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1 Springer Tokyo Berlin Heidelberg New York Hong Kong London Milan Paris

2 K. Aida, K. Tsukamoto K. Yamauchi (Eds.) Eel Biology With 209 Figures, Including 7 in Color Springer

3 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 , Japan Katsumi Tsukamoto, Ph.D. Professor, Ocean Research Institute The University of Tokyo Minamidai, Nakano-ku, Tokyo , Japan Kohei Yamauchi, Ph.D. Professor, Division of Marine Biosciences Graduate School of Fisheries Sciences Hokkaido University Minatomachi, Hakodate , Japan ISBN ISBN (ebook) DOI / 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), II. Tsukamoto, K. (Katsumi), III. Yamauchi, K. (Kohei), QL637.9.A5E '.43--dc21 Printed on acid-free paper Springer-Verlag Tokyo 2003 Softcover reprint of the hardcover 1 st 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, broadcasting, 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 application thereof contained in this book. In every individual case the respective user must check its accuracy by consulting other pharmaceutical literature. SPIN:

4 Preface The eel has long been esteemed in Japan as an important food fish that has a unique taste. We consume as much as 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. However, 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 overfishing 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 approach to gain a complete understanding of the mysterious life cycle of the freshwater 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 maturing and spawning adults and rearing their larvae in order to supply sufficient numbers of reared glass eels to meet the demand of aquaculture facilities, irrespective of fluctuations in wild stocks. Therefore, fundamental research on the reproductive physiology of eels and on the feeding behavior, nutrition, and physiological defense mechanisms of eel larvae is needed. To attain our final goals, both ecologists 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 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

5 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 research from around the world to discuss recent findings about the ecology, population 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 believe that now is an exc~llent time to publish a book that compiles all the important 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 symposia ever held and to publish this book. Katsumi Aida Katsumi Tsukamoto Kohei Yamauchi July 2003

6 Contents Preface... V Part 1 Taxonomy, Phylogeny, Population Structure, and Speciation 1 Taxonomy of the Freshwater Eels, Genus Anguilla Schrank, 1798 s. Watanabe Origin and Evolution of the Freshwater Eels, Genus Anguilla J.Aoyama Catadromous Eels of the North Atlantic: A Review of Molecular Genetic Findings Relevant to Natural History, Population Structure, Speciation, and Phylogeny J.C.Avise Part 2 Life History 4 Leptocephali N. Mochioka Metamorphosis T. Otake The Glass Eel o. Tabeta and N. Mochioka The Yellow Eel C. Moriarty The Silver Eel J. Aoyama and M.J. Miller Part 3 Migration 9 Spawning Area of the Japanese Eel K. Tsukamoto, T.-W. Lee, and H. Fricke

7 VIII Contents 10 Spawning Areas of the Atlantic Eels J.D. McCleave The Worldwide Distribution of Anguillid Leptocephali M.J. Miller Larval Transport of the Japanese Eel S. Kimura The Processes of Onshore Migration of the Japanese Eel Anguilla japonica as Revealed by Otolith Microstructure W.-N. Tzeng 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 Downstream Migration of Silver-Phase Anguillid Eels A. Haro ; Migration from Continental Waters to the Spawning Grounds EW. Tesch and N. Rohlf Part 4 Resources 17 Status of the European Eel Stock and Fisheries W. Dekker Dynamics of Resources of the American Eel, Anguilla rostrata: Declining Abundance in the 1990s J.M. Casselman The Distribution and Biology of the South Pacific Species of Anguilla D.J. Jellyman Eel Resources in East Asia K. Tatsukawa Part 5 Regulatory Mechanisms of Reproduction 21 Oogenesis in the Japanese Eel, Anguilla japonica S. Adachi, S. Ijiri, Y. Kazeto, and K. Yamauchi Spermatogenesis in the Japanese Eel T. Miura, C. Miura, and K. Yamauchi 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 GTH and GnRH Molecules and Their Expression in the Japanese Eel H. Suetake, K. Okubo, Y. Yoshiura, and K. Aida

8 Contents IX 25 Reproductive Endocrinology of the European Eel, Anguilla anguilla S. Dufour, E. Burzawa-Gerard, N. Le Belle, M. Sbaihi, and B. Vidal Part 6 Techniques for Artificial Induction of Maturation 26 Induction of Vitellogenesis N. Sato, I. Kawazoe, Y. Suzuki, and K. Aida Artificial Induction of Oocyte Maturation and Ovulation H. Kagawa Induction of Sperm Maturation H. Ohta and T. Unuma Part 7 Larval Rearing and Physiology 29 Techniques for Larval Rearing H. Tanaka The Digestive System of Eel Larvae T. Kurokawa and B.H. Pedersen Hatching Enzymes in the Japanese Eel J. Hiroi, S. Yasumasu, K. Kawazu, and T. Kaneko Chloride Cells in the Japanese Eel During Their Early Life Stages and Downstream Migration T. Kaneko, S. Hasegawa, and S. Sasai Nonspecific Defense Mechanisms of the Eel Y. Suzuki and S. Tasumi Subject Index