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Impact and Ecological Adaptation of Leptoglossus Occidentalis (Hemiptera, Coreidae) on Pinus Pinea

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Impact and Ecological Adaptation of Leptoglossus Occidentalis (Hemiptera, Coreidae) on Pinus Pinea Impact and ecological adaptation of Leptoglossus occidentalis (Hemiptera, Coreidae) on Pinus pinea Ana Cristina Oliveira Farinha Scientific Advisors Supervisor: Ph.D. Manuela Rodrigues Branco Simões Co-supervisor: Ph.D Edmundo Rodrigues de Sousa Co-supervisor: Ph.D. Alain Roques Thesis presented to obtain the Doctor degree in Forestry Engineering and Natural Resources Programa de doutoramento FCT (Sustainable Forests and Products, SUSFOR) 2019 Page 1 of 164 Impact and ecological adaptation of Leptoglossus occidentalis (Hemiptera, Coreidae) on Pinus pinea Ana Cristina Oliveira Farinha Scientific Advisors: Supervisor: Ph.D. Manuela Rodrigues Branco Simões Co-supervisor: Ph.D Edmundo Rodrigues de Sousa Co-supervisor: Ph.D. Alain Roques THESIS PRESENTED TO OBTAIN THE DOCTOR DEGREE IN FORESTRY ENGINEERING AND NATURAL RESOURCES Jury members President: Ph.D Mª Margarida Tomé Full professor Instituto Superior de Agronomia Universidade de Lisboa Ph.D. Andrea BATTISTI Full Professor Università Degli Studi di Padova, Itália Ph.D. António Marques MEXIA Full professor Instituto Superior de Agronomia Universidade de Lisboa Ph.D. Manuela Rodrigues BRANCO Assistant professor with aggregation Instituto Superior de Agronomia Universidade de Lisboa (supervisor) Ph.D. Maria Isabel CARRASQUINHO Assistant researcher Instituto Nacional de Investigação Agrária e Veterinária. Funding instituition: Doctoral Program FCT (Sustainable Forests and Products, SUSFOR) Doctoral scholarship ref. PD/BD/52403/2013 2019 Page 2 of 164 À Cátia e à pequena Catarina Somos todas raízes da mesma árvore! Page 3 of 164 Table of contents Acknowledgments .......................................................................................... 7 Abstract ........................................................................................................ 9 Resumo …………………………………………………………………………………………… 11 CHAPTER 1 General Introduction and thesis outline ............................................................ 15 Can we measure the effective impact of the bug on Stone pine seeds?......................17 Comparing life history and ecology in the native range and the invaded Portugal....... 18 Can we reconstruct the invasion history of L. occidentalis in the Iberian Peninsula? ... 19 Project plan and objectives ................................................................................. 20 CHAPTER 2 - L. occidentalis and the host Stone pine How important is the non-native seed feeder Leptoglossus occidentalis on the sustainability of the Mediterranean Stone pine? State of the art ......................... 22 Abstract ........................................................................................................... 23 Mediterranean Stone pine and its edible pine nut kernels ....................................... 24 The Western Conifer Seed Bug, Leptoglossus occidentalis ....................................... 30 Leptoglossus occidentalis control ......................................................................... 39 Conclusions and future guidelines ........................................................................ 43 References ....................................................................................................... 44 CHAPTER 3 - How to measure the impact of the bug on Stone pine seeds? Micro-CT and X-ray suggests cooperative feeding among adult invasive bugs Leptoglossus occidentalis on mature seeds of Stone pine Pinus pinea .............. 57 Abstract ........................................................................................................... 58 Introduction ...................................................................................................... 59 Page 4 of 164 Methods ........................................................................................................... 61 Results ............................................................................................................. 64 Discussion ........................................................................................................ 69 Acknowledgments ............................................................................................. 73 References ....................................................................................................... 73 CHAPTER 4 - Does the seed bug prefer stone pine over other mediterranean pines? The Stone pine, Pinus pinea, a new highly rewarding host for the invasive Leptoglossus occidentalis .................................................................................. 78 Abstract ........................................................................................................... 79 Introduction ...................................................................................................... 80 Methods ........................................................................................................... 82 Results ............................................................................................................. 86 Discussion ........................................................................................................ 91 Conclusions ...................................................................................................... 94 References ....................................................................................................... 95 CHAPTER 5 - Does Stone pine management influence this bug impact? Is Leptoglossus occidentalis entirely responsible for the high damage observed on cones and seeds of Pinus pinea? Results from a fertirrigation trial in Portugal .......................................................................................................................... 99 Abstract .......................................................................................................... 100 Introduction ..................................................................................................... 101 Methods .......................................................................................................... 104 Results ............................................................................................................ 108 Discussion ....................................................................................................... 114 Conclusions ..................................................................................................... 119 References ...................................................................................................... 121 Page 5 of 164 CHAPTER 6 - How did the seed feeder get here? Another chapter in the history of the European invasion by the western conifer seed bug, Leptoglossus occidentalis: The Iberian Peninsula ............................ 125 Abstract .......................................................................................................... 126 Introduction ..................................................................................................... 127 Methods .......................................................................................................... 130 Results ............................................................................................................ 134 Discussion ....................................................................................................... 140 Conclusions ..................................................................................................... 144 References ...................................................................................................... 145 CHAPTER 7 Conclusions and guidelines for future research ................................................ 150 Is the seed feeder entirely responsible for the observed decrease in Stone pine seed crop? .............................................................................................................. 151 Plant-insect interaction: the seed feeder and the Stone pine .................................. 153 Bug invasion history in the Iberian Peninsula still to be confirmed .......................... 155 Guidelines for future research ............................................................................ 156 References ...................................................................................................... 158 About the author ………………………………………………………………………………………….…………...164 Page 6 of 164 ACKNOWLEDGMENTS Although presented individually, a PhD project is (or should be) a result of numerous interactions, discussions and sharing with, not only colleagues but also with family and friends. I was fortunate to have had both in equal parts. My greatest thank you is to Cátia! For all the patience, inspiration and love. You have been my compass for the last decade. During the course of the Ph.D. I had my greatest inspiration born, my doughter Catarina. She gave me strength to put up with a non recommended work rhythm, especially in the last year of the project. I have to say thanks to my parents for all the inconditional support since I was born! I love you. Also to my parents in law. Duarte and São are very good friends never saying no to help. From sewing insect bags to take care of Catarina, I could always count on them. Big, big thanks to Professor Manuela! A really (SUPER) supervisor! Always there. Always helping and teaching. Very human. I almost felt like an academic doughter. Manuela is a teacher who gives a lot of herself and truly cares about her students.
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