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Philaenus Spumarius) THE BIOMECHANICS AND ENERGETICS OF XYLEM FEEDING IN THE MEADOW SPITTLEBUG (PHILAENUS SPUMARIUS) by Elisabeth Anne Bergman B.Sc. (Hons.), The University of Arizona, 2017 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in The Faculty of Graduate and Postdoctoral Studies (Zoology) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) January 2021 © Elisabeth Anne Bergman, 2021 The following individuals certify that they have read, and recommend to the Faculty of Graduate and Postdoctoral Studies for acceptance, a thesis entitled: The biomechanics and energetics of xylem feeding in the meadow spittlebug (Philaenus spumarius) submitted by Elisabeth Anne Bergman in partial fulfillment of the requirements for the degree of Master of Science in Zoology Examining Committee: Philip G.D. Matthews, Associate Professor, Department of Zoology, UBC Supervisor Robert E. Shadwick, Full Professor, Department of Zoology, UBC Supervisory Committee Member Katie E. Marshall, Assistant Professor, Department of Zoology, UBC Additional Examiner Additional Supervisory Committee Members: Colin J. Brauner, Full Professor, Department of Zoology, UBC Supervisory Committee Member Sean T. Michaletz, Assistant Professor, Department of Botany, UBC Supervisory Committee Member ii Abstract The watery sap within the xylem vessels of vascular plants is thought to exist under high tensions (i.e., negative pressures) that routinely exceed -1 MPa, as well as being very nutrient poor. While this should make xylem sap an energetically unfavourable source of nutrition, some Hemipteran insects within the suborder Auchenorrhyncha feed on it exclusively, extracting copious quantities of this liquid using a muscular cibarial pump. However, neither the strength of the insect’s suction, and thus the maximum xylem tensions that the insect can feed at, nor the energetic cost of xylem feeding, have been determined. Here I used adult meadow spittlebugs (Philaenus spumarius) to address this gap in knowledge. First, the maximum suction they could generate was calculated from biomechanical principles using morphological data obtained from micro-CT scans of their cibarial pump. Second, the metabolic rates (MR) of adult P. spumarius were measured while feeding on hydroponically-grown plants (Vicia faba, Pisum sativum, and Medicago sativa) with known xylem tensions, while their rate of xylem sap extraction and cibarial pumping frequency (fpump) were obtained from simultaneously recorded video footage. Furthermore, during these feeding experiments, the plants were exposed to the osmolyte polyethylene glycol (PEG), revealing how the insects changed their feeding behaviour in response to increasing xylem tensions. These findings indicate that the cibarial pump is capable of generating an average maximum tension of -1.3 MPa. This is higher than any xylem tension recorded from their food plants using the Scholander-Hammel pressure bomb method. In addition, while it was calculated that the xylem sap likely contains sufficient sugars to sustain the energetic requirements of pumping, the total MR of the feeding insect could be satisfied only by assuming contributions from amino acids. iii Lay Summary Xylem-feeding insects like the meadow spittlebug (Philaenus spumarius) are important agricultural pests. As vectors of Xyllela fastidiosa, these insects are responsible for spreading the various plant diseases that arise from this bacterium. While previous research on P. spumarius has focused on their roles as vectors, there has been less focus on how they extract xylem sap in the first place with plant xylem fluid being under considerable tension. This thesis aimed to determine the range of tensions P. spumarius can successfully feed on, quantify the metabolic cost of feeding on xylem sap, and determine how the adults of this species, called froghoppers, change their feeding behaviour in response to increases in xylem tension. The results provide insight into the feeding mechanics and physiology of P. spumarius, and demonstrate a novel approach of using an insect to measure xylem tensions in situ. iv Preface This thesis is the original, unpublished work by the author, Elisabeth A. Bergman, with editorial feedback from Drs. Philip G.D. Matthews, Colin J. Brauner, Sean T. Michaletz, and Robert E. Shadwick. Elisabeth A. Bergman was responsible for the collection and analysis of all experimental data. Dr. Matthews was the supervisory author and was involved in the conception of all experiments. Micro-CT scans were performed at McGill University. Embedded mouthpart sectioning was performed by Wax-It and TEM was performed at the Bioimaging Facility, both at UBC (Vancouver). v Table of Contents Abstract ......................................................................................................................................... iii Lay Summary ................................................................................................................................ iv Preface ............................................................................................................................................ v Table of Contents .......................................................................................................................... vi List of Tables .................................................................................................................................. x List of Figures ............................................................................................................................... xi List of Symbols and Abbreviations ............................................................................................ xii Acknowledgements ..................................................................................................................... xiv Dedication .................................................................................................................................... xvi Chapter 1: Introduction ................................................................................................................ 1 1.1 Overview ......................................................................................................................... 1 1.2 Xylem tension of plants ................................................................................................... 2 1.3 Anatomy of xylem-feeding insects .................................................................................. 5 1.4 Anatomical and physiological dilemmas ......................................................................... 7 1.5 Research questions .......................................................................................................... 8 Chapter 2: Comparing the xylem tensions obtained phytologically, physiologically, and morphologically ........................................................................................................................... 10 2.1 Introduction ................................................................................................................... 10 2.2 Materials and Methods .................................................................................................. 11 2.2.1 Animals ...................................................................................................................... 11 2.2.1.1 Spittlebug nymphs and froghopper adults ......................................................... 11 vi 2.2.1.2 Body mass ......................................................................................................... 12 2.2.2 Plants ......................................................................................................................... 12 2.2.3 Transmission electron microscopy ............................................................................ 14 2.2.3.1 Preparation ......................................................................................................... 14 2.2.3.2 Sectioning and imaging ..................................................................................... 14 2.2.3.3 Analysis ............................................................................................................. 14 2.2.4 Micro-CT scans ......................................................................................................... 15 2.2.4.1 Preparation ......................................................................................................... 15 2.2.4.2 Scanning ............................................................................................................ 15 2.2.4.3 Reconstruction and segmentation ...................................................................... 16 2.2.4.4 Analysis ............................................................................................................. 18 2.2.5 Respirometry trials .................................................................................................... 19 2.2.5.1 Measuring resting metabolic rate (RMR) .......................................................... 19 2.2.5.2 Measuring feeding metabolic rate ..................................................................... 20 2.2.5.3 Calculating metabolic power from respirometry traces .................................... 22 2.2.5.4 Recording temperature ...................................................................................... 22 2.2.5.5 Recording videos ..............................................................................................
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