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The Ecology and Feeding Biology of Thecate

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The Ecology and Feeding Biology of Thecate -1- THE ECOLOGY AND FEEDING BIOLOGY OF THECATE HETEROTROPHIC DINOFLAGELLATES by Dean Martin Jacobson A.B., Occidental College 1979 SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution February, 1987 e Dean Martin Jacobson The author hereby grants to M.I.T. and W.H.O.I. permission to reproduce and to distribute copies of this thesis document in whole or in part. Signature of Au thor_--.....~-=-~~_ ...........~iIlfII"I'V"-...........,.;..p;-~~ _ Department of Biology, Ma sac usetts Institute of Technology and the Joint Program in Ocea og aphy, Massachusetts Institute of Technology/Woods Hole Ocea graphic Institution, February, 1986. Certified by _----L~...-:c-.:.• ......:::z:..::-~-::..,.c£....=:....------:...---------------­ Donald M. A~rsont Thesis Supervisor Accepted by --"X:,,-==~,e:--..;;-,------.;;;,.--------------------­ Sallie W. Chisholm, Chairman, Joint Committee for Biological Oceanography, Massachusetts Institute of Technology/Woods Hole Oceanographic Institution. -2- -3- Table of Contents List of Figures and Tables 5 Abstract. 7 Aknow1edgements •••••••••••.••••••••••••••••••••••••••.•••••••••••••.•• 9 Introduction 11 References .••••••••••••••••••••••••••••••••••••••••••••••••••••. 21 Chapter 1. Population Dynamics of Heterotrophic Dinoflagellates in a Temperate Esturary •••••••••••••••••••••••••••••••••••• 23 Abstract 25 Introduction ••••..•••.••.••••••.•••••••••••.•••••••••••.•••.••.• 26 Methods and Materials .••.••••.•.••••.•••••••••••••.•.••••••.•••• 28 Taxonomic Notes ..........................................•.. 30 Results •.•••••••.••••.••••••••••••••••••••••••••••••.•••••••.•.• 31 Discussion 34 References •.•••••••••••••.•••• ; •••••••••••••••••••.•••..•.•••••• 40 Chapter 2. Thecate Heterotrophic Dinoflagellates: Feeding Behavior and. Mechanisms ••••••••••••.•••••••••••••••••.••••• 57 Abstract . 59 Introduction . 60 Methods and Materials •••••••••••••••••••••••••••••••••••••••••.• 61 ReBults ..................•...................................... 62 Precapture . 63 Capture . 64 Pseudopod Deployment •••••••••••••••••••••••••••••••••••••••• 66 Digestion . 67 Re tract ion . 69 Discussion ...................................................................... 70 References . 78 Chapter 3. Growth and Grazing Rates of Protoperidinium hirobis Abe, a Thecate Heterotrophic Dinoflagellate ••••••••••••••••••••• 89 Abstract . 91 Introduction .. 92 Methods and Materials .. 93 Culture Conditions and Organism •••••••••••••••••••••••••••• 94 Ingest~on Rates . 95 Experimental Protocol . 96 Diel Time Course Experiment . 97 Results . 98 Discussion . 100 References . 105 Chapter 4. Ultrastructure of the PseudopodaL Feeding Apparatus of Protoperidinium spinu10sum Schiller ••••••••••••••••••••••• 119 Abs tract . 120 Introduction . 122 -4- Contents, cantld. Chapter 4, cont'd Methods and Materials ..•.•....•..•••..••••.•..•••.•••••••••.•.• 122 Results •••••.•••.••••..•••....••••••...•..•.•.••••.•••••.•••••• 125 Feeding cells •••••.......••••••....••.•..•.•••••••••••••••. 126 Non-feeding cells .••.•.....•••••....•••••.....•...••••••••. 133 Miscellaneous organelles ..•..•••....••.••..•......•••.••••• 136 Additional species ..•••..•••••••..••...•.•••....•.•••••..•• 137 Discussion 139 Microtubular basket .....•....••.....•.•.•••••..•••••.••.••• 139 Myonemal sys tern ••••.••......•••.....••••••.•....••••.•••••• 144 Pallium 146 Thecal structures 148 References ..••••..•...••••.••••.....•••••...•••••.••.•.•.••.•.• 151 Conclusions ........................................................ 185 Appendix I. Cells Counts of Dinoflagellates in Perch Pond, 1983-4 •• 189 Appendix II. Taxonomic Drawings of Several Unidentified Dinoflagellates from Perch Pond •.••••••••••••••••••••• 197 Appendix III. The Small-Scale Vertical Distribution of Heterotrophic Dinoflagellates .••••••...••••.••........ 201 Introduction ••••.••••••••.••••..•.•.••••.•.••••••....•••• 202 Methods and Materials •••••••.•.••.•••.•..••••.••.•.•••••• 202 Results and Discussion •••••••••••••....••••••...••••••••• 203 References ••••••.•••••••.••••••••••.••••••••••••••••••••. 205 -5- List of Figures and Tables Introduction Fig. I. Thecate heterotrophic dinoflagellate genera ••••••.•••.. 14 Chapter 1. Table I. Categories of thecate heterotrophic dinoflagellate patterns of occurrence in Perch Pond •..•.•••..•.••.•••. 42 2. Feeding by Oblea rotunda captured together with a field assemblage from Perch Pond on 11 May 1984••.•.••• 43 Fig. I. Map of Perch Pond, Massachusetts •••••.••••••.•••.••••.. 44 2. Surface water temperatures in Perch Pond ••.•••••.••••.• 45 3. Heterotrophic and phototrophic dinoflagellate population dynamics in Perch Pond ••.••••.••••••.••••••• 46 4. Population dynamics of naked and thecate forms of heterotrophic and phototrophic dinoflagellate •••.••••.• 47 5. Relative composition of the dinoflagellate community •.. 48 6. In vivo fluorescence in Perch Pond ••••••••••••.••••••.• 49 7. Diatom and Protoperidinium population dynamics •••••••..• 50 8. Population dynamics of selected Protoperidinium species 51 9. Oblea rotunda and Heterocapsa triquetra population dynamics •••••••••.•••••••••••••.•.•••...••••.••••.••••. 52 10. Ciliate and heterotrophic dinoflagellate population dynamics •.••••••••••••••...••••••.•••••...••••...•..••• 53 II. Seasonal occurrence patterns of selected dinoflagellates 54 12. Population dynamics of potential predators of thecate heterotrophic dinoflagellates •••••••••••.•••..••••••••• 55 Chapter 2 Table I. Predator/prey relationships of thecate heterotrophic dinoflagellates ••••••••••••••••••••••••••••••••••••••.• 80 Fig. I. Swim path of Protoperidinium spinulosum immediately prior to prey capture 82 2. Diagrammatic pallium deployment sequences in three thecate heterotrophic dinoflagellates •••••••••••.•••.•• 83 3-12. Pseudopodal feeding in thecate heterotrophic dinoflagellates ••••••••••••••••••••••.••••••••••..•••.• 84 13-20. Pseudopodal feeding, cont'd•••••••••••••••••.•••.••••.• 86 2l. Drawings of deployed pallium from video recordings .••.• 89 Chapter 3 Fig. I. Morphology of Protoperidinium hirobis •••.••••••••••••. 107 2. Growth curves of ~.hirobis, first grazing/growth experiment. 108 3. Growth curves of ~. hirobis, second grazing/growth experiment ••••••••••.•••••••••••••••••• 109 4. Daily growth rate of ~. hirobis plotted as a function of food abundance •••••.•••••••••••••••••••••• 110 5. Ingestion rate of ~. hirobis plotted as a function of food abundance ••••••••••••••••••••••••••.. 111 -6- Figures and Tables, cont'd, Chapter 3, cont'd Fig. 6. Clearance rates of ~. hirobis plotted as a function of food concentration .......••..•...•.•...•..•••.••••. 112 7. ~. hirobis cell diameter frequencies .••••..•..•...•••• 113 8. Diel growth curve of ~. hirobis ..•••.••••••••.•••••••• 114 9. Diel frequency of division in~. hirobis •••.•••••••••• 115 10. Abundance of empty frustules 116 11. Diel frequencies of feeding in~. hirobis •••..•••••••. 117 Chapter 4 Fig. 1. Diagrammatic overview of Protoperidinium spinulosum cytoplasmic organelles •••.••••••.•......•...••••••..• 154 2-5 Pallium of ~. spinulosum ••.•••.•..••••••.••••••.•...• 156 6-12 Pallium of ~. spinulosum, cant' d. •••••••..•••.•...... 158 13-17 Microtubular basket of ~. spinulosum .••••...•••••••.• 160 18-27 Serial oblique-transverse sections of feeding ~. spinulosum (cell B) 162 28-37 Serial oblique-longitudinal sections of ~. spinulosum (cell C) ••••••.••.•••••••••.•••.••.•••• 164 38-45 Serial oblique-longitudinal sections of ~. spinulosum (cell C), cont'd • ...................... 166 46-53 Non feeding ~. spinulosum (cell E) ••••••..••••••••••• 168 54-60 Non feeding ~. spinulosum (cell F) ••...•••••••••••••• 170 61-69 Non feeding ~. spinulosum (cell F), cont'd ••••••••.•• 172 70-76 Detail of membranous whorls (cell F) .••••••.••••••••• 174 77-83 Miscellaneous organelles in~. spinulosum ••••••••••.• 176 84-92 Feeding apparatus in three other species •.•••.••••••• 178 93 Three-dimensional reconstruction of microtubular basket of cells Band C •••••••••..•••••••••••••••••.• 180 94 Three-dimensional reconstruction of thecal morphology of posterior sulcus of ~. spinulosum •••••• 181 95 Diagrammatic sulcal morphology of ~. spinulosum ••••••• 182 96 Diagrammatic sequence of pallium deployment ••••••••••• 183 Appendix II. Fig. 1 Taxonomical sketches of Protoperidinium sp. A ......... 198 2 Taxonomical sketches of Protoperidinium sp. C ••••••••• 199 3 Taxonomical sketches of Gonyaulax sp. B .•••••.••••••••• 200 Appendix IIr. Fig. 1 Vertical distributions of Heterocapsa triquetra, Gonyaulax tamarensis, and Protoperidinium conicum 206 2. Vertical distributions of Gyrodinium spirale, Zygabikodinium lenticulatum and P. conicum •..••.....•• 208 3. Vertical distributions of Oblea rotunda, ~. c1audicans and P. pellucidum 209 -7- ECOLOGY AND FEEDING BIOLOGY OF THECATE HETEROTROPHIC DINOFLAGELLATES by Dean Martin Jacobson Submitted to the Massachusetts Institute of Technology/ Woods Hole Oceanographic Institution Joint Program in Biological Oceanography in February 1987 in partial fulfillment of the requirements for the degree of Doctor of Philosophy ABSTRACT A group of thecate heterotrophic dinoflagellates (THDs), principally in the diverse and ubiquitous genus Protoperidinium, was investigated both from an ecological and an organismal perspective. When this study was initiated, nothing was known about their feeding mechanisms, rates or food preferences. The population
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