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A Comparative Anatomical Study of Galls Caused by the Major Cecidoqenetic Groups.1 with Special Emphasis on the Nutritive Tissue

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A Comparative Anatomical Study of Galls Caused by the Major Cecidoqenetic Groups.1 with Special Emphasis on the Nutritive Tissue AN ABSTRACT OF THE THESIS OF HIRAM GORDON LAREW for the Ph.D.. in Entomalogy presented on December 17, 1981 Title: A COMPARATIVE ANATOMICAL STUDY OF GALLS CAUSEDBY THE MAJOR CECIDOGENETIC GROUPS. WITH SPECIALEMPHASIS ON THE NUTRITIVE TISSUE Abstract approved: I Peter B.. McEvoy The anatomies of 44 galls are discussed withspecial attention given to the development, longevity, and tannin content of the nutritive tissues. Within the main section of the thesis, representative galls from the major cecidogenetic groups, with the exception of bacterial and Australian scale galls, are studied. These include galls caused by fungi, nematodes, mites, moths, sawflys, scales, aphids, adelgids, tephritids, cecidomyiids, and cynipids. Three leaf mines are also described. Observations were taken from thin sections (plastic embedment) with alight microscope. The galls are arrayed along a continuum of increasing structural complexity, as judged by the degree of gall tissue differentiation. The sclerenchymatous "protective" zone and nutritive cells are used as indicators of gall complexity and of strength of the gall-former's influence over host plant tissue. Starting with the Fungal galls, then moth and sawfly galls, to the thrips, scale, mites, nematode. cecidomyiidand cynipid galls, one sees greater differentiation of gall tissues, with an increasingly distinct nutritive layer. A scierenchyma zone develops only in inidge and wasp galls. The longevity of the nutritive tissue varies from gall to gall. Generally, the nutritive tissue is maintained in an enriched state for an extended period only in galls caused by cynipids (and perhaps by nematodes). The mites and midges show enriched nutritive cells only in early gall development. No distinctive nutritive tissue occurs in the aphid galls that were studied. Generally, nutritive tissue contains less tanniferous material (as detected by the ferrous sulfate stain) than do either peripheral gall tissues or cells of the leaf. Thus, many gall-f ormers avoid tanriins by directing the development of the cells upon which they feed. The epilogue includes a list of features shared by many galls and by gall-forming organisms. Gall-f ormers also share several characteristics with other types of parasites. The three appendices include 1) an anatomical study of eight galls on shrubs from the drylands of eastern Oregon (mite, cecidomyiid, tephritid, and moth galls), 2) a discussion of fossil galls and leaf mines asindicators of the age and stability of these co-evolutionary relationships. Two galled acorns from the La Brea Tar pits (Los Angeles, California) are described in this section. Lastly, 3) a discussion of economically important galls is provided. This last appendix addresses the question of why there are relatively few gall-forming insect pests, and includes a discussion of the supposed benignity of insect galls. A Comparative Anatomical Study of Galls Caused by the Major CecidoQenetic Groups.1 with Special Emphasis on the Nutritive Tissue by Hiram Gordon Larew A THESIS submitted to Oregon State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Completed December 17.,1981 Commencement June 1982 Approved: 6 2'i Assistant Professor à'f Entomology in charge of major Chairman of Department of En,.t)Smology Dean of GraduateS,e4,ol Date thesis is presented December 17, 1981 Typed by Hiram Larew + or Hiram Larew DEDICATION This dissertation is dedicated to my parents, Dr. H. Gordon Larew and Mrs. Mary Jo Larew, and to my two sisters, Jane Larew and Liz Larew. They listen and care. ACKNOWLEDGEMENTS I wish to thank Dr. Peter McEvoy for guidance at appropriate times, and + or his emphasis on a broad view, the large questions. Dr. Fred Rickson was especially generous with his time and laboratory facilities. Dr. Harry Phinney gave invaluable advice on macrophotography, and unselfishly made camera and microscope equipment available. Becky and Gene Fichter were kind enough to let me use their home computer. Dr. Frank Smith lent microscope equipment and provided office space inwhich to work. Mr. Al Soeldner and Dr. Pat Buckley provided convenient access to equipment needed for sectioning. Mr. Kay Fernald provided help and advice on darkroom technique. Ms. Doris Tilles assisted with inter-library loans. The following individuals provided specimens and/or information about specimens; their help has made the study possible: Dr. W. Akersten (Los Angelos County Museum), Dr. A. Menke (United States National Museum), Dr. W. Pulaski (California Academy of Sciences), Dr. H. Schorn (Department of Paleontology, University of California, Berkeley), Dr. B. Tif+ney (Vale University), Dr. D. O'Dawd (CSIRO, Canberra, Australia), Dr. R. E. Evans (Norfolk, England), Dr. A. Raman (Loyala College, India), and Dr.B.. Daniels, (Kansas State University). Faculty and students at Oregon State University who have been o-F help include: Dr. G. Krantz, Dr. A. lloldenke, Dr. L. Moore, Dr. L. Russell, Dr N. Anderson, Dr. F. Smith, Dr. P. Koepsell, Dr. K. Chambers, Dr. R. Hampton, Dr. A. Boucot, Dr. 6. Guppy, Dr. R. Ha].se, Dr. B. Krapp, A. Churchill, 1. Vanderheyden, 6. Nielsen, E. McEvoy, 6. Baker, P. Hessburg, P. Hanson, P. Hennen, B. Simko, D. Henneberger, T. Dudley, K. Gottwald, S. Russell, 3. Pinkerton, and B. Fichter. All of the above as well as other friends have offered help, advice, and encouragement during the study. I thank all of them. Lastly, I wish to thank Dr. Marshall Darley (University of Georgia) for the time and energy he so willingly invested in my undergraduate education. I also want to acknowledge Dr. John Lattin for encouraging my early interest in galls. Section through speckled oak apple gall on Quercus qarryana Dougi. caused by Besbicus inirabilis showing larval cavity (at bottom of photograph) larval capsule wall, and radiating fibers (top of photograph). Specimen collected Vil/lO/BO. 730X. TABLE OF CONTENTS INTRODUCTION 1 LITERATURE REVIEW Classification System Based on Host Tissue Disruption 4 Organoid Galls 4 Histioid Galls 6 Kataplasmas 6 Prosoplasmas S Relationship Between Kataplasmas and Prosoplasmas. - . .9 Classification System Based on Cecidozoan/Plant Interaction 11 Filzgalls - 11 Fold Galls 12 Pouch Galls.... 12 Covering Galls 13 Lysenchyme Galls 14 Mark Galls 14 OtherClassiFicationSystems Gall Anatomy andMorphogenesis . 15 Gall Anatomy .... 15 Gall Morphogenesis: The Chemical Gradient Theory...17 Characteristics of the Nutritive Tissue 19 Definition 19 Development of Nutritive Tissue 21 Replacement and Maintenance of Nutritive Tissue. .22 Are Nutritive Cells Meristematic? 24 Absence of Nutritive Cells 26 How Do Gal 1-Farmers Feed? 27 Characteristics of Nutritive Cells 29 MATERIALS AND METhODS 31 RESULTS 35 Leaf Mines Leaf Mine on Fringe Cup 35 Leaf Mine on Salal 37 Leaf Mine on Black Cottonwood..... 38 Summary 39 Fungal Galls . 40 Gall on Larkspur . 40 Azalea Gall 41 Black Cottonwood Gall 43 Summary 45 Nematode Gall 46 Summary 47 Eriophyoid Galls 48 Willow Leaf Gall 48 Alder Bead Gall 50 Linden Leaf Gall 54 Erineum on Garry Oak ..57 Ash Leaflet Gall 59 Gall on Poison Oak Leaflet 61 Lea-F Gall on Trembling Aspen 62 Leaf Gall on Choke Cherry . 63 BigBud of Filbert... .............. ......-. .....s .64 Summary - 65 Classification 65 Nutritive Layer Dynamics 67 Tannins 69 LepidopteranGall Stem Gall on Peck's Penstemon 71 Summary 73 Sawfly Galls 74 Gall on Snowberry 74 Willow Leaf Gall 75 Summary . 79 Classification 79 Nutritive Cell Dynamics..... 80 Tanni ns 80 Thrips Gall 81 Summary 82 Classification 82 Nutritive Cells 82 Tannins 83 Scale Gall (Oak Pit Gall) 84 Summary 85 Classification 85 Nutritive Cells 85 Aphid and Adelgid Galls 86 Poplar Petiole Gall 86 Poplar Marginal Gall 91 Midvein Gall on Poplar Leaves Leaf Gall on Bearberry 97 Leaf Gall on Witch Hazel 99 Anasas Gall on Engelmann Spruce 100 Summary 102 Classification 102 Diet 102 Tannins 104 Cecidomyiid Galls 106 Hawthorn Leaf Gall 106 Leaf Roll Gall on Snowberry 109 Leaf Gall on Servi ceberry . - - - - . - -113 Poplar Bud Gall 117 Willow Stem Beaked Gall 120 Summary 125 Classification . -125 Nutritive Layer Dynamics and Tannins 126 Cynipid Galls 128 Stem Gall on Cat's Ear 128 Small Leaf Gall on Garry Oak 129 Oak Bullet Gall on Garry Oak 131 Rose Tip Gall 135 Spherical Stem Gall on Garry Oak 136 Mossy Rose Gall 138 Speckled OakAppleonGarryflak..........- l42 Summary 148 Classification 148 Nutritive Tissue and Its Dynamics 148 Sclerid Zone 149 Tannins 150 DISCUSSION - CONCLUSIONS 152 Degree of Reorganization 152 Nutritive Cells 157 Aphid Galls 159 Tanning 161 EPILOGUE: Characteristics of the Gall-Forming Habit 162 Host Plant Specificity 162 Morphological Modifications of the Gall-Former. 164 GallInvaders 166 Parasitoids and Predators .147 Inquilines 169 Galls andAnt Colonies 170 Site ofAttack, and HostResponse 172 Diet Enhancement 174 Symbionts. 176 Galls asMetabolicSinks 177 Unusual Life Cycles and Reproduction 179 Damage to Plant 180 How Does The Host Plant Defend Itself? 180 PLATES 184 BIBLIOGRAPHY 269 APPENDIX 1: EasternOregonGalls...... Published Accounts of Galls on Dryland Shrubs 291 Anatomical Studies 297 Galls on Artemisia tridentata 300 ART 300 ARC . .302 ANP 304 Galls on Chrysothamnus nauseosus. -. - -. ..... ... .307 CRC 307 COT. 308 CPG 310 Galls on Tetradymia spp TES 313 TET 314 Summary of Eastern Oregon Galls 317 Dryland Shrub Galls - A Discussion 318 Pattern 1 319 Pattern 2 319 Pattern 3.. 323 APPENDIX 2: Evidence for Plant-Insect Interactions in the Fossil Record 326 Introduction 326 Fossil Plant Parts ..329 Pollen 329 Fruits and Seeds 330 Bark and Stems 335 Roots 337 Leaves 337 Fossil Galls 339 Gall Insects 344 "Hidden" Fossil Galls 345 A Search Method for Discovering Fossil Galls in Collections 347 Fossil Leaf Mines 350 Domatia 351 Summary and Conclusions 353 APPENDIX 3: SaIls of Importance to Humans. 360 Detrimental Gall-Forming Organisms 361 Slime Molds 361 Bacteria 362 Fungi 365 Characteristics of Gall-Forming Fungi........=365 Nematodes 367 Mites 369 Insects ...... 369 Cecidomyiids 370 Other Diptera 371 Scales 371 Aphids 371 Adelgids 374 Summary of Detrimental Galls 374 Beneficial Gall Organisms 377 Galls as Biocontrol Agents 379 Case 1 380 Case 2 .
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