THE BIOLOGY AND ECOLOGY OF TINTINNID CILIATES T H E B I O L O G Y A N D E C O L O G Y O F T I N T I N N I D C I L I AT E S MODELS FOR M ARINE PLANKTON Edited by John R. Dolan Marine Microbial Ecology Laboratoire d’Océanographie de Villefranche-sur-Mer David J.S. Montagnes Institute of Integrative Biology University of Liverpool Sabine Agatha Department of Organismic Biology University of Salzburg D. Wayne Coats Smithsonian Environmental Research Center Diane K. Stoecker University of Maryland Center for Environmental Science A John Wiley & Sons, Ltd., Publication This edition fi rst published 2013 © 2013 by John Wiley & Sons, Ltd. Wiley-Blackwell is an imprint of John Wiley & Sons, formed by the merger of Wiley’s global Scientifi c, Technical and Medical business with Blackwell Publishing. 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(John Richard), 1955– QL368.T55B56 2012 579.4'9–dc23 2012010713 A catalogue record for this book is available from the British Library. Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic books. Cover image: Morphological diversity in the plankton. A view of a single microscope fi eld (20× objective) of plankton net tow material from the Bay of Villefranche in January 2011. Image by J.R. Dolan. Cover design by: Simon Levy Associates Set in 9/11 pt PhotinaMT by Toppan Best-set Premedia Limited 1 2013 Contents CONTRIBUTORS, vii 3.3 Evolution of tintinnids, 49 3.4 How to read the tintinnid cladogram, 64 3.5 Molecular analysis and comparison with CHAPTER 1 INTRODUCTION TO morphologic data, 69 TINTINNIDS, 1 3.6 Systematics, 75 3.7 Comparison with the evolution of related 1.1 Why a book on tintinnid ciliates?, 2 planktonic ciliates: the aloricate 1.2 What is a tintinnid ciliate?, 3 choreotrichids, oligotrichids, and 1.3 The lorica as the defi ning characteristic of halteriids, 81 tintinnid ciliates, 3 3.8 Key points, 83 1.4 History of tintinnid studies, 7 Acknowledgments, 84 1.5 Tintinnids as model organisms for marine plankton, 13 1.6 Key points, 16 CHAPTER 4 ECOPHYSIOLOGY AND Acknowledgments, 16 BEHAVIOR OF TINTINNIDS, 85 4.1 Introduction, 86 CHAPTER 2 THE TINTINNID LORICA, 17 4.2 Feeding, 86 4.3 Growth, 99 2.1 Introduction, 18 4.4 Swimming behavior, 106 2.2 Diversity, formation, and variability of 4.5 Response to abiotic factors and interactions loricae, 19 with biotic factors, 111 2.3 Ultrastructure of loricae, 32 4.6 Tintinnids as models and in models, 114 2.4 Chemical composition of loricae, 35 4.7 Key points, 121 2.5 Lorica sedimentation, 40 Acknowledgments, 121 2.6 Key points, 41 Acknowledgments, 41 CHAPTER 5 PREDATORS OF CHAPTER 3 SYSTEMATICS AND TINTINNIDS, 122 EVOLUTION OF TINTINNID CILIATES, 42 5.1 Introduction, 123 3.1 Introduction, 43 5.2 Predators of tintinnids, 133 3.2 History of tintinnid taxonomy and 5.3 Anti-predator defenses of tintinnids, 141 systematics, 44 5.4 Top-down control of tintinnids, 142 v vi Contents 5.5 Importance of tintinnids as prey for the 8.4 Mesozoic tintinnids and calpionellids: same predator, 143 shape, different composition, 191 5.6 Tintinnids as vectors for algal toxins, 143 8.5 Cenozoic tintinnids: sparse, 192 5.7 Key points, 144 8.6 Organic and agglutinated phanerozoic fossils: Acknowledgments, 144 the most likely candidates, 193 8.7 Conclusions and perspectives, 195 8.8 Key points, 197 CHAPTER 6 PARASITES OF Acknowledgments, 197 TINTINNIDS, 145 CHAPTER 9 TINTINNIDS IN 6.1 Background, 146 MICROZOOPLANKTON COMMUNITIES, 198 6.2 Dinofl agellate parasites: morphology and infection cycle, 149 9.1 Ecology of microzooplankton, 199 6.3 Molecular evolution of dinofl agellates 9.2 Quantitative importance of tintinnids in parasitizing tintinnids, 160 microzooplankton assemblages, 205 6.4 Ecology of tintinnid parasites, 165 9.3 Characteristics that set tintinnids apart from 6.5 Summary and future directions, 169 other microzooplankton, 211 6.6 Key points, 169 9.4 Key points, 212 Acknowledgments, 170 Acknowledgments, 213 CHAPTER 7 COMPARATIVE BIOLOGY OF CHAPTER 10 DIVERSITY AND TINTINNID CYSTS, 171 DISTRIBUTIONS OF TINTINNIDS, 214 7.1 Introduction, 172 10.1 Introduction, 215 7.2 Morphology, 173 10.2 Biogeography, 215 7.3 Encystment and excystment, 176 10.3 Assemblages of coastal systems, 233 7.4 Ecological function of cysts, 182 10.4 Assemblages of open waters, 239 7.5 Key points, 184 10.5 Key points, 241 Acknowledgments, 185 Acknowledgments, 243 REFERENCES, 244 CHAPTER 8 FOSSIL TINTINNIDS, 186 ORGANISM INDEX, 288 8.1 Introduction: a paucity of data, 187 8.2 Proterozoic tintinnids: no evidence of a SUBJECT INDEX, 293 beginning, 187 8.3 Paleozoic tintinnid reports: too thin The color plate section can be found between to know, 191 pages 136 and 137 Contributors Sabine Agatha Takashi Kamiyama Department of Organismic Biology, University of Tohoku National Fisheries Research Institute Salzburg Fisheries Research Agency Hellbrunnerstrasse 34, 5020 Salzburg, Austria 3 - 27 - 5, Shinhama, Shiogama, Miyagi 985 - 0001, [email protected] Japan [email protected] Tsvetan R. Bachvaroff Smithsonian Environmental Research Center Jere H. Lipps P.O. Box 28, 647 Contees Wharf Rd. John D. Cooper Archaeology and Paleontology Center Edgewater, MD 21037, USA Santa Ana, CA, USA [email protected] [email protected] and D. Wayne Coats University of California Museum of Paleontology Smithsonian Environmental Research Center Berkeley, CA 94720, USA P.O. Box 28, 647 Contees Wharf Rd. [email protected] Edgewater, MD 21037, USA [email protected] George B. McManus Department of Marine Sciences John R. Dolan University of Connecticut Marine Microbial Ecology 1080 Shennecossett Rd. Laboratoire d ’ Oc é anographie de Villefranche - sur - Mer Groton CT 06340, USA CNRS Universit é Paris VI UMR 7093 [email protected] S tation Zoologique, B.P. 28 06230 Villefranche - sur - Mer, France David J.S. Montagnes dolan@obs - vlfr.fr Institute of Integrative Biology University of Liverpool Micah Dunthorn BioSciences Building University of Kaiserslautern Crown Street Department of Ecology Liverpool, L69 7ZB, UK Erwin - Schroedinger Street [email protected] 67653 Kaiserslautern, Germany [email protected] - kl.de Michèle Laval- Peuto Chemin des Campons 144 06480 La Colle - sur - Loup, France [email protected] vii viii Contributors Richard W. Pierce Diane K. Stoecker P.O. Box 132 University of Maryland Center for Environmental North Attleboro Science MA, USA Horn Point Laboratory [email protected] 2020 Horns Point Road P.O. Box 775 Luciana F. Santoferrara Cambridge MD 21613, USA Department of Marine Sciences [email protected] University of Connecticut 1080 Shennecossett Rd. Michaela C. Str üder-Kypke Groton CT 06340, USA Department of Molecular and Cell Biology [email protected] University of Guelph Guelph, ON N1G 2W1, Canada Paul Simon [email protected] Max Planck Institute for Chemical Physics of Solids N ö thnitzer Strasse 40, 01187 Dresden, Germany [email protected] Thorsten Stoeck University of Kaiserslautern Department of Ecology Erwin - Schroedinger Street 67653 Kaiserslautern, Germany [email protected] - kl.de Plate 1.1 Life - cycle stages in E utintinnus inquilinus . (a) A trophont (feeding stage) cell. (b) An early stage of binary fi ssion showing the oral primordium (OP), which will develop into a new mouth. (c) The fi nal stage of cell division. (d) An early stage of conjugation. (e) A conjugating pair showing a well - developed cytoplasmic bridge (CB) through which nuclear material will be exchanged. Loricae are about 100 μ m long. Images are of Lugol ’ s - fi xed cells; sample from a mixed culture provided by F. Lombard. The Biology and Ecology of Tintinnid Ciliates: Models for Marine Plankton, First Edition. Edited by John R. Dolan, David J.S. Montagnes, Sabine Agatha, D. Wayne Coats, and Diane K. Stoecker. © 2013 John Wiley & Sons, Ltd. Published 2013 by John Wiley & Sons, Ltd. Plate 1.4 Some tintinnid species with agglutinated loricae: T intinnopsis radix (a), T. campanula (b), T. dadayi (c), T. spiralis (d), Codonella elongata covered with coccoliths (e), T intinnidium sp. (f), S tenosemella ventricosa (g), L eprotintinnus pellucidus (h), and Codonellopsis schabi (i). Species names are attributed based on lorica morphology. All the specimens are Lugol ’ s - fi xed cells except for Codonella elongata which was a live specimen. Plate 1.5 Examples of tintinnid species with hyaline loricae: A mphorides quadrilineata (a), A mplectella collaria (b), C limacocylis scalaria (c), Acanthostomella conicoides (d), P rotorhabdonella simplex (e), E piplocylis blanda (f), X ystonellopsis paradoxa (g), Ormosella trachelium (h), Proplectella elipisoida (i), Dadayiella ganymedes (j), Dictyocysta lepida (k), Metacylis mediterranea (l), Parafavella parumdentata (m), Parundella messinensis (n), A scampbellia tortulata (o), E utintinnus stramentus (p), Undella hyalina (q), Helicostomella subulata (r), S alpingella acuminata (s), R habdonella spiralis (t), and C yttarocylis cassis (u). All the specimens are Lugol ’ s - fi xed cells.
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