Coral Reefs

, Volume 31, Issue 3, pp 795–806 | Cite as

Sexual reproduction of the Hawaiian black coral Antipathes griggi (Cnidaria: Antipatharia)

  • D. Wagner
  • R. G. Waller
  • A. D. Montgomery
  • C. D. Kelley
  • R. J. Toonen


The Hawaiian black coral fishery has maintained steady catch levels for over 50 years. However, recent declines in the biomass of commercially valuable Hawaiian black corals question whether regulations need to be redefined for sustainable harvesting. Fishery management efforts are complicated by the limited information on the basic life history and reproduction of black corals. To address this knowledge gap, we used histological techniques to investigate sexual reproductive processes within Antipathes griggi, the dominant species targeted by the fishery. Our results indicate that A. griggi is likely gonochoric with a 1:1 sex ratio and has an annual reproductive cycle. Furthermore, the percentage of polyps containing gametes dropped continuously throughout the reproductive season, indicating that spawning occurs in successive events with greatest intensity between November and December. Current fishing regulations prohibit harvesting of colonies <90 cm in height in state waters, and colonies <120 cm in height in federal waters. This study indicates that ~80% meeting the state harvesting limit, and ~90% of colonies meeting the federal limit, are sexually mature. Therefore, increasing these minimum size harvesting limits would ensure that more colonies can reproduce before being exposed to fishing mortality. 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.


Anthozoa Antipathidae Coral spawning Gametogenesis Precious coral 



We thank D. Opresko for taxonomic assistance and J. DeMello for valuable help during this project. Special thanks to the captain and crew of R/V Kaimikai-o-Kanaloa and R/V Hi‘ialakai, and to L. Marsh, J. Heacock, S. Reed, J. Leonard, K. Longenecker, R. Boland, J. Eble, Y. Papastamatiou, F. Parrish, J. Rooney, K. Ryan, R. Pyle, K. Gleason, R. Kosaki, G. McFall, C. Kane, B. Hauk and S. Kahng for help with sample collections. Additional help in the laboratory was provided by T. Carvalho, M. Bellinger, R. Macleod and E. Bates. This work was funded in part by the Western Pacific Fisheries Management Council (NA07NMF4410114 to the University of Hawai‘i through NOAA’s Coral Reef Conservation Grant Program), 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 National Science Foundation (OCE-0623678 to RJT), and the National Marine Sanctuary Program (NWHICRER MOA 2005-008/6882). Submersible support was provided by HURL. This manuscript represents SOEST contribution number 8558 and HIMB contribution number 1484. The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the U.S. Fish and Wildlife Service.


  1. Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawning of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90:379–394CrossRefGoogle Scholar
  2. Babcock RC, Mundy CN, Whitehead D (1994) Sperm diffusion models and in situ confirmation of long-distance fertilization in the free-spawning asteroid Acanthaster planci. Biol Bull 186:17–28CrossRefGoogle Scholar
  3. Bo M (2008) Taxonomy and ecology of antipatharians. Ph.D. thesis, Universita Politecnica Delle Marche, p 212Google Scholar
  4. Bo M, Barucca M, Biscotti MA, Canapa A, Lapian HFN, Olmo E, Bavestrello G (2009) Description of Pseudocirrhipathes (Cnidaria: Anthozoa: Hexacorallia: Antipathidae), a new genus of whip black coral from the Indo-Pacific. Ital J Zool 76:392–402CrossRefGoogle Scholar
  5. Boland RC, Parrish FA (2005) A description of fish assemblages in the black coral beds off Lahaina, Maui, Hawai‘i. Pac Sci 59:411–420CrossRefGoogle Scholar
  6. Brook G (1889) Report on the Antipatharia. Report of the scientific results of the voyage of the H.M.S. Challenger. Zool 32:1–222Google Scholar
  7. Carroll A, Harrison P, Adjeroud M (2006) Sexual reproduction of Acropora reef corals at Moorea, French Polynesia. Coral Reefs 25:93–97CrossRefGoogle Scholar
  8. Castorena V, Metaca M (1979) El coral negro, una riqueza en peligro. Tec Pesq 139:22–27Google Scholar
  9. Cooper CF (1909) Reports of the Percy Sladen Trust Expedition to the Indian Ocean (1905) Antipatharia. Trans Linn Soc Lond Zool Ser 2(12):301–321Google Scholar
  10. Dahan M, Benayahu Y (1997) Reproduction of Dendronephthya hemprichi (Cnidaria: Octocorallia): year-round spawning in an azooxanthellate soft coral. Mar Biol 129:573–579CrossRefGoogle Scholar
  11. Davis TLO (1982) Maturity and sexuality in Barramundi, Lates calcarifer (Bloch), in the Northern Territory and south-eastern Gulf of Carpentaria. Aust J Mar Freshw Res 33:529–545CrossRefGoogle Scholar
  12. Ellis J, Solander D (1786) The natural history of many curious and uncommon zoophytes collected by the late John Ellis, systematically arranged and described by the late Daniel Solander. Benjamin White and Son, LondonGoogle Scholar
  13. Fadlallah YH (1983) Sexual reproduction, development and larval biology in scleractinian corals. Coral Reefs 2:129–150CrossRefGoogle Scholar
  14. Fautin DG (2002) Reproduction of Cnidaria. Can J Zool 80:1735–1754CrossRefGoogle Scholar
  15. Gage JD (1962) Two black coral stories from Maui but with vastly different sequels. Hawai‘i Shell News 9:1 & 6Google Scholar
  16. Gaino E, Scoccia F (2008) Female gametes of the black coral Cirrhipathes cfr. anguina (Anthozoa, Antipatharia) from the Indonesia Marine Park of Bunaken. Invertebr Reprod Dev 51:119–126CrossRefGoogle Scholar
  17. Gaino E, Scoccia F (2009) Release of sperm clusters in spheres by the black coral Cupressopathes pumila (Anthozoa, Antipatharia). Coral Reefs 28:851–857CrossRefGoogle Scholar
  18. Gaino E, Scoccia F (2010) Gamete spawning in Antipathella subpinnata (Anthozoa, Antipatharia): a structural and ultrastructural investigation. Zoomorphology 129:213–219CrossRefGoogle Scholar
  19. Gaino E, Bo M, Boyer M, Scoccia F (2008) Sperm morphology in the black coral Cirrhipathes sp. (Anthozoa, Antipatharia). Invertebr Biol 127:249–258CrossRefGoogle Scholar
  20. Glynn PW, Gassman NJ, Eakin CM, Cortes J, Smith DB, Guzman HM (1991) Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Galapagos Islands (Ecuador). I. Pocilloporidae. Mar Biol 109:355–368CrossRefGoogle Scholar
  21. Goenaga C (1977) Two new species of Stichopathes (Zoantharia; Antipatharia) with observations on aspects of their biology. M.S. thesis, University of Puerto Rico, p 101Google Scholar
  22. Grange KR (1988) Redescription of Antipathes aperta, Totton, (Coelenterata: Antipatharia), an ecological dominant in the southern fiords of New Zealand. N Z J Zool 15:55–61CrossRefGoogle Scholar
  23. Grigg RW (1964) A contribution to the biology and ecology of the black coral, Antipathes grandis in Hawai‘i. M.S. thesis, University of Hawai‘i, p 74Google Scholar
  24. Grigg RW (1975) The commercial potential of precious corals in the western Caroline Islands, Micronesia. Sea Grant Technical Report. UNIHI-SEAGRANT-AR-75-03Google Scholar
  25. Grigg RW (1976) Fishery management of precious and stony corals in Hawai‘i. Sea Grant Technical Report. UNIHI-SEAGRANT-TR-77-03Google Scholar
  26. Grigg RW (1984) Resource management of precious corals: a review and application to shallow water reef building corals. Mar Ecol 5:57–74CrossRefGoogle Scholar
  27. Grigg RW (1993) Precious coral fisheries of Hawai‘i and the U.S. Pacific Islands. Mar Fish Rev 55:50–60Google Scholar
  28. Grigg RW (2001) Black coral: history of a sustainable fishery in Hawai‘i. Pac Sci 55:291–299CrossRefGoogle Scholar
  29. Grigg RW (2003) Invasion of a deep coral bed by an alien species, Carijoa riisei, off Maui, Hawai‘i. Coral Reefs 22:121–122CrossRefGoogle Scholar
  30. Grigg RW (2004) Harvesting impacts and invasion by an alien species decrease estimates on black coral yield off Maui, Hawai‘i. Pac Sci 1:1–6CrossRefGoogle Scholar
  31. Grigg RW (2010) The precious corals fishery management plan of the Western Pacific Regional Fishery Management Council. Pac Isl Fish Monogr 1:1–9Google Scholar
  32. Grigg RW, Grossman EE, Earle SA, Gittings SR, Lott D, McDonough J (2002) Drowned reefs and antecedent karst topography, Au‘au Channel, S.E. Hawaiian Islands. Coral Reefs 21:73–82Google Scholar
  33. Harrison PL (2011) Sexual reproduction of scleractinian corals. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Dordrecht, Heidelberg, London, New York, pp 59–85CrossRefGoogle Scholar
  34. Harrison PL, Jamieson BG (1999) Cnidaria and Ctenophora. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol IX., Part A: Progress in male gamete ultrastructure and phylogenyWiley-Intersience, Chichester, pp 21–95Google Scholar
  35. Harrison PL, Wallace CC (1990) Reproduction, dispersal and recruitment of scleractinian corals. In: Dubinsky Z (ed) Ecosystems of the world 25: coral reefs. Elsevier, Amsterdam, Oxford, New York, Tokyo, pp 133–207Google Scholar
  36. Huang M-H, Ou C-H (2010) Precious coral fisheries management in Taiwan - Past, present & future. Mar Policy 34:1002–1009CrossRefGoogle Scholar
  37. Hyman LH (1940) Order Antipatharia, the black or thorny corals. In: The invertebrates: Protozoa through Ctenophora. McGraw-Hill Book Company, New York and London, pp 625–628Google Scholar
  38. Kahng SE, Grigg RW (2005) Impact of an alien octocoral, Carijoa riisei, on black corals in Hawai‘i. Coral Reefs 24:556–562CrossRefGoogle Scholar
  39. Kahng SE, Kelley CD (2007) Vertical zonation of megabenthic taxa on a deep photosynthetic reef (50–140 m) in the Au‘au Channel, Hawai‘i. Coral Reefs 26:679–687CrossRefGoogle Scholar
  40. Kahng SE, Benayahu Y, Wagner D, Rothe N (2008) Sexual reproduction in the invasive octocoral Carijoa riisei in Hawai‘i. Bull Mar Sci 82:1–17Google Scholar
  41. Kenyon J (1984) Black coral off Cozumel. Sea Front 30:267–272Google Scholar
  42. Levitan DR (1991) Influence of body size and population density on fertilization success and reproductive output in a free-spawning invertebrate. Biol Bull 181:371–378CrossRefGoogle Scholar
  43. Levitan DR, Sewell MA, Chia FS (1991) Kinetics of fertilization in the sea urchin Strongylocentrotus franciscanus: interaction of gamete dilution, age and contact time. Biol Bull 181:371–378CrossRefGoogle Scholar
  44. Levitan DR, Sewell MA, Chia FS (1992) How distribution and abundance influence fertilization success in the sea urchin Strongylocentrotus franciscanus. Ecology 73:248–254CrossRefGoogle Scholar
  45. Maldonado A (2003) Cuba’s environment: today and tomorrow - an action plan. Papers and Proceedings of the Thirteenth Annual Meeting of the Association for the Study of the Cuban Economy 13:63–73Google Scholar
  46. McClintock JB, Watts SA (1990) The effects of photoperiod on gametogenesis in the tropical sea urchin Eucidaris tribuloides (Lamarck) (Echinodermata: Echinoidea). J Exp Mar Biol Ecol 139:175–184CrossRefGoogle Scholar
  47. Miller K (1996) Piecing together the reproductive habits of New Zealand’s endemic black corals. Water Atmos 4:18–19Google Scholar
  48. Miller K, Grange KR (1995) Population genetic studies of antipatharian black corals from Doubtful and Nancy Sounds, Fiordland, New Zealand. Proceedings of the 6th International Conference on Coelenterate Biology:353–363Google Scholar
  49. Molodtsova TN (2006) New species of Hexapathes Kinoshita, 1910 (Anthozoa, Antipatharia, Cladopathidae) from the South-West Pacific. Zoosystema 28:597–606Google Scholar
  50. Molodtsova TN, Pasternak FA (2005) Redescription of Parantipathes euantha (Pasternak, 1958) (Anthozoa: Antipatharia) from Kurile-Kamchatka Trench. Invertebr Zool 2:169–179Google Scholar
  51. Moon HW, Song JI (2008) Taxonomy of the black coral family Myriopathidae (Anthozoa: Antipatharia) from Korea. Korean J Syst Zool 24:251–263CrossRefGoogle Scholar
  52. Noome C, Kristensen I (1976) Necessity of conservation of slow growing organisms like black coral. CCA Ecology Conference Bonaire 11:76–77Google Scholar
  53. Oishi FG (1990) Black coral harvesting and marketing activities in Hawai‘i - 1990. Division of Aquatic Resources, State of Hawai‘iGoogle Scholar
  54. Oliver JK, Babcock RC (1992) Aspects of the fertilization ecology ofbroadcast spawning corals: sperm dilution effects and in situ measurements of fertilization. Biol Bull 183:409–417CrossRefGoogle Scholar
  55. Olsen DA, Wood RS (1980) Investigations on black coral in Salt River Submarine Canyon St. Croix, U.S. Virgin Islands. Final scientific report 80-12. Division of Fish and Wildlife U.S. Virgin Islands NULS-I Mission 79-5 and 80-12Google Scholar
  56. Opresko DM (1972) Redescriptions and reevaluations of the antipatharians described by L.F. de Pourtales. Bull Mar Sci 22:950–1017Google Scholar
  57. Opresko DM (2003) Revision of the Antipatharia (Cnidaria: Anthozoa). Part III. Cladopathidae. Zool Meded (Leiden) 77:495–536Google Scholar
  58. Opresko DM (2005) New genera and species of antipatharian corals (Cnidaria: Anthozoa) from the North Pacific. Zool Meded (Leiden) 79–2:129–165Google Scholar
  59. Opresko DM (2009) A new name for the Hawaiian antipatharian coral formerly known as Antipathes dichotoma (Cnidaria: Anthozoa: Antipatharia). Pac Sci 63: 277––291CrossRefGoogle Scholar
  60. Opresko DM, Genin A (1990) A new species of antipatharian (Cnidaria: Anthozoa) from seamounts in the eastern North Pacific. Bull Mar Sci 46:301–310Google Scholar
  61. Padilla C, Lara M (2003) Banco Chinchorro: the last shelter for black coral in the Mexican Caribbean. Bull Mar Sci 73:197–202Google Scholar
  62. Parker NR, Mladenov PV, Grange KR (1997) Reproductive biology of the antipatharian black coral Antipathes fiordensis in Doubtful Sound, Fiordland, New Zealand. Mar Biol 130:11–22CrossRefGoogle Scholar
  63. Parrish FA, Baco AR (2007) State of deep coral ecosystems: in the U.S. Pacific Islands region: Hawai‘i and the U.S. Pacific territories. In: Lumsden SE, Hourigan TF, Bruckner AW, Dorr G (eds) The state of deep coral ecosystems in the United States. NOAA Technical Memorandum CRCP - 3, Silver Spring, MD, pp 159–194Google Scholar
  64. Pax F (1918) Die Antipatharien. Zool Jahrb Abt Syst Ökol Geogr Tiere 41:419–479Google Scholar
  65. Pax F (1932) Beitrag zur Kenntnis der japanischen Dörnchenkorallen. Zool Jahrb Abt Syst Ökol Geogr Tiere 63:407–450Google Scholar
  66. Pax F, Van-Praët M, Doumenc D (1987) Ordre des antipathaires. In: Doumenc D (ed) Traité de zoologie - anatomie, systématique, biologie. Vol 3(Fasc. 3). Cnidaires anthozoaires. Masson, ParisGoogle Scholar
  67. Pearse JS, Eernisse DJ (1982) Photoperiodic regulation of gametogenesis and gonadal growth in the sea star Pisaster ochraceus. Mar Biol 67:121–125CrossRefGoogle Scholar
  68. Pennington JT (1985) The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol Bull 169:417–430CrossRefGoogle Scholar
  69. Reed JK, Pomponi SA, Weaver D, Paull CK, Wright AE (2005) Deep-water sinkholes and bioherms of south Florida and the Pourtales Terrace - habitat and fauna. Bull Mar Sci 77:267–296Google Scholar
  70. Richmond RH, Hunter CL (1990) Reproduction and recruitment of corals: comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Mar Ecol Prog Ser 60:185–203CrossRefGoogle Scholar
  71. Romero XM (1997) Ecuador’s vanishing black corals. Aquaticus: J Shedd Aquar 26:21–25Google Scholar
  72. Roule L (1905) Description des Antipathaires et Cérianthaires recueillis par S.A.S. le Prince de Monaco dans L’Atlantique nord (1886–1902). Fascicule XXX. Imprimerie de Monaco, MonacoGoogle Scholar
  73. Sakai K (1998) Effect of colony size, polyp size, and budding mode on egg production in a colonial coral. Biol Bull 195:319–325CrossRefGoogle Scholar
  74. Schmidt H (1972) Die Nesselkapseln der Anthozoen und ihre Bedeutung für die phylogenetische Systematik. Helgol Wiss Meeresunters 23:422–458CrossRefGoogle Scholar
  75. Schmidt H, Zissler D (1979) Die Spermien der Anthozoen und ihre phylogenetische Bedeutung. Zoologica (Stuttg) 44:1–97Google Scholar
  76. Schultze L (1896) Beitrag zur Systematik der Antipatharien. Abh Senckenb Natforsch Ges 23:1–39Google Scholar
  77. Schultze LS (1903) Die Antipatharien der deutschen Tiefsee-Expedition 1898–1899. In: Chun C (ed) Wissentschaftliche Ergebnisse der Deutschen Tiefsee-Expedition auf dem Dampfer “Valdivia” 1998–1899. Verlag von Gustav Fischer, Jena, Germany, pp 87–100Google Scholar
  78. Stimson JS (1978) Mode and timing of reproduction in some common hermatypic corals of Hawai‘i and Enewetak. Mar Biol 48:173–184CrossRefGoogle Scholar
  79. Szmant AM (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–54CrossRefGoogle Scholar
  80. Torres JL, Armstrong RA, Weil E (2008) Enhanced ultraviolet radiation can terminate sexual reproduction in the broadcasting coral species Acropora cervicornis Lamarck. J Exp Mar Biol Ecol 358:39–45CrossRefGoogle Scholar
  81. Tsounis G, Rossi S, Grigg RW, Santangelo G, Bramanti L, Gili JM (2010) The exploitation and conservation of precious corals. Oceanogr Mar Biol Annu Rev 48:161–212CrossRefGoogle Scholar
  82. Van Pesch AJ (1914) The antipatharians of the Siboga Expedition. Siboga-Expeditie, 17. E.J. Bill, LeydenGoogle Scholar
  83. Van Woesik R, Lacharmoise F, Köksal S (2006) Annual cycles of solar insolation predict spawning times of Caribbean corals. Ecol Lett 9:390–398PubMedCrossRefGoogle Scholar
  84. Vermeij MJA, Sampayo E, Broeker K, Bak RPM (2004) The reproductive biology of closely related coral species: gametogenesis in Madracis from the southern Caribbean. Coral Reefs 23:206–214CrossRefGoogle Scholar
  85. Von Koch G (1878) Zur Phylogenie der Antipatharia. Morphol Jahrb 4:74–86Google Scholar
  86. Wagner D, Brugler MR, Opresko DM, France SC, Montgomery AD, Toonen RJ (2010) Using morphometrics, in situ observations and genetic characters to distinguish among commercially valuable Hawaiian black coral species; a redescription of Antipathes grandis Verrill, 1928 (Antipatharia : Antipathidae). Invertebr Syst 24:271–290CrossRefGoogle Scholar
  87. Wagner D, Waller RG, Toonen RJ (2011a) Sexual reproduction of Hawaiian black corals, with a review of reproduction of antipatharians (Cnidaria: Anthozoa: Hexacorallia). Invertebr Biol 130:211–225CrossRefGoogle Scholar
  88. Wagner D, Papastamatiou YP, Kosaki RK, Gleason KA, McFall GB, Boland RC, Pyle RL, Toonen RJ (2011b) New records of commercially valuable black corals (Cnidaria: Antipatharia) from the Northwestern Hawaiian Islands at mesophotic depths. Pac Sci 65:249–255CrossRefGoogle Scholar
  89. Wallace CC (1985) Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Mar Biol 88:217–233CrossRefGoogle Scholar
  90. Waller RG, Baco AR (2007) Reproductive morphology of three species of deep-water precious corals from the Hawaiian Archipelago: Gerardia sp., Corallium secundum, and Corallium lauuense. Bull Mar Sci 81:533–542Google Scholar
  91. Waller RG, Tyler PA, Gage JD (2005) Sexual reproduction in three hermaphroditic deep-sea Caryophyllia species (Anthozoa: Scleractinia) from the NE Atlantic Ocean. Coral Reefs 24:594–602CrossRefGoogle Scholar
  92. Walton WH (1948) Feret’s statistical diameter as a measure of particle size. Nature 162:329–330CrossRefGoogle Scholar
  93. Ward S (1995) The effect of damage on the growth, reproduction and storage of lipids in the scleractinian coral Pocillopora damicornis (Linnaeus) J Exp Mar Biol Ecol 187:193–206Google Scholar
  94. Ward S, Harrison P, Hoegh-Guldberg O (2000) Coral bleaching reduces reproduction of scleractinian corals and increases susceptibility to future stress. Proc 9th Int Coral Reef Symp 2:1123–1128Google Scholar
  95. WPRFMC (2006) 2006 black coral science and management workshop report. Western Pacific Regional Fishery Management Council, Honolulu, HIGoogle Scholar
  96. Zakai D, Levy O, Chadwick-Furman NE (2000) Experimental fragmentation reduces sexual reproductive output by the reef-building coral Pocillopora damicornis. Coral Reefs 19:185–188CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • D. Wagner
    • 1
    • 2
  • R. G. Waller
    • 3
  • A. D. Montgomery
    • 4
  • C. D. Kelley
    • 5
  • R. J. Toonen
    • 6
  1. 1.Department of OceanographyUniversity of Hawai‘i at MānoaHonoluluUSA
  2. 2.Papahānaumokuākea Marine National MonumentHonoluluUSA
  3. 3.Darling Marine CenterUniversity of MaineWalpoleUSA
  4. 4.U.S. Fish and Wildlife ServiceHonoluluUSA
  5. 5.Hawai‘i Undersea Research LaboratoryUniversity of Hawai‘i at MānoaHonoluluUSA
  6. 6.Hawai‘i Institute of Marine BiologyKaneoheUSA

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