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The Pennsylvania State University The Pennsylvania State University The Graduate School Department of Plant Pathology and Environmental Microbiology VERTICILLIUM NONALFALFAE: A POTENTIAL BIOLOGICAL CONTROL OF THE INVASIVE AILANTHUS ALTISSIMA IN PENNSYLVANIA A Dissertation in Plant Pathology by Matthew Kasson 2012 Matthew Kasson Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy December 2012 The dissertation of Matt Kasson was reviewed and approved* by the following: Donald D. Davis Professor of Plant Pathology Dissertation Advisor Chair of Committee David Geiser Professor of Plant Pathology Fredrick Gildow Professor of Plant Pathology Daniel Royse Professor of Plant Pathology Michael Saunders Professor of Entomology *Signatures are on file in the Graduate School iii ABSTRACT In this dissertation I had three main objectives. The first was to utilize tree ring analysis, historic records to better understand the history, distribution, spatiotemporal spread, and growth patterns of the invasive Ailanthus altissima (tree-of-heaven) as a means of explaining why naturally occurring Verticillium wilt epidemics have only recently developed in PA despite a long history of colonization by Ailanthus. Furthermore these investigations sought to provide answers to fundamental questions regarding the biology of Ailanthus such as maximum age at which seed production occurs and maximum lifespan, both of which ultimately affect the management of the species. Second, I carried out a series of multi-year experiments to better understand two separate aspects of Verticillium wilt of Ailanthus: efficacy of Verticillium nonalfalfae as a biocontrol agent against the target host, and intra-specific resistance that may be present within established populations in the U.S. that ultimately would affect large scale use of this potential bioncotrol. Host range studies sought to clarify and expand preliminary host-range testing, and also test whether V. nonalfalfae isolate VnAa140 was host-adapted. Finally, I sought to investigate the role of the unbiquitous exotic ambrosia beetle, Euwallacea validus, which attacks declining Ailanthus trees throughout the study area. The latter studies sought to assess what role, if any, the mycangial fungi of these beetles had on tree health and disease progression, as well as clarifying phylogentic relationships of their mycangial fungi. iv TABLE OF CONTENTS List of Figures……………………………………………………………………………….vii List of Tables…………………………………………………………………………………ix List of Appendices……………………………………………………………………………x Chapter 1 The Invasive Ailanthus altissima in Pennsylvania: a Case Study Elucidating Species Introduction, Migration, Invasion, and Growth Patterns in the Northeastern U.S. ..........1 Introduction .................................................................................................................2 Early introductions and observations of Ailanthus in the Northeast .......................2 Comercialization of Ailanthus...............................................................................6 Intra-state migration, proliferation, and growth of Ailanthus in PA........................7 Invasion of PA forests ..........................................................................................9 Persistence of Ailanthus on the landscape .............................................................10 Research objectives ..............................................................................................11 Methods .......................................................................................................................12 Study area ............................................................................................................12 Dendrochronology ................................................................................................12 Age prediction for Ailanthus .................................................................................14 Ailanthus floristic surveys ....................................................................................16 Results .........................................................................................................................17 Tree-ring data .......................................................................................................17 Growth responses and patterns in Ailanthus ..........................................................19 Age prediction for Ailanthus .................................................................................22 Ailanthus floristic field surveys ............................................................................24 Discussion ...................................................................................................................25 Feasability of using Ailanthus in tree-ring studies .................................................25 From cultivation to widespread invasion: a spatiotemporal timeline for Ailanthus .31 Impacts of contemporary and future disturbances on expansion of Ailanthus in PA and beyond ..........................................................................................................36 Conclusions ..........................................................................................................39 Acknowledgements ..............................................................................................40 Literature cited .............................................................................................................41 Appendices ..................................................................................................................85 Chapter 2 Verticillium wilt of Ailanthus altissima by Verticillium nonalfalfae: efficacy and intra- specific resistance screening.........................................................................................94 Introduction .................................................................................................................95 Materials and methods .................................................................................................98 Study area ............................................................................................................98 Fungal isolates, culture maintenance and inoculum preparation.............................98 2006-2009 Ailanthus canopy tree inoculations ......................................................100 Long-term effects of V. nonalfalfae VnAa140 on future Ailanthus establishment and survivorship ..................................................................................................102 Screening A. altissima selections for susceptibility to V. nonalfalfae VnAa140 .....103 v Statistical analyses ................................................................................................105 Results .........................................................................................................................106 Molecular characterization....................................................................................106 2006-2009 Ailanthus canopy tree inoculations ......................................................106 Long term effects on VnAa140 on future Ailanthus survival and establishment .....109 Screening A. altissima selections for tolerance to V. nonalfalfae Isolate VnAa140 111 Discussion ...................................................................................................................113 Literature cited .............................................................................................................121 Chapter 3 Expanded host range testing of Verticillium nonalfalfae from Ailanthus altissima 143 Introduction .................................................................................................................144 Materials and methods .................................................................................................147 Study area ............................................................................................................147 Species selection and stand criteria for non-target species testing ..........................148 Fungal isolates, culture maintenance, and inoculum preparation ............................149 Field evaluations of previous 2007 field inoculations of non-target species ...........150 Field evaluations of non-target species in 2009-2010 ............................................151 2010 greenhouse inoculations of potted non-target species ....................................153 Incidence of Verticillium wilt of non-target species in Ailanthus-inoculated forest stands ...........................................................................................................155 Effect of wilt and vascular discoloration on incremental growth ............................155 Statistical analyses ................................................................................................157 Results .........................................................................................................................158 Field evaluation of previous 2007 field inoculations of on-target species...............158 Field inoculations of non-target species in 2009-2010 ...........................................159 2010 greenhouse inoculations of potted non-taget species .....................................163 Incidence of wilt on no-target species in Ailanthus-inoculated forest stands ..........164 Effect of wilt and vascular discoloration
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