Overcoming the Challenges of Tamarix Management with Diorhabda Carinulata Through the Identification and Application of Semioche

OVERCOMING THE CHALLENGES OF TAMARIX MANAGEMENT WITH DIORHABDA CARINULATA THROUGH THE IDENTIFICATION AND APPLICATION OF SEMIOCHEMICALS by Alexander Michael Gaffke A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Ecology and Environmental Sciences MONTANA STATE UNIVERSITY Bozeman, Montana May 2018 ©COPYRIGHT by Alexander Michael Gaffke 2018 All Rights Reserved ii ACKNOWLEDGEMENTS This project would not have been possible without the unconditional support of my family, Mike, Shelly, and Tony Gaffke. I must thank Dr. Roxie Sporleder for opening my world to the joy of reading. Thanks must also be shared with Dr. Allard Cossé, Dr. Robert Bartelt, Dr. Bruce Zilkowshi, Dr. Richard Petroski, Dr. C. Jack Deloach, Dr. Tom Dudley, and Dr. Dan Bean whose previous work with Tamarix and Diorhabda carinulata set the foundations for this research. I must express my sincerest gratitude to my Advisor Dr. David Weaver, and my committee: Dr. Sharlene Sing, Dr. Bob Peterson and Dr. Dan Bean for their guidance throughout this project. To Megan Hofland and Norma Irish, thanks for keeping me sane. iii TABLE OF CONTENTS 1. INTRODUCTION ...........................................................................................................1 Tamari x............................................................................................................................1 Taxonomy ................................................................................................................1 Introduction and Spread...........................................................................................2 Biology.....................................................................................................................3 Ecology ....................................................................................................................6 Impacts.....................................................................................................................8 Control ...................................................................................................................12 Classical Biological Control ..................................................................................13 Diorhabda carinulata ....................................................................................................14 Evaluation and Selection........................................................................................14 Life Cycle...............................................................................................................16 Dispersal ................................................................................................................19 Release and Establishment.....................................................................................20 Impacts on Tamarix ...............................................................................................21 Challenges and Conflicts .......................................................................................23 Chemical Ecology and Insects.......................................................................................29 Semiochemicals in the D. carinulata/Tamarix System .................................................33 Use of Semiochemicals to Resolve Challenges and Conflicts with D. carinulat a........35 References......................................................................................................................41 2. SEMIOCHEMICALS TO ENHANCE HERBIVORY BY DIORHABDA CARINULATA AGGREGATIONS IN SALTCEDAR (TAMARIX SPP.) INFESTATIONS ...........................................................................................................62 Contribution of Authors and Co-Authors ......................................................................62 Manuscript Information Page ........................................................................................64 Abstract..........................................................................................................................65 Introduction....................................................................................................................65 Materials and Methods...................................................................................................66 Field Experiment Location and Insect Source.......................................................66 Lure and Chemicals ...............................................................................................66 Release Rate Analysis............................................................................................67 Field Study.............................................................................................................67 Statistical Analysis.................................................................................................68 Results............................................................................................................................68 Release Rate Analysis............................................................................................68 Field Study.............................................................................................................68 High-density Site Reproductive Adult Response ......................................68 Low-density Site Reproductive Adult Response .......................................68 iv TABLE OF CONTENTS CONTINUED High-density Site Non-reproductive Adult Response................................68 Low-density Site Non-reproductive Adult Response ................................68 High-density Larval Response...................................................................69 Low-density Larval Response....................................................................69 High-density Damage Rating.....................................................................69 Low-density Damage Rating .....................................................................69 Dieback Rating...........................................................................................70 Canopy Volume Measurements.................................................................70 Discussion......................................................................................................................70 Conclusion .....................................................................................................................73 Acknowledgements........................................................................................................73 Supplemental Material...................................................................................................73 References......................................................................................................................73 3. FIELD DEMONSTRATION OF A SEMIOCHEMICAL TREATMENT THAT ENHANCES DIORHABDA CARINULATA BIOLOGICAL CONTROL OF TAMARIX SPP. ....................................................................................75 Contribution of Authors and Co-Authors ......................................................................75 Manuscript Information Page ........................................................................................77 Abstract..........................................................................................................................79 Introduction....................................................................................................................80 Materials and Methods...................................................................................................84 Field Experiment Location and Insect Source.......................................................84 Lure and Treatment................................................................................................84 Release Rate Analysis............................................................................................85 Field Study.............................................................................................................86 Statistical Analysis.................................................................................................88 Results............................................................................................................................89 Release Rate Analysis............................................................................................89 Field Study.............................................................................................................89 Reproductive Adults ..................................................................................89 Non-reproductive Adults ...........................................................................90 Larval Densities .........................................................................................90 Damage, Dieback, and Canopy Volume....................................................91 Discussion......................................................................................................................92 Acknowledgements........................................................................................................99 References....................................................................................................................107 v TABLE OF CONTENTS CONTINUED 4. ALLEE EFFECTS AND AGGREGATION PHEROMONES: NEW RELEASES OF DIORHABDA CARINULATA REMAIN LONGER IN THE PRESENCE OF PHEROMONE FORMULATIONS ...................................114 Contribution of Authors and Co-Authors ....................................................................114 Manuscript Information Page ......................................................................................116 Abstract............................................................................................................................118 Introduction..................................................................................................................119 Materials and Methods.................................................................................................124 Lures and Chemicals............................................................................................124 Insect Source........................................................................................................125 Site Selection and Setup.......................................................................................126 Field Release Protocol .........................................................................................127 Insect Sampling and Population Survey ..............................................................128 Statistical Analysis...............................................................................................128 Results..........................................................................................................................129 Immediate Dispersal ............................................................................................129 Persistence of Individuals at a Release ................................................................130 Discussion....................................................................................................................131 Acknowledgements......................................................................................................135 Supplemental Material.................................................................................................140 References....................................................................................................................143 5. EVALUATION AND FORMULATION OF REPELLENT SEMIOCHEMICALS FOR DISRUPTION OF DIORHABDA CARINULATA AGGREGATIONS .............................................................................149 Contribution of Authors and Co-Authors ....................................................................149 Manuscript information Page.......................................................................................151 Abstract........................................................................................................................153 Introduction..................................................................................................................154 Materials and Methods.................................................................................................159 Insects ..................................................................................................................159 Hemolymph Collection........................................................................................159 Volatile Collection and Analysis .........................................................................160 Preparation of 4-oxo-(E)-2-hexenal for Bioassays ..............................................161 Electrophysiology ................................................................................................161 Two-choice Olfactometer Bioassay.....................................................................163 Statistical Analyses ..............................................................................................164 Results..........................................................................................................................165 Volatile Collections .............................................................................................165 vi TABLE OF CONTENTS CONTINUED EAG Response.....................................................................................................166 Repellency............................................................................................................166 Discussion....................................................................................................................168 Acknowledgements......................................................................................................172 Supplemental Material.................................................................................................178 References....................................................................................................................182 6. CONCLUSIONS..........................................................................................................188 REFERENCES CITED....................................................................................................193 APPENDIX A: Chapter Two Supplemental Material .....................................................222 vii LIST OF TABLES <ul style="display: flex;"><li style="flex:1">Table </li><li style="flex:1">Page </li></ul>2.1 Mean ± SE (nghr-1) of semiochemicals emitted from 1g dollops of field aged dollops over a 31 day period.......................................................68 4.1 Poisson regression analysis for mean densities per 20 sweeps, and mean counts per 3 mins...........................................................................139 S.4.1 Number of adult D. carinulata released and detected within caged release releases in 2016. Caged releases lost to O. stactogalus damage are designated with (---) ..................................................................142 viii LIST OF FIGURES <ul style="display: flex;"><li style="flex:1">Figure </li><li style="flex:1">Page </li></ul>2.1 Density expressed as mean ±SE capture of reproductive adult D. carinulata per three sweeps in (a) 2013 and (b) 2014 at the high density (HDS) or low density (LDS) site on plants receiving 1 g dollops of treatment formulation. Treatments applied included blank (BL), pheromone (PH), pheromone and plant volatile (PHPL), or plant volatile (PL). Different letters above error bars denote significant differences between treatments. .........................................69 2.2 Density expressed as mean ±SE capture of non-reproductive adult D. carinulata per three sweeps in (a) 2013 and (b) 2014 at the high density (HDS) or low density (LDS) site on plants receiving 1 g dollops of treatment formulation. Treatments applied included blank (BL), pheromone (PH), pheromone and plant volatile (PHPL), and plant volatile. Different letters above error bars denote significant differences between treatments..........................69 2.3 Density expressed as mean ±SE capture of larval D. carinulata per three sweeps in (a) 2013 and (b) 2014 at the high density (HDS) or low density (LDS) site on plants receiving 1 g dollops of treatment formulation. Treatments applied included blank (BL), pheromone (PH), pheromone and plant volatile (PHPL), and plant volatile (PL). Different letters above error bars denote significant differences between treatments ..........................................70 2.4 Mean ± SE damage rating for the high density site (HDS) in (a) 2013 and (b) 2014, and the low density site (LDS) in (c) 2013 and (d) 2014 on plants receiving 1 g dollops of treatment formulation. Treatments applied included blank (BL), pheromone (PH), pheromone and plant volatile (PHPL), and plant volatile (PL). (a): BLa, PHb, PHPLb, PLb; (b): BLa, PHb, PHPLb, PLc; (c): BLa, PHb, PHPLb, PLa; (d): BLa, PHb, PHPLb, PLc. different letters behind each treatment denote significant differences between the means ........................................................................71 2.5 Mean ±SE dieback rating 2014-2015 at the (a) high density site (HDS) or (b) low density site (LDS) on plants receiving 1 g ix LIST OF FIGURES CONTINUED <ul style="display: flex;"><li style="flex:1">Figure </li><li style="flex:1">Page </li></ul>dollops of treatment formulation. Treatments applied included blank (BL), pheromone (PH), pheromone and plant volatile (PHPL), and plant volatile (PL). Different letters above error bars denote significant differences between treatments...................................72 2.6 Mean ± SE canopy volume estimated 2013-2015 for (a) the high density site (HDS) or (b) the low density site (LDS) on plants receiving 1 g dollops of treatment formulation. Treatments applied included blank (BL), pheromone (PH), pheromone and plant volatile (PHPL), and plant volatile (PL). (a): BLa, PHa, PHPLa, PLa; (b): BLa, PHb, PHPLb, PLa, different letters behind each treatment denote significant differences between the means ...........................................................................................72 3.1 Mean ± SE of (2E,4Z)-2,4-heptadien-1-ol emitted from 4-g dollops............................................................................................................100 3.2 Weekly mean ± SE capture per three sweeps of reproductive adult Diorhabda carinulata on plants receiving 4-g dollops of pheromone impregnated SPLAT (PH) or blank SPLAT (BL). Densities captured 2014-15 of P generation overwintered adults (a, c) and F1 first generation of current year adults (b, d) .............................101 3.3 Figure 3: Weekly mean ± SE capture per three sweeps of non-reproductive adult Diorhabda carinulata on plants receiving 4-g dollops of pheromone impregnated SPLAT (PH) or blank SPLAT (BL). Densities of the non-reproductive overwintering F2 generation of adults captured in 2014 (a), and 2015 (b)............................102 3.4 Weekly mean ± SE larval Diorhabda carinulata capture per three sweeps on plants receiving 4-g dollops of pheromone impregnated SPLAT (PH) or 4g dollops of blank SPLAT (BL), in 2014 (a), and 2015 (b)................................................................................103 3.5 Weekly mean ± SE damage rating for plants receiving 4-g dollops of pheromone impregnated SPLAT (PH) or blank x LIST OF FIGURES CONTINUED <ul style="display: flex;"><li style="flex:1">Figure </li><li style="flex:1">Page </li></ul>SPLAT (BL), in 2014 (a) and 2015 (b)..........................................................104 3.6 Mean ± SE dieback rating for plants receiving 4-g dollops of pheromone impregnated SPLAT (PH) or blank SPLAT (BL) in 2015 and 2016................................................................................................105 3.7 Change in canopy volume 2014-2016 for plants receiving 4-g dollops of pheromone impregnated SPLAT (PH) or blank SPLAT (BL)...................................................................................................106 4.1 Sampling for D. carinulata adults for immediate dispersal 10-14 days after the initial release. Mean adult density ± SE per 25 sweeps (a, c) and mean adult density ± SE per 3 min count (b) of D. carinulata at release sites. Releases were made with a pheromone lure (PH) or without a pheromone lure (Control) .......................136 4.2 Sampling for Mean adult density ± SE per 25 sweeps for release persistence after the initial release. Releases were made with a pheromone lure (PH) or without a pheromone lure (Control). Post-release monitoring at 10-14 days after the initial release is designated as generation 0 on x-axis .............................................................137 4.3 Sampling for D. carinulata adults for release persistence after the initial release. Mean adult density ± SE per 25 sweeps (a) and mean adult density ± SE per 3 min count (b) of D. carinulata at release sites. Releases were made with a pheromone lure (PH) or without a pheromone lure (Control). Post-release monitoring at 10-14 days after the initial release designated as generation 0 on x-axis.........................................................................................................138 5.1 Gas chromatography profiles of volatiles collected from A) larval D. carinulata feeding on Tamarix; B) undamaged Tamarix; C) mechanically damaged Tamarix. *Peak identified as 4-oxo-(E)-2-hexenal.......................................................................................173 5.2 Electroantennogram (EAG) response of D. carinulata to a negative control (dichloromethane) and 1,000 ng of 4-oxo-(E)-2-hexenal. xi LIST OF FIGURES CONTINUED

Overcoming the Challenges of Tamarix Management with Diorhabda Carinulata Through the Identification and Application of Semioche

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