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The Pennsylvania State University The Pennsylvania State University The Graduate School College of Agricultural Sciences BEHAVIORALLY ACTIVE SUBSTANCES AFFECTING REPRODUCTIVE SUCCESS OF THE FUNGUS GNAT, LYCORIELLA INGENUA, A PEST OF WHITE BUTTON MUSHROOMS, AGARICUS BISPORUS A Dissertation in Entomology by Kevin R. Cloonan 2017 Kevin R. Cloonan Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy May 2017 The dissertation of Kevin R. Cloonan was reviewed and approved* by the following: Thomas C. Baker Distinguished Professor of Entomology and Chemical Ecology Dissertation Advisor Chair of Committee Nina E. Jenkins Professor of Entomology Shelby Fleischer Professor of Entomology John A. Pecchia Professor of Mushroom Science and Technology Gary Felton Professor of Entomology Department of Entomology, Chair *Signatures are on file in the Graduate School iii ABSTRACT Little is known about the host seeking and courtship behaviors of the fungus gnat, Lycoriella ingenua (Diptera: Sciaridae), one of the most severe insect pests of cultivated white button mushrooms, Agaricus bisporus. Published works concerning L. ingenua focus primarily on aspects of control including: insecticide susceptibility, insecticide resistance, viability of biological control agents, and determining damage thresholds. The work presented in this dissertation examines the host seeking behavior of female flies and the copulatory behavior of male flies. Host seeking and copulatory behaviors in insects involve a complex series of events beginning with signal acquisition, signal transduction, and signal processing. Signal molecules provide the searching insect with information about the quality and location of the host material or potential mate. In this dissertation I present work showing that gravid L. ingenua female flies are attracted the composted substrate that mushrooms are grown on, not the mushrooms themselves, and to the mycoparasitic green mold, Trichoderma aggressivum. Fungi including Penicillium citrinum, Mycothermus thermophilium, and several Aspergillus sp. present in mushroom compost, may be responsible for the initial attraction to female L. ingenua flies. We also isolated a single female produced pheromone component, a germacradienol, that attracts male L. ingenua flies and elicits copulatory behavior including wing fanning and abdomen curling. Ultimately the work presented in this dissertation may provide growers with new tools to manage and control L. ingenua populations in mushroom houses. iv TABLE OF CONTENTS LIST OF FIGURES .................................................................................................................................. vii ACKNOWLEDGEMENTS ........................................................................................................................ ix DEDICATION .......................................................................................................................................... x Chapter 1 - Introduction ....................................................................................................................... 1 Overview of chapters ............................................................................................................... 1 Overview of study organisms ................................................................................................... 3 White button mushroom, Agaricus bisporus ............................................................. 3 Fungus gnats in the family Sciaridae ........................................................................... 6 Pest ecology: Lycoriella. ............................................................................................... 7 Pest ecology: Bradysia. .............................................................................................. 13 Entomophilous fungi. ............................................................................................................. 15 Lycoriella sp. transporting fungal spores. ................................................................. 15 Bradysia sp. transporting fungal spores. .................................................................. 17 Vectoring of fungal spores by L. ingenua: mutualism or coincidence? ................... 18 Chapter 2 – Attraction of female fungus gnats, Lycoriella ingenua, to mushroom-growing substrates and the green mold, Trichoderma aggressivum ................................................. 21 Abstract ................................................................................................................................... 21 Introduction ............................................................................................................................ 22 Materials and Methods .......................................................................................................... 24 Composting phases: preparation of mushroom growing-test substrates .............. 24 Agaricus bisporus mycelia.......................................................................................... 26 Trichoderma aggressivum (green mold) ................................................................... 26 Flies ............................................................................................................................. 26 Two-choice, static-flow olfactometer ....................................................................... 28 Olfactometer experiments ........................................................................................ 30 Statistical analysis....................................................................................................... 31 Results ..................................................................................................................................... 31 Discussion ................................................................................................................................ 33 Acknowledgements ................................................................................................................ 35 Chapter 3 – Attraction, oviposition, and survival of the fungus gnat, Lycoriella ingenua, on fungal species isolated from adults, larvae, and mushroom compost ........................................................ 36 v Abstract ................................................................................................................................... 36 Introduction ............................................................................................................................ 37 Materials and Methods .......................................................................................................... 41 Insects ......................................................................................................................... 41 Fungal cultures ........................................................................................................... 42 Fungal species present in mushroom compost ........................................... 42 Fungal species isolated from adult flies ....................................................... 42 Fungal species isolated from larvae ............................................................. 44 DNA extraction, PCR, sequencing and identification of isolated fungi ....... 45 Two-choice, static flow olfactometer attraction assays .......................................... 46 Two-choice oviposition assays .................................................................................. 49 No-choice assays ........................................................................................................ 50 Larvae-to-adult survival assays .................................................................................. 52 Statistical analysis....................................................................................................... 52 Results ..................................................................................................................................... 53 Discussion ................................................................................................................................ 59 Acknowledgements ................................................................................................................ 64 Chapter 4 – Isolation of a female-emitted sex pheromone component of the fungus gnat, Lycoriella ingenua, attractive to males .............................................................................................. 65 Abstract ................................................................................................................................... 65 Introduction ............................................................................................................................ 66 Materials and Methods .......................................................................................................... 68 Insect rearing .............................................................................................................. 68 Olfactometer choice assays ....................................................................................... 69 Extraction of sex pheromone component ................................................................ 72 GC analysis .................................................................................................................. 73 Mass spectrometry analysis .....................................................................................
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