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The Role of Metabolic Activation and Colony Integration

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The Role of Metabolic Activation and Colony Integration ABSTRACT METABOLIC SCALING IN COLONIAL ANIMALS: THE ROLE OF METABOLIC ACTIVATION AND COLONY INTEGRATION Maram Almegbel, MS Department of Biological Sciences Northern Illinois University, 2018 Neil W. Blackstone, Director Metabolism, one of the canonical features of life, shows a clear correlation to organismal size. Metabolic scaling is explaining the relationship between organism body mass and metabolic rate. To explain the relationship between the metabolism and body size, several factors have to be examined, including resource uptake, usage, and transportation of resources throughout the body. Empirically, metabolism usually scales as approximately mass to the 3/4 power. Many theories seek to explain this relationship in terms of surface area to volume. These theories typically model unitary organisms as spheres, with surface area to volume increasing as roughly volume to the 2/3 power. In this context, the study of metabolic scaling in colonial or modular animals may provide insight. These organisms differ significantly from unitary organism, e.g., in geometry and hence surface -to- volume relationships. Modular organisms can be modeled as “sheet,” with surface area increasing area roughly in proportion to volume. Nevertheless, the biology of colonial organisms remains relatively poorly known. For instance, it is widely recognized that metabolic state affects metabolic scaling in unitary organisms, but the effects of metabolic state on scaling in modular organisms is untested. In this context, the intraspecific metabolic scaling relationships were examined in two colonial cnidarians, Hydractinia symbiolongicarpus and Sympodium species. The former is heterotrophic and circulates gastrovascular fluid using muscular contractions, while the latter has photosynthetic symbionts and circulates gastrovascular fluid using cilia. Nevertheless, both are “sheet-like,” encrusting forms. Experimental colonies of each species were grown on 12 mm diameter cover glass, and metabolism was measured by oxygen uptake in the dark ( Hydractinia 20.5 o C, Sympodium 27o C). Several size variables were measured using a protein assay and image analysis (total protein, total area, feeding polyp area, number of feeding polyps, and number of reproductive polyps). Principal components analysis of the log-transformed variance covariance matrix in Hydractina suggests that the best size measure is based on total protein, feeding polyp area, and number of feeding polyps. Using oxygen uptake regressed against this size measure, the slope was not significantly different from 2/3 or 3/4 but was significantly less than 1. Using the individual variables as size measures yielded various exponents, yet in every case there was no difference between fed (active) and unfed (resting) colonies. The differences in the intercept suggests that feeding activates metabolism by roughly 2.5 times, and a paired comparison t test shows that this difference is highly significant. In corals containing photosynthetic symbionts, light has been shown to activate metabolism in the same manner as feeding activates a heterotroph. Nevertheless, with Sympodium , colonies that were dark adapted exhibited similar oxygen uptake as colonies that were light treated (140 μm) for 90 min. With regard to metabolic scaling in this species, several size variables were measured using a protein assay and image analysis (total protein, total area, polyp area, number of feeding polyps and weight). Principal components analysis of the log- transformed variance covariance matrix in Sympodium suggests that the best size measure is based on total weight, followed by total polyps area and total area. Using oxygen uptake regressed against this size measure, the slope was not significantly different from < 3/4 but was significantly less than 1. As colonial animals can provide more understanding of metabolic scaling, it will possibly need more investigation for these colonial animals and the factors that might be affecting metabolic scaling. NORTHERN ILLINOIS UNIVERSITY DEKALB, ILLINOIS MAY 2018 ROLE OF COLONY INTEGRATION IN METABOLIC SCALING OF COLONIAL ANIMALS BY MARAM ALMEGBEL © 2018 Maram Almegbel A THESIS SUBMITTED TO THE GRADUATE SCHOOL IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE MASTER OF SCIENCE DEPARTMENT OF BIOLOGICAL SCIENCES Thesis Director: Neil W. Blackstone ACKNOWLEDGEMENTS First and foremost, I would like to thank my advisor and mentor, Dr. Neil W. Blackstone, for all of the help and advice he has provided over the past few years. I would also like to acknowledge my committee members, Dr. Jozef J. Bujarski and Dr. Shengde Zhou, for their valued suggestions and advice. DEDICATION This work is dedicated to the soul of my father, Nasser Almegbel, and to the soul my mother, Dulail Alnumai. It is also dedicated to my husband, Mohammed Abahussain, for the invaluable love and support he has given me. TABLE OF CONTENTS Page LIST OF TABLES…………………………………………………………………………... vi LIST OF FIGURES…………………………………………………………………………... vii Chapter 1. INTRODUCTION…………………….…………………………………………….... 1 Metabolic Scaling in Group-Living Organisms………………………………. 4 Metabolic Activation………………………………………………………....... 9 Metabolic Scaling and Modular Animals……………………………………. 10 Current Research……………………………………………………………... 16 2. MATERIALS AND METHODS …………………….………………………………… 18 Laboratory Study Species and Culture Conditions……………………………. 18 General Imaging and Image Analysis Protocols……………………………. 22 Measures of Oxygen Uptake Rate…………………………………………… 24 Protein Assay…………………………………………………………………. 26 Statistical Analysis…………………………………………………………… 28 3. RESULTS…………………….……………………………………………................... 30 Oxygen Uptake for Hydractinia symbiolongicarpus …………………………..... 31 The Best Model for Converting Absorbance to Total Protein…………………... 32 Metabolic Activation…………………………………………….................... 32 Metabolic Scaling in H. symbiolongicarpus with Individual Size Measures……. 33 v Chapter Page Metabolic Scaling in H. symbiolongicarpus with Refined Size Measures…... 40 Oxygen Uptake for Sympodium sp…………………………………………. 45 Metabolic Scaling of Sympodium sp……………………………………….... 47 . 4. DISCUSSION….……………………………………………………........................... 51 Future Directions …………………………………………………………… 54 REFERENCES…………………….……………………………………….…………… 55 LIST OF TABLES Table Page 1. Summary of metabolic activation using the paired-comparison t test………….. 33 2. Least-squares slopes (± standard errors) and intercepts for oxygen uptake and individual size measures under fed unfed conditions …................................... 34 3. The linear combination of different variables included in the principal components analysis…………………… 42 4. Metabolic scaling of log oxygen uptake and PC1 under fed and unfed conditions…………………………………………………………………...… 42 5. Difference in metabolic rates for Sympodium sp. under different experimental conditions……………………………………………………………………… 47 6. Least-squares regression slopes of indicated variable and log oxygen uptake …49 7. The linear combination of different variables included in the principal components analysis………………………………………. .…… 49 8. Combined effect of polyp area, total area, total protein, and number of feeding polyps and weight on oxygen uptake…………………………………… 49 LIST OF FIGURES Figure Page b 1. Kleiber’s law, Y = Y oM …………..…………..…….….......................................... 2 2. Kleiber’s law, Log Y = Log Y o + b log M…....…....…....…....…....…....…....….... 3 3. Schemata of the phylogenetic relationships of cnidarians, showing the affinities of the two -study species.………….. 16 4. Hydractinia symbiolongicarpus species growing on round cover glass.…………… 19 5. Sympodium species growing on terra cotta.............………………………...…............20 6. Oxygen uptake concentration versus time for a representative fed colony of H. symbiolongicarpus …………………………………………………………………….30 7. Oxygen uptake concentration versus time for a representative unfed colony of H. symbiolongicarpus …………………………………………………………………… 31 8. Translating measured absorbance (x axis) into total protein (y axis) for H. symbiolongicarpus using linear values……………………………………………… 31 9. Translating measured absorbance (x axis) into total protein (y axis) for H. symbiolongicarpus using log-linear values………………………………………........32 10. Translating measured absorbance (x axis) into total protein (y axis) for H. symbiolongicarpus using log-log values………………………………………………32 11. The bivariate graph of absolute values of slopes of oxygen uptake regressions for fed and unfed colonies………… ……………………………………………............. 33 12. Least-squares regression of log-transformed oxygen uptake and feeding polyp area for fed colonies of H. symbiolongicarpus , 20.5 C…………………………………… 35 viii Figure Page 13. Least-squares regression of log-transformed oxygen uptake and feeding polyp area for unfed colonies of H. symbiolongicarpus , 20.5 C………... 35 14. Least-squares regression of log-transformed oxygen uptake and total area for fed colonies of H. symbiolongicarpus , 20.5 C…………………………………… 36 15. Least-squares regression of log-transformed oxygen uptake and total area for unfed colonies of H. symbiolongicarpus , 20.5 C……….… 36 16. Least-squares regression of log-transformed oxygen uptake and total protein for fed colonies of H. symbiolongicarpus , 20.5 C…………………………… 37 17. Least-squares regression of log-transformed oxygen uptake and total protein for unfed colonies of H. symbiolongicarpus , 20.5 C…………… 37 18. Least-squares regression of log-transformed oxygen uptake and number of feeding polyps for fed colonies of H. symbiolongicarpus
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