Springer Tokyo Berlin Heidelberg New York Hong Kong London Milan Paris K. Aida, K. Tsukamoto K. Yamauchi (Eds.) Eel Biology With 209 Figures, Including 7 in Color Springer Katsumi Aida, Ph.D. Professor, Department of Aquatic Bioscience Graduate School of Agricultural and Life Sciences The University of Tokyo 1-1 c 1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan Katsumi Tsukamoto, Ph.D. Professor, Ocean Research Institute The University of Tokyo 1-15-1 Minamidai, Nakano-ku, Tokyo 164-8639, Japan Kohei Yamauchi, Ph.D. Professor, Division of Marine Biosciences Graduate School of Fisheries Sciences Hokkaido University 3-1-1 Minatomachi, Hakodate 041-8611, Japan ISBN 978-4-431-65909-9 ISBN 978-4-431-65907-5 (eBook) DOI 10.1007/978-4-431-65907-5 Library of Congress Cata10ging-in-Pub1ication Data Eel biology I K. Aida, K. Tsukamoto, K. Yamauchi (eds.) p.cm. Includes bibliographical references and index. 1. Eels. I. Aida, K. (Katsumi), 1944-II. Tsukamoto, K. (Katsumi), 1948-III. Yamauchi, K. (Kohei), 1942- QL637.9.A5E452003 597' .43--dc21 Printed on acid-free paper © Springer-Verlag Tokyo 2003 Softcover reprint of the hardcover 1s t edition 2003 This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcast ing, reproduction on microfilms or in other ways, and storage in data banks. The use of registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Product liability: The publisher can give no guarantee for information about drug dosage and applica tion thereof contained in this book. In every individual case the respective user must check its accuracy by consulting other pharmaceutical literature. SPIN: 10838146 Preface The eel has long been esteemed in Japan as an important food fish that has a unique taste. We consume as much as 130 000 tons of eel per year, and the grilled eel dish called kabayaki is now one of the representative dishes of traditional Japanese food culture. In Europe, eels also have been an integral part of the cuisine. How ever, the decreases in eel resources have been a serious concern in recent years, and the catches of glass eels as seedlings for aquaculture have shown a long-term decrease in both Europe and East Asia. It is not yet clear if this has been caused by global changes in the ocean-atmosphere system, the human impacts of overfish ing and environmental disruption, or other biological factors. To counteract these decreases in eel resources, we need to understand the causes and mechanisms, and to develop effective management strategies for maintaining stable eel populations. Therefore, the first goal should be to use an ecological ap proach to gain a complete understanding of the mysterious life cycle of the fresh water eel, which has fascinated naturalists since the age of Aristotle. We need to start by gaining a complete understanding of the exact factors that determine the spawning locations of each species and of how global-scale environmental changes may affect their spawning success and glass eel recruitment. Another high priority is the establishment of techniques for artificially matur ing and spawning adults and rearing their larvae in order to supply sufficient num bers of reared glass eels to meet the demand of aquaculture facilities, irrespective of fluctuations in wild stocks. Therefore, fundamental research on the reproduc tive physiology of eels and on the feeding behavior, nutrition, and physiological defense mechanisms of eel larvae is needed. To attain our final goals, both ecolo gists and physiologists must closely collaborate with each other to elucidate the iife cycle of the freshwater eel and to succeed in the artificial production of glass eels. Based on this strategy, we implemented a comprehensive 5-year research project titled "The Elucidation of the Life Cycle of the Eel and Artificial Control of Its Reproduction" beginning in 1997. Funding for this project was provided by the Research for the Future program of the Ministry of Education, Culture, Sports, Science and Technology, and by the Japan Society for the Promotion of Science. This project has resulted in breakthroughs in ecological research on the spawning VI Preface area and migration of the eel, and in research on the reproductive physiology and larval rearing of the Japanese eel. Therefore, in 2001, the last year of the project, we hosted a historic international symposium titled "Advances in Eel Biology" and invited many experts on eel re search from around the world to discuss recent findings about the ecology, popu lation biology, physiology, and artificial production of seedlings of freshwater eels in order to facilitate further progress in these research fields. In response to our invitation, many scientists attended the symposium and presented the results of their scientific work. Motivated by the fruitful discussions in that meeting, we be lieve that now is an exc~llent time to publish a book that compiles all the impor tant recent findings in one volume. We have titled this book Eel Biology, and it is unique because it integrates the present state of knowledge concerning all aspects of eel biology and ecology from the perspective of many authors. We would like to express our sincere thanks to all the authors who have kindly contributed to this landmark book on eel biology and to congratulate them on making this work such a valuable contribution to the literature on anguillid eels. We also express our sincere gratitude to the Ministry of Education, Culture, Sports, Science and Technology and to the Japan Society for the Promotion of Science whose funding has enabled us to organize one of the largest international eel sym posia ever held and to publish this book. Katsumi Aida Katsumi Tsukamoto Kohei Yamauchi July 2003 Contents Preface ........................................................................................................................ V Part 1 Taxonomy, Phylogeny, Population Structure, and Speciation 1 Taxonomy of the Freshwater Eels, Genus Anguilla Schrank, 1798 s. Watanabe ........................................................................................................... 3 2 Origin and Evolution of the Freshwater Eels, Genus Anguilla J.Aoyama ............................................................................................................. 19 3 Catadromous Eels of the North Atlantic: A Review of Molecular Genetic Findings Relevant to Natural History, Population Structure, Speciation, and Phylogeny J.C.Avise .............................................................................................................. 31 Part 2 Life History 4 Leptocephali N. Mochioka ........................................................................................................ 51 5 Metamorphosis T. Otake ................................................................................................................ 61 6 The Glass Eel o. Tabeta and N. Mochioka ................................................................................ 75 7 The Yellow Eel C. Moriarty............. ................................. ............ .......... .......... ........................ .... 89 8 The Silver Eel J. Aoyama and M.J. Miller ...................................•............................................ 107 Part 3 Migration 9 Spawning Area of the Japanese Eel K. Tsukamoto, T.-W. Lee, and H. Fricke .......................................................... 121 VIII Contents 10 Spawning Areas of the Atlantic Eels J.D. McCleave .................................................................................................... 141 11 The Worldwide Distribution of Anguillid Leptocephali M.J. Miller .......................................................................................................... 157 12 Larval Transport of the Japanese Eel S. Kimura ........................................................................................................... 169 13 The Processes of Onshore Migration of the Japanese Eel Anguilla japonica as Revealed by Otolith Microstructure W.-N. Tzeng ....................................................................................................... 181 14 A Review of Upstream Migration and Movements in Inland Waters by Anguillid Eels: Toward a General Theory E. Feunteun, P. Laffaille, T. Robinet, C. Briand, A. Baisez, J.-M.Olivier,andA.Acou ................................................................................. 191 15 Downstream Migration of Silver-Phase Anguillid Eels A. Haro ;. ............................................................................................................. 215 16 Migration from Continental Waters to the Spawning Grounds EW. Tesch and N. Rohlf .................................................................................... 223 Part 4 Resources 17 Status of the European Eel Stock and Fisheries W. Dekker .......................................................................................................... 237 18 Dynamics of Resources of the American Eel, Anguilla rostrata: Declining Abundance in the 1990s J.M. Casselman .................................................................................................. 255 19 The Distribution and Biology of the South Pacific Species of Anguilla D.J. Jellyman ...................................................................................................... 275 20 Eel Resources in East Asia K. Tatsukawa ..................................................................................................... 293 Part 5 Regulatory Mechanisms of Reproduction 21 Oogenesis in the Japanese Eel, Anguilla japonica S. Adachi, S. Ijiri, Y. Kazeto, and K. Yamauchi ................................................ 301 22 Spermatogenesis in the Japanese Eel T. Miura, C. Miura, and K. Yamauchi .............................................................. 319 23 The Physiology of Silvering in Anguillid Eels: Androgens and Control of Metamorphosis from the Yellow to Silver Stage P.M. Lokman, D.H. Rohr, P.S. Davie, and G. Young ........................................ 331 24 GTH and GnRH Molecules and Their Expression in the Japanese Eel H. Suetake, K. Okubo, Y. Yoshiura, and K. Aida .............................................. 351 Contents IX 25 Reproductive Endocrinology of the European Eel, Anguilla anguilla S. Dufour, E. Burzawa-Gerard, N. Le Belle, M. Sbaihi, and B. Vidal ............. 373 Part 6 Techniques for Artificial Induction of Maturation 26 Induction of Vitellogenesis N. Sato, I. Kawazoe, Y. Suzuki, and K. Aida ..................................................... 387 27 Artificial Induction of Oocyte Maturation and Ovulation H. Kagawa .......................................................................................................... 401 28 Induction of Sperm Maturation H. Ohta and T. Unuma ..................................................................................... 415 Part 7 Larval Rearing and Physiology 29 Techniques for Larval Rearing H. Tanaka ........................................................................................................... 427 30 The Digestive System of Eel Larvae T. Kurokawa and B.H. Pedersen ...................................................................... 435 31 Hatching Enzymes in the Japanese Eel J. Hiroi, S. Yasumasu, K. Kawazu, and T. Kaneko ........................................... 445 32 Chloride Cells in the Japanese Eel During Their Early Life Stages and Downstream Migration T. Kaneko, S. Hasegawa, and S. Sasai .............................................................. 457 33 Nonspecific Defense Mechanisms of the Eel Y. Suzuki and S. Tasumi ................................................................................... 469 Subject Index ........................................................................................................... 485 Part 1 Taxonomy, Phylogeny, Population Structure, and Speciation 1 Taxonomy of the Freshwater Eels, Genus Anguilla Schrank, 1798 Shun Watanabe 1. Introduction The freshwater eels of the genus Anguilla Schrank, 1798, are widely distributed in the world and have unique characters such as a catadromous life history strategy, a long spawning migration, and a long leptocephalus larval period. Although there have been a large number of studies on their ecology and physiology, there have been relatively few studies on their taxonomy. Comprehensive revisions of the ge nus Anguilla using most or all the presently recognized species were done by Kaup (1856), Gunther (1870), and Ege (1939) with morphological analysis. However, rela tively little work has been done after the milestone study of Ege (1939). This lack may have been due to the extensive nature of his study, in which he carefully ex amined a large number of specimens of all the species of the genus Anguilla from throughout the world. As a result, it may have been generally thought that all the problems of the taxonomy of the genus Anguilla were completely solved. However, the freshwater eels have several groups of species that have very similar morpho logical features, making them difficult to distinguish, and a recent reexamination of Ege's (1939) study found that there were still several important problems re maining in the present taxonomy of the freshwater eels. The purpose of this chap ter is to introduce the history of the taxonomy of the freshwater eels, to evaluate the presently accepted taxonomy, and to propose a new taxonomy to solve the prob lems of Ege's (1939) study. Department of Marine Bioscience, Ocean Research Institute, The University of Tokyo, 1-15-1 Minamidai, Nakano-ku, Tokyo 164-8639, Japan Tel. +81-3-5351-6520; Fax +81-3-5351-6514 e-mail: [email protected]