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UC Irvine UC Irvine Electronic Theses and Dissertations UC Irvine UC Irvine Electronic Theses and Dissertations Title Ventilatory airflow patterns and control of respiratory gas exchange in insects Permalink https://escholarship.org/uc/item/8h6528f4 Author Heinrich, Erica C. Publication Date 2015 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA, IRVINE Ventilatory airflow patterns and control of respiratory gas exchange in insects DISSERTATION submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY In Ecology & Evolutionary Biology by Erica Christine Heinrich Dissertation Committee: Professor Timothy J. Bradley, Chair Professor Matthew J. McHenry Professor Adriana D. Briscoe 2015 Chapter 1 © 2013 adapted from The Journal of Experimental Biology Chapter 2 © 2014 adapted from The Journal of Experimental Biology All else © 2015 Erica Christine Heinrich DEDICATION To my family for their love and support, to Alex, and to all of my colleagues and friends who have been instrumental in my development as a scientist. “Insects live and feed, move, grow and multiply like other animals; but they are so varied in form, so rich in species, and adapted to such diverse conditions of life that they afford unrivalled opportunities for physiological study.” -V. B. Wigglesworth ii TABLE OF CONTENTS Page LIST OF FIGURES iv LIST OF TABLES vi ACKNOWLEDGMENTS vii CURRICULUM VITAE viii ABSTRACT OF THE DISSERTATION xiii INTRODUCTION 1 The insect respiratory system 1 Ventilation 4 Control of the spiracles 6 Respiratory gas exchange patterns 7 CHAPTER 1: Coordinated ventilation and spiracle activity produce 12 unidirectional airflow in the Madagascar hissing cockroach, Gromphadorhina portentosa CHAPTER 2: Temperature-dependent variation in gas exchange pattern 40 and spiracular control in Rhodnius prolixus CHAPTER 3: The effect of respiratory pattern on oxidative damage in 70 Drosophila melanogaster CONCLUSION 92 REFERENCES 95 iii LIST OF FIGURES Page Figure 1 Schematic of the insect tracheal system 2 Figure 2 Mechanisms of spiracle valve function 4 Figure 3 Defined respiratory gas exchange patterns in insects 8 Figure 4 Discontinuous gas exchange in a Manduca sexta pupa 9 Figure 1.1 Directional airflow test methods 16 Figure 1.2 Discontinuous gas exchange in G. portentosa 23 Figure 1.3 Coordinated CO2 release, spiracle activity, and ventilation 24 Figure 1.4 Spiracle morphology 26 Figure 1.5 Spiracle coordination data from video recordings 27 Figure 1.6 Movement of tracer gas from thoracic chamber 30 Figure 1.7 Movement of tracer gas from abdominal chamber 31 Figure 1.8 Tracer gas movement and pressure differences 32 Figure 1.9 Spiracle activity and ventilatory movements 33 Figure 1.10 Schematic diagram of unidirectional airflow through the 37 tracheal system during ventilation Figure 2.1 Metabolic variation in temperature and feeding trials. 51 Figure 2.2 Respiratory patterns in fed and unfed Rhodnius prolixus 52 Figure 2.3 Activity and CO2 release patterns 53 Figure 2.4 Effects of feeding on respiratory pattern 55 Figure 2.5 Methods of respiratory pattern analysis 56 Figure 2.6 Effects of temperature on respiratory pattern 58 iv Page Figure 2.7 Effects of oxygen availability and feeding on respiratory pattern 60 Figure 3.1 Water release rates in hypercapnia and hyperoxia 83 Figure 3.2 Lipid peroxidation in D. melanogaster 85 Figure 3.3 Protein carbonyl formation in D. melanogaster (calorimetric) 85 Figure 3.4 Protein carbonyl formation in D. melanogaster (ELISA method) 86 Figure 3.5 Superoxide dismutase activity in D. melanogaster 86 v LIST OF TABLES Page Table 1 Summary of hypotheses regarding the function of discontinuous gas exchange 10 Table 1.1 Chi-squared results for independence of spiracle position 28 Table 2.1 Respiratory pattern characteristics in oxygen treatments 59 vi ACKNOWLEDGMENTS Financial support for this research was provided by the National Science Foundation [IOS- 0920683 to Timothy J. Bradley], the US Department of Education (GAANN Fellowship), The Society for Integrative and Comparative Biology, and Sigma Xi. Chapter 1 and 2 of this dissertation are reprinted with permission from The Journal of Experimental Biology. I would like to thank Dr. Timothy J. Bradley for his mentorship and support. His encouragement allowed me to tackle difficult questions while ensuring that I never lost sight of the bigger picture. I would also like to thank my committee members, Dr. Adriana D. Briscoe and Dr. Matthew J. McHenry for their guidance, and for providing feedback on this dissertation. Dr. Samuel E. Schriner and Dr. Donovan P. German provided direction and assistance with much of the biochemical work described in Chapter 3. I thank Dr. German for the kind use of his lab space. James N. Kezos and the Rose Laboratory at UC Irvine provided invaluable assistance with the rearing and collection of Drosophila for the experiments in Chapter 3. I would also like to thank Dr. Jon F. Harrison and Dr. Thomas Förster for sharing their ideas and feedback on this work, and Dr. John R. B. Lighton for his technical assistance with our respirometry systems. I would especially like to thank the UC Irvine Comparative Physiology Group for playing a key role in the development of the work described in this dissertation as well as my own professional development. I am grateful to have shared each Friday with such an exceptional group of scientists. vii CURRICULUM VITAE Erica Christine Heinrich EDUCATION University of California, Irvine, CA Ph.D. in Ecology and Evolutionary Biology, 2015 Dissertation: Ventilatory airflow patterns and control of respiratory gas exchange in insects Advisor: Dr. Timothy J. Bradley Arizona State University, Tempe, AZ B. S. in Molecular Biosciences and Biotechnology, 2010 B. A. in History, 2010 FELLOWSHIPS 2012-2014 Graduate Aid in Areas of National Need (GAANN) Fellowship, US Dept. of Education 2009-2010 School of Life Sciences Undergraduate Research Fellowship, Arizona State University 2008-2009 Beckman Scholar Fellowship, Arnold and Mabel Beckman Foundation 2007 School of Life Sciences Undergraduate Research Fellowship, Arizona State University RESEARCH AND TRAVEL GRANTS 2014 Sigma Xi Grant in Aid of Research 2012 Society for Integrative and Comparative Biology (SICB) GIAR 2011-2014 UCI Department of Ecology and Evolutionary Biology Travel Award 2011-2014 UCI Biological Sciences Dean’s Office Travel Award 2010 The American Physiological Society Research Recognition Travel Award HONORS AND AWARDS 2013 Grover C. Stephens Memorial Fellowship Award, UC Irvine 2011-2013 Charlotte Mangum Student Support Award, SICB 2012 SICB Best Student Poster Award, Division of Comparative Physiology and Biochemistry 2010 Jonathan Wade Psoras Award, Arizona State University 2010 Ametek-Edax Best Poster Award, Arizona Imaging and Microanalysis Society 2006-2010 Provost’s Scholarship, Arizona State University PUBLICATIONS [4] Contreras, H. L., Heinrich, E. C., and Bradley, T. J. (2014) Hypotheses regarding the Discontinuous Gas Exchange Cycle (DGC) of insects. Current Opinion in Insect Science 4: 48-53. [3] Heinrich, E. C. and Bradley, T. J. (2014) Temperature dependent variation in gas exchange patterns and spiracular control in Rhodnius prolixus. The Journal of Experimental Biology 217: 2752-2760. viii (publications continued) [2] Heinrich, E. C., McHenry, M. J., and Bradley, T. J. (2013) Coordinated ventilation and spiracular activity produce unidirectional airflow in the hissing cockroach, Gromphadorhina portentosa. The Journal of Experimental Biology. 216: 4473-4482. [1] Heinrich, E. C., Farzin, M., Klok, C.J., McKinley, B., Harrison, J.F. (2011) The effect of developmental stage on the sensitivity of cell and body size to hypoxia in Drosophila melanogaster. The Journal of Experimental Biology 214: 1419-1427. IN PREPARATION [1] Heinrich, E. C., Fragata, I. Kezos, J. N., Rose, M. R., Matos, M., Bradley, T. J., Mueller, L.D., and Santos, M. Confounding factors in thermal ramping assays: An empirical test of mechanistic models. [2] Heinrich, E. C., Gray, E. M., Vorhees, A. S., Meigher, S., Schriner, S. E., Grun, F., and Bradley, T. J. Studies of Insects Provide Insights into the Thermal Death of Mitochondria. (submitted) [3] Heinrich, E. C., German, D. P., and Bradley, T. J. The effect of respiratory pattern on oxidative damage in insects. PUBLISHED ABSTRACTS [8] Heinrich, E. C. and Bradley, T. J. (2015) Oxidative stress during disruption of gas exchange patterns in insects. Integrative and Comparative Biology. 55: e76. [7] Heinrich, E. C., Gray, E. M., Vorhees, A., Bradley, T. J. (2014) Post-mortal CO2 release in insects after death at high temperature. FASEB J. 28: 1101.14. [6] Heinrich, E. C. and Bradley, T. J. (2014) Post-mortal CO2 release by insects at high temperatures. Integrative and Comparative Biology. 54: e88. [5] Heinrich, E. C. and Bradley, T. J. (2013) Temperature dependent variation in respiratory patterns and spiracular control in Rhodnius prolixus. FASEB J. 27: 1149.6. [4] Heinrich, E. C. and Bradley, T. J. (2013) Temperature dependent variation in respiratory patterns and spiracular control in Rhodnius prolixus. Integrative and Comparative Biology. 53: e89. [3] Heinrich, E. C., McHenry, M. J., and Bradley, T. J. (2012) Spiracular activity and respiratory airflow in the Madagascar hissing cockroach (Gromphadorhina portentosa). Integrative and Comparative Biology. 52: e260. [2] Heinrich, E.C., Klok, C.J., Harrison, J.F., Farzin, M., and McKinley, B. (2010)
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