Patterns and Impact of Herbivory by a Biological Control Insect on Its Target Weed and a Native Nontarget Plant
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PATTERNS AND IMPACT OF HERBIVORY BY A BIOLOGICAL CONTROL INSECT ON ITS TARGET WEED AND A NATIVE NONTARGET PLANT by HALEY AUTUMN CATTON Bachelor of Science, University of Manitoba, 2001 Master of Science, University of Manitoba, 2005 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE COLLEGE OF GRADUATE STUDIES (Biology) THE UNIVERSITY OF BRITISH COLUMBIA (Okanagan) April 2014 © Haley Autumn Catton, 2014 ABSTRACT Classical biological control (biocontrol) of weeds involves importing foreign, host- specific insects with the intent of reducing the fitness of invasive plants in their introduced range. When anticipated risks to nontarget species are low, insects capable of feeding and developing on some native nontarget plants have been given regulatory approval for release. In this thesis, I study patterns and impacts of herbivory by the root- feeding weevil Mogulones crucifer on its target weed Cynoglossum officinale and a native nontarget plant Hackelia micrantha. I released large numbers of M. crucifer into naturally-occurring patches of H. micrantha growing with or without C. officinale to simulate a ‘worst case’ scenario of high insect density and low target plant density, and subsequently recorded herbivory patterns and plant demographic parameters for two years on release and non-release sites. Additionally, I collected oviposition data from non-experimental sites 0-4 years after M. crucifer release. Compared to the target weed, H. micrantha use by M. crucifer was temporary, rare, mild, and limited to immediately around release points, suggesting that the nontarget plant is buffered from population- level effects by spatial, temporal and probabilistic refuges from biocontrol herbivory. M. crucifer did not persist 2 years after release in the absence of C. officinale, indicating that the insect is limited to ‘spillover’ nontarget use. A separate mark-release-recapture experiment indicated that M. crucifer has reduced host-finding behaviours for its novel host compared to its evolutionary host. Plant demographic data indicated that outbreak densities of M. crucifer appeared to impact C. officinale populations by increasing rosette mortality. While there was some evidence of impact to individual H. micrantha plants immediately adjacent to release points (i.e., plant death or dieback of flowering shoots), these effects did not translate to the population level. I synthesize this information to suggest why M. crucifer has been an effective biocontrol agent against C. officinale in Canada, and why H. micrantha is unlikely to incur population-level effects from the weevil. This study is a clear example of how nontarget use of individual plants can be noticeable yet not have population-level implications, and demonstrates the importance of post-release research in weed biocontrol. ii PREFACE The research in this dissertation was designed, performed, analyzed and written by me, Haley Catton, in collaboration with my supervisory committee Drs. Robert Lalonde, Rosemarie De Clerck-Floate, Karen Hodges, Jason Pither, and Rebecca Tyson. Data were collected with the help of field research assistants Jordan Bannerman, William Van Der Weide, Shelby McLeod and Karma Tiberg. Statistical analysis of the demographic data in Chapter 4 was supervised by Prof. Yvonne Buckley (formerly of the University of Queensland and the Commonwealth Scientific and Industrial Research Organisation, Brisbane, Australia, and currently of Trinity College Dublin, Ireland). iii TABLE OF CONTENTS ABSTRACT…………………………………………………………………...…………ii PREFACE…………………………………………………………………...………..…iii TABLE OF CONTENTS….…………………………………………………………….iv LIST OF TABLES………………………………………………………………………vi LIST OF FIGURES……………………………………………………………………..vii ACKNOWLEDGMENTS………...……………………………………………………..ix DEDICATION…………………………………………………………………………..xi CHAPTER 1: Introduction: benefits, risks and challenges regarding classical biological control of weeds………………………………………………………1 1.1. Invasive plants and biological control……………………………………....1 1.2. Nontarget use…………………………………………………….......……...2 1.3. Challenges in studying impact of biocontrol agents………………………..4 1.4. Study system………………………………………………………………...6 1.5. Thesis overview………………………………………………………….......8 CHAPTER 2: Intensity and temporal patterns of M. crucifer herbivory on target and nontarget plants……………………………………………………………..10 2.1. Literature review and objectives…………………………………………..10 2.2. Methods……………………………………………………………………15 2.2.1. Study system……………………………………………………..15 2.2.2. Rangeland experiment (visual use assessments and destructive sampling)……………………………………………………......15 2.2.3. Non-experimental release sites…………………………………..17 2.2.4. Data analysis……………………………………………………..18 2.3. Results……………………………………………………………………..19 2.3.1. Visual indications of use……………………………………..….19 2.3.2. Destructive sampling and dissections……………………………20 2.4. Discussion……………………………………………………………….....22 CHAPTER 3: Differential within-patch target and nontarget use following M. crucifer releases: spatial patterns and underlying mechanisms…...………...33 3.1. Literature review and objectives……………………………………….….33 3.2. Methods……………………………………………………………………37 3.2.1. Study system…………………………………………………......37 3.2.2. Rangeland experiment…………………………………………...38 3.2.3. Mark-release-recapture experiment……………………………...39 3.2.4. Data analysis…………………………………………………......41 iv 3.3. Results……………………………………………………………………..43 3.3.1. Rangeland Experiment…………………………………………..43 3.3.2. Mark-release-recapture experiment……………………………...44 3.4. Discussion………………………………………………………………....47 CHAPTER 4: Individual and population-level impacts to target and nontarget plants following M. crucifer release…………………………………………………...56 4.1. Literature review and objectives…………………………………………..56 4.2. Methods……………………………………………………………………60 4.2.1. Study system……………………………………………………..60 4.2.2. Rangeland release experiment…………………………………...62 4.2.3. Seedling emergence experiment…………………………………65 4.2.4. Analysis of weevil impact to vital rates......……………………..66 4.2.5. Transition matrix construction, parameterization, and analysis…67 4.3. Results……………………………………………………………………..69 4.3.1. C. officinale dynamics…………………………………………...70 4.3.2. H. micrantha dynamics………………………………………….71 4.3.3. Effect of distance from release points…………………………...72 4.3.4. Use scars as indicators of demographic impact………………….73 4.4. Discussion………………………………………………………………....74 4.4.1. Impact of M. crucifer on C. officinale…………………………...75 4.4.2. Impact of M. crucifer on H. micrantha………………………….78 4.4.3. Implications for impact monitoring……………………………...81 CHAPTER 5: Conclusions: implications of M. crucifer herbivory patterns and demographic effects………………..………………………………………….108 5.1. Why M. crucifer has been an effective biocontrol agent against C. officinale in Canada…………………………………………………...111 5.2. Reasons for lack of effect of M. crucifer on H. micrantha populations….112 5.3. Management recommendations………………………………………..…113 5.4. Future work……………………………………………………………....115 5.4.1. Refining and expanding population models………………...….115 5.4.2. Further exploration of M. crucifer herbivory effects on individual plants……………………….……………………....117 5.4.3. Investigating potential changes in M. crucifer host preference and performance……….……………………………………....119 5.5. Final thoughts…………………………………………………………….120 REFERENCES CITED………………………………………………………………..122 APPENDICES…………………………………………………………………………138 APPENDIX A: Plant fecundity calculations………………………………….138 APPENDIX B: Calculating upper and lower parameter boundaries from the seedling emergence experiment………………………...140 APPENDIX C: Individual site demographic parameters…...………………...145 v LIST OF TABLES Table 2.1. Numbers of M. crucifer eggs and larvae found in C. officinale and H. micrantha plants.…………………………………………………………..28 Table 4.1. Symbols and definitions for annual probability and fecundity parameters used in matrix models.………………………………...…………………..84 Table 4.2. Annual transition values for C. officinale on sites grouped by M. crucifer releases…………………………………………………………...85 Table 4.3. Annual transition values for H. micrantha on sites grouped by M. crucifer releases and abundance of C. officinale (“target common” and “target rare”)………….…………………………………………………...86 Table A.1. Sources of the values of the number of tetrads per bolting stems used for calculating plant fecundity values……..…………………………………139 Table B.1. Parameter values for C. officinale and H. micrantha seed and seedling dynamics………..…………………………………………………….…..143 Table C.1. Overall C. officinale rosette and bolting transitions for each site-year combination...…………………………………………………………….146 Table C.2. Overall H. micrantha rosette and bolting transitions for each site-year combination...…………………………………………………………….149 vi LIST OF FIGURES Figure 2.1. Probabilities of C. officinale and H. micrantha plants exhibiting M. crucifer use scars 0, 1, and 2 years after weevil release in the rangeland experiment……………………………………...……………...29 Figure 2.2. Frequency and intensity of M. crucifer colonization with varying plant size in C. officinale and H. micrantha …………….……………………...30 Figure 2.3. Frequency and intensity of M. crucifer colonization in H. micrantha in relation to site-level colonization in C. officinale ………...……………...31 Figure 2.4. Probabilities of C. officinale and H. micrantha being colonized by at least one M. crucifer egg or larva when displaying above-ground use scars…………………………………………………………..…………...32 Figure 3.1. Schematic diagram of mark-release-recapture experiment....………….....52 Figure 3.2. Within-patch