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TO TEMPERATE FOREST NUTRIENT CYCLING by ANGELA MYER

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TO TEMPERATE FOREST NUTRIENT CYCLING by ANGELA MYER CONTRIBUTIONS OF SUBTERRANEAN TERMITES (RETICULITERMES) TO TEMPERATE FOREST NUTRIENT CYCLING by ANGELA MYER (Under the Direction of Brian T. Forschler) ABSTRACT Subterranean termites (Reticulitermes spp.) are abundant insects that are ecosystem engineers. This work includes a series of reductionist experiments that investigate the contributions of native subterranean termites (Reticulitermes spp.) to temperate forest nutrient cycling through their roles as wood degraders, soil fauna, and contributors of greenhouse gases. The first research study considers subterranean termites as a member of the saproxylic insect guild and surveyed the elemental composition of frass from various wood-feeding insects. The second study aimed to ‘follow the frass’ of Reticulitermes to gauge their contributions to soil nutrient cycling and provided quantitative evidence that subterranean termites translocate C and Ca from wood to soil. The third study used wood grown in elevated CO2 as a stable isotope tracer to measure wood-based carbon flow within a closed system. INDEX WORDS: Subterranean termites, ecology, ecosystem engineers, wood decomposition, soil processes, biogenic structures, saproxylic insects, nutrient cycling, elemental composition, frass, shelter tubes, greenhouse gas emissions, cryptic, isotope tracer, carbon cycle CONTRIBUTIONS OF SUBTERRANEAN TERMITES (RETICULITERMES) TO TEMPERATE FOREST NUTRIENT CYCLING by ANGELA MYER B.S.E.S, University of Georgia, 2013 A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY ATHENS, GEORGIA 2019 © 2019 Angela Myer All Rights Reserved CONTRIBUTIONS OF SUBTERRANEAN TERMITES (RETICULITERMES) TO TEMPERATE FOREST NUTRIENT CYCLING by ANGELA MYER Major Professor: Brian T. Forschler Committee: Michael D. Ulyshen Kamal J.K. Gandhi Electronic Version Approved: Suzanne Barbour Dean of the Graduate School The University of Georgia August 2019 DEDICATION I dedicate this work to my husband and child, who were with me for this journey and provided me with unconditional love. iv ACKNOWLEDGEMENTS I would like to thank Dr. Forschler for his support as my advisor and for the travel opportunities and professional mentorship he has provided me throughout the years. I also want to show appreciation to all the people who made my dissertation possible, including Kim Hunter, Samantha Joye, Tom Maddox, Jeff Minucci, Gerd Gleixner, Carl Trettin, Mike Ulyshen, Kamal Gandhi, Joe McHugh, Christie Stegall, Scott Horn, Jena Johnson, Zhe Lyu, Taiwo Soloman, Bernie Whitman, Tae Young Lee, Charlie Braman, Mark Myer, Allison Johnson, Kelly Mayes, and many more not listed here. v TABLE OF CONTENTS Page ACKNOWLEDGEMENTS .............................................................................................................v CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW .....................................................1 Termite taxonomy ....................................................................................................1 Wood decomposers ..................................................................................................2 Soil fauna .................................................................................................................5 Source of greenhouse ..............................................................................................7 Ecosystem engineers ...............................................................................................9 Organization of thesis ...........................................................................................11 Bibliography .........................................................................................................12 Figures ...................................................................................................................28 2 ELEMENTAL CONCENTRATIONS IN THE FRASS OF SAPROXYLIC INSECTS SUGGEST A ROLE IN NUTRIENT CYCLING .......................................................31 Abstract ..................................................................................................................32 Introduction ............................................................................................................33 Methods..................................................................................................................36 Results ....................................................................................................................39 Discussion ..............................................................................................................42 Acknowledgements ................................................................................................47 vi Bibliography ..........................................................................................................48 Tables .....................................................................................................................54 Figures....................................................................................................................55 Appendix ................................................................................................................60 3 EVIDENCE FOR THE ROLE OF SUBTERRANEANT TERMITES (RETICULITERMES SPP.) IN TEMPERATE FOREST NUTRIENT CYCLING ...63 Abstract ..................................................................................................................64 Introduction ............................................................................................................65 Methods..................................................................................................................67 Results ....................................................................................................................73 Discussion ..............................................................................................................75 Acknowledgements ................................................................................................86 Bibliography ..........................................................................................................87 Tables .....................................................................................................................99 Figures..................................................................................................................100 Appendices ...........................................................................................................105 4 THE FATE OF CARBON UTILIZED BY THE SUBTERRANEAN TERMITE RETICULITERMES FLAVIPES ..............................................................................118 Abstract ................................................................................................................119 Introduction ..........................................................................................................120 Methods................................................................................................................122 Results ..................................................................................................................128 Discussion ............................................................................................................130 vii Bibliography ........................................................................................................136 Tables ...................................................................................................................145 Figures..................................................................................................................149 Appendices ...........................................................................................................156 5 SUMMARY ...............................................................................................................168 viii CHAPTER 1 INTRODUCTION AND LITERATURE REVIEW The purpose of this work is to provide quantitative evidence on how the ecological roles of subterranean termites (Reticulitermes spp.) as wood degraders, soil fauna, and greenhouse gases emitters contribute to nutrient cycling. The following review examines Reticultermes as ecosystem engineers in temperate forests and discusses current knowledge regarding their role in recycling nutrients found in wood. Despite their prevalence, there is scant information regarding how these eusocial, cryptic soil animals influence resource flows in the temperate forest environment they inhabit. My research considered, based on the theoretical framework provided by Wood and Sands (1978), that Reticulitermes alter nutrient availability to other organisms through ecological pathways analogous to their mound-building relatives (Figure 1.1). The pathways considered included consumption and transformation of food (mainly woody debris), influence on nutrient cycles, and the emission of greenhouse gases in a series of reductionist experiments (Figure 1.1). Termite Taxonomy Termites are insects that were previously placed in order Isoptera but are now taxonomically nested in the cockroach order Blattodea (Blatteria), placed either as the Infraorder Isoptera or the epifamily Termitoidae (Beccaloni and Eggleton 2013, Krishna et al. 2013). All families except Termitidae are considered “lower” termites, which are characterized by the presence of gut protists (Krishna
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