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Coral Reef Marine Plants of Hainan Island E.A. Titlyanov, T.V. Titlyanova, Xiubao Li, Hui Huang South China Sea Institute of Oceanology, Chinese Academy of Sciences; A.V. Zhirmunsky Institute of Marine Biology Far East Branch of the Russian Academy of Sciences 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 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1800, San Diego, CA 92101-4495, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom Copyright © 2017 China Science Publishing & Media Ltd. Published by Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability 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. Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library ISBN: 978-0-12-811963-1 For information on all Academic Press publications visit our website at https://www.elsevier.com/ Publisher: Glyn Jones Acquisition Editor: Simon Tian Editorial Project Manager: Naomi Robertson Production Project Manager: Stalin Viswanathan Designer: Matthew Limbert Typeset by TNQ Books and Journals Biography Titlyanov Eduard Antoninovich Prof. Eduard Titlyanov graduated from Far Eastern State University at Vladivostok in 1963 where he received his Dr’s degree. He went on to receive his master’s degree specializing in plant biochemistry in 1966 from Leningrad State University. In 1981 Titlyanov Eduard defended degree of Doctor Biological Sciences. He is the head of the Laboratory of the Physiology of Marine Autotrophic Organisms, A.V. Zhirmunsky Institute of Marine Biology, Far Eastern Branch of the Russian Academy of Sciences. His research areas include macroalgae and coral distribution dependent on light and other environmental factors and the autotrophic and heterotrophic functions of the various reef-building coral species and the range of their habitat. During last 15 years Prof. Titlyanov E.A. has carried out investigations in the field of adaptation of marine algae, both multicellular and unicellular (zooxanthellae), and in the spectral composition of light. He has published more than 200 papers and 5 books. Titlyanova Tamara Viktorovna Titlyanova Viktorovna is scientific researcher at the Laboratory of the Physiology of Marine Autotrophic Organisms, A.V. Zhirmunsky Institute of Marine Biology, Far Eastern Branch of the Russian Academy of Sciences. Her areas of special interests are the taxonomy of marine plants of the tropical and subtropical zones. She has published more than 50 papers and 3 books. Xiubao Li Associate professor in coral reef ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences. vii viii Biography Hui Huang Professor Huang is currently leading a research group on coral reef ecology and coral taxonomy with 10 faculty members and 6 graduate students. Her recent research work focuses on (1) coral taxonomy; (2) status and species WWdistribution of coral-reef and coral communities in China’s coastal and oceanic waters, and in particular the taxonomy of stony corals and gorgonian; (3) the health status and evaluation of coral-reef and coral communities in China, especially the deg- radation process under local sediment/eutrophication stress and global change ambi- ence; and (4) conservation and management strategy of coral-reef ecosystem and marine biodiversity. Introduction Hainan Island is located in the north tropical periphery of the Indo-Pacific Ocean in the South China Sea. It has a land area of 33.920 km2 and its coastline is more than 1000 miles. The major habitat of Hainan Island is the coral reefs, which occupy the shallow subtidal areas between 3 and 10 m depths, and the seagrass beds, estuaries, and mangrove swamps are less com- monly found. Marine plants occur in all habitats (ecosystems) but with the highest species richness on coral reefs (Zhang et al., 2006). There are several reasons for this, which is why we focus this book on the marine plants on the coral reefs of Hainan Island. First of all, studies on the marine plants of the island, especially the ones on coral reefs, are insufficient for us to estimate the recent status of coral reefs—the main coastal ecosystem of Hainan Island—or to pr edict the fate of the ecosys- tem. Secondly, Hainan Island has become very popular and attracts thousands of tourists from all over the world. Therefore people need a guidebook on the marine plants around the island when they explore along the Hainan coast. In addition, the Marine Biological Station of the South China Sea Institute of Oceanology, Chinese Academy of Sciences is situated in the Sanya Bay (Hainan Island). Many students and scientists from both China and abroad come here every year to do research. It would be very helpful for these researchers (especially students) to have a book on the marine plants of Hainan Island. This book summarizes the literature on the roles of marine plants in the coral-reef ecosystem, as well as their use, e specially in China and the countries in the Asian-Pacific region. It includes the studies from us and other groups. The authors of this book are professionals in different fields of coral-reef science: E.A. Titlyanov is a sp ecialist in the biochemistry, physiology, and ecology of marine benthic algae and hermatypic corals; T.V. Titlyanova is a sp ecialist in the taxonomy and ecology of macroalgae in the temperate and tropical zones; Huang Hui and Li Xiubao are oc eanologists studying coral reefs as ecosystems. This book includes both scientific works and popular publications that will not only help students and researchers but will also benefit tourists and everyone interested in the underwater plant world. The first chapter of this book focuses on the description of coral-reef ecosystems, the architecture of coral reefs, and the st atus of Hainan Island coral reefs. The second chapter focuses on common knowledge of marine plants, such as their cl assification, identifying characteristics of different phyla, morphology, reproduction, life forms, main algal co mmunities on coral reefs, distribution of algae on coral reefs and their roles, the use of seaweeds in cookery, me dicine, industry, and agriculture. The third chapter on the seaweed flora of Hainan Island contains species co mposition of the marine benthic flora, a complete list of marine plants found by researchers from all the studies, and historical and se asonal changes in the flora. The last chapter of this book shows how to identify common species of marine plants on the coral reefs of Hainan Island. We are sincerely grate- ful to everyone who reads this book and is interested in the s ubject. We hope you all enjoy the live plant world of the ocean! Tropical Marine Biological Research Station in Hainan, Chinese Academy of Sciences, Sanya, Luhuitou, where were carried out main studies have been carried out from 2008 to 2015. ix Chapter 1 Coral Reefs 1.1 C ORAL REEF ECOSYSTEMS The coral reef ecosystem is a collection of diverse species that interact with each other and with the physical environment. The latitudinal distribution of coral reef ecosystems in oceans (geographical distribution) is determined by the seawater tem- perature, which influences the reproduction and growth of hermatypic corals—the main component of the ecosystem. Thus coral reefs only occupy tropical and subtropical zones. The vertical distribution (in depth) is limited by light. Sunlight is the main energy source for this ecosystem, which is produced through photosynthesis of symbiotic microalgae—zooxanthellae living in corals, macroalgae, seagrasses, and phytoplankton. The hard substratum for the majority of recent corals is mainly limestone basis which was formed from fossil hermatypic organisms. The other hard substrata colonized by hermatypic corals are underwater rocks and stones, which later form coral reefs. Moreover, coral reef can also be built on the basis of artificial substrata (e.g., oil towers or underwater constructions of mariculture farms in tropical regions of oceans) (Titlyanov and Titlyanova, 2012a). The main difference between coral reefs and other underwater ecosystems is the formation of hard substratum, which is based on hermatypic coral colonies dying off and subsequent colonization by animals includ- ing corals and seaweeds. Coral reefs are the most diverse ecosystem and provide the largest primary production among all underwater ecosystems on the coastal shelf. They occupy less than 0.1% of the world’s ocean surface, but provide habitat and refuge for 25% of all marine organisms, including fish, mollusks, worms, crustaceans, echinoderms, sponges, tunicates, etc. Competition for resources such as food, space, and sunlight are the primary determining factors for the abundance and diversity of the organisms on a reef. 0 Coral reefs are less resistant to the natural and anthropogenic catastrophes that disturb the established balance between producers and consumers, predators and tolls, and symbionts and their hosts. This indicates that fluctuations in the abundance of one species can drastically alter the diversity and abundance of others. Hurricanes and other large storm events can be the stimulus for such alterations, but anthropological forces more commonly influence the ecosystem. For example, overfishing of herbivorous fish often results in increased growth of algae and seagrasses. The disturbance of symbiotic interactions between corals and algae zooxanthellae leads to coral bleaching and to subsequent mortality. Dead coral colonies are rapidly colonized by algae, which causes shift of coral reef to “plant reef” with the predominance of macrophytes in the ecosystem. After decades, this “plant” reef (although its biodiversity and primary production are simi- lar to coral reef) will be destroyed by waves due to the mortality of hermatypic corals and the loss of the ability to create carbonate calcium for reef formation (Titlyanov and Titlyanova, 2012a). 1.2 A RCHITECTURE OF CORAL REEFS Coral reefs have calcium carbonate-based structures that are constructed by communities of reef-building stony corals or scleractinian corals (Fig. 1.1). Coral reefs are generally divided into four main types: (1) fringing reef is the most common type and develops adjacent and parallel to the shoreline; (2) barrier reef is an actively growing type that also occurs parallel to the coastline but relatively further away from the shore; (3) atoll is a ring of calcareous reefs that is often interspersed with low sandy isles and a relatively shallow, sheltered lagoon; and (4) patch reef appears as small mounds or cup-shaped structures growing on hard substrates that are cast into the lagoons of barrier reefs or atolls (Littler and Littler, 2003). The first zone of reefs is on the beach or rocky intertidal. It occurs adjacent and parallel to the intertidal shoreline, consisting of a shallow reef platform followed by a lagoon. The depth of the lagoon varies from less than a meter to 10–30 m. The lagoon with a sediment bottom is protected from intense wave actions by the offshore barrier reef. Lagoons can contain complex patch reefs that harbor a variety of delicate corals. Mangrove trees can also grow on the sandy and muddy bottom of lagoons. Channels that connect the lagoons with the open waters provide fresh and cold water for the lagoons. The channels enter lagoons via reef flat, a broad, shallow, and flat part of a reef that is protected from heavy surf by reef crest (reef rim). Reef crest is the top of the reef slope, and descends as deep as 5–15 m. The seaward side of the spur and groove is the fore-reef slope, drop-off, reef face, or wall that rises from the depths to a level just below or at the surface. Low-barrier islands are formed behind the reef crest (Littler and Littler, 2003). Both hermatypic corals and marine plants can inhabit in all these types of coral reefs. Coral Reef Marine Plants of Hainan Island. http://dx.doi.org/10.1016/B978-0-12-811963-1.00001-9 Copyright © 2017 China Science Publishing & Media Ltd. Published by Elsevier Inc. All rights reserved. 1 2 Coral Reef Marine Plants of Hainan Island FIGURE 1.1 Architecture of coral reefs (most of the coral reefs around Hainan Island and neighboring islands are fringing reefs and patch reefs) Modified according to Littler, M.M., Littler, D.S., 2003. South Pacific Reef Plants. A Divers’ Guide to the Plant Life of South Pacific Coral Reefs. Offshore Graphics, Washington, 331 pp. Marine plants on coral reefs consist of photosynthetic micro- and macroorganisms that live in the water column (phytoplankton), on the bottom (phytobenthos), or on the artificial substrates (phytofouling). Benthic marine plants play a leading role in the formation and functioning of the coral reef ecosystem. 1.3 S TATUS OF HAINAN ISLAND CORAL REEFS Hainan Island is located in the north tropical periphery of the Indo-Pacific Ocean in the South China Sea. It is characterized by a tropical monsoon climate, with the dry winter season occurring from November to April and the rainy summer season from May to October. The island is affected by northeast wind and waves in the winter and by south wind and waves in the summer. During summer, the eastern and southern coast of Hainan Island is also affected by seasonal upwelling. Except for the ecological functions that benefit fisheries, tourism, and shoreline protection, the coral reefs in Hainan Island may also act as coral larvae pathways from the South China Sea to the mainland coast (Wang et al., 2011). Moreover, the coral reefs in upwelling regions are also considered as potential refuges for corals in response to global climate change. In the past, coral reefs were abundantly distributed in shallow waters (<10 m) in coastal areas. According to the investigation in 2005–06, the live reef area of Hainan Island was about 140.04 km2 and was mainly distributed in Wenchang, Qionghai, Sanya, Wanning, Lingshui, Changjiang, Danzhou, and Lingao (Li et al., 2012, 2013a,b, 2015). The total live coral cover was 29.42%. Overall, 102 species of sclearactinian corals, including 42 genera and 14 families, were recorded in Hainan Island in history. According to preliminary investigations in the Sanya Coral Reef National Marine Nature Reserve we found 77 species of scleractinian corals belonging to 30 genera and 13 families (Fig. 1.2). The genera Porites, Montipora, and Galaxea were dominant. The mean live coral cover was 21.2% and the mean juvenile coral density was 18.2 colonies·m−2. In Wenchang, 53 species of scleractinian corals including 29 genera and 13 families were recorded in 2010 (Fig. 1.3). The massive corals (Favites, Porites, and Favia) dominated at places close to the river mouth, while the branch corals (Acropora) dominated at places far away. The mean live coral cover was 15.0%, ranging from 5.6% to 26.5%, and the mean juvenile coral density was 14.6 colonies·m−2, ranging from 4.8 to 22.6 colonies·m−2. Coral abundance has declined by at least 80% over the past 30 years for coastal fringing reefs along the China mainland and adjacent Hainan Island (Hughes et al., 2013) (Fig. 1.4). Climate change has affected these reefs, but to a much less extent than coastal development, pollution, overfishing, tourism impact, and destructive fishing practices. In Sanya, live FIGURE 1.2 Coral reefs in Sanya from 2010 to 2014. FIGURE 1.3 Coral reefs in Wenchang in 2010 and 2011. FIGURE 1.4 Percentage of coral cover over time on China’s inshore and offshore reefs in the South China Sea. According to Hughes, T.P., Huang, H., Young, M.A.L., 2013. The wicked problem of China’s disappearing coral reefs. Conservation Biology 27 (2), 261–269. 4 Coral Reef Marine Plants of Hainan Island coral cover decreased from 42.6% in 2006 to 14.1% in 2014 at a depth of 3 m, and from 33.3% in 2006 to 19.1% in 2014 at a depth of 6 m. Anthropogenic disturbances, such as dredging, sedimentation, overfishing, nutrient pollution, and macroalgal blooms were considered the main causes of coral degradation in Sanya Bay, since coral reefs can recover from coral bleaching and typhoon impacts (Li et al., 2012, 2013a,b; Fig. 1.2). Moreover, live coral cover declined dramatically from about 50% to 60% in 1980 to 15.2% in 2010 and then to 9.8% in 2011 in Wenchang after the Hainan flood. The Hainan flood in 2010 caused severely detrimental effects on shallow coral reefs in Wenchang (Huang et al., 2014). Terrestrial runoff (river discharges and aquaculture effluents) and seasonal upwelling have also influenced coastal reef waters and caused nutrient enrichment. “Top-down” (i.e., overfishing) and “bottom-up” (i.e., nutrient and cold-water) processes have likely resulted in the overgrowth of macroalgae and a phase shift from coral dominance to macroalgae dominance in most places in Wenchang (Li et al., 2015). With ongoing global climate change and coastal development, the coastal coral reefs in Hainan Island will continue to suffer from natural (e.g., coral bleaching, floods, and typhoons) and anthropogenic disturbances (e.g., sediment, nutrient, and other pollutants) in the future. Xiaodong Hai coral reef, March 2015. Chapter 2 Marine Plants of Coral Reefs All marine plants are autotrophic organisms (independent of their systematic status). They contain chlorophyll а and execute a photosynthetiic process that produces organic matter and oxygen by absorbing sunlight, carbon dioxide, and water. Marine plants belong to three groups of organisms: microalgae (blue-green, diatoms, dinoflagellates, zooxanthellae); macroalgae (green, brown, and red); and higher plants or seagrasses. The latter two groups are also called macrophytes. Marine algae and seagrasses form the base of the oceanic food chain. They are the primary producers that convert sunlight energy and nutrients into plant materials and oxygen. Moreover, marine plants provide food and shelter for many types of animals and contribute to the biological diversity of coastal habitats (Littler and Littler, 2003). 2.1 CLASSIFICATION The classification of living organisms (marine plants) is called systematics or taxonomy, which reflects the evolutionary tree (phylogenetic tree) of different organisms. Taxonomy classifies organisms into different groups called taxa, while sys- tematics identifies their relationships. In algology, the Linnaean taxonomy is dominant and includes ranks and binominal nomenclature. Plants are named according to the International Code of Botanical Nomenclature (ICBN). According to modern Linnaean taxonomy, the marine plants described or mentioned in this book belong to two empires and four king- doms. The Empire Eukaryota is comprised of three kingdoms: Plantae, Chromista, and Protozoa, and the Empire Prokaryota includes the Kingdom Eubacteria. The Kingdom Plantae consist of seagrasses (Phylum Tracheophyta, or marine flower- ing plants), green algae (Phylum Chlorophyta), and red algae (Phylum Rhodophyta). The Kingdom Chromista includes brown algae (Phylum Ochrophyta, Class Phaeophyceae, and Bacillariophyceae). The Kingdom Protozoa is comprised of unicellular algae-dinoflagellates (Phylum Myzozoa). The Kingdom Eubacteria is comprised of blue-green algae (Phylum Cyanobacteria). Each phylum (division) is divided into several classes, and every class is divided into several orders. Then orders are divided into families, families into various genera, and genera into species. The classification of marine plants is given in Latin. The major differences among representatives of different Phyla (Divisions) are in their somatic and reproductive structures, life histories, photosynthetic pigments, biochemistry of their storage products, and cell-wall ultrastructure. A scientific name is given to each species, which consists of two names: the first is the generic name (genus) and the second is the specific name (species). The first letter of the generic name is capitalized and the specific name is written in lowercase. Both are italicized or underlined. It is also customary that a binomial is followed by the author of that binomial. Recently, plant names were formatted by the “International Code of Nomenclature for algae, fungi, and plants (Melbourne Code) adopted by the Eighteenth International Botanical Congress Melbourne, Australia, July 2011” and a global spe- cies database on all groups of algae (Guiry and Guiry, 2016). According to the code, the green alga Caulerpa racemosa (Fig. 2.1) are presented as follows: Empire Eukaryota/Kingdom Plantae/Phylum Chlorophyta/Class Ulvophyceae/Order Bryopsidales/Family Caulerpaceae/Genus Caulerpa. 2.2 IDENTIFYING THE CHARACTERISTICS OF REPRESENTATIVES FROM DIFFERENT PHYLA Phylum Tracheophyta, Order Alismatales (Seagrasses) Seagrasses (marine flowering plants), inhabiting sandy and silty-sandy areas of the bottom, are one of the main compo- nents of the reef ecosystem. Some of them are able to attach to the hard base of the reef (e.g., Thalassodendron ciliatum). Seagrasses can form extensive beds or meadows in shallow-sheltered coastal waters. Similar to the terrestrial higher plants, seagrasses have roots, stems, leaves, and flowers (Fig. 2.2). Coral Reef Marine Plants of Hainan Island. http://dx.doi.org/10.1016/B978-0-12-811963-1.00002-0 Copyright © 2017 China Science Publishing & Media Ltd. Published by Elsevier Inc. All rights reserved. 5

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