Post-Embryonic Development of the Copepoda CRUSTACEA NA MONOGRAPHS Constitutes a Series of Books on Carcinology in Its Widest Sense

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Post-Embryonic Development of the Copepoda CRUSTACEA NA MONOGRAPHS Constitutes a Series of Books on Carcinology in Its Widest Sense Post-embryonic Development of the Copepoda CRUSTACEA NA MONOGRAPHS constitutes a series of books on carcinology in its widest sense. Contributions are handled by the Editor-in-Chief and may be submitted through the office of KONINKLIJKE BRILL Academic Publishers N.V., P.O. Box 9000, NL-2300 PA Leiden, The Netherlands. Editor-in-Chief: ].C. VON VAUPEL KLEIN, Beetslaan 32, NL-3723 DX Bilthoven, Netherlands; e-mail: [email protected] Editorial Committee: N.L. BRUCE, Wellington, New Zealand; Mrs. M. CHARMANTIER-DAURES, Montpellier, France; D.L. DANIELOPOL, Mondsee, Austria; Mrs. D. DEFAYE, Paris, France; H. DiRCKSEN, Stockholm, Sweden; J. DORGELO, Amsterdam, Netherlands; J. FOREST, Paris, France; C.H.J.M. FRANSEN, Leiden, Netherlands; R.C. GuiA§u, Toronto, Ontario, Canada; R.G. FIARTNOLL, Port Erin, Isle of Man; L.B. HOLTHUIS, Leiden, Netherlands; E. MACPHERSON, Blanes, Spain; P.K.L. NG, Singapore, Rep. of Singapore; H.-K. SCHMINKE, Oldenburg, Germany; F.R. SCHRAM, Langley, WA, U.S.A.; S.F. TIMOFEEV, Murmansk, Russia; G. VAN DER VELDE, Nij- megen, Netherlands; W. VERVOORT, Leiden, Netherlands; H.P. WAGNER, Leiden, Netherlands; D.L WILLIAMSON, Port Erin, Isle of Man. Published in this series: CRM 001 - Stephan G. Bullard Larvae of anomuran and brachyuran crabs of North Carolina CRM 002 - Spyros Sfenthourakis et al. The biology of terrestrial isopods, V CRM 003 - Tomislav Karanovic Subterranean Copepoda from arid Western Australia CRM 004 - Katsushi Sakai Callianassoidea of the world (Decapoda, Thalassinidea) CRM 005 - Kim Larsen Deep-sea Tanaidacea from the Gulf of Mexico CRM 006 - Katsushi Sakai Upogebiidae of the world (Decapoda, Thalassinidea) CRM 007 - Ivana Karanovic Candoninae(Ostracoda) fromthePilbararegion in Western Australia CRM 008 - Frank D. Ferrari &Hans-U. Dahms Post-embryonic development of the Copepoda In preparation (provisional titles): CRM OOx - Darren C. Yeo & Peter K.L. Ng Southeast Asian freshwater crabs CRM OOy - Chang-tai Shih Marine Calanoida of the China seas CRM OOz - Katsushi Sakai Axiidae of the world (Decapoda, Thalassinidea) Author's addresses: Dr. F.D. Ferrari, Department of Invertebrate Zoology, MRC-534, National Museum of Natural History, Smithsonian Institution, 4210 Silver FEU Road, Suitland, Maryland 20746, U.S.A.; e-mail: [email protected] Dr. FL-U. Dahms, Institute of Marine Biology, National Taiwan Ocean University, 2 Pei-Ning Road, Keelung, Taiwan 202, Rep. of China; e-mail: [email protected] Manuscript first received 25 September, 2006; final version accepted 18 December, 2006. Cover: A combination of figs. 30-32, showing adult first swimming legs in three species of calanoid copepods, on which the development of Von Vaupel Klein's Organ, an alleged synapomorphy of the Calanoida, is evident; see pp. 000-000. P OS t-embry onic Development of the Copepoda By Frank D. Ferrari and Hans-Uwe Dahms CRUSTACEANA MONOGRAPHS, 8 •'68^' BRILL LEIDEN • BOSTON 2007 This book is printed on acid-free paper. Library of Congress Cataloging-in Publication data Tlie Library of Congress Cataloging-in-Publication Data is available from the Publisher. ISSN: 1570-XXXX ISBN-13: 978 90 04 XXXXX X ISBN-10: 90 04 15713 1 Copyright 2007 by Koninklijke Brill NV, Leiden, The Netherlands. Koninklijke Brill NV incorporates the imprints BRILL, Hotel Publishing, IDC Publishers, Martinus Nijhoff Publishers and VSP. All rights reserved. No part of this publication may be reproduced, translated, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without prior written permission from the publisher. Authorization to photocopy items for internal or personal use is granted by Koninklijke Brill NV provided that the appropriate fees are paid directly to The Copyright Clearance Center, 222 Rosewood Drive, Suite 910, Danvers, MA 01923, USA. Fees are subject to change. PRINTED IN THE NETHERLANDS CONTENTS Preface 1 An introduction to copepods with a brief history of studies of their development ... 3 Methods and constraints 8 The nauplius and naupliar development 12 Variation in the number of naupliar stages 22 Variation in the order of appearance of limb buds 26 Variation in transformed appendages 28 Variation in setation of limb buds 30 Internal anatomy 31 Ecology 33 The copepodid phase of development 37 Variation in the number of copepodid stages 53 Stage correspondence of copepods with chalimus stages 54 Addition of appendages 56 Variation in transformed appendages 58 Internal anatomy 61 Functional morphology, swimming, and feeding behavior 63 Seasonal cycles, vertical distribution, vertical migration 63 Development times, mortality, etc 65 Patterning the copepod body 66 Patterning the appendages of copepods 74 Antenna 1 74 Exopod of antenna 2 78 Exopod of the mandible 82 Maxilla 1 and maxilla 2 82 Endopod of the maxilliped 82 Rami of the remaining limbs 85 Caudal ramus 90 Contrasting early development of swimming leg 1 with swimming legs 2-4 90 Von Vaupel Klein's Organ 94 Thoracopods: maxilliped and swimming legs 100 The protopod 101 Generalities of limb patterning 104 VI CONTENTS The molt from the last nauplius to the first copepodid and the number of naupliar somites 106 Implications of development for phylogeny 113 Summary and recommended studies 119 Bibliography 126 Papers on the post-embryonic development of copepods cited herein 126 Other cited literature 141 Papers about the post-embryonic development of copepods not cited 144 Appendix I 211 Glossary 216 Taxonomic index 223 Subject index 227 Authorities with dates of description of all species names mentioned in the main text, captions, and tables, can be found in the Appendix. PREFACE Copepod development has been studied for almost 250 years, and pub- lished descriptions of the exoskeletal morphology have been the dominant theme for most of that time. Almost half a century transpired between the first description of a post-embryonic developmental stage and a description that included a complete set of all developmental stages of a copepod. Interpretive questions about post-embryonic development based on an incomplete set of stages date from the early nineteenth century, but more recently researchers have discovered that interpretations are more interesting and nuanced if all developmental stages can be incorporated into the analysis. In this monograph, we focus, whenever possible, on interpretations derived from a complete set of all developmental stages. We diagnose both the nau- plius and the copepodid in order to promote such interpretations. We discuss variation in the number of naupliar stages and of copepodid stages among copepods, and also outline variation in the exoskeletal morphology of both the naupliar and copepodid phases of development. Internal anatomy is of interest to us, as is behavior and ecology, although observations from a com- plete set of developmental stages usually are not available on these topics. We find it interesting that at present stage-specific studies of internal anatomy during the naupliar phase of development are more complete than studies of the copepodid phase, while distributions in space and through time are more apt to be completely known for the copepodid phase of development. We spend some time discussing variations of the order in which somites are added to the copepod body, and analysing the order segments are added to its limbs during development. One result of particular interest to us is how often the architecture of the body or configuration of the limbs are shaped by failure to form arthrodial membranes, resulting in somite or segment complexes. A model for patterning the body of copepodids has been known for almost a century, and that model is used to help us infer the somite number of the naupliar stages. Observations of limb patterning date from the early twentieth century, but models have been proposed only recently. Because the architecture of the naupliar body and the configuration of its limbs are quite different from the situation for the copepodid body, we analyse in detail the transition between these two phases of development. 2 CRM 008 - Frank D. Ferrari & Hans-Uwe Dahms Phylogenetic analyses are the coin of the contemporary realm for mor- phologists, and post-embryonic development has contributed to many phylo- genetic hypotheses. We are pleased to discuss them. Finally, we close with suggestions for future studies that seem to us technically possible and intel- lectually valuable. We dedicate this work to the memories of Patricia Dudley, late of Columbia University, and Paul Illg, late of the University of Washington, whose think- ing about copepod development, and particularly how limbs are patterned, appeared to be so far ahead of their time. We are pleased to extend our thanks to the following individuals who helped make this work possible. Lana Ong and Molly Kelly Ryan, Smithso- nian Institution, prepared the illustrations. David Damkaer of Cocker Creek, Washington, answered questions historical. Mark Grygier, Lake Biwa Mu- seum, collected nauplii of Leptestheria kawachiensis; Ted Durbin, Univer- sity of Rhode Island, cultured developmental stages of Calanus finmarchicus; Wim Klein Breteler, Royal Netherlands Institute for Sea Research, cultured stages of Temora longicomis; Debbie Steinberg, then at the Bermuda Sta- tion for Biological Research, collected copepodids of Euchirella messinen- sis; John Fornshell, Cambridge Scientific Press, collected stages of Longi- pedia americana, Acrocalanus gibber, and Derocheilocaris
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