Novel Monitoring and Biological Control of Invasive Insect Pests
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Doctoral School in Civil, Environmental and Mechanical Engineering Robert Malek Novel Monitoring and Biological Control of Invasive Insect Pests Doctoral School in Civil, Environmental and Mechanical Engineering Topic 1. Civil and Environmental Engineering - XXXII cycle 2016/2019 Doctoral Thesis April 2020 Robert Malek Novel Monitoring and Biological Control of Invasive Insect Pests Supervisors Prof. Gianfranco Anfora University of Trento Prof. Marco Ciolli University of Trento Novel Monitoring and Biological Control of Invasive Insect Pests by Robert Malek Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy to the Department of Civil, Environmental and Mechanical Engineering of the University of Trento and to the Fondazione Edmund Mach Thesis supervisors Prof. Gianfranco Anfora Prof. Marco Ciolli April 2020 Abstract of The Dissertation Invasive species are alien to the ecosystem under consideration and cause economic or environmental damage or harm to human health. Two alien insects that fit this description are the brown marmorated stink bug, Halyomorpha halys and the spotted lanternfly, Lycorma delicatula. Both invaders are polyphagous pests that feed on a myriad of plant species and inflict severe crop losses. As sustainable control methods depend on the accurate monitoring of species’ invasion and involve the use of natural enemies, we addressed these two facets by exploring novel monitoring techniques and deciphering host-parasitoid interactions for improved integrated pest management. Thus, we adopted ‘BugMap’, a citizen science initiative that enables students, farmers and everyday citizens to report sightings of H. halys from Italy, with emphasis on Trentino-Alto Adige. Aside from fostering citizen participation in scientific endeavors and the enhanced literacy that ensues, BugMap helped uncover the invasion dynamics of H. halys and forecast its potential distribution in Trentino, all while coordinating technical monitoring and informing management strategies. The most promising agent currently under study for the classical biological control of H. halys is the Asian egg parasitoid Trissolcus japonicus. To assess the wasp’s potential non-target impacts, we investigated its foraging behavior in response to chemical traces ‘footprints’ deposited by its main host H. halys and by a suboptimal predatory species, the spined soldier bug, Podisus maculiventris. Wasps exhibited a ‘motivated searching’ when in contact with footprints originating from both species. However, T. japonicus arrestment was significantly stronger in response to H. halys footprints, compared with P. maculiventris, implying the presence of underlying chemical cues that shape its natural preferences. A series of GC-MS chemical analyses revealed that n-tridecane and (E)-2-decenal were more abundant in H. halys footprints and are probably the key components utilized by the wasp for short range host location. The function of the aforementioned compounds was studied, n- tridecane acted as an arrestant, prolonging T. japonicus residence time, whereas (E)- 2-decenal fulfilled its presumed defensive role and repelled the wasp. These results shed new light on the chemical ecology of T. japonicus and help expand the understanding of parasitoid foraging and its implications for classical biological control. Moving to the other invader L. delicatula, an egg parasitoid Anastatus orientalis was reported attacking it at high rates in its native range in Eastern Asia and may play a key role in reducing its populations there. A series of bioassays revealed that wasps responded to footprints deposited by L. delicatula gravid females by initiating a strong searching behavior. Moreover, A. orientalis preferred to oviposit in egg masses with intact oothecae, suggesting that the host’s egg covering functions as a trigger for A. orientalis probing and oviposition. Thus, A. orientalis not only overcomes, but also reverses an important line of host structural defense for its own fitness gains. This dissertation discusses the benefits of combining citizen science with traditional monitoring, and the usefulness of decoding host-parasitoid interactions to design more efficacious management strategies of invasive insect pests. Acknowledgments My sincere gratitude goes to everyone who supported me throughout this journey, your encouragement strengthened my resolve, and for that I am grateful. I would first like to thank my advisors, Gianfranco Anfora and Marco Ciolli, your help, flexibility and guidance allowed the exploration of various research lines that converged to serve the same purpose. Many thanks are also extended to Clara Tattoni, your generous dedication and enthusiasm made this project even more productive and enjoyable. I also thank the University of Trento and Fondazione Edmund Mach for granting me a scholarship that made all the work herein presented a viable reality. My gratitude extends to the PhD offices in both these institutions, Claudia Fraizingher and Elisabetta Perini, thank you for your assistance and advice in navigating the cumbersome bureaucratic maze. I am forever indebted to Kim Hoelmer and Don Weber for hosting me at the USDA-ARS. Your generous hospitality had a tremendous impact on this project and taught me endless career and life lessons. Joe Kaser, Keith Hopper, Xingeng Wang and Jeff Wildonger, thank you for your stimulating input and for the generous volunteering of your time, our enthralling discussions were deeply nourishing and mind-opening. Many thanks to the people behind the scenes who made this research possible, Kathleen Tatman, Patricia Stout and Marco Deromedi, your problem-solving skills and assistance are very inspiring. My sincere gratitude to all the volunteers who took part in our citizen science project, a big portion of this work would not have been possible without you. To my colleagues in Italy, Valerio Mazzoni, Eric Conti and Gabriele Rondoni, thank you for your contribution and for hosting me at Fondazione Edmund Mach and at the University of Perugia. I extend special gratefulness to my previous mentors, Wassim Habib and Thérèse Atallah, your continuous support and guidance is always appreciated and helps keep me on the right track. My experience in the US and in Italy would have lacked flavor if not shared with very special people who helped make these three years very enjoyable. In no particular order, many thanks to Kun Huang, Caterina Ciani, Roel Smits, Cris Müller, Federico Pedrazzoli, Andrea Silverj, Khalil Ghanem and Jon Almeras for making life outside work much more amusing. To my ‘entomo-partner’ Aya Ibrahim, I am extremely fortunate to have you by my side, your boundless love and unwavering support brings out the best in me and makes me a better person. To all my friends and family in Lebanon and overseas, thank you for being there for me, your selfless support and encouragement made this possible. To Marie, Nehme and Georges, you believed in me, and for that I am forever grateful. “Each one of us is a tiny being, permitted to ride on the outermost skin of one of the smaller planets for a few dozen trips around the local star.” Carl Sagan and Ann Druyan This dissertation is dedicated to even smaller beings, arthropods, the little things that run our world. Table of contents Chapter 1 ................................................................................................................................ 1 1 Invasive species .............................................................................................................. 1 1.1 Agriculture and species invasion ................................................................................... 2 1.2 Effects of invasive species .............................................................................................. 4 1.2.1 Economic damage ................................................................................................ 5 1.2.2 Ecological impact ................................................................................................. 6 2 Invasive species monitoring and citizen science ........................................................... 7 2.1 Challenges facing traditional monitoring ..................................................................... 8 2.2 Benefits of citizen participation ..................................................................................... 9 2.3 Citizen science and species distribution models ..........................................................11 3 The invasive brown marmorated stink bug .................................................................14 3.1 Distribution and life history .........................................................................................14 3.2 Host range and damage ................................................................................................16 3.3 Management techniques of Halyomorpha halys ..........................................................17 4 Biological control ...........................................................................................................19 4.1 Types of biological control .............................................................................................22 4.2 Peaks and valleys of classical biological control ..........................................................25 4.3 Biological control of Halyomorpha halys ......................................................................29 5 Another invasion nightmare .........................................................................................32