RESPIRATORY MECHANICS OF HIGH ALTITUDE WATERFOWL by Julia McRae York B.Sc., The University of British Columbia 2015 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) August, 2016 © Julia McRae York, 2016 ABSTRACT Birds living at high altitude (>3,000 meters) are not only able to cope with reduced oxygen availability due to hypobaria, but they are also able to achieve one of the most metabolically costly form of locomotion at these altitudes: flight. To perform such a metabolically demanding activity, in addition to energetically expensive daily tasks such as foraging, predator escape, and reproduction, all in oxygen limited (hypoxic) conditions, means that high altitude birds must enhance oxygen supply to maintain oxygen homeostasis. The primary means of increasing oxygen supply is increasing ventilation of the respiratory gas exchange surface. However, the metabolic cost of ventilation is unknown for birds at rest, as is whether this cost varies among bird species. In this thesis, the cost and work of breathing are compared in fourteen avian species to determine whether variation in the work of breathing is due to mechanical or morphological changes in the respiratory system, and if any observed changes are associated with living at high altitude. High altitude birds tended to have large and compliant respiratory systems compared with low altitude taxa, which reduces the work of breathing. However, the evidence also suggests that respiratory morphology and mechanics in birds may be more constrained by life history strategy than by evolutionary time at altitude, although species in this study that have no high altitude sister taxa (their lineages have never radiated to high altitude) struggled the most with increasing oxygen supply. Finally, birds at rest were estimated to have a lower cost of breathing than mammals, contrary to the hypothesis that cost of breathing would be high in birds due to the heavy flight muscles weighing down the sternum. ii PREFACE This thesis is the original intellectual product of the author, J. York, under the supervision of W.K. Milsom. Experimental procedures were performed according to UBC Animal Care Committee protocols A12-0013 and A16-0019 under the guidelines of the Canadian Council on Animal Care. Wild animals were collected in accordance with Oregon Department of Fish and Wildlife Scientific Taking Permit 101-15 and el Ministerio del Ambiente de Perú carta numero 005-2014 y resolución directoral numero 36087-2012. The data chapters in this thesis (chapters 2 and 3) are being prepared to submit for publication. The contributions of the listed authors are as follows: Chapter 2: JMY collected and analyzed the data, prepared the figures, and wrote the manuscript. MS analyzed the CT scan data. WKM assisted with data collection and manuscript revisions. Chapter 3: JMY collected and analyzed the data, prepared the figures, and wrote the manuscript. BAC assisted in animal care during experiments. CMI and SLL provided hypoxic ventilatory response data. LA and RC assisted with animal capture and care. GRS, NJD, and PBF assisted with field work. KGM assisted with field work and provided phylogenetic data. WKM assisted with data collection and manuscript revisions. iii TABLE OF CONTENTS Abstract .......................................................................................................................... ii Preface .......................................................................................................................... iii Table of Contents ........................................................................................................ iv List of Tables ................................................................................................................ vi List of Figures ............................................................................................................ vii List of Symbols and Abbreviations ............................................................................ ix Acknowledgements ....................................................................................................... x Chapter 1: Introduction ................................................................................................. 1 Definitions ........................................................................................................... 7 Compliance ................................................................................................ 7 Resistance ................................................................................................. 9 Tau ............................................................................................................ 9 Respiratory system volumes ...................................................................... 9 Effective ventilation, efficacy, and optimal breathing ............................... 10 Chapter 2: Respiratory mechanics, morphometrics, and cost of breathing of the bar-headed goose (Anser indicus), barnacle goose (Branta leucopsis), and Andean goose (Chloephaga melanoptera) ............................................................... 13 Introduction ....................................................................................................... 13 Methods ............................................................................................................. 17 Respiratory mechanics ............................................................................ 17 Lung mass and tracheal volumes ............................................................ 17 CT scans .................................................................................................. 20 Results .............................................................................................................. 20 Respiratory capacities.............................................................................. 20 CT scans ................................................................................................. 21 Static mechanics ...................................................................................... 21 Dynamic mechanics ................................................................................. 21 Discussion ........................................................................................................ 24 Future directions ...................................................................................... 29 Chapter 3: Respiratory mechanics of eleven avian species resident at different altitudes ....................................................................................................................... 43 Introduction ....................................................................................................... 43 Methods ............................................................................................................. 47 Results .............................................................................................................. 50 Respiratory system morphology and static mechanics ............................ 51 Cost and benefit of increasing tidal volume ............................................. 52 Dynamic mechanics and work of breathing in vivo .................................. 53 Do birds use an energetically optimal combination of tidal volume and breathing frequency ................................................................................. 54 Discussion ........................................................................................................ 55 Morphological and mechanical variation associated with altitude ............ 55 Costs and benefits of deep versus rapid breathing .................................. 56 Cost of breathing in vivo .......................................................................... 58 When do birds breathe optimally? .......................................................... 58 Those ruddy ducks! ................................................................................. 59 iv Chapter conclusions ................................................................................ 60 Future directions ...................................................................................... 62 Chapter 4: Discussion ................................................................................................ 83 Sternal recumbency ........................................................................................... 83 Subtracting endotracheal tube resistance .......................................................... 84 Lung volume estimates ....................................................................................... 85 Avian respiratory morphometry .......................................................................... 86 Tracheal volumes ............................................................................................... 88 Avian respiratory mechanics .............................................................................. 90 Cost of breathing ................................................................................................ 90 References ................................................................................................................. 100 Appendix ...................................................................................................................