Staghorn Corals of the World: A Revision of the Genus Acropora

STAGHORN CORALS OF THE WORLD

STAGHORN CORALS OF THE WORLD

A revision of the coral genus Acropora

(Scleractinia; Astrocoeniina; Acroporidae) worldwide,

with emphasis on morphology, phylogeny and

biogeography

Carden C. Wallace

Museum of Tropical Queensland Australia

National Library of Australia Cataloguing-in-Publication

Wallace, Carden C.

Staghorn corals of the world: a revision of the coral genus Acropora.

Bibliography.

Includes index

ISBN 0 613 06391 9.

      1. Acropora. 1. CSIRO

593.6

© CSIRO 1999

(150 Oxford Street)

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Cover photo:      Ed Lovell

Endpapers:         Emre Turak

Printed and bound in Australia

DEDICATED

TO THE MEMORY OF

ERNEST HORAN,

THE CHIEF INVESTIGATOR.

Frontispiece Acropora colonies on the top of a back-reef patch reef at Ribbon Reef Number 3, Great Barrier Reef of Australia, indicate some of the variety and compatibility of species within this genus. From the top can be seen: A. hyacinthus, A. intennedia, A. florida, A. cytherea (bottom left) and A. muricata. (photo Michael Aw, courtesy Ocean’n Environment)

FOREWORD

If ever a creature’s name evokes images of tropical seas and coral reefs, it is staghorn cora], the common name for the coral genus Acropora. Divers and those of us lucky enough to have developed a naturalist’s interest in coral reefs, to have studied them at school or university, or to have conducted research on aspects of reef life, will be aware that there are many different types of Acropora – not just stag horns, but plates, mounds, tables and bushes. The many species within each of these growth forms can be a real headache for anyone who attempts to make a list of the species on just a small section of a single reef. A headache for most of us, perhaps, these 114 species described here, but for Carden Wallace, a source of inspiration, a lifetime’s work, and – in creating this monograph – a labour of love that rewards all of us. Among the luckiest of all are those of us who have been treated by Carden to a showing of the Worldwide Acropora Collection at the Museum of Tropical Queensland, Townsville. As museum specimens, as well as living colonies out on the reef, they are truly beautiful corals and they deserve the beautiful book you hold in your hand.

However, Acropora corals are much more than beautiful and diverse ornaments that adorn coral reefs. In most places where coral reefs occur, species of Acropora contribute by far the greatest mass and percentage bottom cover to their living habitats and their underlying foundations. Their complex morphologies create habitats for myriad forms of other reef life. Robust mounds and encrusting forms of Acropora can withstand the fiercest of storm waves, while Acropora plates and bushes may from time to time succumb, to be tossed up to help form and sustain rubbly or sandy coral islands. They feed the delicately nipping coral fishes without lasting injury, but they die en-masse under depredations of coral-eating snails and starfish, they are killed by microbial diseases, and they bleach white and die if the water becomes too hot, cold, salty or fresh. In the Caribbean, their very existence seems threatened; in the Indo-Pacific, their capacity to bounce back is one of their most spectacular attributes. In this book, their success as a group is shown to have built on the evolution of a variety of life history strategies and morphologies. Their global distribution patterns and their morphological affinities provide new insights into their likely evolution and dispersal.

This book is an important and timely contribution to the immense task of documentation and understanding of one of the Earth’s most beautiful, precious and vulnerable ecosystems – the coral reef. At this time when there are serious concerns about human impacts on coral reefs and marine biodiversity in general, the distributional and taxonomic database that underlies this work represents an important benchmark for the coral reefs of the future.

The international coral reef community will thus greatly benefit from this work, and, indirectly, so will those who seek to manage coral reefs and develop policies and practices for their protection and sustainable use.

Dr Terry Done

President, International Society for Reef Studies

May 1999

ABSTRACT

The reef-building coral genus Acropora worldwide is reviewed and revised on the basis of skeletal morphology and field characteristics, using new data from a specimen datahase of 15500 specimens from around 800 sites. All type collections in museums throughout the world are reviewed, and lectotypes are designated from syntype series in order to stabilise nomenclature. The question of the identity of the type species of the genus, Acropora muricata (Linnaeus, 1758) is addressed, and a neotype for this species is designated. The fossil species and their distributions through time and space are briefly reviewed. Issues of species boundaries, reticulate phylogenies, hybridisation and genetic delimitation of species are discussed from the literature and some predictions about future changes to taxonomic treatment of the genus are made. The literature on life histories, anatomy, biology and ecology is reviewed. Using the specimen database and the literature, distribution ranges of species are delimited and biogeographic patterns are recognised. Phylogenetic analyses, based on skeletal characters, are presented, and the implications for groupings of species and relationships of species groups are outlined. The resulting revised classification of Acropora is used for the systematic discussion of species. Transformation of character stales is followed through the proposed phylogeny, leading to an hypothesis about the pattern of evolution of characters and character combinations in Acropora. The genus is distinguished by the characters of corallite dimorphism and axial budding and is proposed to be most closely related to Astreopora amongst the extant Acroporidae. The division into two subgenera A. (Acropora) and A. (lsopora) is maintained. The subgenus A. (Acropora) is seen to have evolved from simple, sturdy species whose axial corallites provide the bulk of the branch and whose coenosteum is uniform and dense, into more complex, slender-branched species with a greater relative number of axial corallites but less bulk. During this process, the radial corallites became less like the axial corallites and a number of lineages with unique radial corallite shapes developed. Coenosteal structure of the axial and radial corallites is seen to have become uncoupled during this process, leading to some lines in which the coenosteum is highly differentiated between axial and radial corallites, but the two become equivalent again in the most derived clades. The character of determinate versus indeterminate colony growth mode does not influence the phylogeny. When the cladograms of species relationships are examined in terms of the biogeographic ranges of species, coupled with the fossil records of Acropora, an hypothesis of origination within the African-European region during or before the Paleocene is favoured. This event is seen to be followed by an expansion to the east and west. Closure of the Mediterranean in the early Miocene probably began the process of isolation of the Atlantic fauna. The genus is seen to have diversified in the central Indo-Pacific during the Neogene. Peripheral species, found in the western Indian Ocean and the central Pacific, and the rarity of several species in the Indo-Australian Arc, are taken to indicate some isolation and expansion of the central Indo-Pacific marine region during late Neogene to Holocene times. The youngest clades in the subgenus A. (Acropora) are dominated by species with ranges in the Indo-Australian Arc or western Pacific. In conclusion, the hypothesis of a gradual transfer of the centre of greatest diversity of the genus from the African-European region to the central Indo-Pacific, with various vicariant events mediating, is favoured.

ACKNOWLEDGEMENTS

It is a pleasure to acknowledge the role played by numerous friends and colleagues in the development of this monograph. Those throughout the world who collected Acropora, either for mutual research benefit or solely for this project, are listed in Appendix Table 1. To them I am indebted for the specimens that made a worldwide revision possible and for the generous way that they shared the data associated with the specimens. Many also allowed me to use their field photographs. Charles and Ann Sheppard, Emre Turak, Lyndon Devantier, Martha Collard, Michael Aw, Neville Coleman, Geoff Kelly, Russell Kelley, Ed Lovell, Peter Harrison, Doug Fenner, Arjan Rajasuriya, Niphon Phongsuwan, Mark Erdmann, Takashi Hayashibara, Chang-Feng Dai, Mary Gleason, Hans Ditlev, Andrew Baker and Terri Seaman provided particular feedback and photographs from the field that were invaluable.

My taxonomic colleagues Brian Rosen, Steve Cairns and Bert Hoeksema have kindly reviewed the text and given me the benefit of their experience and their access to early literature and specimens. Their advice and encouragement and their willingness to follow up every request helped me through some tough times.

The review of type material was done with the cooperation and assistance of curators and collection managers and 1 am grateful to Mireille Guillaume (MNHN), Sheila Halsey (NHM), Steve Cairns (USNM), R.C. Pangulayan (UP), Elizabeth Hoenson (SAM), Yuri Latypov (IMBR), Dieter and Karin Kühlmann and Peter Bartsch (MNB), Helmut Sattmann (MNW), D.A. Locohen (MMI) and Penny Behrents (AM). Photographs and details of types were also provided by Monica Payne who researched type material in London, Emre Turak who researched Paris material, Chiara Bertelli, Nancy Budd, and Jason McKenzie.

Heather Winsor and colleagues at the James Cook University Advanced Analytical Centre provided the electron microscopy expertise. Black and white photography was done mostly by Jeff Wright and Bruce Cowell of Queensland Museum, but also by Zollie Florian and Andrew Elliott. Reef Colour and Aussie Photographics of Townsville provided me with rapid and helpful photographic work. Mareya Dashorst and Marion Gaemers pasted up the plates, with Denise Seabright and Barbara Done assisting me with the preliminary paste-ups. Mandy Young and James True prepared the maps while Barbara Done and James True managed the database and Barbara Done managed the collection. Jackie Wolstenholme, initially an assistant, became a colleague who helped with decisions.

Students working within the project included Michelle Lee, Kevin Whysall, Cathie Page and Ruby Moothien Pillay, all from James Cook University Townsville, and I acknowledge the Queensland Museum Studentship Scheme and the CRC Reef Studentship for support of these students.

Memories and results of field trips in the company of Russ Babcock, Gordon Bull, Allen Chen, Chang-Feng Dai, Peter Harrison, Vicki Harriott, Jamie Oliver, Takeshi Hayashibara, Pascale Juanot, Judy Lang, Ed Lovell, Mack Omori, Len :McKenzie, John Pandolfi, Niphon Phongsuwan, Keryea Soong, John (Charlie) Veron, Bette Willis, Jackie Wolstenholme, Mandy Young, Anmarie and Tom Tomascik, Bert Hoeksema, Andreas Kunzman, Joe Connell, Terry Hughes, Michael Aw and numerous other colleagues and friends, not to mention members of dive expeditions who became accidental participants in my research, and often good friends form the background to this book.

To my late mentors Dr John West Wells, Dr Jan Verwey and Professor Dorothy Hill, giants of Science who accomplished so much, I owe gratitude for the generosity with which they shared their knowledge and support. Other valuable mentors have been Drs Dieter Kühlmann, Michel Pichon, Maya Borel-Best and Georg Scheer. Charlie Veron at the Australian Institute of Marine Science made it possible for me to revise and broaden my first revision of Great Barrier Reef Acropara soon after it was done.

The Australian Research Council (ARC) and its predecessors, ARGG and AMSTAC and the Crown of Thorns Grants Committee provided the funding that has allowed me to pursue a number of research programs with the eventual goal of an Acropora monograph, and I thank the ARC Committee for their patience in awaiting its rather slow delivery. The Indonesian Institute of Sciences (LIPI) and its Director and staff, especially Dr Suharsono my counterpart in Indonesia are thanked for their scientific sponsorship of the research, as are the Academica Sinica of Taiwan and the Tokyo University of Fisheries.

Others who donated ship and diving facilities to the project, including Max and Cecily Benjamen of Walindi Plantation, Alan Raabe of MV.FeBrina (PNG), Michael Cortenbach of Bali Hai Cruises and Michael and Alison Aw of Ocean n Environment, Aka Jima Marine Lab, Japan, Academica Sinica of Taiwan and Phuket Marine Station, Thailand. Many others paved the way for me to work with the least amount of difficulty, but especially Dr Hanni Batuna, Otti Lalamentik, Andreas Kunzmann, John Rewald, Phil Munday and Nel and Rick Braley.

My friend Penny Young gave a month of her time to help me finish the job. The devotion to this project by my fellow workers at Museum of Tropical Queensland has always exceeded the call of duty, and I simply could not have completed this work without Jackie Wolstenholme, Barbara Done, Mandy Young, Denise Seabright, Marion Gaemers, James True and Monica Payne who added their expertise and support in so many substantial and different ways including collection and database management, GIS and other computing, figure layout and editing, and of Peter Arnold who ran a museum for eight months so that I could finish the work. Bert Furse, Jeff Bolger and Cheryl Lloyd cleaned 15000 plus coral specimens as an adjunct to their duties as museum attendants; Aileen Rinaldo and Bernice Gordon held the fort. Many of the Museum of Tropical Queensland’s volunteers helped also, but in particular Dominique Hall, Margaret Pickersgill, Veronica Corstorphine, May McCool, Derrick Monz and Betty O’Connor contributed their considerable expertise.

Bronwen Scott’s involvement in the phylogenetic analysis was invaluable, as was Barry Goldman’s in the analysis of the biogeographic data and that of John Pandolfi in the early phases of both of these projects.

It has been a pleasure to work with Kevin Jeans and staff of CSIRO Publishing and to have the expertise of Andrea Jordon in editing the keys as well as Scott Howard, Melissa Gibson and Sylvana Scannapiego of Publishing Solutions for managing the design and production of the book. The final job of preparing the index was done by May McCool

Last and most importantly I thank Andrew who minded the kids and the kids themselves, Denis and Michael, who grew up with Acropora and helped with everything from underwater videos to photographic paste-ups and cups of coffee.

TABLE OF CONTENTS

ABSTRACT

ACKNOWLEDGEMENTS

INTRODUCTION

REVIEW OF LITERATURE

Nomenclatural history of the genus

Type species

Trends in the taxonomy of Acropora

Classification

Sub-generic classification

Super-generic classification

SUMMARY OF TYPE MATERIAL

Background

Designation of lectotypes

France

Germany

America

England

Philippines

Australia

Africa

Russia

Austria

Italy

India

FOSSIL RECORD

Distribution of fossil assemblages

Fossil species

ANATOMY, PHYSIOLOGY AND BIOLOGY

Soft structures

Colouration

Skeleton and growth

Gastrovascular system

Gonads

General

Female gonads and oocytes

Testes and spermatozoa

Sexual reproduction

General

Fertilisation and development

Reproductive effort and fecundity

Hybridisation

Asexual reproduction

Ecology

General

Zonation patterns

Life histories

Recruitment

Maturation and senescence

Mortality

Associations and interactions

Diseases

GENETICS AND MOLECULAR BIOLOGY

General

Chromosome number

Genetic characters

Evolutionary signature of hybridisation

SKELETAL MORPHOLOGY

General

Terminology

Recognition of juvenile Acropora colonies

Colony form

General

Nomenclature of colony forms

Corallites

Axial corallites

Radial corallites

Coenosteum

Variations in morphology

METHODS USED FOR REVISION AND ANALYSES

The Worldwide Acropora Database

Locations

Sampling and database protocol

Mapping of distributions for species descriptions

Format of synonymies

Citation of localities for material examined

Characters used in descriptions of species

Biogeographic analyses

Phylogenetic analyses

Development of a LucID interactive key

Photo library of type specimens

REVISION OF THE BIOGEOGRAPHY OF ACROPORA

Background

Groupings of records

Species composition of areas, regions and super regions

Similarities between areas and regions

Types of distributions exhibited by species

Distribution characteristics of the fauna of areas and regions

REVISION OF THE PHYLOGENY AND CLASSIFICATION OF ACROPORA

Background

Methodology

Taxa

Characters

Programs

Phylogeny of the family Acroporidae

Phylogeny of the genus Acropora

Cladograms

Clades

Species groupings in the subgenus Acropora

General

Monophyletic groups

Paraphyletic groups

Misplaced species

Patterns of character transformation in Acropora phylogeny

General

Colony form and branches

Skeletal density

Coenosteal characteristics

Radial corallites

Axial corallites

Summary of transformations and relationships of species groups

SYNTHESIS OF BIOGEOGRAPHIC, FOSSIL AND PHYLOGENETIC DATA

Evidence for the origination and evolution of Acropora

General

Cladograms in terms of habitat

Cladograms in terms of fossil history

Cladograms in terms of the biogeographic patterns

Chronology of the origination of clades

Hypothesis

Colour Plates

SYSTEMATIC ARRANGEMENT OF SPECIES

FAMILY ACROPORIDAE VERRILL, 1902

GENUS ACROPORA OKEN, 1815

TYPE SPECIES MILLEPORA MURICATA LINNEAUS, 1758

SUBGENUS ACROPORA OKEN, 1815

The Acropora rudis group

Acropora (Acropora) rudis (Rehberg, 1892)

Acropora (Acropora) variolosa (Klunzinger, 1879)

Acropora (Acropora) austera (Dana, 1846)

Acropora (Acropora) hemprichii (Ehrenberg, 1834)

The Acropora humilis group

Acropora (Acropora) humilis (Dana, 1846)

Acropora (Acropora) globiceps (Dana, 1846)

Acropora (Acropora) gemmifera (Brook, 1892)

Acropora (Acropora) monticulosa (Brüggemann, 1879)

Acropora (Acropora) samoensis (Brook, 1891)

Acropora (Acropora) digitifera (Dana, 1846)

Acropora (Acropora) multiacuta Nemenzo, 1967

Acropora (Acropora) retusa (Dana, 1846)

The Acropora nasuta group

Acropora (Acropora) nasuta (Dana, 1846)

Acropora (Acropora) cerealis (Dana, 1846)

Acropora (Acropora) valida (Dana, 1846)

Acropora (Acropora) arabensis Hodgson & Carpenter, 1995

Acropora (Acropora) secale (Studer, 1878)

Acropora (Acropora) lutkeni Crossland, 1952

Acropora (Acropora) kimbeensis sp. nov. 146

The Acropora divaricata group

Acropora (Acropora) divaricata (Dana, 1846)

Acropora (Acropora) solitaryensis Veron & Wallace, 1984

Acropora (Acropora) kosurini Wallace, 1994

Acropora (Acropora) hoeksemai Wallace, 1997

Acropora (Acropora) clathrata (Brook, 1891) 158

The Acropora lovelli group

Acropora (Acropora) lovelli Veron & Wallace, 1984

Acropora (Acropora) bushyensis Veron & Wallace, 1984

Acropora (Acropora) glauca (Brook, 1893)

The Acropora verweyi group

Acropora (Acropora) verweyi Veron & Wallace, 1984

The Acropora cervicornis group

Acropora (Acropora) cervicornis (Lamarck, 1816)

Acropora (Acropora) palmata (Lamarck, 1816)

Acropora (Acropora) prolifera (Lamarck, 1816)

The Acropora muricata group

Acropora (Acropora) muricata (Linneaus, 1758)

Acropora (Acropora) grandis (Brook, 1892)

Acropora (Acropora) acwninata (Verrill, 1864)

Acropora (Acropora) valenciennesi (Edwards & Haime, 1860)

Acropora (Acropora) pharaonis (Edwards & Haime, 1860)

The Acropora robusta group

Acropora (Acropora) robusta (Dana, 1846)

Acropora (Acropora) abrotanoides (Lamarck, 1816)

Acropora (Acropora) palrmerae Wells, 195’1

Acropora (Acropora) intermedia (Brook, 1891)

Acropora (Acropora) polystoma (Brook, 1891)

Acropora (Acropora) downingi sp. nov.

Acropora (Acropora) listeri (Brook, 1893)

Acropora (Acropora) sukarnoi Wallace, 1997

The Acropora togianensis group

Acropora (Acropora) togianensis Wallace, 1997

The Acropora selago group

Acropora (Acropora) selago (Studer, 1878)

Acropora (Acropora) tenuis (Dana, 1846)

Acropora (Acropora) eurystorna (Klunzinger, 1879)

Acropora (Acropora) striata (Verrill, 1866)

Acropora (Acropora) donei Veron & Wallace, 1984

Acropora (Acropora) yongei Veron & Wallace, 1984

Acropora (Acropora) loisetleae Wallace, 1994

Acropora (Acropora) dendrurn (Bassett-Smith, 1890)

The Acropora aspera group

Acropora (Acropora) aspera (Dana, 1846)

Acropora (Acropora) pulchra (Brook, 1891)

Acropora (Acropora) millepora (Ehrenberg, 1834)

Acropora (Acropora) spathulata (Brook, 1891)

Acropora (Acropora) spicifera (Dana, 1846)

Acropora (Acropora) papillare Latypov, 1992

Acropora (Acropora) roseni sp. nov.

The Acropora florida group

Acropora (Acropora) florida (Dana, 1846)

Acropora (Acropora) sarrnenlosa (Brook, 1892)

The Acropora hyacinthus group

Acropora (Acropora) hyacinthus (Dana, 1846)

Acropora (Acropora) tanegashimensis Veron, 1990

Acropora (Acropora) anthocercis (Brook, 1893)

Acropora (Acropora) cytherea (Dana, 1846)

Acropora (Acropora) microclados (Ehrenberg, 1834)

Acropora (Acropora) paniculata Verrill, 1902

Acropora (Acropora) indonesia Wallace, 1997

The Acropora latistella group

Acropora (Acropora) latistella (Brook, 1892)

Acropora (Acropora) subulata (Dana, 1846)

Acropora (Acropora) nana (Studer, 1878)

Acropora (Acropora) aculeus (Dana, 1846)

The Acropora horrida group

Acropora (Acropora) horrida (Dana, 1846)

Acropora (Acropora) vaughani Wells, 1954

Acropora (Acropora) tortuosa (Dana, 1846)

Acropora (Acropora) abrolhosensis Veron, 1985

Acropora (Acropora) microphthalma (Verrill, 1869)

Acropora (Acropora) kirstyae Veron & Wallace, 1984

Acropora (Acropora) derawanensis Wallace, 1997

Acropora (Acropora) halmaherae Wallace &Wolstenholme, 1998

The Acropora (Acropora) plumosa group

Acropora (Acropora) plumosa Wallace & Wolstenholme, 1998

The Acropora elegans group

Acropora (Acropora) elegans (Edwards & Haime, 1860)

Acropora (Acropora) pichoni sp. nov.

Acropora (Acropora) tenella (Brook, 1892)

Acropora (Acropora) walindii sp. nov.

Acropora (Acropora) canlenae Wells, 1985

Acropora (Acropora) torihalimeda Wallace, 1994

Acropora (Acropora) russelli Wallace, 1994

The Acropora loripes group

Acropora (Acropora) loripes (Brook, 1892)

Acropora (Acropora) squarrosa (Eherenberg, 1834)

Acropora (Acropora) chesterfieldensis Veron & Wallace, 1984

Acropora (Acropora) willisae Veron & Wallace, 1984

Acropora (Acropora) lokani Wallace, 1994

Acropora (Acropora) granulosa (Edwards & Haime, 1860)

Acropora (Acropora) speciosa (Quelch, 1886)

Acropora (Acropora) suharsonoi Wallace, 1994

Acropora (Acropora) caroliniana Nemenzo, 1976

Acropora (Acropora) desalwii Wallace, 1994

Acropora (Acropora) jacquelineae Wallace, 1994

Acropora (Acropora) simplex Wallace & Wolstenholme, 1998

The Acropora echinata group

Acropora (Acropora) echinata (Dana, 1846)

Acropora (Acropora) batunai Wallace, 1997

Acropora (Acropora) subglabra (Brook, 1891)

Acropora (Acropora) carduus (Dana, 1846)

Acropora (Acropora) awi Wallace & Wolstenholme, 1998

Acropora (Acropora) elseyi (Brook, 1892)

Acropora (Acropora) longicyathus (Edwards & Haime, 1860)

Acropora (Acropora) turaki Wallace, 1994

SUBGENUS ISOPORA STUDER, 1878

Acropora (Isopora) palifera (Lamarck, 1816)

Acropora (Isopora) cuneata (Dana, 1846)

Acropora (Isopora) crateriformis (Gardiner, 1898)

Acropora (Isopora) brueggemanni (Brook, 1893)

INSERTAE SEDIS ACROPORA SQUAMATA LATYPOV, 1992

REFERENCES

APPENDIX

GLOSSARY

ABBREVIATIONS

INDEX

SPECIES INDEX

Many of the terms for Acropora structures were coined by Dana (1846). This plate from his Atlas from the US Exploring Expedition shows most of the range of radial corallite shapes encountered in Acropora species (courtesy D. Kühhnann, P. Bartsch).

INTRODUCTION

The taxonomy of scleractinian corals, and particularly of the large and important genus Acropora, might be said to have reached a watershed. Species boundaries, traditionally based on morphology, are being challenged by possible alternatives based on breeding and genetics. Events that shaped the world’s oceans and habitats have also been involved in disrupting and realigning species ranges, as suggested by misalignments of species boundaries determined by different methods. A broadening interest in comparing the reefs of different geographic regions requires that estimates of distribution ranges of species be available, to allow for cross-comparisons of species composition and biodiversity. Added to this is a demand, as never before, for tools for identifying live animals in the field, for the purpose of monitoring and managing coral reefs. When proposing new solutions to the old problem of how to define and delimit species and their relationships to each other, workers need to assess their findings against a clearly expressed traditional scheme which applies, as far as possible, to all species from all locations. It seems that at a time when we are on the brink of a possible new scheme of taxonomy, the demand for traditional morphological recognition of species and a morphologically based classificatory system is stronger than ever before.

Acropora is by far the largest extant genus of reef-building corals, and among the most widespread. Few studies of any aspect of reef coral biology, ecology and distribution can avoid the necessity to refer to this genus. As the first full monograph of the genus since that of Brook (1893), this revision focuses on the geographic ranges and lineages of morphologically recognisable species. It brings together new species described in short publications since the major revision of Eastern Australian species (Wallace, 1978; Veron & Wallace, 1984) and new information about the biology and ecology of species of Acropora. In the process, a collection of 15500 specimens from around 800 sites throughout the world is documented. The data on morphology and distribution provided by this collection allow hypotheses to be developed about the phylogenetic relationships of species and transformation of characters through time, as well as a revision of the species-level biogeography of the genus. The status and availability of type specimens in museums throughout the world are also documented. It is the intention of this revision to provide coverage of all the old reference material as well as new findings. This monograph may bring to an end the period of categorisation of the genus solely on morphology and its variability, a process officially begun by Linnaeus and Lamarck.

REVIEW OF LITERATURE

Nomenclatural history of the genus

The name Acropora Oken, 1815 was officially validated by the International Commission of Zoological Nomenclature in 1963 (China, 1963), following a submission to the Commission by Boschma (1961). Acropora had been in general use since its reintroduction by Verrill (1901), but a formal validation was necessary because Oken’s 1815 paper was regarded as a work rejected for nomenclatural purposes by the Commission. There was also some confusion and unwillingness to accept this name instead of the previously widely used Madrepora Linnaeus, e.g.: "It is with a feeling of regret that we are forced to abandon the use of a generic name [Madrepora] which remained unquestioned by four generations of authors during the golden days of systematic zoology (Mayor, 1924, p.vii); Mais cette modification est-elle bien nécessaire?" (Bedot, 1907 p. 244). Another name, Heteropora Ehrenberg, 1834, was used also for the genus by some nineteenth century authors until its invalid status as a junior homonym of Heteropora Blainville, 1830 (a genus of bryozoans) became known.

The origins and application of the generic name Madrepora are clearly and thoroughly outlined in Brook (1893), the only full monograph of the genus. Brook pointed out the anomaly by which that name came to be erroneously applied to the genus. Linnaeus in his Systema Naturae Edition 10 (1758) had established three generic names Tubipora, Millepora and Madrepora, but the only species of the current genus Acropora included in his long listings of species was erroneously listed as Millepora muricata. In Edition 12 (Linnaeus, 1767), he corrected this to Madrepora muricata. Lamarck (1801) restricted Madrepora to two species M. muricata and M. porites (now genus Porites). Thus Madrepora, as delimited by Lamarck (1801), contained none of the original species included in Madrepora by Linnaeus in 1758, the starting date for zoological nomenclature. Brook (1893) concluded "We must therefore regard Madrepora ss as a generic name which, like Holothuria, depends for its justification on custom rather than on priority" (p.3).

Despite the strong influence of Brook’s judgement, the issue re-surfaced, as nomenclatural issues tend to do. Vaughan (1901) recommended that Madrepora not be used for this genus and elevated the subgenus Isopora Studer, 1878. Verrill (1901) argued against this as: an objectionable name ... originally applied to a small section of the genus in which the axial corallites are indistinct or clustered. He proposed Acropora Oken, 1815 as most suitable for the genus because of its reference to the most prominent character of the genus, the central or axial corallite. He later repeated these ideas in a list (Verrill, 1902). In his submission to the International Commission, Boschma (1961) reiterated Brook’s and Verrill’s analyses of the nomenclatural situation and proposed official status for the use of Acropora Oken, 1815 for this genus, with Millepora muricata Linnaeus, 1758 as the type species. (Madrepora remains a genus in the family Oculinidae, represented by the type species M. oculata Linnaeus, 1758.)

Type species

Boschma’s intention to stabilise the nomenclature of this, the largest extant genus of reef-building corals, was laudable. However, his choice of the species Millepora muricata Linnaeus, 1758 as the type species, although unavoidable, resurrected another argument about the identity of that species. No specimen in his own collection was referred to by Linnaeus in his description of Millepora muricata, and there has always been debate about the provenance of the species. When he defined the species, Linnaeus (1758) clearly had in mind the descriptions of several authors, including Rumphius in his Herbarium Amboinense, and he defined its distribution thus: Habitat in Pelago Asiatico. This would seem to clearly eliminate all of the Atlantic species as possible candidates for the name.

Many authors, however, regarded this species as a senior synonym of one or all of the extant Atlantic Ocean species (Acropora cervicornis, A. palmata and A. prolifera). In this they were following the usage of Brook (1893), but Brook had also included some Indo-Pacific specimens in his wide-ranging description of the species. Both Verrill (1901) and Vaughan quoted by Verrill (1902) followed Brook in regarding A. muricata as a West Indian species encompassing all extant forms of Acropora from that region. After seeing the West Indian reefs for himself, however, Vaughan (1919) changed his mind about the synonymy, recognising three separate species again, but he still regarded one of them (A. cervicornis) as a junior synonym of A. muricata.

Gregory (1900) also contested Brook’s synonymy after observing the West Indian corals live. Not only was Gregory convinced that the West Indian Acropora represented three species, separate from A. muricata, but also he argued that A. muricata should be restricted to an Indo-Pacific species. His rationale (Gregory, 1900 p. 28) was as follows: "To take one of the many corals included by Linnaeus in M. muricata would be an arbitrary proceeding; but if it is to be done the name ought to be applied to an Indo-Pacific species, both since Linnaeus assigned it to that area (i.e. Pelago Asiatico) and as the best figures are those in Rumphius’ Herbarium Amboinense".

FIGURE 1 Acropora muricata (Linnaeus, 1758): Illustration from Rumphius, 1750 Herbarium Amboinense quoted by Linnaeus as one of the sources of his species (courtesy B. Hoeksema).

Wells (1936 p.99) re-opened the long quiescent issue of the provenance of Acropora muricata, commenting: "In fact, I cannot find that any author has actually restricted or confined muricata to either an Indo-Pacific or West-Indian species although several ... have implied it". In this publication, he took the further step of declaring Acropora muricata to be synonymous with A. formosa of the Indo-Pacific. Following the advice of Gregory (1900), he sourced the figure of Rumphius (1750), and made the following statement: "Rumphius’ figure and description both pertain to a species now known as Acropora formosa (Dana), I am informed by Dr J. Verwey, who is best qualified to decide questions concerning the various species of Acropora. The species muricata is therefore here restricted to that described by Rumphius in his Herbarium Amboinense, vi, 1750, p1.lxxxvi, Fig.1, an Indo-Pacific species. A. cervicornis (Lamarck) 1816 should be applied to the West Indian form usually known as A. muricata." (Wells, 1936 p.100).

Acropora cervicornis has since been used stringently as the name for the arborescent Atlantic Ocean species. Zlatarski & Estalella (1982), in a review of the corals of Cuba, declared that the type of the genus was actuelle de I’Île Amboine, Moluques. Unfortunately no Indo-Pacific worker has followed Well’s decision about A. muricata, not even Wells himself (e.g. Wells, 1954, –54a). Boschma (1956) failed to mention that there was any problem with the taxonomic resolution of the type species of the genus. Thus in 1999 we find ourselves in a situation described by a reviewer thus: The largest and most important extant genus of hermatypic Scleractinia does not have a recognisable type species (S. Cairns, pers. comm.).

It seems the time has come to rectify this situation by the designation of a neotype for Acropora muricata. The figure from Rumphius (1750) of a coral from Ambon (or from the neighbouring reefs in the Banda and Molucca Seas) in Indonesia, that is regarded as providing the most inspiration for Linnaeus’ Millepora muricata (later Madrepora muricata) (Gregory, 1900; Wells, 1954; Zlatarski & Estalella, 1982) is illustrated in Figure 1. This clearly shows a species with evenly sized and distributed tubular radial corallites (see description of this feature in Skeletal morphology below). The branches are tapering and some are curved.

In order to determine a specimen that best represents the nature and the source of Rumphius’ illustrated specimen, I have studied a suite of specimens from the island of Ambon and nearby locations in the Banda, Molucca and Sulawesi Seas, collected over several field trips in Indonesia. Among the specimens available to me, Rumphius’ figure is best matched by G49167 from the reef at Gunung Api in the Banda Islands, Banda Sea (Figure 2). This specimen is herein designated as the neotype for Millepora muricata Linnaeus, 1758.

Trends in the taxonomy of Acropora

Some 370 species (not including nomina nuda) have been described in this genus, with approximately 15 further being described from fossil material only. The early descriptions came from the founding European systematists, working with expeditionary material brought to them by adventurers and field naturalists, or sometimes collected by themselves. The Historical section of Brook’s (1893) introductory chapter, covering localities sampled and expeditions yielding new authors, nomina nuda and other issues, should be read by anyone wishing to study the work of the nineteenth century authors.

Ehrenberg (1834), working with material mostly from the Red Sea, is credited with giving the genus its current limits, as he included all species known to have an axial corallite: as Brook (1893) pointed out, some of these species had been placed elsewhere by Lamarck. The influence of this axial corallite on the mode of budding, described as centrifugal as against the centripetal method of budding in Montipora and his newly described genus Anacropora, was recognised first by Ridley (1884). The most significant 19th century authors for this genus, after Lamarck and Ehrenberg, were Dana (1846), who examined the specimens from the US Exploring Expedition and brought in 53 new species names, Edwards and Haime (1860), who created 18 new species, Klunzinger (1879; 18 new species) and Brook (1891, -92, -93). Brook catalogued the specimens in the then British Museum (Natural History) and examined types and mentioned material in the museums of Europe, bringing in a total of 91 new species names, including some for specimens in the European collections. Thus the authorship of valid names for Acropora is dominated by these early workers. Brook’s work, with its excellent photographs of types and its clear delimitation of the contemporary systematics, was a benchmark for coral taxonomy. When Brook died only months after completing his work, Haddon (1894) was moved to remark "Those who have