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

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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

  • Table
  • Page

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

  • Figure
  • Page

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

  • Figure
  • Page

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

  • Figure
  • Page

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

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    insects Article Adhesion Performance in the Eggs of the Philippine Leaf Insect Phyllium philippinicum (Phasmatodea: Phylliidae) Thies H. Büscher * , Elise Quigley and Stanislav N. Gorb Department of Functional Morphology and Biomechanics, Institute of Zoology, Kiel University, Am Botanischen Garten 9, 24118 Kiel, Germany; [email protected] (E.Q.); [email protected] (S.N.G.) * Correspondence: [email protected] Received: 12 June 2020; Accepted: 25 June 2020; Published: 28 June 2020 Abstract: Leaf insects (Phasmatodea: Phylliidae) exhibit perfect crypsis imitating leaves. Although the special appearance of the eggs of the species Phyllium philippinicum, which imitate plant seeds, has received attention in different taxonomic studies, the attachment capability of the eggs remains rather anecdotical. Weherein elucidate the specialized attachment mechanism of the eggs of this species and provide the first experimental approach to systematically characterize the functional properties of their adhesion by using different microscopy techniques and attachment force measurements on substrates with differing degrees of roughness and surface chemistry, as well as repetitive attachment/detachment cycles while under the influence of water contact. We found that a combination of folded exochorionic structures (pinnae) and a film of adhesive secretion contribute to attachment, which both respond to water. Adhesion is initiated by the glue, which becomes fluid through hydration, enabling adaption to the surface profile. Hierarchically structured pinnae support the spreading of the glue and reinforcement of the film. This combination aids the egg’s surface in adapting to the surface roughness, yet the attachment strength is additionally influenced by the egg’s surface chemistry, favoring hydrophilic substrates.
  • Tamarisk Beetle (Diorhabda Spp.) in the Colorado River Basin: Synthesis of an Expert Panel Forum Benjamin R

    Tamarisk Beetle (Diorhabda Spp.) in the Colorado River Basin: Synthesis of an Expert Panel Forum Benjamin R

    Scientific and Technical Report No. 1 JANUARY 2016 Tamarisk beetle (Diorhabda spp.) in the Colorado River basin: synthesis of an expert panel forum Benjamin R. Bloodworth1, Patrick B. Shafroth2, Anna A. Sher 3, Rebecca B. Manners4, Daniel W. Bean5, Matthew J. Johnson6, and Osvel Hinojosa-Huerta7 1Tamarisk Coalition, Grand Junction, CO 2U.S. Geological Survey, Fort Collins, CO 3University of Denver, Denver, CO 4University of Montana, Missoula, MT 5Colorado Dept. of Agriculture, Palisade Insectary, Palisade, CO 6Colorado Plateau Research Station, Northern Arizona University, Flagstaff, AZ 970.248.1968 7Pronatura Noroeste, La Paz, Mexico 1100 North Avenue Grand Junction, CO 81501-3122 coloradomesa.edu/water-center © 2016 COLORADO MESA UNIVERSITY 1 Tamarisk Beetle in the Colorado River Basin Contents Acknowledgements ............................................................ 2 List of Figures Executive Summary Executive Summary ............................................................. 3 Figure 1 — Close-up of an adult tamarisk beetle In 2001, the U.S. Department of Agriculture approved the release of a biological control agent, the tamarisk beetle (Diorhabda Introduction ......................................................................... 4 (Diorhabda spp.). (Photo by Ed Kosmicki). .......................... 3 spp.), to naturally control tamarisk populations and provide a less costly, and potentially more effective, means of removal compared with mechanical and chemical methods. The invasive plant tamarisk (Tamarix spp.; saltcedar)