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The Sea Cucumber Apostichopus japonicus History, Biology and Aquaculture Edited by Hongsheng Yang Jean-François Hamel Annie Mercier AMSTERDAM • BOSTON • HEIDELBERG • LONDON NEW YORK • OXFORD • PARIS • SAN DIEGO SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier Academic Press is an imprint of Elsevier 32 Jamestown Road, London NW1 7BY, UK 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA 225 Wyman Street, Waltham, MA 02451, USA The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK Copyright © 2015 Elsevier Inc. All rights reserved No part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means electronic, mechanical, photocopying, recording or otherwise without the prior written permission of the publisher Permissions may be sought directly from Elsevier’s Science & Technology Rights Department in Oxford, UK: phone (+44) (0) 1865 843830; fax (+44) (0) 1865 853333; email: [email protected]. Alternatively, visit the Science and Technology Books website at www.elsevierdirect.com/rights for further information Notice No responsibility is assumed by the publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is availabe from the Library of Congress ISBN: 978-0-12-799953-1 For information on all Academic Press publications visit our website at http://store.elsevier.com/ Typeset by Thomson Digital Printed and bound in USA List of Contributors Jun Akamine Institute for the Study of Global Issues, Graduate School of Social Sciences, Hitotsubashi University, Kunitachi City, Tokyo, Japan Yucen Bai Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Muyan Chen College of Fisheries, Ocean University of China, Qingdao, Shandong, PR China Fei Gao Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, PR China Jean-François Hamel Society for the Exploration and Valuing of the Environment (SEVE), Portugal Cove-St. Philips, NL, Canada Seonggul Hong Marine Policy Research Division, Korea Maritime Institute, KBS Media-Center 15F #45, Maebongsonro, Seoul, Republic of Korea Yao Huang Department of Preschool Education, South Sichuan Preschool Education College, Longchang, Sichuan, PR China Jong Yong Ho External Economic Cooperation Department, Ministry of Fisheries, Pyongyang, Democratic People’s Republic of Korea Chenggang Lin Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Guangbin Liu Benthic Biology Research Centre, Marine Biology Institute of Shandong Province, Qingdao, Shandong, PR China Jinxian Liu Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Shilin Liu Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Quan Liu Sea Cucumber Culture Research Association of Zibo Nutrition Society, Zibo, Shandong, PR China xv xvi List of Contributors Alessandro Lovatelli FAO Fisheries and Aquaculture Department, Aquaculture Branch (FIRA), Viale delle Terme di Caracalla, 00153 Rome, Italy Yuze Mao Mariculture Ecology Division, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, PR China Annie Mercier Department of Ocean Sciences, Memorial University, St. John’s, NL, Canada Yang Pan Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Sungjun Park Marine Policy Research Division, Korea Maritime Institute, KBS Media-Center 15F #45, Maebongsonro, Seoul, Republic of Korea Tianlong Qiu Marine Biotechnology Research and Development Center, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Xiaoshang Ru College of Fisheries, Ocean University of China, Qingdao, Shandong, PR China Hao Song Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Xiaoyue Song Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Lin Su Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Jingchun Sun Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Lina Sun Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Fangyu Wang Key Laboratory of Animal Immunology, Henan Academy of Agricultural Sciences, Zhengzhou, PR China Qing Wang Key Laboratory of Coastal Environmental Processes and Ecological Remediation, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, Shandong, PR China List of Contributors xvii Tianming Wang Marine Science and Technology College, Zhejiang Ocean University, Zhoushan, Zhejiang, PR China Xiaoyu Wang Laboratory of Fishery Resources and Marine Ecology, Tianjin Fisheries Research Institute, Tianjin, PR China Sudong Xia Department of Modern Aquaculture Technology Research, Tianjin Fisheries Research Institute, Tianjin, PR China Kun Xing School of Marine Science and Environment Engineering, Dalian Ocean University, Dalian, PR China Dongxue Xu Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Qiang Xu Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Hongsheng Yang Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Injoo Yoon Marine Policy Research Division, Korea Maritime Institute, KBS Media-Center 15F #45, Maebongsonro, Seoul, Republic of Korea Zonghe Yu Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, PR China Xiutang Yuan Key Laboratory of Coastal Ecology and Environment, National Marine Environmental Monitoring Center, State Oceanic Administration, Dalian, Liaoning, PR China Libin Zhang Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Shanshan Zhang College of Fisheries, Ocean University of China, Qingdao, Shandong, PR China Tao Zhang Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Heling Zhao Asian Herpetological Research Editorial Office, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan Province, PR China xviii List of Contributors Huan Zhao School of Fisheries and Life Science, Dalian Ocean University, Dalian, PR China Peng Zhao Department of Marine Planning, Strategy and Rights, National Marine Data & Information Service, Tianjin, PR China Yi Zhou Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, Shandong, PR China Aijun Zhu College of Fisheries, Ocean University of China, Qingdao, Shandong, PR China Preface Sea cucumbers are one of the most important marine resources supporting coastal livelihoods around the world. They are widely distributed, from the shores to deep ocean trenches, inhabit diverse habitats, and often exhibit large biomasses. The Western Pacific coast hosts a rich diversity of sea cucumbers, among which Apostichopus japonicus is a focal species. Sea cucumbers, and A. japonicus in particular, are closely woven into the history and culture of China and neighboring East Asian countries. The Chinese character “ ,” which refers to sea cucum- ber, can be traced back to the Oracle Bone inscriptions from the Shang Dynasty, 1300 B.C. The first record of sea cucumber consumption is found as early as the Three Kingdoms Period. For hundreds of years, sea cucumber has been considered among the most nutritious foods in China; it is now a prized delicacy alongside the well-known birds’ nests and abalones. As such, it is at the forefront of many regional cuisines of China, especially at important banquets. The medicinal properties of sea cucumber are recorded in famous Chinese books such as “A Supplement to the Compendium of Materia Medica” and “New Compilation of Materia Medica.” The singularities and significance of sea cucumber are also recorded in Chinese literature. Many folk tales highlight its special morphological characters and tonic effects. Today, A. japonicus has incontestable economic value and potential; it is at the heart of a huge industry worth over 5 billion USD. This species exhibits many fascinating biological characters such as aestivation, evisceration, regeneration, albinism, and autolysis. The peculiar biological features, mythical curative properties, and unique traditional culture surrounding A. japonicus have inspired our research interests. Why has the sea cucumber played such a long-standing and important role in Chinese traditional culture? Why do the Chinese love eating sea cucumber so much? What curative effects does it really have? How is sea cucumber best cooked? What is the best aquaculture model for sea cucumber? How can environmentally friendly and sustainable development of the sea cucumber industry be achieved? For many years, research groups at the Institute of Oceanology, Chinese Academy of Sciences (IOCAS) have carried out studies on the biology, physiology, ethology, and aquaculture of A. japonicus. With our growing knowledge of A. japonicus, we became even fonder of this ancient and mysterious animal. The idea to compile this knowledge in a book first emerged in November 2011, following an academic exchange with Canadian colleagues who were equally fascinated with sea cucumbers. Our discussions were both informative and fruitful. They expressed a desire to help us disseminate findings that were largely confined to Chinese publications, for the benefit of researchers and industries who were preoccupied with A. japonicus and other species of sea cucumber in the rest of the world. The draft outline of the book was prepared in March 2012, and the chapters fleshed out during our visit to Canada in September 2012. Invitations were thereafter extended to colleagues outside IOCAS with compatible interests, to capture the full scope of research areas surrounding A. japonicus. Given the language bar- rier, it was admittedly challenging to summarize the biological studies, the development of the aqua- culture industry and to present both the traditional and modern culture methods of A. japonicus. The Chinese contributors prepared the initial drafts either in their native language or in tentative English. Each chapter was then revised internally at IOCAS until a full preliminary English version was obtained xix xx Preface in May 2013. It took another 15 months for my English-speaking co-editors to lead contributors through several additional rounds of revision, until the book was finally ready. Special thanks should be given to my esteemed co-editors, who put a lot of time and effort into this book. It was quite an undertaking! They not only planned the structure of the book with us, but also invited researchers from Democratic People’s Republic of Korea, Republic of Korea, and Japan to take part in the project. I was impressed by their rigorous and careful editing, great attitude, and hard work. Without their efforts, the book could not have been completed and published successfully. Hongsheng Yang Institute of Oceanology, Chinese Academy of Sciences Preface xxi Of all the creatures humans consume, sea cucumbers might well qualify as the weirdest. Worm-shaped and slimy, smooth or horny, with no clear front and rear ends and no easily discernible movements, these ocean dwellers are anything but endearing. The fact that many of them feed on detritus does noth- ing to improve their image. Yet, in their infinite wisdom, East Asian people have marked sea cucumbers as one of our planet's most valuable gifts, with such emphasis that sea cucumber is one of the most prized seafood in the world today. Among the approximately 1200 known species of sea cucumber, some 70 are harvested worldwide. But the undisputed favorite, the so-called king of sea cucumbers, is Apostichopus japonicus, sometimes referred to in English literature as the Japanese sea cucumber. This species is not larger or more colorful than others, but its native populations extend along the coasts of the Northwest Pacific, where the love of sea cucumber first bloomed. A millennium later, this adoration has taken its toll; with a market value peaking close to 3000 USD per dry kilo, A. japonicus is now officially an endangered species, as most of its wild populations are dwindling dangerously. On the other hand, there is no shortage of captive- bred specimens in China, where sea cucumber is now the number one aquaculture industry. The Chinese people’s enduring relationship with sea cucumber has had far-reaching repercussions over the past century. On a planetary scale, it has led to overfishing of most commercial species, some to the brink of extinction, followed by countless initiatives to breed sea cucumbers of every denomina- tion across the globe. All this in an effort to sustain the mythical appetite of 1.5 billion people living in China, in neighboring East Asian nations and in Chinatowns worldwide. Nearly everywhere we go, we meet people involved in sea cucumber conservation or production initiatives, from remote islands of the Indo-Pacific, to coastal nations of South and Central America, Asia, and Africa, all the way to Russia and North America, including Newfoundland, where we currently live. Our own fascination with sea cucumbers was born out of curiosity for their strange looks and be- haviors. We initially strove to understand how they reproduce, feed, and communicate with each other, and to assess the role they play in marine ecosystems from shallow to deep-sea environments. Our fundamental interest in their biology eventually drove us toward more applied projects, first in Canada and then abroad, as our expertise was sought to assist fisheries and aquaculture ventures. To this day, all things sea cucumber still guide our travels around the world. We suspect that A. japonicus is the most studied sea cucumber by a fair margin, and perhaps even the most studied echinoderm. The number of English publications on this species is already high, without counting those in Chinese, Japanese, Korean, and Russian. This led us to ponder how much information lay underused and underappreciated in foreign-language or gray literature. Hence came the idea to ask our Chinese colleagues to share their knowledge with us through this book. Our initial aim was to fulfill the curiosity of sea cucumber aficionados and researchers like us and to help stakehold- ers around the world understand the cultural background and success of China when it comes to sea cucumber production and trade. We have tried to solicit contributions from experts in nearly all aspects of the biology, ecology, captive breeding, and commerce of A. japonicus. Admittedly and despite our best efforts, this book is not comprehensive; we recognize that much more information could have been included. Notwithstanding space constraints, emphasis was definitely placed on information that had not previously been published in English. We broke a number of language barriers, but certainly not all of them. The initial focus was on China; ultimately, Japan and the two Koreas joined in. In all, 42 contributors from 16 institutions and six countries were directly involved in this project (aside from external collaborators and reviewers; see Acknowledgments). We take this opportunity to apologize for the imprecisions and inaccuracies xxii Preface that have doubtless evaded our scrutiny. Please be reminded that they are not necessarily the fault of the contributors, but perhaps an unfortunate outcome of their meaning being lost in translation. The world of sea cucumber research is an ever-evolving one and we hope that this contribution will inspire and fuel many investigations to come! The adventure of this book was a challenging yet rewarding one. We wish to warmly thank all the contributors for sharing their insight, for working hard over the course of nearly two years, and for replying quickly to our many requests, comments, and suggestions. Of course, none of this would have been possible without the support and dedication of our friend and co-editor Hongsheng Yang, and of his team. May the sea cucumber god grant them wisdom and prosperity in this life and beyond! Annie Mercier & Jean-François Hamel Newfoundland (Canada)

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