Coral Reefs of the World

Volume 12

Series editors

Bernhard M. Riegl, Nova Southeastern University, Dania Beach, USARichard E. Dodge, Nova Southeastern University, Dania Beach, USA

Coral Reefs of the World is a series presenting the status of knowledge of the world’s coral reefs authored by leading scientists. The volumes are organized according to political or regional oceanographic boundaries. Emphasis is put on providing authoritative overviews of biology and geology, explaining the origins and peculiarities of coral reefs in each region. The information is so organized that it is up to date and can be used as a general reference and entry-point for further study. The series will cover all recent and many of the fossil coral reefs of the world.

Prospective authors and/or editors should consult the Series Editors B.M.  Riegl and R.E. Dodge for more details. Any comments or suggestions for future volumes are welcomed:

Dr. Bernhard M. Riegl/Dr. Richard E. Dodge Nova Southeastern University Dania Beach, FL 33004 USA

e-mail: rieglb@nova.edu and dodge@nova.edu

More information about this series at http://www.springer.com/series/7539

Yossi Loya • Kimberly A. Puglise Tom C.L. BridgeEditors

Mesophotic Coral Ecosystems

EditorsYossi LoyaGeorge S. Wise Faculty of Life Sciences School of ZoologyTel Aviv UniversityTel Aviv, Israel

Tom C.L. BridgeBiodiversity and Geosciences ProgramMuseum of Tropical Queensland, Queensland Museum NetworkTownsville, QLD, Australia

Australian Research Council Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsville, QLD, Australia

Kimberly A. PugliseNational Centers for Coastal Ocean Science, National Oceanic and Atmospheric Administration (NOAA)Silver Spring, MD, USA

ISSN 2213-719X ISSN 2213-7203 (electronic)Coral Reefs of the WorldISBN 978-3-319-92734-3 ISBN 978-3-319-92735-0 (eBook)https://doi.org/10.1007/978-3-319-92735-0

Library of Congress Control Number: 2018965735

© Springer Nature Switzerland AG 2019, This work is subject to copyright. All rights are reserved by the Publisher, 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 any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed.The use of general descriptive names, registered names, trademarks, service marks, 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.The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Cover illustration: Photo Credit: Luis A. Rocha, www.mesophotic.org, can be reused under CC BY license

This Springer imprint is published by the registered company Springer Nature Switzerland AG.The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

corrected publication 2019

This book is dedicated to the memory of John Wells, Tom F. Goreau, and Kiyoshi Yamazato, research pioneers of mesophotic coral ecosystems.

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A diver heading to explore the mesophotic coral ecosystems (MCEs) of Eilat, Red Sea. Due to the depth of MCEs (> 30 m), researchers are often assisted by diver propulsion vehicles to save precious bottom time. (Photo credit: Gal Eyal)

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Preface

Mesophotic coral ecosystems (MCEs) are unique tropical and subtropical ecosystems charac-terized as light-dependent reef communities typically found at depths ranging from 30 to 40 m and extending to over 150 m in clear waters. The dominant habitat-forming communities can be hard and soft corals, algae, and/or sponges. They are populated with the same types of organisms typically associated with shallow coral reefs but also support species unique to mesophotic depths. MCEs represent a significant component of coral reef ecosystems—poten-tially up to 80% of reef habitat worldwide (based on depth). Given their vast areal extent, it is hardly surprising that MCEs support a diverse range of species.

During the past decade, there has been increased scientific and management interest in MCEs as illustrated by the exponential increase in the number of publications studying this unique environment. In fact, more than 70% of the research on MCEs has been published only within the past 7 years (see Chaps. 1 and 52). This increase is largely due to an increased awareness of the existence of MCEs, as well as increased access and affordability of advanced technologies including advanced diving technologies (see Chap. 50) and autonomous under-water vehicles, submersibles, and remotely operated vehicles (see Chap. 51).

In 2008, the first international MCE workshop of scientists and managers was held in Jupiter, Florida, to determine the state of knowledge of MCEs and identify management infor-mation needs. In 2014, the second international MCE workshop (Eilat, Israel) set out to deter-mine the advances and gaps in knowledge of MCEs since the first workshop. In June 2018, a Gordon Research Conference (Lewiston, Maine) brought scientists and managers together to discuss the multiple factors controlling the structure and function of MCE communities world-wide. It is clear from these meetings and current literature that many gaps remain in our knowl-edge of MCEs—a point highlighted in many chapters of this book.

This book provides the first comprehensive synthesis of the state of knowledge about MCEs worldwide. It also highlights how much we still have to learn. We invited authors to submit manuscripts focused on identified topics, with the co-authors of their choosing. Each manu-script underwent technical review by scientific and management experts to ensure its scientific integrity. The peer-review process consisted of over 200 individual reviews that were used by the authors to improve their manuscripts. We are deeply indebted to our reviewers for their time and effort, and thank you for greatly improving and ensuring the quality of this book.

The book is divided into five parts by (a) geography, highlighting regional variation among MCEs; (b) environments, biodiversity, and ecology, identifying similarities and differences between MCEs and shallow reefs by taxa and biotic and abiotic conditions; (c) connectivity, discussing potential connectivity between MCEs and shallow reefs; (d) conservation, manage-ment, and threats to MCEs; and (e) technologies used for MCE research and future research needs. The purpose of summarizing MCEs in specific geographic locations was to provide the reader with a snapshot of what we know about that specific location, including the history of MCE research, environmental setting, habitat description, biodiversity of the major reef flora and fauna, ecology, and threats and conservation issues. The geographic areas covered include

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26 localities arranged according to regional oceanographic boundaries representing all oceans where MCEs occur (i.e., the Atlantic Ocean, the Gulf of Mexico, the Caribbean Sea, the Pacific Ocean, and the Indian Ocean). The geographic coverage of chapters documents not only what we know but also how much we don’t know about these locations. Significant gaps in our understanding exist where the vast majority of MCEs occur in the western Indian Ocean and much of the Coral Triangle.

In addition to summarizing MCEs by geographic location, authors documented what is known by taxa [microbes, Symbiodiniaceae, Foraminifera, scleractinian corals (biodiversity, ecology of Indo-Pacific upper MCE corals, sclerochronology, and reproduction), octocorals, gorgonians, antipatharians, and fishes (biodiversity)], abiotic factors (light, photosynthesis, heterotrophy, geology, and geomorphology), bioerosion, and disease problems. This is fol-lowed up by a discussion of reframing the “deep reef refuge” hypothesis, coral ecosystem connectivity between the Pulley Ridge MCE and the downstream Florida Keys, disturbances to MCEs, the invasive lionfish and MCEs, and the potential ecosystem services provided by MCEs. Lastly, the final part of the book highlights those technologies used in MCE research and identifies 25 questions to guide future research.

We would like to thank all the authors who contributed chapters; without you, there would not be a book. We pay our respects to the family and friends of John Rooney and Thiony Simon, both of whom lost their lives studying MCEs. Lastly, we hope that this book will inspire both current and future scientists to continue to explore and better understand MCEs.

Tel Aviv, Israel Yossi LoyaSilver Spring, MD, USA Kimberly A. Puglise Townsville, QLD, Australia Tom C.L. Bridge

Preface

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Part I Introduction

1 Mesophotic Coral Ecosystems: Introduction and Overview ................................ 3Richard L. Pyle and Joshua M. Copus

Part II Regional Variation in Mesophotic Coral Ecosystems

2 Bermuda .................................................................................................................... 31Gretchen Goodbody-Gringley, Timothy Noyes, and Struan R. Smith

3 The Bahamas and Cayman Islands ........................................................................ 47Marc Slattery and Michael P. Lesser

4 Pulley Ridge, Gulf of Mexico, USA ........................................................................ 57John K. Reed, Stephanie Farrington, Andy David, Stacey Harter, Shirley A. Pomponi, M. Cristina Diaz, Joshua D. Voss, Keith D. Spring, Albert C. Hine, Villy H. Kourafalou, Ryan H. Smith, Ana C. Vaz, Claire B. Paris, and M. Dennis Hanisak

5 The Mesoamerican Reef .......................................................................................... 71Erika Gress, Joshua D. Voss, Ryan J. Eckert, Gwilym Rowlands, and Dominic A. Andradi-Brown

6 Discovery Bay, Jamaica ........................................................................................... 85Phillip Dustan and Judith C. Lang

7 Puerto Rico ............................................................................................................... 111Richard S. Appeldoorn, Monica Alfaro, David L. Ballantine, Ivonne Bejarano, Hector J. Ruíz, Nikolaos V. Schizas, Wilford E. Schmidt, Clark E. Sherman, and Ernesto Weil

8 The United States Virgin Islands ............................................................................ 131Tyler B. Smith, Marilyn E. Brandt, Viktor W. Brandtneris, Rosmin S. Ennis, Sarah H. Groves, Sennai Habtes, Daniel M. Holstein, Elizabeth Kadison, and Richard S. Nemeth

9 Bonaire and Curaçao ............................................................................................... 149Pedro R. Frade, Pim Bongaerts, Carole C. Baldwin, Arthur C. Trembanis, Rolf P. M. Bak, and Mark J. A. Vermeij

10 Brazil ......................................................................................................................... 163Ronaldo Bastos Francini-Filho, Viviana Márquez Velásquez, Marianna Barbosa da Silva, Marcos Rogerio Rosa, Paulo Yukio Gomes Sumida, Hudson Tercio Pinheiro, Luiz Alves Rocha, Carlos Eduardo Leite Ferreira, Carlo Leopoldo Bezerra Francini, and Ricardo de Souza Rosa

Contents

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11 The Red Sea: Israel .................................................................................................. 199Gal Eyal, Raz Tamir, Netanel Kramer, Lee Eyal-Shaham, and Yossi Loya

12 The Chagos Archipelago .......................................................................................... 215Dominic A. Andradi-Brown, Zena Dinesen, Catherine E. I. Head, David M. Tickler, Gwilym Rowlands, and Alex D. Rogers

13 Ryukyu Islands, Japan ............................................................................................ 231Frederic Sinniger, Saki Harii, Marc Humblet, Yohei Nakamura, Hideo Ohba, and Rian Prasetia

14 Taiwan ....................................................................................................................... 249Vianney Denis, Derek Soto, Stéphane De Palmas, Yu Ting Vicky Lin, Yehuda Benayahu, Yusheng Michael Huang, Shao-Lun Liu, Jian-Wen Chen, Qi Chen, Nicolas Sturaro, Ming-Jay Ho, Yeng Su, Chang Feng Dai, and Chaolun Allen Chen

15 The Philippines ......................................................................................................... 265Patrick C. Cabaitan, Timothy Joseph R. Quimpo, Edwin E. Dumalagan Jr., Jeffrey Munar, Mary Ann C. Calleja, Ronald Dionnie D. Olavides, Kevin Go, Ritzelle Albelda, Dominic Cabactulan, Erin Joy Capdos Tinacba, Ma. Angelique A. Doctor, Cesar L. Villanoy, and Fernando P. Siringan

16 Palau .......................................................................................................................... 285Patrick L. Colin and Steven J. Lindfield

17 Pohnpei, Federated States of Micronesia ............................................................... 301Sonia J. Rowley, T. Edward Roberts, Richard R. Coleman, Heather L. Spalding, Eugene Joseph, and Mae K. L. Dorricott

18 Papua New Guinea ................................................................................................... 321Ken Longenecker, T. Edward Roberts, and Patrick L. Colin

19 Northwest Australia ................................................................................................. 337Andrew Heyward and Ben Radford

20 The Great Barrier Reef and Coral Sea .................................................................. 351Tom C.L. Bridge, Robin J. Beaman, Pim Bongaerts, Paul R. Muir, Merrick Ekins, and Tiffany Sih

21 Fiji .............................................................................................................................. 369Richard L. Pyle

22 American Samoa ...................................................................................................... 387Anthony D. Montgomery, Douglas Fenner, Randall K. Kosaki, Richard L. Pyle, Daniel Wagner, and Robert J. Toonen

23 Cook Islands ............................................................................................................. 409Richard L. Pyle, Joshua M. Copus, and Gerald McCormack

24 French Polynesia ...................................................................................................... 425Michel Pichon

25 The Hawaiian Archipelago ...................................................................................... 445Heather L. Spalding, Joshua M. Copus, Brian W. Bowen, Randall K. Kosaki, Ken Longenecker, Anthony D. Montgomery, Jacqueline L. Padilla- Gamiño, Frank A. Parrish, Melissa S. Roth, Sonia J. Rowley, Robert J. Toonen, and Richard L. Pyle

Contents

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26 Isla del Coco, Costa Rica, Eastern Tropical Pacific .............................................. 465Jorge Cortés

27 Chile and the Salas y Gómez Ridge ........................................................................ 477Erin E. Easton, Matthias Gorny, Ariadna Mecho, Javier Sellanes, Carlos F. Gaymer, Heather L. Spalding, and Jaime Aburto

Part III Environments, Biodiversity, and Ecology of Mesophotic Coral Ecosystems

28 The Mesophotic Coral Microbial Biosphere ......................................................... 493William Leggat, Sarah Gierz, Alejandra Hernandez- Agreda, and Tracy Danielle Ainsworth

29 Macroalgae ............................................................................................................... 507Heather L. Spalding, Gilberto M. Amado-Filho, Ricardo G. Bahia, David L. Ballantine, Suzanne Fredericq, James J. Leichter, Wendy A. Nelson, Marc Slattery, and Roy T. Tsuda

30 Symbiodiniaceae Genetic Diversity and Symbioses with Hosts from Shallow to Mesophotic Coral Ecosystems .................................................... 537Tamar L. Goulet, Matthew Q. Lucas, and Nikolaos V. Schizas

31 Large Benthic Foraminifera in Low-Light Environments ................................... 553Willem Renema

32 Sponges...................................................................................................................... 563Shirley A. Pomponi, M. Cristina Diaz, Rob W. M. Van Soest, Lori J. Bell, Linnet Busutil, Deborah J. Gochfeld, Michelle Kelly, and Marc Slattery

33 Biodiversity of Reef-Building, Scleractinian Corals ............................................. 589Paul R. Muir and Michel Pichon

34 Reef-Building Corals of the Upper Mesophotic Zone of the Central Indo- West Pacific ............................................................................. 621Emre Turak and Lyndon DeVantier

35 Sexual Reproduction of Scleractinian Corals in Mesophotic Coral Ecosystems vs. Shallow Reefs ....................................................................... 653Tom Shlesinger and Yossi Loya

36 Coral Sclerochronology: Similarities and Differences in the Coral Isotopic Signatures Between Mesophotic and Shallow-Water Reefs ........................................................................................ 667Tsuyoshi Watanabe, Takaaki K. Watanabe, Atsuko Yamazaki, Shiori Yoneta, Kohki Sowa, Frederic Sinniger, Gal Eyal, Yossi Loya, and Saki Harii

37 Antipatharians of the Mesophotic Zone: Four Case Studies ............................... 683Marzia Bo, Anthony D. Montgomery, Dennis M. Opresko, Daniel Wagner, and Giorgio Bavestrello

38 Octocorals of the Indo-Pacific ................................................................................. 709Yehuda Benayahu, Tom C.L. Bridge, Patrick L. Colin, Ronen Liberman, Catherine S. McFadden, Oscar Pizarro, Michael H. Schleyer, Erez Shoham, Bastian T. Reijnen, Michal Weis, and Junichi Tanaka

Contents

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39 Gorgonian Corals ..................................................................................................... 729Juan A. Sánchez, Luisa F. Dueñas, Sonia J. Rowley, Fanny L. Gonzalez- Zapata, Diana Carolina Vergara, Sandra M. Montaño-Salazar, Iván Calixto- Botía, Carlos Edwin Gómez, Rosalinda Abeytia, Patrick L. Colin, Ralf T. S. Cordeiro, and Carlos D. Pérez

40 Fishes: Biodiversity .................................................................................................. 749Richard L. Pyle, Randall K. Kosaki, Hudson T. Pinheiro, Luiz Alves Rocha, Robert K. Whitton, and Joshua M. Copus

41 Disease Problems ...................................................................................................... 779Ernesto Weil

42 Light, Temperature, Photosynthesis, Heterotrophy, and the Lower Depth Limits of Mesophotic Coral Ecosystems ........................... 801Samuel E. Kahng, Derya Akkaynak, Tom Shlesinger, Eric J. Hochberg, Jörg Wiedenmann, Raz Tamir, and Dan Tchernov

43 Bioerosion ................................................................................................................. 829David K. Weinstein, Rebecca L. Maher, and Adrienne M. S. Correa

44 Geology and Geomorphology .................................................................................. 849Clark E. Sherman, Stanley D. Locker, Jody M. Webster, and David K. Weinstein

Part IV Are Shallow and Mesophotic Coral Ecosystems Connected?

45 Beyond the “Deep Reef Refuge” Hypothesis: A Conceptual Framework to Characterize Persistence at Depth ................................................ 881Pim Bongaerts and Tyler B. Smith

46 Coral Ecosystem Connectivity Between Pulley Ridge and the Florida Keys ................................................................................................ 897Su Sponaugle and Robert K. Cowen

Part V Conservation, Management, and Threats to Mesophotic Coral Ecosystems

47 Disturbance in Mesophotic Coral Ecosystems and Linkages to Conservation and Management.......................................................................... 911Tyler B. Smith, Daniel M. Holstein, and Rosmin S. Ennis

48 Invasive Lionfish (Pterois volitans and P. miles): Distribution, Impact, and Management ....................................................................................... 931Dominic A. Andradi-Brown

49 Ecosystem Services of Mesophotic Coral Ecosystems and a Call for Better Accounting ............................................................................ 943Daniel M. Holstein, Pamela Fletcher, Sarah H. Groves, and Tyler B. Smith

Contents

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Part VI Mesophotic Coral Ecosystems Research: Technologies and Future Directions

50 Advanced Technical Diving ..................................................................................... 959Richard L. Pyle

51 Underwater Robotic Technology for Imaging Mesophotic Coral Ecosystems ..................................................................................................... 973Roy A. Armstrong, Oscar Pizarro, and Christopher Roman

52 Key Questions for Research and Conservation of Mesophotic Coral Ecosystems and Temperate Mesophotic Ecosystems ................................. 989Joseph A. Turner, Dominic A. Andradi-Brown, Andrea Gori, Pim Bongaerts, Heidi L. Burdett, Christine Ferrier-Pagès, Christian R. Voolstra, David K. Weinstein, Tom C.L. Bridge, Federica Costantini, Erika Gress, Jack Laverick, Yossi Loya, Gretchen Goodbody-Gringley, Sergio Rossi, Michelle L. Taylor, Nuria Viladrich, Joshua D. Voss, Joel Williams, Lucy C. Woodall, and Gal Eyal

Correction to: The Great Barrier Reef and Coral Sea ................................................. C1

Contents