Corals and Reefs: From the Beginning to an Uncertain Future 3031168860, 9783031168864

Table of contents :
Preface
Contents
1: Introduction: The Reef Phenomenon
References
2: Into the Intimacy of Corals, Builders of the Sea
2.1 Taxonomic Affiliation
2.1.1 Systematic Classification of Cnidarians
2.1.2 Scleractinians
2.2 Morphology and Anatomy
2.2.1 Polyp Anatomy
2.2.2 Reproduction
2.2.2.1 Sexual Reproduction
2.2.2.2 Asexual Reproduction
2.2.3 Anatomy of Calcareous Skeletons
2.2.4 Coral Colonies
2.2.4.1 Corallite Arrangement
2.2.4.2 Colony Morphology
2.3 Symbiosis
2.4 Biomineralisation
2.4.1 Calicoderm and Biomineralisation
2.4.2 Skeletons and Biomineralisation
2.4.3 Interface Between Calicoderms and Skeletons
2.4.4 Principles of Calcification
2.5 Nutrition
2.5.1 Prey Capture
2.5.2 Food
2.5.3 Autotrophy
References
3: The Modern Times
3.1 Biozonation
3.2 Reef Morphotypes
3.2.1 Fringing Reefs
3.2.2 Barrier Reefs
3.2.3 Atolls
3.2.4 Bank Reefs
3.2.5 High Carbonate Islands
3.3 Geographical Distribution
3.3.1 Ecological Control
3.3.2 Tectonic Control
3.3.3 Eustatic Control
3.3.4 Topographic Control
3.4 Reef Growth
3.4.1 Vertical Growth Strategies
3.4.1.1 Controlling Factors
3.4.1.2 Give-Up Growth
3.4.1.3 Keep-Up Growth
3.4.1.4 Catch-Up Mode
3.4.2 Lateral Growth
3.5 Morpho-Sedimentary Processes
3.5.1 Bioconstruction
3.5.2 Erosion
3.5.3 Bioaccumulation
3.5.4 Cementation
3.6 Internal Structure
3.6.1 Nature and Distribution of Facies
3.6.1.1 Framework Facies
3.6.1.2 Detrital Facies
Sand-Dominated Facies
Mud-Dominated Facies
3.6.1.3 Facies Distribution and Hydrodynamics
3.6.2 The Different Structural Models
3.7 A Brief History of Reef Development
3.7.1 The Climatic Context
3.7.2 History of Reef Development Since the Last Deglaciation
3.7.3 Reef History Throughout the Pleistocene
3.8 Record of Environmental Changes
3.8.1 Record at the Coral Colony Scale
3.8.1.1 Temperature
3.8.1.2 Salinometry
3.8.1.3 Rainfall
3.8.1.4 pH Measurement
3.8.1.5 Photometry
3.8.1.6 Current Measurement
3.8.2 Record at the Scale of a Reef Edifice
3.8.2.1 Reef Flats and Micro-atolls
3.8.2.2 Arrangement of Coral Communities
3.8.2.3 Arrangement of Reef Edifices
References
4: The Long March of Corals
4.1 The Time of the Origins
4.1.1 Early Earth and the First Traces of Life
4.1.2 Evolution of the Atmosphere
4.1.3 Geochemical Model of the Early Ocean
4.1.4 Emergence of Biomineralisation
4.1.5 The Early Calcifying Organisms and Cnidarians
4.1.6 The Earliest Corals
4.1.7 The Appearance of Scleractinian Corals
4.2 The Time of Diversification
4.2.1 Coral-Algae Symbiosis
4.2.1.1 Acquiring Photosymbiosis
4.2.1.2 Evidence of Photosymbiosis
4.2.1.3 Symbiosis and Coloniality
4.2.2 A Brief History of Coral and Reef Building
4.2.2.1 Paleozoic Times
The Cambrian
The Ordovician
The Silurian
The Devonian
The Carboniferous
The Permian
4.2.2.2 Mesozoic Times
The Triassic
The Jurassic
The Cretaceous
4.2.2.3 Cenozoic Times
The Paleogene
The Neogene
References
5: The Highs and Lows of the Reef Phenomenon
5.1 Causes
5.1.1 Causal Relationships
5.1.2 Gas Emissions and Volcanic Products
5.1.3 Methane Emissions
5.1.4 Thermogenic Gases
5.1.5 The Fall of Celestial Bodies
5.1.6 Behaviour of Organisms Facing Environmental Disturbances
5.1.7 Disturbances Induced by CO2 and Ocean Acidification
5.1.8 Thermal Shocks
5.1.9 Disturbances Induced by Ocean Deoxygenation
5.2 The Main Biological Crises
5.2.1 The Cambrian Crises
5.2.2 The Major Crisis of the Ordovician End
5.2.3 The Minor Crises of the Silurian
5.2.4 The Successive Crises of the Devonian
5.2.5 The Permian Crises
5.2.6 The Triassic Crises
5.2.7 The Lower Jurassic Crisis
5.2.8 The Jurassic-Cretaceous Transition (J-K)
5.2.9 The Cretaceous-Paleogene Crisis
5.2.10 The Paleocene-Eocene Crisis
5.2.11 The Eocene-Oligocene Transition
5.2.12 The Oligocene End to the Plio-Quaternary
5.3 The Response of Corals and Reefs to Crises: From Extinction to Recovery
5.3.1 At the Ordovician End
5.3.2 During the Silurian
5.3.3 During the Devonian
5.3.4 At the Permian
5.3.5 At the Permian-Triassic Boundary
5.3.6 From the Middle to the End of the Triassic
5.3.7 During the Jurassic
5.3.8 From the Upper Jurassic to the Lower Cretaceous
5.3.9 At the Cretaceous-Paleogene (K-Pg) Transition
5.3.10 From the Paleocene to the Eocene
5.3.11 From the Oligocene to the Miocene
5.3.12 During the Plio-Quaternary
5.4 Conclusions
References
6: Coral Reefs in the Face of Their Fate
6.1 Disruptive Agents in Action
6.1.1 Carbon Dioxide and Rising Surface Water Temperatures
6.1.2 Carbon Dioxide and Its Effects on the Carbonate Cycle
6.1.3 Carbon Dioxide and Ocean Acidification
6.1.4 The Other Disruptive Agents
6.2 The Response of Corals and Coral Reefs
6.2.1 Temperature Rise of Surface Waters
6.2.2 To Acidification
6.2.3 To Other Disruptive Agents
6.3 The Evolution of Coral Islets
6.3.1 The Modes of Low-Lying Islet Formation
6.3.2 Future Evolution of Low-Lying Islet: Maintenance, Reduction or Destruction?
References
Conclusions
Index

Citation preview

Coral Reefs of the World 16

Bertrand Martin-Garin Lucien F. Montaggioni

Corals and Reefs From the Beginning to an Uncertain Future

Coral Reefs of the World Volume 16 Series Editors Bernhard M. Riegl, Nova Southeastern University, Dania Beach, FL, USA Richard E. Dodge, Nova Southeastern University, Dania Beach, FL, 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: [email protected] and [email protected]

Bertrand Martin-Garin • Lucien F. Montaggioni

Corals and Reefs From the Beginning to an Uncertain Future

Bertrand Martin-Garin Aix Marseille Univ, CNRS, IRD, INRAE, CEREGE Marseille, France

Lucien F. Montaggioni Aix Marseille Univ, CNRS, IRD, INRAE, CEREGE Marseille, France

ISSN 2213-719X ISSN 2213-7203 (electronic) Coral Reefs of the World ISBN 978-3-031-16886-4 ISBN 978-3-031-16887-1 (eBook) https://doi.org/10.1007/978-3-031-16887-1 0th edition: # Presses Universitaires de Provence 2020 # Springer Nature Switzerland AG 2020, 2023 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of 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, expressed 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: Massive colony of a scleractinian coral of the genus Porites. Left: fossil Porites from the Miocene (-23 Ma) of the Côte-Bleue (France). Right: recent Porites from Lizard Island (Australia). Photography and editing by B. Martin-Garin This Springer imprint is published by the registered company Springer Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Preface

Life emerged on our planet about 3.8 billion years ago. However, it had to wait more than 3 billion years for the earliest pluricellular animals to start secreting a mineralised exoskeleton, more frequently, composed of calcium carbonate. Appearing about 600 million years ago, these organisms were millimetre- to centimetre-sized. Some, taxonomically linked to the Cnidaria phylum, were likely ancestors of earlier corals. Although small-sized, it seems that these were able to build decimetre- to metre-thick reliefs on sea floors. True framework reefs, probably not, true buildups, undoubtedly. Over the Paleozoic times, shallow, warm-water environments were dominated, from about 500 million years ago, by two primitive coral groups (Tabulata and Rugosa) which ended up disappearing about 252 million years ago. The first scleractinian species, which are the reef-building coral forms today, appeared presumably -300 million years ago. Already suspected in primitive coral forms, photosymbiosis between corals and microalgae, regarded as a major physiological innovation, will greatly contribute to the expansion and success of scleractinians in all warm seas worldwide, mainly from about 240 million years. However, the history of coral evolution was not as just going on and on. Life has been hit by numerous crises and suffered the effects of weapons of mass destruction at various dates, extraterrestrial (bolide fall) or terrestrial (volcanism, mainly). Whilst a great number of groups of organisms have since been eradicated, scleractinian corals have always managed to avoid the worst and to survive owing to their particularly efficient adaptive capacities. Current global warming and its serious harms to the environment and biodiversity are offering a real challenge to reef-building corals. Will corals be able to face up to this new crisis, although environmental changes do not operate currently at rates of the order of a few million years, but of human lifespan? It is this long history of corals and reef phenomenon that we attempt to reconstruct in this book, the history of emblematic biota throughout the evolution of Earth over the last 600 million years. The book includes a short introductory chapter, in which the term corals is defined and the concepts of reef and coral reef are addressed, five descriptive chapters, a list of references, and one index. Chapter 2 is devoted to coral taxonomy and the biology—reproduction, biomineralisation processes—anatomy, structure, and ecophysiology—symbiosis, trophic regime—of scleractinian corals. Chapter 3 aims at describing all attributes of modern coral reefs and their history over the Quaternary era. The chapter presents the different reef morphotypes and relevant biozonations, major controls of coral and reef growth, of geographical distribution patterns, and of internal reef structure, nature, and distribution, and sedimentary biofacies. Then, the reef growth throughout the Pleistocene and, especially, since the last deglaciation is summarised. The chapter ends with a short description of methods used to reconstruct paleoclimatic and paleoenvironmental parameters based on biometric and biochemical analyses from individual coral colonies to reef scale.

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Preface

Chapter 4 addresses the questions about physicochemical conditions that would have driven the emergence of life on Earth. The chapter then addresses how and when biomineralisation, early calcifying organisms, early cnidarians, early corals, and early scleractinians appeared and how and when coral–algal photosymbiosis was acquired. Finally, the history of builders and relevant buildups and reefs throughout the Phanerozoic times is told, step by step, from the lower Cambrian to the Pliocene end. Chapter 5 examines the biological crises and mass extinctions suffered by floral and faunal organisms since the beginning of the Phanerozoic and, more specifically, corals and other reefdwelling organisms. The respective role and compared effects of terrestrial and extraterrestrial killing agents are addressed as well as responses of corals and reefs to resulting environmental disturbances. Finally, the major crises regarded as responsible for coral disappearance and reef demise and episodes of reef recovery are reviewed. Chapter 6 explores the question of the future of coming coral generations and coral reefs in today’s context of climate change. The different factors that are controlling climate and environmental changes are described, and their effects on oceans and coral ecosystems are explained. Special attention is given to the response of low-lying coral islands—atolls, especially—to ongoing and future climatic disturbances including a rapid rise in sea level and increasing storm energy. The book ends with conclusive remarks, focused on the major role played by corals, mainly symbiotic scleractinian corals, in tropical marine ecology over the Phanerozoic, their great resilience to mass extinctions, and thus the dominant role of reef features in the Earth’s history. The authors are particularly grateful to personalities and colleagues who, in varying capacities, have allowed this book to be written and published. Firstly, many thanks are offered to colleagues who, in our respective careers, have been able to create conditions to our professional growth. Bertrand Martin-Garin acknowledges the help given early by Bernard Lathuillière, Professor at the université de Lorraine (Nancy, France), and Jörn Geister, PrivatDocent at Universität Bern (Switzerland). Lucien Montaggioni owes a debt to Bernard Salvat, Professor Emeritus and former Director of the Institute for Coral Reef Studies in French Polynesia, and late Guy Cabioch, formerly Research Director at the French Institute for Development. We would also like to thank Perle Abbrugiati, Chief Editor, and Jean-Claude Bertrand and Ivan Dekeyser, Co-Editors of Science Series at Aix-Marseille université (France) Press for granting authorisation to publish an English version of the book. Thanks are due to André Strasser, Professor Emeritus at the université de Fribourg (Switzerland), and Julien Denayer, Assistant Professor at the université de Liège (Belgium), for their comments and reviews of an early version of the manuscript. Marseille, France

Bertrand Martin-Garin Lucien F. Montaggioni

Contents

1

Introduction: The Reef Phenomenon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1 6

2

Into the Intimacy of Corals, Builders of the Sea . . . . . . . . . . . . . . . . . . . . . . . . 2.1 Taxonomic Affiliation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.1 Systematic Classification of Cnidarians . . . . . . . . . . . . . . . . . . . . . . 2.1.2 Scleractinians . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Morphology and Anatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.1 Polyp Anatomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.2 Reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.3 Anatomy of Calcareous Skeletons . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.4 Coral Colonies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3 Symbiosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4 Biomineralisation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.1 Calicoderm and Biomineralisation . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.2 Skeletons and Biomineralisation . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4.3 Interface Between Calicoderms and Skeletons . . . . . . . . . . . . . . . . . 2.4.4 Principles of Calcification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5 Nutrition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5.1 Prey Capture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5.2 Food . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.5.3 Autotrophy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

7 7 7 9 11 11 13 15 15 18 22 22 22 24 24 25 25 26 26 26

3

The Modern Times . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1 Biozonation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Reef Morphotypes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.1 Fringing Reefs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.2 Barrier Reefs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.3 Atolls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.4 Bank Reefs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2.5 High Carbonate Islands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3 Geographical Distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.1 Ecological Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.2 Tectonic Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.3 Eustatic Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3.4 Topographic Control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4 Reef Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.1 Vertical Growth Strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4.2 Lateral Growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5 Morpho-Sedimentary Processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5.1 Bioconstruction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

31 31 32 33 35 38 40 40 40 40 43 45 46 47 47 49 50 50 vii

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Contents

3.5.2 Erosion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5.3 Bioaccumulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5.4 Cementation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6 Internal Structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6.1 Nature and Distribution of Facies . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6.2 The Different Structural Models . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.7 A Brief History of Reef Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.7.1 The Climatic Context . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.7.2 History of Reef Development Since the Last Deglaciation . . . . . . . . 3.7.3 Reef History Throughout the Pleistocene . . . . . . . . . . . . . . . . . . . . . 3.8 Record of Environmental Changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.8.1 Record at the Coral Colony Scale . . . . . . . . . . . . . . . . . . . . . . . . . . 3.8.2 Record at the Scale of a Reef Edifice . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

51 52 53 54 55 61 64 64 64 66 66 67 72 76

4

The Long March of Corals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79 4.1 The Time of the Origins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79 4.1.1 Early Earth and the First Traces of Life . . . . . . . . . . . . . . . . . . . . . . 79 4.1.2 Evolution of the Atmosphere . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80 4.1.3 Geochemical Model of the Early Ocean . . . . . . . . . . . . . . . . . . . . . 81 4.1.4 Emergence of Biomineralisation . . . . . . . . . . . . . . . . . . . . . . . . . . . 82 4.1.5 The Early Calcifying Organisms and Cnidarians . . . . . . . . . . . . . . . 84 4.1.6 The Earliest Corals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86 4.1.7 The Appearance of Scleractinian Corals . . . . . . . . . . . . . . . . . . . . . 88 4.2 The Time of Diversification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89 4.2.1 Coral–Algae Symbiosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89 4.2.2 A Brief History of Coral and Reef Building . . . . . . . . . . . . . . . . . . . 93 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115

5

The Highs and Lows of the Reef Phenomenon . . . . . . . . . . . . . . . . . . . . . . . . . 5.1 Causes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1.1 Causal Relationships . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1.2 Gas Emissions and Volcanic Products . . . . . . . . . . . . . . . . . . . . . . . 5.1.3 Methane Emissions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1.4 Thermogenic Gases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1.5 The Fall of Celestial Bodies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1.6 Behaviour of Organisms Facing Environmental Disturbances . . . . . . 5.1.7 Disturbances Induced by CO2 and Ocean Acidification . . . . . . . . . . 5.1.8 Thermal Shocks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1.9 Disturbances Induced by Ocean Deoxygenation . . . . . . . . . . . . . . . . 5.2 The Main Biological Crises . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.1 The Cambrian Crises . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.2 The Major Crisis of the Ordovician End . . . . . . . . . . . . . . . . . . . . . 5.2.3 The Minor Crises of the Silurian . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.4 The Successive Crises of the Devonian . . . . . . . . . . . . . . . . . . . . . . 5.2.5 The Permian Crises . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.6 The Triassic Crises . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.7 The Lower Jurassic Crisis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.8 The Jurassic–Cretaceous Transition (J–K) . . . . . . . . . . . . . . . . . . . . 5.2.9 The Cretaceous–Paleogene Crisis . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.10 The Paleocene–Eocene Crisis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.11 The Eocene–Oligocene Transition . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2.12 The Oligocene End to the Plio-Quaternary . . . . . . . . . . . . . . . . . . . 5.3 The Response of Corals and Reefs to Crises: From Extinction to Recovery . .

121 121 121 122 124 124 125 126 126 127 127 127 127 128 128 129 129 130 131 131 131 132 132 133 133

Contents

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5.3.1 At the Ordovician End . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3.2 During the Silurian . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3.3 During the Devonian . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3.4 At the Permian . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3.5 At the Permian–Triassic Boundary . . . . . . . . . . . . . . . . . . . . . . . . . 5.3.6 From the Middle to the End of the Triassic . . . . . . . . . . . . . . . . . . . 5.3.7 During the Jurassic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3.8 From the Upper Jurassic to the Lower Cretaceous . . . . . . . . . . . . . . 5.3.9 At the Cretaceous–Paleogene (K–Pg) Transition . . . . . . . . . . . . . . . 5.3.10 From the Paleocene to the Eocene . . . . . . . . . . . . . . . . . . . . . . . . . 5.3.11 From the Oligocene to the Miocene . . . . . . . . . . . . . . . . . . . . . . . . 5.3.12 During the Plio-Quaternary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

133 135 135 135 135 135 137 137 138 138 140 141 141 141

Coral Reefs in the Face of Their Fate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1 Disruptive Agents in Action . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.1.1 Carbon Dioxide and Rising Surface Water Temperatures . . . . . . . . . 6.1.2 Carbon Dioxide and Its Effects on the Carbonate Cycle . . . . . . . . . . 6.1.3 Carbon Dioxide and Ocean Acidification . . . . . . . . . . . . . . . . . . . . . 6.1.4 The Other Disruptive Agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2 The Response of Corals and Coral Reefs . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2.1 Temperature Rise of Surface Waters . . . . . . . . . . . . . . . . . . . . . . . . 6.2.2 To Acidification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2.3 To Other Disruptive Agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3 The Evolution of Coral Islets . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.3.1 The Modes of Low-Lying Islet Formation . . . . . . . . . . . . . . . . . . . . 6.3.2 Future Evolution of Low-Lying Islet: Maintenance, Reduction or Destruction? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

145 145 145 145 147 148 149 149 152 153 154 154 155 157

Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 159 Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161

1

Introduction: The Reef Phenomenon

“Corals are the noblest plants in the Ocean, they are the roses of the capricious sea goddess, as rich in forms and colors as the whims of these same goddesses” in Joseph Roth, the Merchant of Corals, The Leviathan (1938).

Though they have a mineral skeleton, corals have been classified amongst invertebrates—animals without a spinal column and bone structures—a term without taxonomic value created by Jean-Baptiste de la Lamarck at the beginning of the nineteenth century. Corals are eumetazoans (higher metazoans), meaning pluricellular animals with more advanced cellular differentiation. However, it was not until the mid-eighteenth century that corals were recognised as animals. Since ancient Greece, corals and especially the Mediterranean red coral were considered as flowering plants, the flowers corresponding to the polyps spread out on the surface of the stony mass, therefore considered as stone plants: Lithodendron—in Greek. In this case, coral polyps possess a calcareous skeleton and have the capacity to develop more or less bushy encrustations, such as the species Corallium rubrum—Mediterranean red coral—living at depths going down to -200 m, or even deeper, to construct edifices of meter to pluridecameter thickness as do species belonging to the order Scleractinia (hard corals). Amongst scleractinians, the distinction between those able to build wave-resistant buildups, referred to as hermatypic— herms: reef, buildup, in the Greek language—and those not able to produce reefs and buildups, referred to as ahermatypic, is classically used (Wells 1933). The former are predominantly found in warm, shallow waters. The latter are regarded to be more adapted to colder and deeper waters, at depths—to many thousands of metres—but capable of producing edifices at least as high and wide as those created by tropical corals. Hermatypic forms are concentrated within the photic zone, i.e. the bathymetric range receiving a luminous flux high enough to allow for photosynthesis to occur, as they are living in association with symbiotic microalgae (zooxanthellae). Ahermatypic forms, usually regarded as

lacking symbiotic algae, do not have such light-related constraints. However, the classic distinction between hermatypic, reefbuilding and ahermatypic, non-reef-building forms appears to be arbitrary and confusing (Schuhmacher and Zibrowius 1985). Hermatypic forms can possess symbiotic algae (zooxanthellate) or be devoid of algal symbionts (azooxanthellate). All zooxanthellate hermatypic forms are constructional. Amongst zooxanthellate ahermatypic species, some can be constructional, and others are non-constructional. Some azooxanthelle hermatypic forms can be constructional. Amongst azooxanthellate ahermatypic corals, some can be constructional or non-constructional. The term reef is derived from the word arrecife in Spanish, its roots originating from the Arabian word ar-raṣīf, name given to a causeway or a key. According to the Dictionary, the word reef refers to a rock or group of rocks, a shoal located on the water’s edge of coastal areas. In addition, a coral reef corresponds to a rocky outcropping mass, a topographic anomaly built by corals in warm and clear waters, capable of resisting the action of storm waves. Unfortunately, the term reef has been overused. It has also been erroneously used to describe coral constructions from cold and deep waters, so qualified as deep-water coral reefs, and also often used by a number of authors to define organic edifices in the geological record, which are actually an assemblage of organisms with a mineralised skeleton that possess a variable construction power, or yet, to define muddy masses produced by microbes with strong power of retention, whilst all these structures have developed at depth, often far from the sea surface. In fact, the terms bioconstructions (buildups) or bioaccumulations would be more appropriate to describe the last two cases than the word reef. Although it is true that in the geological record, it is often difficult to differentiate the structures that developed near the sea surface from those that flourished several meters deeper. The word reef will be applied here to any structure resulting from the direct

# The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. Martin-Garin, L. F. Montaggioni (ed.), Corals and Reefs, Coral Reefs of the World 16, https://doi.org/10.1007/978-3-031-16887-1_1

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or indirect activity of living organisms, whether it is a real built structure or a simple accumulation. Owing to their large variety of forms and compositions, bioconstructions and bioaccumulations are classified in many ways, the most used being that of Riding (2002). It is based on the spatial arrangement and composition of reef structures. The structures result from the action of diverse processes put into play—construction, sedimentation and cementation—processes which ultimately determine the composition of sediment, or the respective proportions of each of the principal constituents: (1) in-place or reworked skeletons of building, (2) bioclastic sediments (matrices), a product of skeleton breakdown, filling inter- and intraskeletal spaces, cavities, pores, and residual spaces, and (3) inter- and intra-skeletal cements that ensure structure consolidation. According to Riding, organic reefs can be described on the basis of a triangular diagram, of which the peaks correspond respectively to the following three major components: S (skeletons essentially in growth position), M (matrix fillings), and C (cavities and cements)—(Fig. 1.1). In this context, organic reefs are identified amongst three categories: (1) matrix-supported reefs that include agglutinated microbial reefs, cluster reefs, and segment reefs, (2) skeleton-supported reefs or framework reefs, and (3) cement reefs. Microbial reefs are composed of stacked micro-laminae or clotted and granular masses that result from trapping of particles by a mucilage (mucus) and precipitation of calcium carbonate; these are controlled by microbial activity. Skeletons in growth position and inter- and intra-skeletal primary cavities are rare or even absent. Early marine cementation favours the consolidation and maintenance of the structure, the latter generally forming reliefs, which can attain many metres high depending on sediment supply by marine currents. Cluster reefs consist of skeletal organisms in growth position, but scattered throughout the structure. Inter-skeletal areas are occupied generally by bioclastic matrices. The amount of early cements outside of intra-skeletal cavities remains limited. The absence of coalescing framework limits both the vertical and lateral expansion of edifices, thus producing low-lying topography in the surrounding environment. Segment reefs are structures in which in-place skeletons can be relatively dense, even in close contact, but most often are reworked and partly removed. Matrix deposits form the main parts of the buildup volumes, but are weakly affected by early cementation. The resulting reliefs remain poorly developed. Framework reefs are characterised by the predominant building role of skeletons. These skeletons are in contact or coalescent, consisting of a continuous and rigid framework, capable of forming topographic anomalies of great amplitude

1 Introduction: The Reef Phenomenon

Fig. 1.1 Ternary classification of different reef types based on their major components—in-place skeletons, sedimentary (detrital) matrices, and cavities—cements. At the apices, the amount of the components is 100%, whilst it regularly decreases towards the opposite sides along the lines perpendicularly running from the apices. Accordingly, at each side, the amount of the relevant component is zero. For instance, the openframework reef type contains 50–90% of in-place skeletal products, 10% of detrital matrices, and 0–30% of cements. Frame reefs, cluster reefs, and segment reef have relatively similar compositional patterns; cluster reefs have lower percentages of in-place skeletal products, but higher amounts of detrital material. By contrast, there is no overlap between microbial reefs, mud mounds, and cement reefs. Modified from Riding (2002)

over the surrounding environments, regardless of the rate of particulate sedimentation and cementation. Intra-skeletal spaces are occupied by fine-grained sediments and early marine cements, and inter-skeletal spaces as well, but partly. Two types of framework reefs can be distinguished, those with open cavities (open-framework reefs) and those with sealed cavities ( filled framework reefs). In the former, the cavities remain open during the first stages of reef building, in turn allowing cryptic and sciaphilic organisms to colonise them, and are eventually filled with matrices and cements. In the latter, infilling of inter-skeletal space occurs coevally with skeletal growth. Cement reefs result from cementation of skeletal organisms, dominantly in growth position. These cements are an important part of the structure; their forms are often derived from those of skeletal growth. It is important to note that microbial, cluster, and segment reefs are structurally simple, consisting of low-amplitude reliefs (decimetric to metric scale), usually stratified. Framework and cement reefs possess a more complex and massive internal structure, due to the absence of stratifications, and create reliefs of greater amplitude (plurimetric to decametric scale). To this list of reef structures must be added carbonate mud mounds, which can create structures of great amplitude, without any skeletal elements. They generally result from biochemical processes controlled by the activity of microbial

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Introduction: The Reef Phenomenon

communities, which are capable of calcifying or precipitating cements to their surroundings. The majority of modern organic reefs—coral and algal reefs, mollusc- and tubeworm-built structures—are rigid structures that sometimes emerge at low tides and are resistant to wave energy. Except for structures created by worms which arise from bioaccumulation, modern reefs can be generally classified amongst framework reefs, even though, in the case of coral reefs, due to the fact that the amount of coral detritus is often much higher than that of in situ corals, the term “detritus reefs” can be applied. When comparing recent reefs (modern and Quaternary) and Pre-Neogene reefs—more than 23 million years; Fig. 1.2—it appears that these have morphological and structural dissimilarity. Indeed, beyond the nature and type of testaceous organisms implicated in their formation, one of the main causes responsible for disparity between recent and older reefs is to be sought in the very marked cyclicity of climate change. It began in the Miocene—about 15 million years ago—then greatly amplified during the Quaternary— from 2.5 million years ago. Glaciation and deglaciation have driven sea level fluctuations of great amplitude, which have

3

favoured the development of vast and thick reef systems with great structural complexity. The majority of modern coral reefs have developed during the last deglacial sea level rise, starting approximately 19,000 years ago and ending less than 6000 years ago. Reef drilling indicates that reef settlement has been initiated at around 10,000–8000 years ago (see Montaggioni 2005). However, a number of bioconstructions and bioaccumulations of the Paleozoic, Mesozoic, and part of the Cenozoic have been able to develop over periods of a few tens to hundreds of thousands of years, often encompassing several biostratigraphic zones. Consequently, modern and Quaternary coral reefs cannot serve as a robust baseline for interpretating the palaeoecological reef record, if not for brief periods during the Phanerozoic—last 541 million years; Fig. 1.2. The evolutionary history of corals and coral reefs would have started at the beginning of the Ordovician period (Fig. 1.2), around 470 million years ago. It has known a number of highs and lows from the beginning. Perhaps, the present times are merely another challenge for these great architects to overcome.

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1 Introduction: The Reef Phenomenon

Fig. 1.2 International Stratigraphic Chart published by the International Commission on Stratigraphy and used in this book. The chart provides two distinct time scales in which the history of the Earth is inscribed: the relative, chronostratigraphic scale and the absolute, chronometric scale expressed in million years. From Cohen et al. (2013)

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Introduction: The Reef Phenomenon

Fig. 1.2 (continued)

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References Cohen KL, Finney SC, Gibbard PL, Fan JX (2013) The ICS international chronostratigraphic chart. Episodes J Int Geosci 36:199–204 Montaggioni LF (2005) History of Indo-Pacific coral reef systems since the last glaciation: development patterns and controlling factors. Earth Sci Rev 71:1–75

1 Introduction: The Reef Phenomenon Riding R (2002) Structure and composition of organic reefs and carbonate mud-mounds: concepts and categories. Earth Sci Rev 58:163– 231 Schuhmacher H, Zibrowius H (1985) What is hermatypic? A redefinition of ecological groups in corals and other organisms. Coral Reefs 4:1–9 Wells JW (1933) Corals of the Cretaceous of the Atlantic and Gulf coastal plains and the western interior of the United States. Bull Am Paleontol 18:85–288

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Into the Intimacy of Corals, Builders of the Sea

“It’s in this last that precious coral belongs, an unusual substance that, at different times, has been classified in the mineral, vegetable, and animal kingdoms [. . .] A coral is a unit of tiny animals assembled over a polypary that’s brittle and stony in nature. These polyps have a unique generating mechanism that reproduces them via the budding process, and they have an individual existence while also participating in a communal life” in Jules Verne, Twenty thousand leagues under the sea (1869–1870).

The phylum Cnidaria is particularly diversified, including organisms such as medusas, sea anemones and corals, and also lesser-known organisms such as alcyonarians, zoanthids, siphonophores, or even myxozoans. There are no less than 11,000 species today (Brusca and Brusca 2003; Zapata et al. 2015) that belong to the phylum of cnidarians the name of which refers to the urticant characteristics of some of their cells: knidē (κνίδη) meaning stinging nettle in ancient Greek.

2.1

Taxonomic Affiliation

2.1.1

Systematic Classification of Cnidarians

Cnidaria is a phylum of the Metazoa kingdom (Metazoan, animal) composed of two groups: Anthozoan and Medusozoan—(Zapata et al. 2015); Fig. 2.1. These clades are well identified today from phylogenetic analyses of molecular data (Bridge et al. 1992; Berntson et al. 1999; Collins et al. 2006; Kitahara et al. 2010; Zapata et al. 2015) and are typified by highly specific morphological characteristics (Bridge et al. 1995; Marques and Collins 2004; Collins et al. 2006; Zapata et al. 2015). However, for a long time, the understanding of the main relationships between Anthozoa and Medusozoa have proved difficult (McFadden et al. 2006; Rodríguez et al. 2014) partly due to

divergences in form and structure between some fossil groups of the Cambrian—geological period between—541 million years ago (Ma) and—485.4 Ma—within the phylum Cnidaria (Cartwright and Collins 2007). As a result, a number of hypotheses have been proposed regarding the relationships between the different taxa. – The clade Medusozoa—often considered as a subphylum—would include the classes Hydrozoa, Scyphozoa, Staurozoa and Cubozoa (Fig. 2.1). Hydrozoans are the “false jellyfish” rhythmed by ontogenesis with a polyp and medusa stages, and comprising hydras and siphonophores, with free-floating and drifting colonial forms. Scyphozoans are free and swimming “true jellyfish”—with or without a polyp stage. Stauromedusae never have a polyp stage and remain blocked at the medusa stage, but they are fixed to their substrate throughout their entire life. Meanwhile, Cubomedusae, called “sea wasps”, with a more or less cubic form, are particularly urticant and dangerous, even deadly. – Studies using ribosomal DNA (France et al. 1996; Odorico and Miller 1997; Song and Won 1997; Berntson et al. 1999; Zapata et al. 2015) have revealed the monophyly of the Anthozoa clade—considered to be a class. It includes approximately 7500 existing species that have been described (Daly et al. 2007) and is composed of two main sub-classes: Hexacorallia and Octocorallia (Fig. 2.1). Octocorallians include soft corals (alcyonarians), gorgonians and sea pens (Pennatulacea). Hexacorallians comprise six orders currently: cerianthids (Ceriantharia), zoanthids (Zoanthidea), black corals (Antipatharia), sea anemones (Actinaria), corallimorphs (Corallimorpharia) and hard corals—Scleractinia (Fig. 2.1).

# The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. Martin-Garin, L. F. Montaggioni (ed.), Corals and Reefs, Coral Reefs of the World 16, https://doi.org/10.1007/978-3-031-16887-1_2

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Fig. 2.1 Taxonomic relationships between modern Metazoa and Cnidaria—lower part of the cladogram—and between the Orders from the Sub-class Hexacorallia (hexacorallians)—upper part of the cladogram. Modified, synthetised and adapted from Kitahara et al. (2010),

2 Into the Intimacy of Corals, Builders of the Sea

Kitahara (2011), Zapata et al. (2015), Lin et al. (2016). Photographs by B. Martin-Garin and F. Bassemayousse with the kind permission of the author

2.1 Taxonomic Affiliation

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Fig. 2.2 Distributional map of zooxanthellate scleractinian species. Ahermatypic, non-building species are living in seas in which winter temperatures fall below 20 °C—isochryme 20 °C. Hermatypic, reefbuilding scleractinian species are living within the intertropical zone, except in areas subjected to coastal upwellings. The highest

scleractinian diversity is found in the Pacific Ocean, within the zone bounded by Malaysia, Indonesia, Philippines, and Solomon Islands as usually referred to as the Coral Triangle. Modified and adapted from Veron et al. (2016)

2.1.2

– The group of symbiotic zooxanthellate corals represent the other half of the order (Fig. 2.2). They can live in temperate waters where winter temperatures can be below 20 °C—or the 20 °C isochryme—as in the Mediterranean (Fig. 2.2). However, these are not able to produce buildups. – The others, said to be hermatypic, are reef-building corals. Principally colonial, they live in clear and relatively shallow marine waters of the tropics (Fig. 2.2). They are at the root of all bioconstructions and currently observable coral reefs from around the world: for example, the great barrier reefs of Australia, New Caledonia or of Belize, coral islands of the Pacific, of the Indian Ocean or the Caribbean, and the reefs of the Red Sea. Coral reefs represent only 0.15% of the area of oceans, but nonetheless accommodate a quarter of the world’s marine biodiversity. The Coral Triangle is a geographical zone in the Pacific Ocean delineated by Malaysia, Indonesia, the Philippines and the Salomon Islands. Its surface area represents 1% of the planet’s marine and continental surface, but his zone encloses 30% of coral reefs and 75% of the species richness of hermatypic scleractinians on the global scale (Fig. 2.2).

Scleractinians

Scleractinian corals are present in all oceans in tropical, temperate and polar regions, at shallow to abyssal depths. They are characterised by small-sized organisms, their polyps, which secrete a calcium skeleton—have been present in the fossil record since, at least, the Middle Triassic— Ladinian (about -240 Ma), perhaps even since the end of the Paleozoic—before—250 Ma; see chapter The long march of corals. About 1300 existing species have been described (Cairns 1999; Veron 2000; Budd et al. 2010), belonging to two main groups: – The group of scleractinian corals that do not host unicellular algae (zooxanthellae). Often solitary and asymbiotic—azooxanthellate—these corals represent about half of the species from the scleractinian order and live in all regions, including those at great depths and at very low temperatures. This is the case for both species Madrepora oculata and Lophelia pertusa living in North Atlantic and in the Mediterranean at various depths, respectively, between -80 m to -1500 m, and -40 m to –3600 m, in seawater temperatures oscillating preferentially between +5 and + 8 °C (Naumann et al. 2014). These are able to produce buildups.

The remaining forms are tropical reef-building corals. Principally colonial, they live in clear and relatively shallow marine waters (Fig. 2.2). They form the dominant framework

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parts and are currently observable from coral reefs around the world: for example from the Great Barrier Reef of Australia, New Caledonia or Belize, coral islands in the Pacific and Indian Oceans, in the Caribbean and the Red Sea. Coral reefs represent only 0.15% of the oceanic area, but nonetheless house a quarter of the world's marine biodiversity. The Coral Triangle is a geographical zone in the Pacific Ocean delineated by Malaysia, Indonesia, the Philippines and the Salomon Islands. Its surface area represents 1% of the marine and continental global surface, but the zone encloses 30% of coral reefs and 75% of the species richness in reef-building scleractinians globally (Fig. 2.2). Even though there are known exceptions, the majority of azooxanthellate are solitary and have large polyps, whereas the grand majority of zooxanthellate corals are colonial (Kitahara 2011). The relationship between the presence of symbiotes and colonialism is believed to be an evolutionary response of species living in shallow waters (Stanley and Swart 1995). Until recently, the scleractinian classification was primarily based on the morphometric attributes of their calcium skeleton—see Budd et al. (2010) for summary and Stolarski and Roniewicz (2001) for descriptive classification. Wells (1956) recognised 5 suborders and 33 families, 20 still existing today. All of them would have derived from two lineages which appeared at the end of the Triassic. Alloiteau (1952) identified 8 suborders and 65 families, 35 of which are extinct. Chevalier and Beauvais (1987) recognised 11 suborders and 55 families, 25 of which are extinct. After two decades, Veron (1995, 2000) added 2 new suborders— 13 in total—and 5 new families, totalizing 60 families, 25 of which have disappeared. Meanwhile, in the past two decades, analysis of molecular phylogenetics has profoundly changed the understanding of scleractinian evolution (Fukami et al. 2008; Budd et al. 2010; Veron 2013). The works by Fukami et al. (2008) suggest that classifications based on molecular characteristics of a variety of mitochondrial and nuclear markers present very large differences compared to those based on morphological characteristics. Thus, molecular phylogenetic hypotheses related to scleractinians provide a more complex perspective on the relationships between families and genera than the morphological ones. All molecular analyses to date confirm the existence of two lineages, respectively called clade Complexa and clade Robusta (Romano and Cairns 2000; Kerr 2005; Fukami et al. 2008; Kitahara et al. 2010). A third lineage could even be identified through basal taxa, the taxonomic position of which remains still uncertain (Fukami et al. 2008; Kitahara et al. 2010), each lineage having representatives in a number of suborders and families. Some families are not monophyletic (Romano and Cairns 2000; Fukami et al. 2008) whilst eight of these families have representatives in both Robusta and Complexa clades— see Kerr (2005) and Fig. 2.3 as an example. Even

2 Into the Intimacy of Corals, Builders of the Sea

Fig. 2.3 The classical taxonomic classification of Scleractinaria was based originally on morphological attributes of their skeletons. With the advent of coral molecular datasets, two clades were delineated: Robusta and Complexa—respectively, labelled as Vacatina and Refertina by Okubo (2016). The tree generated from the synthetised morphological and molecular attributes of scleractinian corals, as proposed by Kerr (2005), shows that species belonging to the same family—coloured frames—can be encountered within the two clades

monophyletic families seem to include representatives traditionally placed in other families. The works by Fukami et al. (2008) and Huang et al. (2019) also demonstrate that some genera are not monophyletic and that many relationships between Complexa and Robusta remain unresolved. Additionally, molecular phylogenetic analyses were focused on reef building, zooxanthellate corals. Adding azooxanthellate taxa in such analyses could greatly affect the relationships amongst the clades. For example, the Caryophylliidae, a family living in deep waters, including the azooxanthellate genus Lophelia, is polyphyletic and, at the same time, their representatives are distributed both amongst Complexa and Robusta clades—Romano and Cairns 2000, Kerr 2005; (Fig. 2.3). Based on works on the embryogenetic morphological characteristics and the molecular data of various species, Okubo (2016) proposed a new classification by attributing

2.2 Morphology and Anatomy

new suborder names to Complexa and Robusta (Fig. 2.3). The so-called complex corals are now referred to as the suborder Refertina, derived from the Latin word refertus, meaning filled, as a reference to their solid embryo. The robust corals are classed into the suborder Vacatina, meaning vacatus in Latin, which signifies empty. Differences between Vacatina and Refertina lie in the fact that corals from the suborder Refertina do not possess a blastula stage during embryogenesis and therefore do not have a blastocoel, i.e. a cavity filled with water and salt deriving from the first divisions or segmentation of zygote (fertilised egg) during the embryonic development. The relationships at lower taxonomic levels should be better understood, using analyses combining morphological and molecular characteristics (Budd et al. 2010; Kitahara 2011; Veron 2013) and coupled with embryogenesis (Okubo 2016), molecular phylogeny allowing a better understanding of the evolution of morphological characteristics. This approach results in the integration of modern and fossil taxa in a unified system for all scleractinians. It would therefore not be surprising that other classifications will be proposed in the near future, especially as skeletogenesis is being examined in detail for an increasing number of groups. Hoping to see a stable classification for the Scleractinia order.

2.2

Morphology and Anatomy

The scleractinian order includes solitary and colonial, sessile marine organisms, sometimes free living. The polyps possess anatomical attributes very similar to those of actinarians—sea anemones and relatives—but contrary to actinarians, they are able to secrete an external calcium skeleton, called corallite. Hence, a scleractinian is characterised by two body parts: – If solitary, the soft part is formed from a single polyp, whilst colonial, it comprises multiple polyps. – The stony part is a calcium carbonate skeleton (often in aragonite), called corallum, made up of one or many corallites.

2.2.1

Polyp Anatomy

Scleractinian polyps are usually small-sized bodies, organisms, ranging from millimetre up to about 30 cm in diameter (solitary individuals). They possess a mouth and a coelenteron, i.e. a bag-shaped, gastrovascular cavity, open towards the outside via a short tube called stomedeum—or pharynx, that can be highly extensible, especially in Alveopora and Goniopora genera, thus allowing tentacles to be thrown forward to facilitate prey catching (Fig. 2.4). – The coelenteron has many functions, notably digestion and fluid circulation respectively related to nutrition and

11

respiration. It is separated by soft walls called mesenteries, arranged radially in pairs, grouped by six or multiples of six. The mesenteries, therefore, offer a large surface area for promoting digestion, photosynthesis and respiration. In addition, they contain reproductive organs. Mesenterial filaments, as coiled filaments, are wrapped along the inner margins of mesenteries. Furthermore, these filaments, extending over the mesentery surface, can be devaginated for prey capture and to eat neighbouring coral polyps in order to expand territory. – The mouth is usually split and can be encircled by an oral cone. Tentacles are tubular and serve as an extension of the coelenteron, in the form of one or more rings called circlets around the mouth. Usually, tentacles are smallsized, absent as in Pachyseris or large-sized as in Alveopora and Goniopora.

Similarly to all cnidarians, scleractinians are diploblastic metazoans and, thus, are composed of two cell layers separated by mesoglea, with the ectoderm outside and the endoderm inside (Fig. 2.4). In fact, there are two types of tissues: oral tissues composed of an oral ectoderm and an oral endoderm, and aboral tissues—close to the skeleton—composed of an aboral endoderm and an aboral ectoderm, known as calicoblastic, where skeletogenesis takes place. The two epithelial layers, termed ectoderm and endoderm during embryogenesis, are defined as epidermis and gastrodermis to the adult stage (Fautin and Mariscal 1991). However, the embryological terms remain largely overused in scientific literature to anatomically describe the polyp at its adult stage. The mesoglea does not contain any cell at the juvenile stage, but may then contain a large number of different cell types during polyp ontogenesis. Strongly hydrated, it is mainly composed of collagen fibres. Very thin in corals with small-sized corallites, mesoglea can be several millimetres thick in corals with large corallites. – The oral ectoderm is composed of epithelial cells— supporting cells—of sensorial, ciliated cells playing a role in receiving stimuli—of glandular cells containing fluorescent pigments—of amoeboid cells playing an immunological role—a nerve plexus—a muscle layer surrounding mesoglea—and finally, cnidocytes. The latter are cells containing venomous organelles called nematocysts (or cnidocystes), able, through stimulus, to liberate an urticant product typical of cnidarians—see anatomy of cnidocyte and envenomation mechanism in Fig. 2.5. – The aboral ectoderm—or calicoderm; Galloway et al. (2006)—is composed of a few granular cells, of desmocytes—which firmly attach the polyp to the skeleton—and of calicoblasts. The latter, as small-sized, very flattened cells contain many mitochondria, endoplasmic reticula, Golgi complexes and vesicles transporting

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Fig. 2.4 (a) Simplified anatomy of a coral scleractinian colony showing individuals—polyps—interconnected with the coenosarc. Original design of a Jurassic coral Isastrea colony by B. Lathuilière with the kind permission of the author. (b) Tentacles are composed of

2 Into the Intimacy of Corals, Builders of the Sea

oral tissue whilst the coenosarc (c) is made up of both oral and aboral gastrodermal tissues. Composite design from Brusca and Brusca (2003), Vidal-Dupiol et al. (2009) and Tambutté et al. (2011)

2.2 Morphology and Anatomy

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Fig. 2.5 Simplified anatomy of a cnidocyte—also known as nematocyte—before evagination (a) and after evagination (b). Modified and adapted from Brusca and Brusca (2003). Every cnidocyte contains an organelle referred to as nematocyste. The latter consists of a bulbshaped, operculum-capped capsule containing a tubular, hollow, and coiled structure attached. An immature cnidocyte is labelled as a cnidoblast. The outer part of a cnidocyte has a hair-like trigger referred to as cnidocil (a), which is a chemical mechanical sensor. When the

cnidocil is bent into contact with a prey (or anything), the locking bar of the cnidocyste releases the filament urticant still rolled in the nematocyste capsule. The filament pulls out the operculum and penetrates the targeted prey. This process takes a few microseconds only, perhaps 700 ns (700
10-9 s), and can accelerate to 40,000 g until 5,410,000 g (Nüchter et al. 2006). After the filament point has penetrated, the toxin contained by the urticate liquid within the nematocyst capsule is inoculated into the target through the filament

one or many aragonite crystals, that are the first components of scleractinian skeletons (see von Euw et al. 2017). – The oral endoderm is composed of epithelial, glandular and amoeboid cells—playing an acting role in excretion processes—of a nerve plexus, a muscular layer, but also symbiotic, unicellular algae (zooxanthellae) in reefbuilding, shallow-water corals. – The aboral endoderm is mainly composed of glandular and amoeboid cells, which both enclose numerous mitochondria.

In that respect, 25% of coral species have internal fertilisation in which spermatozoids, attracted to pheromones, migrate into the gastrovascular cavity via the mouth of a female polyp in order to fertilise its eggs. These are brooding species, meaning that after fertilisation, eggs develop and then change into a ciliated larva (planula) which rapidly hosts symbiotic algae prior to being released into the ocean—for instance, species related to Pocillopora, Dendrophyllia and Tubastrea. The other 75% are referred to as diffusing species, and have external fertilisation in which ovules and sperm are expulsed into the ocean. Each genus possesses its own reproductive technique. For example, Favites successively expulse streams of ovocytes, then sperm, whilst Acropora release clusters of oocytes containing tiny quantities of sperm—see the complete reproductive cycle of Acropora in Fig. 2.6. Fertilisation then occurs when ovocytes and sperm meet. This results in egg formation and then in the development of planktonic planula larvae. On many reefs, spawning occurs during synchronised mass events, during which every coral species within a given area releases eggs and sperm almost synchronously. Synchronisation is a key step in the reproduction of diffusing corals, since males and females cannot enter into contact. Given colonies can be separated by large distances, this release must be broad and time controlled. It generally occurs as a response to multiple environmental signals: water temperature, lunar cycle, nycthemeral cycles—length of day and night—winds and tides, and lastly, time of the day—egg release occurs generally at sunset (Veron 2000).

2.2.2

Reproduction

Scleractinian corals can reproduce sexually or asexually. Thus, corals have a biphasic life cycle, planktonic larval phase and a benthic (sessile) adult phase, during which most species live attached onto the reef (Fig. 2.6).

2.2.2.1 Sexual Reproduction About 75% of sleractinians are hermaphrodite forms and therefore produce male or female gametes, as they possess the reproductive organs of both sexes. The other corals are gonochoric, meaning they have distinct male and female colonies as in Porites genus or as in solitary Fungia. The coral sexuality tends to be similar within given species and genera, though there are exceptions. Sometimes, sexual behaviours vary with geographic areas within the same species (Veron 2000).

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2 Into the Intimacy of Corals, Builders of the Sea

Thus, a great number of planulae are produced to compensate for many risks, such as predation, during transport by marine currents. The time between the formation of planulae and substrate colonisation represents a period of particularly high coral mortality (Barnes and Hughes 1999). After floating, planulae come back to the sea bottom where they settle if conditions are favourable (Barnes and Hughes 1999). For most species, larvae settlement occurs within a couple of days, though some can swim up during 3 weeks, and even during 2 months (Jones and Endean 1973). Long travels of planulae as planktonic particles ensure species to be spread over the oceans. This process largely explains the distribution of species and of coral provinces (Fig. 2.2). Once planulae have fixed themselves onto a hard substrate, they are transformed into juvenile polyps. These build a limestone floor before producing the early walls of their calyxes.

Thereafter, asexual reproduction allows to form colonies that increase in size over time.

Fig. 2.6 Reproductive cycle of the scleractinitian coral Acropora genus, including diffusing species—releasing both female and male gametes for external fertilisation. The cycle starts and ends with gametogenesis that develops in mature coral colonies across reef zones, with a suite of complex, spatially and temporally separated phases. Fertilisation occurs in open water after a number of coral colonies have released clusters of oocytes and sperm within the upper water column. They are operating the earlier embryogenetic stages. Embryos grow to broadly sphere-shaped larvae and 36 h later, acquire a system of lashes at the

surface of the epiderm. These vibrate rhythmically allowing planula larvae to move. Larvae progressively elongate, then look for and settle on hard substrates. Later, these change into juvenile polyps with mouth and tentacles when symbiotic algae penetrate coral endoderm. The coral–algae symbiosis enhances coral calcification. Polyps began sprouting at base, resulting in a new colony. This process is the starting point of the asexual stage that promotes colony growth size. From studies by Hayashibara et al. (1997), Ball et al. (2002), Okubo and Motokawa (2007) and Jones et al. (2015)

2.2.2.2 Asexual Reproduction In asexual reproduction, new clonal polyps emerge from the parent polyps to spread over or create new colonies (Sumich 1996). This occurs when the parent polyp reaches a given size and divides into new polyps. This process remains active throughout the whole coral life (Barnes and Hughes 1999). All colonial scleractinians develop through a budding process—or gemmation—where the parent polyp divides into two or many child polyps. Intratentacular—or intracalicinal—budding occurs in the tentacular ring (or circlet) of parent polyps. Extratentacular—or extra-calicinal—budding occurs at the periphery of tentacle rings, whilst child corallites are forming close to parent ones (Figs. 2.6 and 2.7).

2.2 Morphology and Anatomy

2.2.3

Anatomy of Calcareous Skeletons

Individual skeletons are called corallites (Fig. 2.4)—which are tubular structures made up of two elements: at the lower part, a calcareous lamella (the basal plate) which the wall, or theca, arises from. The basal plate and the wall delineate a cavity, called the lumen, from which vertical radial elements (septa) spread over. In most scleractinians, septa are of varying lengths and exhibit cyclic symmetry. Generally, there are 6 septa in the first cycle, 6 in the second cycle, 12 in the third, 24 in the fourth and so on, or in orders typified by indeterminate numbers of septa of a given length. Practically, this cyclic arrangement is often inconsistent. In many corals, especially in Turbinaria, fourth cycle-related septa bend towards those of the third cycle to undergo fusion. This seems to be an early characteristic of scleractinians, since it occurs sporadically in various families and can be also observed in the earliest fossil corals. Porites species display a unique septal plan that is used extensively in taxonomy. The number of septa varies between 12, for instance, in Acropora, Stylophora or Porites, and many hundreds as in some solitary Fungia species. Throughout ontogenesis, the occurrence rate and growth of septa are species specific (see, for example Fig. 2.8). Depending on the genera, septa grow out of walls in the form of costae. In coral species where walls are not distinguishable—as in Agaricia, Coscinaraea, Leptoseris, Pavona and Psammocora—the biseptal sheets are continuous from one corallite to the next one (Fig. 2.9). Lumen can be occupied (or not) by a vertical skeletal structure known as columella, exhibiting different shapes: styliform, lamellar, parietal, trabecular, trabecular and continuous, and trabecular and discontinuous (Fig. 2.10). Lumen also contains an endotheca composed of irregular elements—dissepiments— and of horizontal, more or flattened calcium carbonate sheets—the floor or tabula (Fig. 2.4). The calyx is the uppermost part of the corallite delineated by the wall. Polyps can have an additional, thin skeletal structure at the outer part of walls, called epitheca. For colonial corals, walls are connected to one another by a number of structures, horizontal or not, all named as coenostum.

2.2.4

Coral Colonies

2.2.4.1 Corallite Arrangement In a coral colony, the arrangement of corallites determines the budding type—intratentacular or extratentacular—unique to each scleractinian genus. Colonies which present corallites separated by walls can have two types of budding: intratentacular or extratentacular, whereas if they have

15

common walls, the budding can be exclusively intratentacular (Veron 2000). If the corallites in a colony do not possess any common walls—the coenosteum being present only at the base and therefore barely visible—the arrangement is said to be phaceloid as for species of the genus Cladocora (Figs. 2.11 and 2.12). The dendroid arrangement should not be confounded with the phaceloid one. The corallites are arranged like tree branches and there is no coenosteum (Figs. 2.11 and 2.12). Corallites that slightly protrude and have their own walls but that are separated by a more or less developed coenosteum are said to be plocoid—as in Favia (Figs. 2.11 and 2.12). Some colonies develop both intra- and extratentacular budding, such as in Acanthastrea and Astrea. Another budding form occurs in the depressed parts (valleys) at the surface of the so-called meandroid coral colonies—e.g. in Platygyra where the calicinal centres are aligned and delineated by a common wall—or cerioid—e.g. in Favites— depending on whether they form valleys or not (Figs. 2.11 and 2.12). The cerioid arrangement results from the fusion of walls from different corallites in the absence of a coenosteum. If they are meandroid and have their own walls without a coenosteum, they are of flabello-meandroid type—as observed in some Eusmilia (Figs. 2.11 and 2.12). Finally, there exist three other rare arrangements. The first is the hydnophoroid type—characteristic of Hydnophora— where the corallite centres are arranged around crests or hills of the coenosteum. The second is the thamnasterioid type, in which the corallites are separated by a poorly defined and barely visible wall, and are linked to one another by costosepta, forming biseptal lamellae (Figs. 2.9 and 2.11). The third is the fungioid type, in which the calyx centres are irregularly or evenly distributed over the colony and interconnected by septal elements. The wall is present, but only visible on the lower side—e.g. the genus Herpolitha. Of course, there are also corals with only one calyx. There is therefore not a colony of several individuals, but a single individual. The type of arrangement of the corallites is therefore not applicable, the corals are said to be solitary—e.g. most of the genera of the family Fungiidae.

2.2.4.2 Colony Morphology Amongst scleractinians, solitary individuals—that participate weakly in reef building—can be distinguished from colonial individuals formed from budding. Only some scleractinian species have a single growth morphology—e.g. Pavona cactus—which dictates them to live in specific habitats. For most other corals, colony morphology is not genetically constrained; it presents not only a great variability but also a high phenotypic plasticity—this

16 Fig. 2.7 Effects of asexual reproduction by budding (or gemmation) on the development of scleractinian colonial skeletons. Budding occurs when a part of parent polyps divides to form a new clonal individual—or a new corallite. (a) Intra-tentacle or intra-calicinal budding: buds develop from oral discs of the parent polyp resulting in new, equally sized polyps within the tentacle ring. From Matthaï (1926). (b, c) Examples from the Caribbean Mussa and Dichocoenia genera. (d) Extratentacle or extra-calicinal budding: buds develop at external sites of the tentacle ring from the parent polyp, resulting in new, smaller polyps. (e, f) Examples from the Caribbean Siderastrea and Stephanocoenia genera. The red arrows show location of new individuals. Photographs by B. Martin-Garin

2 Into the Intimacy of Corals, Builders of the Sea

2.2 Morphology and Anatomy Fig. 2.8 Skeletal growth patterns of a solitary scleractinian coral (Turbinolia sulcata) from the Lutetian (about-43 Ma), Parisian Basin (France). (a) Development of septa. Modified and adapted from Alloiteau (1959). (b) Development of radial elements during ontogenesis

Fig. 2.9 Septa morphology types. (a) Simple septa from a Madracis decatis colony. (b) Costo-septa from a Stephanocoenia intersepta colony: costae of adjacent corallites are distinguishable. (c) Biseptal sheet from an Agaricia lamarcki colony: costae extend laterally from corallite to corallite. Photographs of coral specimens from San Andrés Archipelago, Providencia and Santa Catalina, Colombia. Collections from J. Geister and B. Martin-Garin. Photographs by B. Martin-Garin

17

18

Fig. 2.10 Columella morphology types. (a) Styliform: massive and protruding structure at which septa are merged through a secondary stereome. (b) Lamellar: plate-shaped structure, oriented parallel to the main axis of a corallite or a series of corallites; (c) Parietal. (d) Trabecular and continuous: spongy and continuous structure between the centre of corallites. (e) Trabecular and discontinuous: spongy and

property permits to express various phenotypes from a given genotype depending on physico-chemical environmental parameters (see Todd 2008; Fig. 2.13). In other words, many corals can adapt their forms to the habitat they occupy. For example, variations in available light—depending on water depth or turbidity—or wave energy—related to exposure—will have a profound impact on coral colony morphology. Living corals living close to reef crests are continuously beaten by waves, so will adopt robust forms with small-sized, short and thick branches, encrusting or massive colonies. These same species, if growing along lower reef slopes, will produce arborescent or tabular forms with thinner and longer branches due to lower wave energy and reduced light intensity (Fig. 2.14). Thus, depending on environmental conditions—i.e. light, water energy, rate of sedimentation, depth—and of course, budding types, scleractinian colonies will exhibit the following shapes: massive—a more or less prominent spheric or hemispheric dome—encrusting—forming a thin plate on substrates—laminar—forming large slats sometimes arranged in a tiered layout—foliaceous—resembling lettuce leaves—columnar—forming columns—and robust or slender branches—see Fig. 2.11: corallite arrangement versus colony morphology and Fig. 2.14: morphology of coral colonies in response to environmental conditions.

2 Into the Intimacy of Corals, Builders of the Sea

discontinuous structure. (f) Columella missing. Photographs from specimens collected in San Andrés Archipelago, Providencia and Santa Catalina, Colombia: Madracis decactis (a), Meandrina meandrites (b), Orbicella cavernosa (c), Diploria strigosa (d), Scolymia lacera (e), Acropora cervicornis (f). Collections from J. Geister and B. Martin-Garin. Photographs by B. Martin-Garin

2.3

Symbiosis

A hermatypic scleractinian coral is within a symbiotic association between a polyp, the host—and a unicellular dinoflagellate alga (zooxanthellae) varying in size between 6 and 15 μm. In this association, zooxanthellae that belong to the genus Symbiodinium (Fig. 2.15) inhabit the endodermic cells of polyp hosts at 1–5 million individuals per square centimetre (Schuhmacher 1988). Originally, only a single zooxanthellate species had been identified in association with corals. However, it is now understood that Symbiodinium is genetically diverse, composed of eight major diverging clades (clades A–H). Each clade contains multiple subclade genotypes (Baker 2003). The genetically different zooxanthellate types are mainly distinguished by their phenotypic response—such as growth rates or photosynthetic efficiency—and physico-chemical constraints, particularly to light intensity and temperature (Rowan 2004). The evolutionary success of the symbiotic association between reef-building scleractinians and Symbiodinium algae drives the high carbonate productivity and resulting deposition in tropical reef ecosystems in shallow waters (LaJeunesse 2004).

2.3 Symbiosis

19

Fig. 2.11 Arrangement of corallites and morphology of coral scleractinian colonies. Different colony types can display a similar arrangement. Modified from Martin-Garin et al. (2012)

Zooxanthellae are generally contained in young corals derived from asexual and sexual reproduction. In the case of sexual reproduction, zooxanthellae are directly transmitted to coral buds or to fragments that form new colonies. In corals derived from sexual reproduction, zooxanthellae are acquired either directly via the parents, or indirectly via the environment. Each coral species has a particular method by which symbiotes are acquired and their eggs may or may not contain zooxanthellae (Muller-Parker et al. 2015). During direct transmission of zooxanthellae through sexual reproduction, algae are transferred to eggs or to the larvae brooded by the parents. Most species do not have eggs that contain zooxanthellae. In species containing algae, freeliving zooxanthellae of the parental gastrovascular cavity can be ingested by gastrodermic follicle cells and then expelled by oocytes whilst passing through temporary gaps in the mesoglea, where they are phagocytosed by mature oocytes (Hirose et al. 2001). If fertilised eggs do not contain zooxanthellae, larvae brooded by the parent at the primary stages of development can absorb zooxanthellae at any time before release.

Corals which do not inherit parental zooxanthellae have to obtain them from seawater. As seawater bathing reefs tend to have a relatively low concentration of zooxanthellae under normal conditions, corals can gain zooxanthellae via reefal sediments (Takabayashi et al. 2012), by ingesting faeces released by corallivores, or via zooplankton prey ingested by polyps (Baker 2003). Corals provide a protective environment to algae and components required for photosynthesis— predominantly inorganic nitrogen and phosphate (PO43-); Fig. 2.16. In return, zooxanthellae produce oxygen, help coral polyps to eliminate metabolic waste and provide corals fatty acids, amino acids and organic carbon in the form of glucose, glycerol and glycolic acid—products of photosynthesis. Corals use these products to build proteins, fats and carbohydrates, and calcium carbonate is crucial for secreting skeletons—see Barnes and Hughes (1999), Lalli and Parsons (1995), Sumich (1996), Fig. 2.16. In fact, no less than 90–95% of organic matter produced by zooxanthellae in photosynthesis is transferred to polyp tissues (Sumich 1996; Fournier 2013). This is a key process for reef carbonate productivity (Levinton 1995).

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2 Into the Intimacy of Corals, Builders of the Sea

Fig. 2.12 Arrangement of corallites within coral colonies according to budding type. Pinkcoloured: intra-tentacle budding; green-coloured: extra-tentacle budding: blue-coloured: transerval division. Modified from Wells (1956)

Fig. 2.13 Changes in skeletal structure and colony morphology of Orbicella annularis as indicative of phenotypic plasticity according to irradiance and habitat location in reef environments. From personal

observations by B. Martin-Garin—Albuquerque Cay, San Andrés and Providencia (Colombia); Anse Dufour and Anse Noire (Martinique, France); Ambergis Cay and Half Moon Cay (Belize)

2.3 Symbiosis

21

Fig. 2.14 Changes in coral colony morphology according to different environmental parameters. Adapted from Chappell (1980)

In addition, zooxanthellae are behind coloured corals, since these algae contain photosynthetic pigments such as chlorophyll a—principally blue and red colours—and b— (blue and orange), carotenoids (yellow and orange), and xanthophylls—derived from yellow-coloured carotenoids. Pigment type and content vary according to coral species and colony morphology—e.g. laminar forms are rather rich in chlorophyll a, whilst massive meandroid forms are rich in carotenoids—but also according to irradiance—carotenoid and chlorophyll content decreasing with depth together with density of zooxanthellae in polyp tissues (Roos 1967).

Nevertheless, coral–algal symbiosis remains precarious at times, particularly when corals are stressed—generally due to increasing water temperature, rise in irradiance or nutrification, i.e. increasing nutrient supply (phosphates and nitrates). For example, when surface water temperature exceeds the maximum average summer temperature by 1–2 °C, polyps expel zooxanthellae and adopt an immaculate white appearance. This phenomenon is known as coral bleaching. When it persists and increases, symbiosis cannot be restored and the coral host dies. Nevertheless, despite the fragility of the coral–algal association, coral reefs still are the

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2 Into the Intimacy of Corals, Builders of the Sea

most productive and diversified marine environments, harbouring 25% of the world's marine biodiversity (Fox et al. 2003).

2.4

Biomineralisation

Scleractinians play a major role amongst mineralising organisms. They generate the most voluminous buildups ever produced through different biological and geochemical processes (Spalding et al. 2001). Each year, they release up to 0.83 Gt of calcium carbonate (Vecsei 2004). Apart from their contributions to reef framework building, scleractinians also participate in light absorption (Enriquez et al. 2005) and skeletons capture valuable information about past climatic and environmental conditions—(Adkins et al. 2003) see Chap. 3.

2.4.1

Calicoderm and Biomineralisation

The living parts of polyps always cover skeletons, in either solitary or colonial corals. In this latter case, polyps are linked together by a tissue named as coenosarc (Fig. 2.4). Of the four epithelial polyp layers, the calicoderm—aboral ectoderm—is the finest (Figs. 2.4 and 2.16). It is during embryogenesis that aboral ectodermic cells give birth to calicoblasts once planula larvae have changed into primary polyps after settling onto a hard substrate (Vandermeulen 1974); Fig. 2.16. Calicoblasts can be long, thin, flat, thick or cup-shaped depending on their level of calcification Fig. 2.15 Microphotograph of the zooxanthellate Symbiodinium genus by Blickwinkel Alamy

activity (Tambutté et al. 2007; Tambutté et al. 2011). Flat calicoblast cells are associated with low calcification activity, whilst cup-shaped cells are associated with high calcification activity (Tambutté et al. 2007, 2011). Calicoblastic cells also contain many mitochondria (Tambutté et al. 2007), regarded as indispensable “powerhouses” (Figs. 2.4 and 2.16).

2.4.2

Skeletons and Biomineralisation

Morphogenesis of scleractinian skeletons is typical of species and thus partially controlled by genetics. However, physicochemical factors intensively interact with genetics. Therefore, coral colonies often have an important phenotypic plasticity—see Sect. 3.4.2 and Garland and Kely (2006). Despite the large spectrum of growth forms in coral colonies, all scleractinians have similar underlying structures (Tambutté et al. 2011). Coral skeletons are composite structures comprising, at the same time, inorganic (97% of aragonite) and organic components such as proteins (0.07%) and water associated with organics—up to 2.5% (Sun et al. 2020). Skeletons can be analysed at four structural levels: – The macrostructural level refers to polyp organisation within colonies, i.e. arrangement of corallites and colony morphology—see Sect. 3.4 and Figs. 2.11, 2.12 and 2.17a, b. – The mesostructure level involves spatial arrangement of skeletal elements, including septa, costae, endothecae, dissepiments, columellae and eventual epithecae.

2.4 Biomineralisation

Fig. 2.16 Symbiosis processes between coral polyp and zooxanthellae algae. Polyps mainly provide inorganic nitrogen (Ni) and phosphate (PO43-). Algae provide oxygen and 95% of energy necessary to coral host metabolism in the form of fatty acids, amino acids and organic carbon—glucose, glycerol, glycolic acid etc. The calicoblastic ectoderm

23

and the calcifying extracellular environment as well play a prominent role in coral skeletogenesis through ion exchanges and higher pH values compared to those in the open sea. ADP adenosine diphosphate, ATP adenosine triphosphate. Modified from Fournier (2013)

24

2 Into the Intimacy of Corals, Builders of the Sea

– The microstructure and nanostructure levels involve the arrangement of basic elements, i.e. fibres. These are orthorhombic aragonite crystals forming needles, 0.2–1 μm in diameter, and up to 50 μm in length. Two skeletal growth regions can be identified: (1) centres of rapid accretion (CRA)—with fibro-radial aragonite bundles organised in centres of calcification (CoC; Fig. 2.17c, d)—in which alternations of magnesium-rich organo-mineral deposits and organics take place (von Euw et al. 2017), and (2) thickening deposits—TD; (Fig. 2.17c, e)—which are skeletal structures deposited at the margins of rapid skeletal accretion (Stolarski 2003). In a number of species, fibro-radial aragonite bundles are composed of fine growth lamellae (Ogilvie 1895, 1896) in which light and dark bands alternate (Bourne 1887). They are daily growth bands due to activity of daily cycles in zooxanthellae corals (see Risk and Pearce 1992; Stolarski 2003). The alternating bands were suggested to be basic calcification units (Cuif and Dauphin 2005). Accordingly, coral skeletons should be considered to be a series of stacked growth layers (Tambutté et al. 2011), or sclerobands.

In that respect, even though all coral skeletons inherently share same crystal morphologies, the way along which scleractinians arrange skeletal aragonite crystals is speciesspecific, allowing them to be taxonomically identified based on microstructural attributes of their centres of calcification and of their radiating fibres (see Wells 1956; Alloiteau 1957; Stolarski 2003; Kitahara et al. 2010).

2.4.3

Interface Between Calicoderms and Skeletons

Calicoderms are located at the interface with skeletons via extracellular calcifying medium (ECM) the thickness of which varies from a few nanometres to more than a micrometre—(Johnston 1980; Tambutté et al. 2007, 2011; Sevilgen et al. 2019); Figs. 2.14 and 2.16. The composition of the ECM is still being actively discussed, but it would appear to contain hydrated proteins and a gelatinous substance (Johnston 1980). Hermatypic scleractinians would be able of controlling nucleation and rapid growth of crystals by modifying carbonate chemistry in calcifying fluids. Microelectrodes bathed in calcifying fluids reveal a pH of 9.3 or greater (Al-Horani et al. 2003; Ries 2011; Cai et al. 2016), which is significantly higher than that of the ambient seawater—generally between 8.0 and 8.2. Nevertheless, pH data are not sufficient to completely constrain chemical changes in calcifying fluids. Measurements of skeletal

uranium–calcium (U/Ca) ratios could overcome such an insufficiency, as speciation of uranium in seawater is controlled by ion carbonate [CO32-] concentrations (Djogic et al. 1986). Meanwhile, the role of abiogenic temperature and carbonate chemistry on skeletal aragonite U/Ca ratios is still poorly known, thus preventing to use U/Ca data to understand mechanisms of coral biomineralisation (DeCarlo et al. 2015).

2.4.4

Principles of Calcification

Corals construct their skeletons by precipitating and forming aragonite crystals, regarded as biogenic (orthorhombic CaCO3). Tropical surface waters are saturated with respect to aragonite, meaning that it can naturally precipitate from seawater physico-chemically. Nevertheless, the rates at which scleractinians are capable of secreting aragonite skeletons are significantly higher than those at which abiogenic aragonite precipitates, suggesting that corals have significant control on this process, known as vital effect. Coral calcification is a reaction requiring four molecules (Allemand et al. 2011) also involved in photosynthesis— inherent to the metabolic activity of zooxanthellae; CO2 + H2O →light CH2O + O2—and in respiration—or the complete oxidation of a glucose molecule; C6H12O6 + 6O2 → 6CO2 + 6H2O. Works by Goreau (1959) and Goreau and Goreau (1959a, b) delivered the first physiological data on ion input in coral skeletogenesis, with the following reaction: Ca2+ + CO32- ) CaCO3. However, in this reaction, the ratios of concentrations in CO32- and HCO3-—[CO32-]/[HCO3-]—that are extremely low compared to measured intracellular physiological pH values (between 7.5 and 9.3), cannot directly control the formation of skeletons (CaCO3). The effective reaction is the following: Ca2+ + HCO3- (bicarbonate) → CaCO3 + H+ (Ichikawa 2007). Polyps absorb seawater containing calcium (Ca2+) and carbonate (CO32-) and transfer them into extracellular calcifying medium (ECM) between calicoderm and existing skeleton (Fig. 2.16). They also eliminate hydrogen ions (H+), expelling them to reduce bicarbonate amount, in order to produce more carbonate ions (CO32-) which will link to calcium ions (Ca2+) to produce skeletons (Fig. 2.16). Within extracellular calcifying medium (ECM): – There is regulation of Ca2+ within the calcium channels of calicoderms (Fig. 2.16). – pH is always higher than that of seawater. – In polyps, calcium carbonate content increases in order to rise aragonite saturation rate—abbreviated Ωarag and expressed by the relationship [CO32-] × [Ca2+]/Ksp

2.5 Nutrition

where Ksp is the product of apparent solubility—compared to seawater. – All factors are thus combined to favour the precipitation of skeletal aragonite (Sevilgen et al. 2019).

2.5

25

matter. Corals are also known as autotrophs, since they obtain the required energy from the symbiotic relationship with zooxanthellae. The products derived from photosynthesis are glucose, glycerol and amino acids (Fig. 2.16). Polyps thereby use them to generate carbohydrates, proteins, lipids and calcium carbonate necessary for skeletogenesis.

Nutrition

Similar to all metazoans, scleractinian corals must extract nutrients from food. They are therefore heterotrophic (Goreau et al. 1971; Houlbrèque and Ferrier-Pagès 2009). As sessile organisms, they cannot move to feed. Corals get nutrients by using diverse strategies—tentacles, mucus, ciliary currents—to capture zooplankton, phytoplankton, bacteria, suspended organic particles and organic and mineral Fig. 2.17 Skeletal microstructure of a coral scleractinian Acropora colony. (a) Close-up of a branching Acropora colony. (b) Close-up of several adjacent calyxes. (c) One of the two three-dimensional models of septal microstructures in corals was proposed by Stolarski (2003). This model displays a discontinuity between organomineral phases of the two regions: deposits of Centres of rapid accretion (dCRA) and Thickening deposits (TD). (d) SEM photograph of a centre of calcification (CoC) composed of a bundle of fibro-radial aragonite crystals. (e) SEM photograph of a thickening deposits (TD). Photographs a, b by B. MartinGarin, Pigeon Island, Sri Lanka. SEM photographs d, e by A. Ribaud-Laurenti with the kind permission of the author

2.5.1

Prey Capture

Predation can be achieved in five ways, during day or night, depending upon considered coral species: – In corals with long tentacles, nematocysts are used to paralyse preys (Fig. 2.5). After capture, preys are brought

26

–

– – –

2 Into the Intimacy of Corals, Builders of the Sea

to the mouth by tentacles to be absorbed. In the mouth, mucus is secreted to coat preys, thus facilitating ingested preys to move towards coelenteron via stomodeum (Fig. 2.4). Ciliary currents are acting to eliminate any waste from coelenteron. In corals with short tentacles, preys that have been paralysed by nematocysts from coenosarc, are covered by mouth mucus filaments. Then, ciliary currents displace food to coelenteron. In most corals, prey are trapped by tentacles and mucus production, and accompanied by ciliary currents. Preys can also be captured by mesenteries (Fig. 2.4), which possess numerous nematocysts. Finally, some species, including Leptoseris fragilis, devoid of tentacles, use filtration to feed. Water enters coelenteron via the mouth or via microscopic pores (1–2 μm in diameter) located near scleroseptal crests in the oral epithelium. Water circulation is ensured by flagellar activity and probably by muscular activity. This system thus allows organic material in suspension such as bacteria to be absorbed (Schlichter and Liebezeit 1991).

2.5.2

Food

Corals mainly feed off zooplankton. Biggest individuals are captured by tentacles, whilst nanoplankton by mucus. These are particularly available at night. As for phytoplankton, it is absorbed sporadically. After ingested in the stomodeum, preys are not able to be rejected and are assimilated (Chevalier and Tiffon 1987). Organic particles produced by metabolic activity of various marine organisms—for example protein aggregates, colloids, mucus and faeces—are resuspended through water agitation and ingested via mucus and ciliary currents (Sorokin 1973). Large quantities of bacteria are ingested and well assimilated. These would represent from 1 to 7% of daily carbon uptake (Houlbrèque and Ferrier-Pagès 2009). The ectodermic tissues of polyps particularly absorb dissolved organic matter, mainly including glucose, glycerol and amino acids (Goreau et al. 1971). Dissolved mineral substances are directly absorbed via seawater: calcium—in the form of calcium bicarbonate, phosphorus—in phosphate form—or nitrogen in the form of ammonia, nitrites. Phosphates and nitrates locally are abundantly brought back into reef environments, mainly due to human agricultural activity. In too large quantities, these products are particularly harmful to corals—see Chap. 3.

2.5.3

Autotrophy

Symbiosis plays a significant role in coral nutrition. Hosted zooxanthellae systematically extract waste resulting from metabolism, such as CO2, to produce sulphur, nitrogen and phosphorus in order to synthesise proteins. Zooxanthellae also provide carbohydrates and lipids, but most importantly, participate in skeletogenesis—see paragraph 3: Symbiosis. The two trophic regimes are indispensable. If heterotrophy represents only 15–35% of daily metabolic uptake for healthy corals—and autotrophy 65–85%—it represents 100% for stressed corals and those that have lost zooxanthellae (Houlbrèque and Ferrier-Pagès 2009). Post-bleaching recovery imperatively requires heterotrophy and autotrophy coupling. By combining both modes, increasing zooxanthellae density, in turn, increases the rate of photosynthesis, protein and tissue synthesis, and, finally, calcification (Houlbrèque and Ferrier-Pagès 2009). The source and incorporation process of zooxanthellae after coral bleaching is still poorly understood to date (Muller-Parker et al. 2015). Tremblay et al. (2016) demonstrated that the percentage of autotrophic carbon retained by algal symbiontes is significantly higher during thermal stress than under non-stressful conditions. Higher retention of photosynthetic products in symbiontes results in lower translocation rates, forcing polyp hosts to use energetic reserves in order to respond to respiratory requirements. As calcification rates are directly driven by carbon translocation, there is a significant decrease in skeletal growth throughout the entire period of thermal stress. Tremblay et al. (2016) also showed that heterotrophy promotes the recovery of normal nutritional exchanges between both symbiotic associates.

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The Modern Times

“Still water is supporting my body. Behind my mask’s glass, I see the coral cliff going to widen and to deepen; purple spots, golden pools, red and yellow arborescences plunged in the deep blue. I cross the reef margin; deeper, are flourishing calcareous umbrellas, Acropora with branches as large as those of trees” in Philippe Diolé and Jacques-Yves Cousteau, Life and Death in a Coral Sea (1971).

Coral reefs considered to be modern are herein, by convention, those which developed during the Quaternary times, spanning the last 2.58 million years, a period characterised by important climate changes—alternations between glaciation and deglaciation periods. As a reminder, the Quaternary is subdivided into two series of very unequal durations: the Pleistocene, from 2.58 million years to 11,700 years before present (BP) and the Holocene, the last 11,700 years.

3.1

Biozonation

Modern coral reefs have a large variety of habitats (or biozones) in which the community structure—rate of surface coverage, spatial organisation and biodiversity—is controlled by a combination of physicochemical factors— mainly hydrodynamics, irradiance and nutrient levels. Regardless of its general physiography and its position relative to a land mass (see Sect. 3.2), a coral reef offers, from the open sea towards the most proximal parts, the following successive biozones (Figs. 3.1 and 3.2): 1. The outerslope zone (or fore reef zone) is the subtidal frontal part of the reef. It exhibits a morphology, which expresses the adaptation of building organisms to local energy requirements. In high water energy conditions, it forms a system of spurs—coral ridges perpendicularly aligned to the reef margin—and grooves—linear depressions between the spurs, allowing water bodies to evacuate to the open sea—of which the slope angle decreases with the increasing energy of breaking waves. In low water energy mode, the outer slope zone is

generally a subvertical drop. It often ends in a sandy bottom (sandy plain) or a coral terrace, situated at varying depths—from a few metres to many tens of metres—or is prolonged towards the deep sea by a subvertical cliff. 2. The reef-flat zone is the subhorizontal reef top surface, generally emerging during low tides, where coralgal communities proliferate. Several subzones usually occur from the outer reef margin inwards: a compact reef flat (with or without calcareous algal crusts), a transverse reef flat with coral alignments perpendicular to reef margin, a coral massive reef flat (locally composed of micro-atolls) or a reef flat of tabular or branching corals, and a reef flat of more or less dispersed coral elements. This zonal pattern can locally be simplified by the absence of one or more subzones, depending on local water energy requirements. 3. The backreef zone (or depression) corresponds to sandy spreads, at varying depths (metric to decametric) locally colonised by coral bushes or patches. Depending on the reef type, this zone is named as a boat channel or a lagoon. 4. The margino-coastal sedimentary deposits are sandy to rubble accumulations produced by reef-dwelling calcifying organisms. They occur on reef flats as islets, or along backreef coastlines as beaches.

Due to the ubiquity of several coral species, found in different biozones, it is difficult, especially in the Indo-Pacific region, to characterise each biozone or subzone from the specific composition of coral communities. However, coral colony shapes, along with the presence of an algal ridge, are locally useful criteria for identifying a given biozone. Six types of coral assemblages have been identified on the basis of their predominant colony forms (Figs. 3.3, 3.4 and 3.5): 1. Robust-branching coral-dominated assemblages (Fig. 3.4) are found preferentially on outer reef flats, reef fronts and outer slopes at less than—6 m deep, subjected to high

# The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 B. Martin-Garin, L. F. Montaggioni (ed.), Corals and Reefs, Coral Reefs of the World 16, https://doi.org/10.1007/978-3-031-16887-1_3

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Fig. 3.1 Typical morphology of a coral reef system

2.

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4.

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water energy conditions. These predominantly belong to the genera Acropora, Pocillopora and Stylophora (Fig. 3.5a). In higher agitated environments, where corals are not able to settle, thick calcareous red algal (Rhodophyta) crusts develop as algal ridges. These are found frequently along the outer edges of atolls subjected to large ocean swells (Fig. 3.5b). Massive (domal) coral-dominated assemblages are present within different, more or less agitated biozones (Fig. 3.4), from reef flats and backreef zones to outer slopes, between 0 and 25 m deep (Fig. 3.5c). The predominant forms belong to the genera Porites, Favia, Favites, Goniastrea, Platygyra, Diploria, Diploastrea and Pavona. On reef flats emerging at low tide, these corals can develop as top-flattened, dome-shaped colonies (micro-atolls) through necrosis of their uppermost parts as they reach mean low sea level (Fig. 3.6a). Tabular coral-dominated assemblages (Fig. 3.4) mainly occupy low to medium water energy environments, from upper to middle outer slope zones, outer to inner flats to backreef zones down to 20 m deep. These are usually associated with arborescent or thin-branching coral forms, predominantly composed of Acropora species (Fig. 3.5d). Arborescent or thin-branching coral-dominated assemblages are represented by forms belonging to Acropora species, which coexist with those from Porites, Pocillopora and Seriatopora (Fig. 3.5c). Foliaceous coral-dominated assemblages occur predominantly in low water energy, generally low light intensity zones, from sea surface to depths greater than 30 m (Fig. 3.6b). The most abundant forms are Agaricia, Pachyseris, Turbinaria, Merulina, Montipora, Cyphastrea and Pavona.

6. Encrusting coral-dominated assemblages are observed in a great variety of environments, from highly agitated zones to turbid and low irradiance zones, at depths from surface to greater than 100 m (Fig. 3.6b). Thanks to their flattened or even laminar form (Fig. 3.4), the colonies are capable of resisting powerful swell surges on uppermost fore reef zones and of optimising low solar radiation levels received at depth. These forms belong to Montipora, Leptoseris, Echinophyllia, Leptastrea, Echinopora, Cyphastrea and Alveopora.

3.2

Reef Morphotypes

Modern coral reefs are generally classified according to their form, size and relationships to landmasses. The first classification of reef morphotypes was elaborated by Charles Darwin (1842) following his journey to the Central Pacific aboard the ship HMS “Beagle” between 1831 and 1836. It is based on the observation of different reef forms associated with volcanic islands. Darwin, therefore, defined three main types of reefs constituting an evolutionary line derived from subsiding volcanic substrates. The lineage begins with fringing reefs, usually not exceeding a few hundred metres in width, with shallow backreef zones, surrounding young volcanic islands. Following these are barrier reefs with deeper and wider backreef zones, usually bordering older islands, then ring-shaped atolls resting on submerged volcanic basements. However, the fringing-barrier-atoll reef genetic lineage can only be applied to a limited number of configurations at the global scale. In fact, beyond the geodynamic behaviour of substrates, the modern reef

3.2 Reef Morphotypes

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Fig. 3.2 Aerial view of the fringing reef at Saint-Leu—western coast, Réunion Island, Western Indian Ocean—showing the successive biozones from the open sea landwards: outer reef (forereef) zone (visible

through sea transparency), reef-flat zone, backreef zone, and sandy beaches. Photograph by B. Martin-Garin. Figure modified from Montaggioni (1978)

morphotypes are controlled by a number of other factors, including availability, size and topography of the underlying foundations, sea-level variation and nutrient supply. By putting aside the genetic component and only retaining the physiographic aspects, it was possible to subsequently extend the Darwinian classification—fringing, barrier and ringshaped reefs—to reefs bordering the continents (Figs. 3.7, 3.8 and 3.9).

3.2.1

Fringing Reefs

Fringing reefs (Figs. 3.7, 3.8 and 3.9a) are found in the form of narrow ribbons which rarely exceed 2 km in width and are in direct continuity with the coastline, their geometry conforming to the meaning of the term fringing. These refer to the most common morphotype, covering more than 50% of the total reef surface in the modern seas. They are characterised by water depths always less than 10 m and

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Fig. 3.3 Distributional pattern of coral assemblages across modern Indo-Pacific coral reef systems as a function of water energy and depth. Note the presence of an outer algal ridge at high water energy,

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reef-crest settings. Modified from Montaggioni (2005), Montaggioni and Braithwaite (2009) and Martin-Garin (personal observations)

3.2 Reef Morphotypes

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Fig. 3.4 Distributional pattern of coral assemblages across modern Indo-Pacific coral reef systems as a function of water energy, irradiance and depth. Modified from Montaggioni and Faure (1980), Cabioch et al. (1999a, b). Photographs by F. Bassemayousse—foliaceous morphologies, Egypt—and by B. Martin-Garin—lamellar morphologies, Huahine Island, French Polynesia; massive, robust-branching and gracile-branching morphologies, Lizard Island, Australia; tabular morphologies, Maayafushi, Maldives

mostly less than 2 m, in what the backreef zone adjoining the coastline is called “boat channel” (Fig. 3.2). Their relatively simple morphology could mislead to think that their biodiversity, in particular that of corals, is weak. However, this is far away from the truth for the majority of them. Some fringing reef systems, which laterally expand in a discontinuous manner over a few hundred kilometres, such as in the Red Sea, contain over 220 coral species. The distinction between fringing and barrier reefs can be ambiguous. Thus, the term “almost barrier reefs” was introduced following observations in Micronesia in order to define narrow reef systems separated from the coast by water depths greater than 10 m. Likewise, a fringing reef can laterally change into a barrier reef, as observed in the islands of Moorea (French Polynesia) or Mauritius (Indian Ocean).

3.2.2

Barrier Reefs

Barrier reefs either surround islands or are encountered parallel to continental margins, at distances ranging from a few hundred metres to tens of kilometres far from the coast (Figs. 3.7, 3.8 and 3.9b). Backreef depressions reach local depths of many tens of metres, forming true interior basins. As a consequence, their morphology is even more complex than that of fringing reefs. Particularly, isolated or coalescing

coral buildups called patch reefs can be scattered on the adjacent backreef basins. The barrier morphotype is the least common of the three defined by Darwin. The most famous barrier reef, if not the most studied, is the Australian Great Barrier Reef, which stretches for over 2300 km along the north-eastern coast of the island continent, at a distance varying from 30 to 260 km. In fact, the term barrier is not quite used appropriately here, as it is not a unified reef, but a linear and discontinuous reef complex comprising about 2900 scattered individual reefs delineating an “inland” sea with depths greater than 30 m. Different reef types are distinguished, in accordance with Hopley (1982) and Andréfoüet et al. (2009), depending on their forms and location on the continental shelf, as (1) ribbon reefs, linear structures situated on the external part of the continental or insular shelves (outer shelf-barrier reefs), (2) platform reefs with ring-shaped or oblong forms, most frequently, situated in the middle section of the shelf (mid-shelf barrier reefs) and (3) fringing-barrier reefs, linear structures situated in the innermost part of the shelf or bordering the coast (intrashelf barrier reefs). Otherwise, a true continental barrier reef exists against the coast of Belize (north-east of South America) and extends almost continuously over 250 km, at a distance of 20–40 km from the shore. The classification established for the Australian Great Barrier Reef is applicable to the vast insular reef complexes, such as that of New

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Fig. 3.5 Dominant coral-assemblage types. (a) Robust-branching coral assemblage—dominated by Acropora group robusta—from a reef-crest (outer reef-flat) zone, carved out by a series of grooves, north of the Great Barrier Reef of Australia. Acroporid colonies are about 0.30 m in diameter. (b) Outermost part of an algal ridge developing as massive spurs and carved out by grooves, Takapoto Atoll, French Polynesia. (c)

Assemblage composed of massive, flat-topped Porites corals, robustbranching (staghorn), and gracile-branching Acropora colonies, north of the Great Barrier Reef of Australia. (d) Assemblage of diverse gracilebranching and tabular Acropora species, north of the Great Barrier reef of Australia. Photographs by L. Montaggioni

Fig. 3.6 Dominant coral-assemblage types. (a) Massive (domal) Porites colonies in the form of micro-atolls in an inner reef-flat zone, north of the Great Barrier Reef of Australia. (b) Assemblage of

encrusting and foliaceous corals, outer reef slope at about 35 m deep, Takapoto Atoll, French Polynesia. Photographs by L. Montaggioni

3.2 Reef Morphotypes Fig. 3.7 Different oceanic coralreef morphotypes and model of reef development based on subsidence of volcanic reefbearing islands according to Darwin’s theory

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Fig. 3.8 Dominant coral-reef morphotypes—fringing reef, reef barrier, atoll and reef bank

Caledonia (Western Pacific) which extends near continuously over a length greater than 1200 km, with an average width of 25 km. The barrier-reef type, amongst others, is exemplified in the Indian Ocean by the Great Reef of Toliara (south-west of Madagascar), those of the island of Mayotte and of the south-eastern coast of Mauritius.

3.2.3

Atolls

Atolls are low-lying, ring-shaped coral islands (Figs. 3.7, 3.8 and 3.9c), in mid-plate geodynamic position, which generally

are incorporated into an alignment of volcanic islands. They possess an outer reef rim that is mostly emergent and delimitates a central depression (lagoon). Reef rims are locally interspersed with coral detritus supplied from neighbouring outer reef slopes by storms and cyclones. These debris accumulate to form the emergent parts of the atoll, more or less continuous islets—called motu by the Polynesians, usually culminating between +2 and +5 m (Fig. 3.9d). These are mostly fixed by a dense vegetation, natural or cultivated (coconut groves). Islets are locally interrupted by narrow, shallow channels (less than 1 m at low tide), called hoa, that ensure water exchanges between

3.2 Reef Morphotypes

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Fig. 3.9 Views of different coral-reef morphotypes. (a) Fringing reef, south-west of Reunion Island, Western, Indian Ocean—photograph by B. Martin-Garin. (b) Barrier reef, south-east of Huahine Island, French Polynesia, photograph by B. Martin-Garin. (c) Mataiva Atoll, northwest of the Tuamotu Archipelago, French Polynesia—satellite view from Google Earth. The lagoon, subdivided in a number of pounds, is of reticulated type. (d) Aerial view of Takapoto Atoll, north-west of Tuamotu, French Polynesia, showing the successive morphological zones from the open sea inwards: reef-flat zone, sandy shoreline, gravel ridges, emergent islets (motu), lagoon—photograph courtesy of Samuel

Etienne. (e) Motu One, a submerged reef bank, located east of Eiao and Hatutu Islands, north of the Marquesas Archipelago, French Polynesia—satellite view from Google Earth—the white arrows delineate the reef bank. (f) Makatea, a high carbonate island, French Polynesia; in the foreground, exposed reef-flat zone of late Holocene age—younger than 5000 years BP—and Last Interglacial—about 125,000 years BP—reef unit, respectively, at elevations of 0.50 and 6 m above present mean sea level; in the background, carbonate cliffs made up of reef limestones of early Miocene age, the top of which culminates at about 70 m high—photograph by L. Montaggioni

the lagoon and the open sea. The sizes of so-called oceanic atolls vary between a few kilometres to several tens of kilometres. Thereby, Rangiroa, the second largest after Kwajalein Atoll (Marshall Islands, Western Pacific) measures 80 km in length and 32 km in width, although the depth of its lagoon does not exceed 35 m. In the Maldives, on Huvadhoo Atoll, the lagoon is 90 m in maximum depth. Atolls consist of a limestone pile built upon a volcanic basement, which rises above ocean floors between 2000 m and more than 4000 m deep. The original basements were generally created from the activity of mid-ocean hotspots— for instance, as the Hawaiian, the Society, the Maldives Islands and the Tuamotu Archipelago. By morphological

analogy, low-lying, sub-circular coral islands, with an external rim and a central lagoon, are sometimes qualified as atolls, but are localised on or at the edge of continental shelves—for example, the so-called shelf atolls associated with the Belize Barrier Reef. Genetically speaking, these are platform reefs. A variant of atoll is almost-atoll, which is characterised by the presence of a residual, partially submerged volcanic basement in central, lagoonal position. Bora Bora, in the Society Islands and Aitutaki, in the southern Cook Islands, are typical almost-atoll examples. Atolls are thought to derive from a certain type of isolated carbonate platforms that have originally developed atop of a

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submerged volcanic basement. In agreement with the Darwinian theory of reef formation, such carbonate platforms have to be regarded as the intermediate stage between barrier reefs and atolls. As a barrier-bearing volcanic island or high has been totally submerged by thermal subsidence of the underlying oceanic crust, coral communities and associated calcifying organisms through their carbonate production are able to produce shoals and banks close to or at sea surface, above volcanic foundations. Based on stratigraphical and sedimentological observations from French Polynesian high carbonate islands (see Sect. 3.2.5), these reef platforms appear to have been originally flat topped, usually devoid of central, deep basins, contrary to most modern atolls displaying lagoons. In French Polynesia, where Darwin has laid down the basis for his theory, the atoll supporting volcanic basements are older than 10 million years in the diverse archipelagos (Society, Austral, Gambier, southern Tuamotu), and then 50 million years in northern Tuamotu (Ito et al. 1995; Patriat et al. 2002) and there, the overlying carbonate pile is more than 1500 thick (Talandier and Okal 1987). This means that, as previously suggested by Darwin (1842), subsidence has been initially the major geodynamic control of vertical reef accretion and morphogenesis. This has occurred throughout the Eocene to the end of the Neogene, in a context of relatively low amplitude, low frequency sea-level fluctuations. With the establishment of a regime of higher amplitude, higher frequency sea-level changes from the beginning of the Quaternary (see Sect. 3.7), long-term emergence of carbonate platforms during low sea-stands has favoured sub-aerial chemical erosion, resulting in the development of wide and deep basins in the platform internal parts from which the current atoll morphology has been inherited (Droxler and Jorry 2021). Re-flooding of residual karstified reliefs during high sea levels has resulted in a resettlement of coral buildups mostly along the outer platform margins. Since the beginning of the Quaternary, the sea-level regime becomes the major control of reef morphological evolution.

known examples are the Flower Garden Banks situated on the U.S. continental margin, northern Gulf of Mexico, between approximately -15 and -50 m depth, and the Saya de Malha Bank in the Western Indian Ocean, between -5 and -30 m depth. The Great Chagos Bank is found in the same region, submerged between -3 and -20 m, and considered as the world’s biggest submerged atoll, with a surface area of 18,000 km2. There are also many of them in the Marquesas archipelago (French Polynesia): Motu One, Clark Bank, Bank Jean Goguel, Hatu Iti, Fatu’Uku, and Motu Nao.

3.2.5

Bank Reefs

The term bank reefs (Figs. 3.7, 3.8 and 3.9e) was proposed to define generally isolated reef-related edifices of varying form (sub-circular to elongated), partially or completely submerged at depths of a few metres to tens of metres on a continental or insular shelf or on an ocean ridge (Fig. 3.9e). Generally, bank reefs are flat-topped and colonised, in the photic zone, by coral and algal communities. Bank reefs are analogues of submerged atolls or isolated platform reefs. Some would fit into the Darwinian reef evolutionary scheme and would constitute one of the end members. There are several submerged atolls or platform reefs. The most well-

High Carbonate Islands

On uplifted oceanic seafloors (Figs. 3.9f and 3.10), the last developmental stage of an atoll, a bank reef or a carbonate platform corresponds to an emergent pile known as a high carbonate island. In the Indo-Pacific region, the general morphology of these islands is similar to that of modern atolls, with an elevated external rim relative to a central depression. The top parts culminate at altitudes ranging from a few metres to more than +100 m. In the north-western part of the Tuamotu archipelago (French Polynesia), there appears a series of islands—Rangiroa, Tikehau, Kaukura, Niau, Anaa—that possess remnants of ancient limestone reliefs (Miocene and late Quaternary) referred to as feo by the Polynesians and attaining elevations of +1 to +12 m. The most elevated is Makatea Island, at about +110 m (Figs. 3.9f and 3.10). Their ring-shaped architecture is due to a differential dissolution of carbonate surfaces (karstification), with a more prominent effect on the central than the marginal parts. Karstification has been facilitated by relative variations in sea level, controlled by successive periods of sea level drops during the Quaternary as well as uplift movements (Montaggioni 1985).

3.3 3.2.4

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Geographical Distribution

The spatial distribution of modern coral reefs is governed by various environmental, ecological and geodynamic constraints.

3.3.1

Ecological Control

The growth of most tropical corals requires strict environmental conditions (Fig. 3.11): warm and clear waters, shallow, oligotrophic (nutrient poor) and normal salinity (33–36). In regions where these conditions are not found, coral communities may still develop and survive, but without the capacity to construct substantial reliefs; they are known as

3.3 Geographical Distribution

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Fig. 3.10 Bathymetry and structure of the sea floor between the eastern areas of the Society Archipelago—composed of volcanic Moorea, Tahiti and Mehetia Islands—and the north-west Tuamotu Islands, French Polynesia. The volcanic load due to these three islands is considered to have flexed the underlying oceanic lithosphere resulting in an adjacent moat and a compensatory peripheral arc (or bulge) at up to 250 km from the load. Makatea Island would be just located above the main axis of the arch and as a consequence has experienced the highest uplift—>100 m according to the present-day elevation—whilst the

surrounding, north-west Tuamotu atolls, including Rangiroa, that lie on the flanks of the bulge, have experienced smaller uplift—