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THE BIOLOGY AND ECOLOGY OF HAWAIIAN BLACK CORALS (CNIDARIA: ANTHOZOA: HEXACORALLIA: ANTIPATHARIA) A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAWAI‘I IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN OCEANOGRAPHY (MARINE BIOLOGY) DECEMBER 2011 By Daniel Wagner Dissertation Committee: Robert J. Toonen, Chairperson Jeffrey C. Drazen Mark A. Merrifield Christopher D. Kelley Leslie E. Watling We certify that we have read this dissertation and that, in our opinion, it is satisfactory in scope and quality as a dissertation for the degree of Doctor of Philosophy in Oceanography (Marine Biology). DISSERTATION COMMITTEE Chairperson ii iii Copyright © 2011 by Daniel Wagner iv ACKNOWLEDGEMENTS First and foremost, I would like to express my profound gratitude to my faculty advisor Rob Toonen, for giving me the opportunity to pursue my graduate education in Hawaiʻi, and for always believing in me. It is only through his continuous guidance and support that I have been able to complete this work. I would also like to thank my committee members Chris Kelley, Jeff Drazen, Mark Merrifield and Les Watling for their time and effort in providing valuable feedback on my research. Special thanks to Dennis Opresko for sparking my interest in black corals, encouraging my research, and providing invaluable feedback along the way. I am further indebted to Tony Montgomery, whose pursuit to study black corals in Hawaiʻi has been inspirational, and provided a wealth of baseline information from which my research undoubtedly benefited. Rhian Waller provided constant encouragement, guidance, and feedback, for which I am especially thankful. Ruth Gates, Xavier Pochon and Leslie Irwin generously offered their laboratory resources, time and expertise to contribute to the study of Symbiodinium within black corals. I also thank Mercer Brugler and Scott France for all their time and efforts in providing molecular sequence data and valuable contributions to the taxonomic study of numerous black coral species. Joshua DeMello provided invaluable logistical and administrative support to this work. Help with sample collections was provided by the captain and crew of R/V Kaimikai-o-Kanaloa and R/V Hi‘ialakai, and by Terry Kerby, Max Cremer, Tony Montgomery, Jason Leonard, Paul Murakawa, Brett Schuhmacher, Ken Longenecker, v Linda Marsh, Joe Heacock, Scott Reed, Peter Ricciardi, Chris Kelley, Yannis Papastamatiou, Randy Kosaki, Kelly Gleason, Greg McFall, Rich Pyle, Kyle Ryan, Ray Boland, John Rooney, Frank Parrish, Cori Kane, Joey DiBattista, Sam Kahng, Jeff Eble, Greg Concepcion, Zach Caldwell, Kydd Pollock, Robin Lee, Jill Quaintance, Kent Bachman, Dave Pence, Kevin Flanagan, Derek Smith, Keoki Stender, Brian Hauk, Kaylyn McCoy, Rhian Waller, Colleen Moriarty, Elizabeth Bates, Brian Bowen, Michelle Gaither, Tonatiuh Trejo, Matt Iacchei and Matt Craig. I thank the staff of the National Museum of Natural History, Smithsonian Institution, for providing help in accessing material housed in their invertebrate zoology collections, and in particular to Stephen Cairns, Cheryl Bright, Geoff Keel and Bill Moser for their hospitality and support. Special thanks to Holly Bolick for facilitating work with the collections housed at the at Bernice P. Bishop Museum. Dan Luck provided precious assistance with performing a thorough review of the literature, for which I am particularly grateful. Special thanks to Marzia Bo, Tina Molodtsova, Elda Gaino, Karen Miller and Jim Maragos for supplying important information. Help with the analyses using scanning electron microscopy was provided by Tina Carvalho, Marylin Dunlap and Scott Whittacker. Rhian Waller, Chris Kelley, Miyoko Bellinger, Ryan Macleod and Elizabeth Bates provided assistance with histological preparations. Help with molecular laboratory work was provided by Rob Toonen, Jinchen Guo, Roxanne Havernkort and Michelle Gaither. Thanks to Rob Toonen, Brian Bowen, Ruth Gates, Michael Rappe, Rhian Waller, Tina Carvalho, Les Watling, Vivek Nerurkar vi and Rick Grigg for providing space in their laboratories. I am further indebted to the entire staff of the Hawaiʻi Undersea Research Laboratory (HURL), and in particular to Chris Kelley and Deetsie Chave for help with surveying their archived video/photo records. Financial support for this research was provided by the National Oceanic and Atmospheric Administration (NOAA) Coastal Ocean Program (NA07NOS4780189 to the State of Hawai‘i Department of Land and Natural Resources [DLNR]), the NOAA Coral Reef Conservation Program (NA05OAR4301108 to HURL), the NOAA Fisheries Disaster Relief Program (NA03NMF4520452 to the State of Hawai‘i/DLNR), the Western Pacific Regional Fishery Management Council (NA09NMF4410038 and NA07NMF4410114 to the University of Hawai‘i through NOAA’s Coral Reef Conservation Grant Program), the National Science Foundation (OCE-0623678 to RJT), and the National Marine Sanctuary Program (NWHICRER MOA 2005-008/6882). Submersible support was provided by HURL. Finally, I would like to thank the Hawaiʻi Institute of Marine Biology (HIMB), and in particular Jo-Ann Leong, Malia Rivera and Mark Heckman, for providing me with a graduate assistantship to support my studies. vii ABSTRACT Antipatharians, commonly known as black corals, are treasured by many cultures for medicinal purposes and to produce jewelry. Despite their economic and cultural importance, very little is known about the basic biology and ecology of black corals, because most species inhabit deeper-water environments (> 50 m) which are logistically challenging to study. The objectives of this dissertation were to (1) comprehensively review the literature on the biology and ecology of black corals worldwide, (2) provide a taxonomic guide to the shallow-water (<200 m) antipatharian fauna from the Hawaiian Archipelago, and (3) examine sexual reproductive processes within Antipathes griggi, the dominant species targeted by the Hawaiian black coral fishery. The literature review reveals that despite encompassing close to 240 species that are found in diverse environments, there are a number of generalities in the biology and ecology of black corals. Most antipatharian species are found in tropical and subtropical regions below depths of 50 m, on areas with hard substrates, low-light and strong currents. Antipatharians are generally slow-growing and long-lived organisms with longevities ranging from decades to millennia. With the exception of a few predators, antipatharians appear to be little impacted by predation. Like other corals, antipatharians can be habitat engineers of importance to a myriad of associated fish and invertebrates, several of which are adapted to live exclusively on black corals. A taxonomic guide to the shallow-water (<200 m) antipatharian fauna of the Hawaiian Archipelago was created by examining all available museum specimens from viii Hawaiian waters, as well as type material from species collected outside of Hawaiʻi. Based on these examinations eight species are identified from Hawaiʻi including (1) Antipathes griggi Opresko, 2009, (2) Antipathes grandis Verrill, 1928, (3) Stichopathes echinulata Brook, 1889, (4) an undescribed Stichopathes sp., (5) Cirrhipathes cf. anguina Dana, 1846, (6) Aphanipathes verticillata Brook, 1889, (7) Acanthopathes undulata (Van Pesch, 1914), and (8) Myriopathes cf. ulex (Ellis & Solander, 1786). The sexual reproduction of Antipathes griggi was investigates using histological techniques. The results indicate that A. griggi is likely gonochoric with a 1:1 sex-ratio, and spawns continuously between June and December when temperatures are highest. Although, A. griggi can be found to depths of 100 m, it is rare below the 75 m depth limit at which commercial harvest occurs in Hawai‘i. Thus, the supposed depth refuge from harvest does not really exist, thereby calling into question population models used for the management of the Hawaiian black coral fishery. ix TABLE OF CONTENTS ABSTRACT ................................................................................................................... viii TABLE OF CONTENTS ................................................................................................ x LIST OF TABLES ......................................................................................................... xii LIST OF FIGURES ...................................................................................................... xiii CHAPTER 1. INTRODUCTION .................................................................................. 1 CHAPTER 2. LITERATURE REVIEW ...................................................................... 6 Introduction ..................................................................................................................... 6 Materials and methods .................................................................................................... 8 General morphology ....................................................................................................... 9 Biogeography ................................................................................................................ 11 Habitat requirements ..................................................................................................... 14 Population densities ...................................................................................................... 16 Feeding and nutrition ...................................................................................................
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