Arthropod Predation in Brassica Agroecosystems: Effects of Latitude, Community Composition, and Diet Breadth A Dissertation SUBMITTED TO THE FACULTY OF THE UNIVERSITY OF MINNESOTA BY Hannah Louise Gray IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY David A. Andow (Advisor) George E. Heimpel (Co-Advisor) April 2020 © Hannah L. Gray, 2020 Acknowledgements This dissertation represents the culmination of almost six years of learning, growing, and living. I would like to express my immense gratitude to my advisor and mentor Dave Andow. He never took no for answer, because he believed I could do whatever was needed, even when I doubted myself. He supported me through all my ideas and diversions and provided wisdom and perspective to get back on course. I am also extremely thankful for the steady support of my co-advisor George Heimpel. He welcomed me into his lab community and provided invaluable insights into my research and academic life. I would also like to extend my deepest gratitude to Dr. Débora Pires Paula for her mentorship and guidance. Her enthusiasm and eagerness to support my work in Brazil and in the molecular lab was limitless and pushed me to be a better scientist. To the Ecology Group and EMBRAPA-Cenargen in Brasília, this work would not have been possible without your participation. I am especially thankful for my mentor at EMBRAPA, Edison Sujii who facilitated my fieldwork helped me navigate the complex process of doing research abroad. I could not have pulled off my work at EMBRAPA without Lucas Machado de Souza and Alex Cortês, who provided unwavering guidance and friendship in the field. I would also like to thank my collaborators in the latitudinal transect experiment, Madelaine Venzon, Jorge Torres, Juliano Farias, Rafael Aita, and Luan Rodrigues. Thank you for taking on my “dummy” experiment and helping me answer important questions in places I could not physically visit myself. I would also like to acknowledge my appreciation for Alfried Vogler and his research group at Imperial College, London. Alfried welcomed me into his lab on short notice and made sure that my time in the Beetle Lab was productive and engaging. Though my stay was brief, the warmth and good humor among my friends in the Beetle Lab set me up for success interpreting my molecular data. I’d like to thank my committee members, Marla Spivak and Elizabeth Borer, who provided critical perspectives on my research and kept me pushing further with my questions. I am grateful for the time they have invested in my development as a scientist. I am also grateful for the funding I received throughout graduate school. Without these crucial resources neither my development as a scientist nor this research would have been i possible. Within the University of Minnesota, I thank the Department of Entomology, the International Center for Global Change, the Graduate Student Board of the College of Food, Agriculture, and Natural Resource Sciences, the Graduate School, and the MnDRIVE Global Food Ventures and Bioinformatics programs. I am also immensely grateful for the support I received from USAID’s Borlaug Fellows Program to conduct my research in Brazil and from EPA STAR Fellows Program which supported three years of my education. To my friends and colleagues, I thank you for your research, academic and moral support over the years: Kathleen Barrett, Rafaela Mendes Assunção, Michely Aquino, Gabriel Borges, Becky Boulton, Julia Brokaw, Elizabeth Brosius, Mariana Bulgarella, Carla Caixeta, Jonathan Dregni, Monika Egerer, Angelina Ceballos-Escalera Fernández, Fionna Gault, Marla Hassemer, Zafar Iqbal, Joe Kaser, Matt Kaiser, Diego Magalhães, James Miksanek, Hannah Norman, Liz Perkus, Sharon Perrone, Milan Plecas, Gowri Prakesh, Kristina Prescott, Ismael Ramierez, Elise Rosengren, Mary Marek-Spartz, Eric Middleton, Maggie Shanahan, Carl Stenoien, Marissa Streifel, Anh Tran, Chawatat Thanoosing, Vivian Waters, J.J. Weiss, and Jake Wittman. Your collective love of science and insects heartened me in times of struggle and got me to where I am today. I am deeply grateful to my parents David and Brenda Rowley Gray. From an early age they raised me to be curious and confident exploring new places and ideas. I appreciate my sister, Rachel Gray, for her continued love and interest in my research, despite her strong aversion to insects and all things ‘creepy’. I extend thanks to my cousin Tommy Saller, who proceeded me in the Ph.D. process and helped me navigate the academic maze with humor and wisdom. I’d like to thank my partner Randall Beaman, for grounding me in reality and supporting me on this entomological adventure. Finally, I would like to express my heartfelt gratitude to the farmers who hosted this research with patience, curiosity, and kindness. For “It is not the critic who counts…The credit belongs to the man who is actually in the arena” (Roosevelt 1910). Thank you farmers for being in the arena of agriculture and leading the way to a resilient food system. ii Dedication To my grandmother, Gladys Louise Rowley iii Abstract Arthropod predators provide crucial pest management services by consuming herbivore prey in agroecosystems. Yet, variation in arthropod predation strength among cropping systems and regions can prevent farmers from taking advantage of this alternative pest management strategy. This research examines underexplored potential causes of variation in arthropod predation in agroecosystems. Arthropod predation increases at lower latitudes. However, it is unknown whether this gradient extends to agroecosystems. Diet breadth of an arthropod predator can influence whether a predator can adequately control resident herbivore populations and can impact predation in a community context by determining whether predatory taxa will compete over shared prey, attack each other as intraguild prey, or partition herbivore taxa into distinct prey niches. To assess the effect of latitude, I first compared predation rates on live and artificial sentinel prey in Brassica agroecosystems between the tropical Federal District, Brazil and temperate Minnesota, United States. Contrary to expectations, I found that predation rates on all bait types were similar between the two localities and that reduced predation rates in the Federal District may be related to higher prey densities. Next, to further explore latitudinal effects, I assessed predation rates in Brassica agroecosystems across 15 degrees of latitude in the United States and 21 degrees of latitude in Brazil. Surprisingly, my results revealed a reverse predation gradient whereby arthropod predation increased with latitude in both countries. To examine the role of diet breadth, I first tested methods to improve molecular gut content analysis of arthropod predators by verifying broad metabarcoding results with species-specific melting curve analysis. This study documented common false positive and false negative taxonomic results and suggested that a species-specific verification step is necessary to ensure accurate depictions of arthropod trophic interactions. Lastly, I use the results of the gut content analysis to characterize the diet breadth of three coccinellid predator species (Coleomegilla maculata, Hippodamia convergens, and Harmonia axyridis) collected from a Brassica agroecosystem in Minnesota. I found that both herbivore and intraguild prey consumption were common among coccinellid species, but that C. maculata was least likely to engage in intraguild predation of fellow coccinellids. iv Table of Contents Acknowledgements ........................................................................................................... i Dedication ....................................................................................................................... iii Abstract ........................................................................................................................... iv List of Tables ................................................................................................................ viii Lists of Figures ............................................................................................................. xiii Introduction .................................................................................................................... 1 Latitudinal gradients in biotic interactions ............................................................ 2 Ecological function ................................................................................................ 2 Diet breadth ............................................................................................................ 3 Arthropod predator function in agroecosystems .................................................... 3 Latitudinal gradients in arthropod predation .............................................. 4 Diet breadth and arthropod predation ........................................................ 4 Chapters ................................................................................................................. 5 Chapter 1: Arthropod predation strength is similar between a temperate and tropical Brassica agroecosystem ..................................................................................... 9 Summary ................................................................................................................ 9 Introduction .........................................................................................................
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