IMPLICATIONS OF HABITAT RESTORATION FOR BUMBLE BEE POPULATION DYNAMICS, FORAGING ECOLOGY, AND EPIDEMIOLOGY By Knute Baldwin Gundersen A DISSERTATION Submitted to Michigan State University in partial fulfillment of the requirements for the degree of Entomology—Doctor of Philosophy Ecology, Evolutionary Biology and Behavior—Dual Major 2018 ABSTRACT IMPLICATIONS OF HABITAT RESTORATION FOR BUMBLE BEE POPULATION DYNAMICS, FORAGING ECOLOGY, AND EPIDEMIOLOGY By Knute Baldwin Gundersen Many insects provide valuable ecosystem services, including those that support our food supply. Beneficial insects such as pollinators fulfill part of this role by contributing to approximately one third of the global food crop production. Over the past few decades, pollinators have faced declining populations due to a variety of factors such as agricultural intensification, lack of floral and nesting resources, and disease. One method used in agricultural settings to help sustain pollinator populations is designating unfarmed habitat such as ditches and field margins for habitat enhancement in the form of hedgerows and wildflower strips. These floristically rich areas can be tailored to bloom both before and after crop bloom to help sustain pollinators during the time when crops are not in bloom. In turn, bee populations can benefit from the consistent availability of resources in these areas of habitat enhancement. This dissertation explores how habitat enhancement affects nesting density of a common wild pollinator, Bombus impatiens . Further, this research also aims to determine how foraging preferences change and how bumble bee disease transmission and prevalence respond to habitat enhancement. Research was conducted at 15 commercial highbush blueberry ( Vaccinium corymbosum ) fields in southwest Michigan containing either no restoration, a newly planted restoration, or a mature (5-8 year old) restoration in the field margin from 2015 to 2017. I found that sites with new and mature restorations significantly boosted B. impatiens population abundance in the surrounding landscape. Sites with new restorations also had significant increases in B. impatiens colonies within one year of establishment and a tripling in density over the course of the three-year study. In my second study, at sites without restorations bumble bees foraged on a variety of flowers, whereas in sites with new and mature restorations, greater numbers of highly attractive flowers allowed bumble bees to retain floral constancy. Further, this study reveals the sensitivity of plant-pollinator networks to variation in habitat management in similar environments, highlighting the need for greater replication in studies that monitor changes in plant-pollinator networks over time. Finally, I found that the prevalence of Crithidia bombi , a common pathogen of bumble bees, in bumble bee gut tissue and on flower surfaces is significantly increased at sites with habitat enhancement. Flowers that were considered highly attractive were more likely to screen positive for a pathogen, highlighting the important role that flowers play in the horizontal transmission of pathogens. The results of this work shed new light on the underlying complexity of bee restoration in agricultural settings and will help inform best management practices for bee conservation in the future. This dissertation is dedicated to Kateri, who has supported my work in countless ways. iv ACKNOWLEDGEMENTS Thank you to everyone who has helped make this research happen and contributed to my growth as a person and as a scientist. A special thank you to Dr. Rufus Isaacs for his never ending support throughout my Ph.D. Rufus, I thank you profoundly for providing an atmosphere where I was encouraged to develop my own ideas and was able to grow as a scientist. Without your patience and constant enthusiasm for science, I would not have been able to complete my program. It truly has been a pleasure to work with you and have you as a mentor over the past four and a half years. Also, thank you to Dr. Brudvig, Dr. Huang, and Dr. Smith for your guidance and support. Our conversations not only helped me focus and develop my research ideas, but also provided sound career advice over the years. I would also like to give a big thank you to Dr. Jamie Strange, Dr. Amber Tripodi, Joyce Knoblett, and Dr. Jonathan Koch at the USDA-ARS Bee lab in Utah who spent countless hours teaching and troubleshooting molecular methods alongside me as I learned new techniques in their lab. I am so fortunate to be able to have such enthusiastic and fun collaborators. Thank you to everyone In the Isaacs lab who has helped me work on my project at any point in time. Thank you to Lauren Agnew, Gabe Trujillo, and Dr. Jason Gibbs in particular for your hard work during the field seasons. Also, thank you to everyone else who was able to help me sample during my crazy field seasons when others were unable to make it. Lastly, I want to give a big shout out to Keith Mason for his continued support throughout my program. Thank you Keith for always being willing to answer my questions as well as helping me organize my summer research plans. v I would like to thank Dr. Zsofia Szendrei for allowing me to perform my lab work in the Molecular and Chemical Ecology core facility over the past two years as I worked through my microsatellite analysis and pathogen screening. I would also like to give a special thanks to Dave VanderZee and Michael Pham for their persistence while troubleshooting and processing my bee and flower samples. Further, I thank Dr. Peter Graystock for his input and methods development for my pathogen screening research. I would also like to thank the Michigan State University Department of Entomology for their continued support of my research, funding, and development as a scientist. Further, I want to thank my other funding sources that have made my dissertation work possible. These funding sources include the Michigan State University College of Agriculture and Natural Resources and the USDA-NIFA SCRI program for the Integrated Crop Pollination project. Lastly, I would like to thank my friends and family for being a constant source of joy and moral support throughout my dissertation. In particular, I want to extend a very special thank you to my loving wife, Kateri. Thank you for being my friend and emotional support throughout my program and thank you for pushing me to be the best I can be. vi TABLE OF CONTENTS LIST OF TABLES ......................................................................................................................... ix LIST OF FIGURES ....................................................................................................................... xi CHAPTER 1: INFLUENCE OF HABITAT ENHANCEMENT ON BUMBLE BEE ECOLOGY AND PATHOGEN INTERACTIONS ............................................................................................1 INTRODUCTION ...............................................................................................................2 BUMBLE BEES ..............................................................................................................................6 WILDFLOWER PLANTINGS ...........................................................................................8 BUMBLE BEE NEST DENSITY .................................................................................................10 PLANT-POLLINATOR NETWORKS .............................................................................12 THE ROLE OF PATHOGENS IN BUMBLE BEE DECLINE ....................................................17 SUMMARY .......................................................................................................................21 CHAPTER 2: HABITAT ENHANCEMENT FOR POLLINATORS INCREASES LOCAL POPULATIONS OF BUMBLE BEES ..........................................................................................23 INTRODUCTION .............................................................................................................24 METHODS ....................................................................................................................................28 Site selection .......................................................................................................... 28 Habitat establishment .....................................................................................................................29 Floral surveys ........................................................................................................ 30 Sampling and observations ............................................................................................................30 Microsatellite analysis ...................................................................................................................31 Data analysis ..................................................................................................................................32 RESULTS ..........................................................................................................................33 Bombus impatiens collections .......................................................................................................33 Bombus impatiens colony estimation ..................................................................... 36 DISCUSSION ....................................................................................................................41 Bombus impatiens colony