Dissertations. 402. https://scholarworks.umass.edu/open_access_dissertations/402 This Open Access Dissertation is brought to you for free and open access by ScholarWorks@UMass Amherst. It has been accepted for inclusion in Open Access Dissertations by an authorized administrator of ScholarWorks@UMass Amherst. For more information, please contact [email protected]. ARMILLARIA IN MASSACHUSETTS FORESTS: ECOLOGY, SPECIES DISTRIBUTION, AND POPULATION STRUCTURE, WITH AN EMPHASIS ON MIXED OAK FORESTS A Dissertation Presented by NICHOLAS JUSTIN BRAZEE Submitted to the Graduate School of the University of Massachusetts Amherst in partial fulfillment of the requirement for the degree of DOCTOR OF PHILOSOPHY May 2011 Plant, Soil, and Insect Sciences i © Copyright by Nicholas Justin Brazee 2011 All Rights Reserved ii ARMILLARIA IN MASSACHUSETTS FORESTS: ECOLOGY, SPECIES DISTRIBUTION, AND POPULATION STRUCTURE, WITH AN EMPHASIS ON MIXED OAK FORESTS A Dissertation Presented by NICHOLAS JUSTIN BRAZEE Approved as to style and content by: ________________________________________ Robert L. Wick, Chair ________________________________________ Robert E. Marra, Member ________________________________________ Geunhwa Jung, Member ______________________________________ Matthew J. Kelty, Member _________________________________ Stephen M. Rich, Department Head Department of Plant, Soil, and Insect Sciences iii DEDICATION This work is dedicated to the countless trees that have been killed by Armillaria, for surely the number of deceased is too large to fathom. iv ACKNOWLEDGEMENTS This work would not have been possible without the continued support of Dr. Robert L. Wick. His expertise, interest in the field plant pathology, and sincere desire to educate is an inspiration to all his students. I would like to sincerely thank Dr. Robert E. Marra for all his support during the course of this project. I would also like to thank Dr. Geunhwa Jung and Dr. Matthew J. Kelty for their support. v ABSTRACT ARMILLARIA IN MASSACHUSETTS FORESTS: ECOLOGY, SPECIES DISTRIBUTION, AND POPULATION STRUCTURE, WITH AN EMPHASIS ON MIXED OAK FORESTS MAY 2011 NICHOLAS J. BRAZEE, B.S., UNIVERSITY OF MASSACHUSETTS AMHERST M.S., UNIVERSITY OF WASHINGTON Ph.D., UNIVERSITY OF MASSACHUSETTS AMHERST Directed by: Professor Robert L. Wick The ecology, species distribution, and population structure of Armillaria was investigated in the forests of Massachusetts. From 64 plots at 16 sites, 640 isolates of Armillaria were collected from six forest types (northern hardwoods, mixed oak, pitch pine, white pine, white pine/mixed oak, and eastern hemlock). Armillaria gallica proved to be the most abundant species, making up 316/640 (52%) of all isolations. This was followed by A. solidipes (219/640; 34%), A. mellea (46/640; 7%), A. calvescens (36/640; 6%), A. gemina (16/640; 3%), and A. sinapina (7/640; 1%). Armillaria gallica was routinely encountered causing significant decay of the lower bole on living hardwood hosts, especially oaks. The population structure of 153 isolates of A. gallica collected from mixed oak forests was investigated using amplified fragment length polymorphisms (AFLPs). From a total sampling area of 4.51 ha, 38 AFLP genotypes were discovered, yielding a figure of eight genets per hectare with the average A. gallica genet occupying 0.13 ha. When the effects of hydrolyzable tannins on in vitro growth were compared between A. calvescens and A. gallica, it was A. gallica that appeared better at oxidizing and metabolizing commercial tannins (tannic acid and gallic acid) along with black oak root bark extracts. This was determined through measurements of colony area and dry biomass, and suggests that A. gallica may be a better adapted pathogen of oak. In order to more accurately distinguish between isolates of A. calvescens and A. gallica, a three-gene phylogeny was reconstructed, using partial sequences of the elongation factor 1-alpha (tef1), RNA polymerase II (rpb2) and nuclear large subunit (nLSU) genes. After comparing 12 isolates each of A. calvescens and A. gallica that originated from across northeastern North America, only the tef1 gene could accurately distinguish these two species. Five single nucleotide polymorphisms were present between the two species and maximum likelihood and maximum parsimony methods grouped A. calvescens and A. gallica into monophyletic clades. vi TABLE OF CONTENTS Page ACKNOWLEDGEMENTS ........................................................................................................ v ABSTRACT .............................................................................................................................. vi LIST OF TABLES..................................................................................................................... ix LIST OF FIGURES .................................................................................................................. xii CHAPTER 1. ARMILLARIA SPECIES DISTRIBUTION ON SYMPTOMATIC HOSTS IN NORTHERN HARDWOOD AND MIXED OAK FORESTS IN WESTERN MASSACHUSETTS...................................................................................................... 1 Introduction.................................................................................................................... 1 Materials and Methods ................................................................................................... 3 Site Selection..................................................................................................... 3 Vegetation Sampling and Site Characteristics..................................................... 7 Sampling of Armillaria and Pathogenicity.......................................................... 7 Isolation, PCR, and Sequencing ......................................................................... 8 Statistical Analysis........................................................................................... 10 Results ......................................................................................................................... 11 Vegetation Sampling........................................................................................ 11 Armillaria Species Incidence, Distribution, and Infection Type ........................ 11 Host Preference................................................................................................ 17 Incidence by Crown Class and Soil Drainage Classes....................................... 20 Discussion.................................................................................................................... 21 2. ARMILLARIA SPECIES DISTRIBUTION AND SITE RELATIONSHIPS IN PINUS- AND TSUGA-DOMINATED FORESTS IN MASSACHUSETTS ............................... 27 Introduction.................................................................................................................. 27 Materials and Methods ................................................................................................. 29 Site Selection................................................................................................... 29 Vegetation Sampling, Elevation, Parent Material, and Soils.............................. 34 Sampling and Isolation of Armillaria ............................................................... 35 Identification of Unknown Isolates................................................................... 37 Statistical Analysis........................................................................................... 38 Results ......................................................................................................................... 39 All Forest Types .............................................................................................. 39 Pitch Pine Forest Type ..................................................................................... 44 White Pine & White Pine/Mixed Oak Forest Types.......................................... 44 Eastern Hemlock Forest Type .......................................................................... 46 Site Variables................................................................................................... 48 Discussion.................................................................................................................... 50 All Forest Types .............................................................................................. 50 Pitch Pine Forest Type ..................................................................................... 51 vii White Pine and White Pine/Mixed Oak Forest Types ....................................... 52 Eastern Hemlock Forest Type .......................................................................... 54 3. GENOTYPIC DIVERSITY OF ARMILLARIA GALLICA FROM MIXED OAK FORESTS USING AMPLIFIED FRAGMENT LENGTH POLYMORPHISMS..........
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