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The Cascading Effects of Invasive Sitka Black-Tailed Deer (Odocoileus Hemionus Sitchensis) on the Soils, Plants and Fungal Communities of Haida Gwaii

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The Cascading Effects of Invasive Sitka Black-Tailed Deer (Odocoileus Hemionus Sitchensis) on the Soils, Plants and Fungal Communities of Haida Gwaii THE CASCADING EFFECTS OF INVASIVE SITKA BLACK-TAILED DEER (ODOCOILEUS HEMIONUS SITCHENSIS) ON THE SOILS, PLANTS AND FUNGAL COMMUNITIES OF HAIDA GWAII by DYLAN THOMAS MENDENHALL B.Sc., University of Washington, 2011 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Forestry) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) December 2018 © Dylan Thomas Mendenhall, 2018 The following individuals certify that they have read, and recommend to the Faculty of Graduate and Postdoctoral Studies for acceptance, a thesis entitled: The cascading effects of invasive Sitka black-tailed deer (Odocoileus hemionus sitchensis) on the soils, plants and fungal communities of Haida Gwaii submitted by Dylan Thomas Mendenhall in partial fulfillment of the requirements for the degree of Master of Science in Forestry Examining Committee: Dr. Sue Grayston Chair of Supervisory Committee Dr. Melanie Jones Supervisory Committee Member Dr. Suzanne Simard Supervisory Committee Member Dr. Mary Berbee Non-departmental Examiner ii Abstract In Haida Gwaii, the invasion of Sitka black-tailed deer (Odocoileus hemionus sitkensis) has decreased the abundance and diversity of plant communities, but little is known about their indirect effects on the activity, abundance, diversity and structure of soil fungal communities. In a natural experiment, I compared the edaphic properties, understory plants and soil fungi of deer-invaded and non-invaded islands. Soils on deer-invaded islands had significantly higher penetration resistance, higher phosphate concentrations and lower pH than soil on non-invaded islands. Understory plants on deer- invaded islands had significantly lower cover-abundance, higher species evenness and significant shifts in community composition, largely driven by differences in the abundances of Gaultheria shallon, Polystichum munitum, Lonicera involucrata and Menziesia ferruginea. Ergosterol, a biomarker of fungal biomass, was similar between deer-invaded and non-invaded islands. Illumina sequencing revealed significant differences in the species evenness and composition of the soil fungal community, but similar relative abundances of arbuscular mycorrhizal fungi, ectomycorrhizal fungi, ericoid mycorrhizal fungi and saprotrophic fungi between non-invaded and deer-invaded islands. Differences in the fungal community were significantly correlated with the cover-abundance of understory plants, the depth of the organic horizons, pH and concentrations of ammonium. In a greenhouse bioassay, Thuja plicata seedlings grown in living soils from deer-invaded islands had significantly lower chlorophyll fluorescence values (Fv/Fm), an indicator of plant stress, than seedlings grown in living soil from non-invaded islands, but there were no significant differences in the biomass, root:shoot ratios or the inoculum potential of arbuscular mycorrhizal fungi and dark septate endophytes in Thuja plicata. There were no significant differences in the biomass, root:shoot ratios, Fv/Fm values or inoculum potential of ectomycorrhizal fungi in Tsuga heterophylla grown in soils from deer-invaded and non-invaded islands. Fluorescence-based enzyme assays reveal significantly higher phosphatase activity, lower β-glucosidase and lower cellobiohydrolase activity in soils from deer-invaded islands. Through changes in the physiochemical soil properties and understory plant abundance, Sitka black-tailed deer initiate a cascade of indirect effects on the activity, diversity and composition of the soil fungal community. iii Lay Summary In this study, I investigated the effects of invasive deer on the soils of Haida Gwaii by comparing the plants and soil fungi of invaded and non-invaded islands. I measured plant abundance, soil nutrients, fungal biomass, and used genetic techniques to identify fungal species. I grew trees in the soil to determine the amount of symbiotic fungi colonizing their roots. I also measured the activity of soil enzymes involved with decomposition and nutrient acquisition. I found that invasive deer were associated with differences in the composition of the fungal community. Cedar trees grown in soil from deer-invaded islands had greater stress than those grown in soil from non-invaded islands. Soils from deer-invaded islands had greater enzyme activity associated with nutrient acquisition and less enzyme activity associated with decomposition. In conclusion, invasive deer indirectly alter the soil fungi of Haida Gwaii. iv Preface This thesis represents original, unpublished work by Dylan Thomas Mendenhall. I was responsible for developing the research questions, analyzing the data, and writing the manuscript. The experimental design and field protocols of this study were co-created by Dr. Sue Grayston, Catch Catomeris and me. Soil samples and field data were collected by Dr. Sue Grayston, Dr. Jean-Louis Martin, Catch Catomeris, Dr. Simon Chollet, Morgane Maillard, Maria Continentino, Yonadav Anbar and me. Soil moisture was measured by Maria Continentino, Yonadav Anbar and me. pH was determined by Catch Catomeris, Morgane Maillard and me. Ammonium, nitrate and ergosterol concentrations were determined by the Analytical Chemistry Laboratory of the BC Ministry of Environment and Climate Change Strategy. Phosphate concentrations were determined by me. The results of Chapter 4 were presented at the Society for Ecological Restoration Western Canada Conference in 2018. DNA extraction, initial PCR, DNA quantification and DNA purification were performed by me. Secondary PCR and Illumina sequencing was performed by Dr. Sunita Sinha at the University of British Columbia Sequencing and Bioinformatics Consortium. Dr. David Levy-Booth assisted with the processing of sequencing data through the PIPITS bioinformatics pipeline. The greenhouse bioassay was conducted by Ruby Pyke, Jonathan Zajonc and me. Chlorophyll fluorescence data, microscopy and biomass data were collected by me. The enzyme assays were designed by me, based on methods developed by Beth Brockett. The enzyme assays were conducted by Kate Kourbatova and me. v Table of Contents Abstract .......................................................................................................................................... iii Lay Summary .................................................................................................................................. iv Preface ............................................................................................................................................. v Table of Contents ........................................................................................................................... vi List of Tables .................................................................................................................................... x List of Figures .................................................................................................................................. xv List of Abbreviations and Symbols ................................................................................................ xx Acknowledgements ...................................................................................................................... xxii Dedication.................................................................................................................................... xxiii Chapter 1 – Introduction ................................................................................................................. 1 1.1. Research Overview ............................................................................................................ 1 1.2. Background........................................................................................................................ 2 1.2.1. The Functions and Diversity of Soil Fungi .............................................................. 2 1.2.2. Effects of Herbivores on Plant Communities ......................................................... 4 1.2.3. Effects of Herbivores on Soil Properties ................................................................ 5 1.2.4. Effects of Herbivores on Soil Fungal Communities ................................................ 8 1.2.5. Effects of Herbivores on Soil Microbial Activity ................................................... 13 1.2.6. Methods of Studying Herbivore-Soil Interactions ............................................... 17 1.3. Sitka Black-Tailed Deer on Haida Gwaii ........................................................................... 18 1.4. Research Questions and Objectives ................................................................................ 20 1.5. Thesis Outline .................................................................................................................. 20 Chapter 2 – Study Area and Experimental Design ....................................................................... 22 2.1. Study Area ....................................................................................................................... 22 2.1.1. Islands .................................................................................................................. 22 2.1.2. Browsing History .................................................................................................. 23 2.1.3. Anthropogenic Plant Communities .....................................................................
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