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Diverse Allochthonous Resource Quality Effects on Headwater Stream Communities Through Insect-Microbe Interactions

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Diverse Allochthonous Resource Quality Effects on Headwater Stream Communities Through Insect-Microbe Interactions DIVERSE ALLOCHTHONOUS RESOURCE QUALITY EFFECTS ON HEADWATER STREAM COMMUNITIES THROUGH INSECT-MICROBE INTERACTIONS By Courtney Larson 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 2020 ABSTRACT DIVERSE ALLOCHTHONOUS RESOURCE QUALITY EFFECTS ON HEADWATER STREAM COMMUNITIES THROUGH INSECT-MICROBE INTERACTIONS By Courtney Larson Freshwater resources are vital to environmental sustainability and human health; yet, they are inundated by multiple stressors, leaving aquatic communities to face unknown consequences. Headwater streams are highly reliant on allochthonous sources of energy. Riparian trees shade the stream, limiting primary production, causing macroinvertebrates to consume an alternative food source. Traditionally, leaf litter fallen from riparian trees is the primary allochthonous resource, but other sources, such as salmon carrion associated with annual salmon runs, may also be important. An alteration in the quantity or quality of these sources may have far reaching effects not only on the organisms that directly consume the allochthonous resource (shredders), but also on other functional feeding groups. Allochthonous resources directly and indirectly change stream microbial communities, which are used by consumers with potential changes to their life histories and behavior traits. The objective of my research was to determine the influence allochthonous resources have on stream communities of macroinvertebrates and microbes using two systems: salmon carrion decomposition and emerald ash borer (EAB), Agrilus planipennis Fairmaire (Coleoptera: Buprestidae) invasion. It was hypothesized that with an alteration in allochthonous resource quantity and/or quality, the aquatic community would be altered. When salmon carcasses, a heterotrophic allochthonous resource, are introduced to a stream, the macroinvertebrate and microbial (bacteria and microeukaryotes) communities changed compared to a control stream reach without salmon carcasses over time. Specifically, Heptagenia (Heptageniidae: grazer) density was five times higher in the salmon reach compared to the control. In the salmon reach during year one, Stramenopiles (i.e., eukaryotic microbes) decreased in biofilm communities after two weeks of decomposition. Although unique microbial taxa, introduced to the naïve stream via salmon carrion, persisted in biofilms on benthic substrate and internal to insects during both years, those taxa represented <2% of the relative abundance in microbial communities. These results highlight the importance of allochthonous carrion resources in the microbial ecology of lotic biofilms and macroinvertebrates. Mortality of ash trees along stream corridors as a result of EAB invasion can result in canopy light gaps, which potentially alter subsequent organic matter subsidies into streams. We characterized the coarse woody debris, leaf litter and their associated bacterial communities (terrestrial and aquatic), and macroinvertebrate communities upstream, downstream, and at the center of one EAB-related canopy gap in six headwater streams of Michigan. Downstream locations had significantly lower dissolved oxygen and macroinvertebrate diversity, but we did not detect watershed and gap location effects on aquatic leaf litter. These findings reveal EAB invasion impacts stream ecosystems through indirect routes downstream of canopy gaps, yet leaf litter subsidies are resilient. Decomposition rates and macroinvertebrate colonization in leaf packs of four species (ash, oak, buckthorn, and cotton control) upstream, downstream, and at the center of one EAB-related canopy gap were assessed. There was no gap effect on decomposition rates. Shredder genera were more abundant on ash compared to buckthorn leaves, and macroinvertebrate diversity was significantly higher in the gap, compared to upstream and downstream. Our findings suggest a shift in macroinvertebrate communities in response to EAB by indirect routes of leaf litter subsidies and light availability. From these results, it can be concluded that allochthonous resources were a significant contributor to stream biodiversity patterns, and my dissertation research represents a significant contribution of knowledge on community assembly in streams. Dedicated to my father, Loren Larson, and my friend, Shengpan Lin, who both showed me the joy found in lakes, streams, and rivers. iv ACKNOWLEDGEMENTS First, I would like to thank my advisor, Eric Benbow, on his inspiration and guidance throughout my degree. I also thank my graduate committee; Michael Kaufman, Deborah McCullough, Jennifer Pechal, and Jan Stevenson; for their support through my studies. Additionally, gratitude is expressed to Rich Merritt for reviewing materials and sharing advice learned over years of studying Michigan’s streams. I would like to thank Patrick Engelken for his work on riparian forests affected by EAB, without which this research would not be possible. For funding this work I thank the National Science Foundation Graduate Research Fellowship Program; Great Lakes Fishery Trust; Hutson Memorial Endowment Fund; Gordon E. Guyer Endowed Fellowship in Aquatic Entomology; Merritt Endowed Fellowship in Entomology; MSU EEBB Summer Fellowship; KBS Graduate Student Research Fellowship; T. Wayne and Kathryn Porter Scholarship; Society for Freshwater Science General Endowment Fund; MSU CANR; AgBioResearch; and the College of Osteopathic Medicine. Countless MSU student employees and volunteers contributed to this work including Caleb Armstrong, Nicholas Babcock, Benjamin Bejek, McKinley Brewer, Nikki Cavalieri, Hepsiba Chepngeno, Saavas Constantinou, Rebecca Drenth, Emmy Fedor, Juanjuan Guo, Rachel Harvey, Daniel Hulbert, Katie Kierczynski, Heather Kittredge, Kelsie Kroll, Shengpan Lin, Sydney Manning, Jason Matlock, Mack McGinn, Nell McGuan, Robert Mobley Jr., Michael Orbain, Rachel Osborn, Emilie Parkansky, Dustin Phelps, Joseph Receveur, Connie Rojas, Katelyn Smiles, Brianna Timmons, Ariana Troia, Ryan Walquist, Courtney Weatherbee, Nicole Wonderlin, Allie Yackley, and Alison Zahorec, for assistance with fieldwork, lab work, and copy editing. Finally, I would like to thank my friends and family for their support. v PREFACE In this preface, I must address the current events that are challenging our world and hindering the goals of this dissertation. As of submission, There are 20.9 million cases of COVID- 19 caused by SARS-CoV-2, resulting in 760,000 deaths, and society has drawn to a halt to stop the spread (WHO, 2020). The MSU community was under a “Stay at home, stay safe” executive order from March 24 – June 1, 2020, effectively stopping all on campus research activities. Writing this dissertation during the COVID crisis was a challenge, and the closures directly impacted my ability to complete research goals for my dissertation. Specifically, DNA samples required to complete Chapters 3 and 4 were not able to be sequenced by the Michigan State University (MSU) genomics core. Chapter 3 uses a reduced bacterial dataset (nine samples missing), and Chapter 4 does not have any bacterial data associated with it at this time. The genomics core officially reopened on June 9, 2020, and eventual peer-reviewed publications of these chapters will include the complete bacterial datasets. vi TABLE OF CONTENTS LIST OF TABLES ......................................................................................................................... ix LIST OF FIGURES .........................................................................................................................x KEY TO ABBREVIATIONS ...................................................................................................... xiii CHAPTER 1: THE RIVER CONTINUUM CONCEPT: LESSIONS FROM THE PAST AND PERSPECTIVES FOR THE FUTURE ...........................................................................................1 Abstract ................................................................................................................................1 Introduction ..........................................................................................................................1 Stream ecology pre-1980 and the development of the RCC................................................5 The role of natural discontinuities .....................................................................................10 From the longitudinal gradient to patchy-structured systems ............................................15 Stream metacommunities as a conceptual framework for large-scale studies ...................17 Assessing the position in the river network and its effects on aquatic biodiversity ..........23 Conclusions ........................................................................................................................25 CHAPTER 2: MICROBIAL COMMUNITY RESPONSE TO A NOVEL SALMON RESOURCE SUBSIDY…... ...............................................................................................................................27 Preface................................................................................................................................27 Abstract ..............................................................................................................................27 Introduction ........................................................................................................................29
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