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

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Abstract

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.

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References

  • 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 90:379–394

    Article  Google Scholar 

  • 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 186:17–28

    Article  Google Scholar 

  • Bo M (2008) Taxonomy and ecology of antipatharians. Ph.D. thesis, Universita Politecnica Delle Marche, p 212

  • 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 76:392–402

    Article  CAS  Google Scholar 

  • Boland RC, Parrish FA (2005) A description of fish assemblages in the black coral beds off Lahaina, Maui, Hawai‘i. Pac Sci 59:411–420

    Article  Google Scholar 

  • Brook G (1889) Report on the Antipatharia. Report of the scientific results of the voyage of the H.M.S. Challenger. Zool 32:1–222

    Google Scholar 

  • Carroll A, Harrison P, Adjeroud M (2006) Sexual reproduction of Acropora reef corals at Moorea, French Polynesia. Coral Reefs 25:93–97

    Article  Google Scholar 

  • Castorena V, Metaca M (1979) El coral negro, una riqueza en peligro. Tec Pesq 139:22–27

    Google Scholar 

  • Cooper CF (1909) Reports of the Percy Sladen Trust Expedition to the Indian Ocean (1905) Antipatharia. Trans Linn Soc Lond Zool Ser 2(12):301–321

    Google Scholar 

  • Dahan M, Benayahu Y (1997) Reproduction of Dendronephthya hemprichi (Cnidaria: Octocorallia): year-round spawning in an azooxanthellate soft coral. Mar Biol 129:573–579

    Article  Google Scholar 

  • 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 33:529–545

    Article  Google Scholar 

  • 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, London

  • Fadlallah YH (1983) Sexual reproduction, development and larval biology in scleractinian corals. Coral Reefs 2:129–150

    Article  Google Scholar 

  • Fautin DG (2002) Reproduction of Cnidaria. Can J Zool 80:1735–1754

    Article  Google Scholar 

  • Gage JD (1962) Two black coral stories from Maui but with vastly different sequels. Hawai‘i Shell News 9:1 & 6

    Google Scholar 

  • 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 51:119–126

    Article  Google Scholar 

  • Gaino E, Scoccia F (2009) Release of sperm clusters in spheres by the black coral Cupressopathes pumila (Anthozoa, Antipatharia). Coral Reefs 28:851–857

    Article  Google Scholar 

  • Gaino E, Scoccia F (2010) Gamete spawning in Antipathella subpinnata (Anthozoa, Antipatharia): a structural and ultrastructural investigation. Zoomorphology 129:213–219

    Article  Google Scholar 

  • Gaino E, Bo M, Boyer M, Scoccia F (2008) Sperm morphology in the black coral Cirrhipathes sp. (Anthozoa, Antipatharia). Invertebr Biol 127:249–258

    Article  Google Scholar 

  • 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 109:355–368

    Article  Google Scholar 

  • 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 101

  • Grange KR (1988) Redescription of Antipathes aperta, Totton, (Coelenterata: Antipatharia), an ecological dominant in the southern fiords of New Zealand. N Z J Zool 15:55–61

    Article  Google Scholar 

  • 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 74

  • Grigg RW (1975) The commercial potential of precious corals in the western Caroline Islands, Micronesia. Sea Grant Technical Report. UNIHI-SEAGRANT-AR-75-03

  • Grigg RW (1976) Fishery management of precious and stony corals in Hawai‘i. Sea Grant Technical Report. UNIHI-SEAGRANT-TR-77-03

  • Grigg RW (1984) Resource management of precious corals: a review and application to shallow water reef building corals. Mar Ecol 5:57–74

    Article  Google Scholar 

  • Grigg RW (1993) Precious coral fisheries of Hawai‘i and the U.S. Pacific Islands. Mar Fish Rev 55:50–60

    Google Scholar 

  • Grigg RW (2001) Black coral: history of a sustainable fishery in Hawai‘i. Pac Sci 55:291–299

    Article  Google Scholar 

  • Grigg RW (2003) Invasion of a deep coral bed by an alien species, Carijoa riisei, off Maui, Hawai‘i. Coral Reefs 22:121–122

    Article  Google Scholar 

  • Grigg RW (2004) Harvesting impacts and invasion by an alien species decrease estimates on black coral yield off Maui, Hawai‘i. Pac Sci 1:1–6

    Article  Google Scholar 

  • Grigg RW (2010) The precious corals fishery management plan of the Western Pacific Regional Fishery Management Council. Pac Isl Fish Monogr 1:1–9

    Google Scholar 

  • 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 21:73–82

    Google Scholar 

  • 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 59–85

    Chapter  Google Scholar 

  • 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 21–95

    Google Scholar 

  • 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 133–207

    Google Scholar 

  • Huang M-H, Ou C-H (2010) Precious coral fisheries management in Taiwan - Past, present & future. Mar Policy 34:1002–1009

    Article  Google Scholar 

  • 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 625–628

  • Kahng SE, Grigg RW (2005) Impact of an alien octocoral, Carijoa riisei, on black corals in Hawai‘i. Coral Reefs 24:556–562

    Article  Google Scholar 

  • 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 26:679–687

    Article  Google Scholar 

  • Kahng SE, Benayahu Y, Wagner D, Rothe N (2008) Sexual reproduction in the invasive octocoral Carijoa riisei in Hawai‘i. Bull Mar Sci 82:1–17

    Google Scholar 

  • Kenyon J (1984) Black coral off Cozumel. Sea Front 30:267–272

    Google Scholar 

  • Levitan DR (1991) Influence of body size and population density on fertilization success and reproductive output in a free-spawning invertebrate. Biol Bull 181:371–378

    Article  Google Scholar 

  • 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 181:371–378

    Article  Google Scholar 

  • Levitan DR, Sewell MA, Chia FS (1992) How distribution and abundance influence fertilization success in the sea urchin Strongylocentrotus franciscanus. Ecology 73:248–254

    Article  Google Scholar 

  • 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 13:63–73

    Google Scholar 

  • 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 139:175–184

    Article  Google Scholar 

  • Miller K (1996) Piecing together the reproductive habits of New Zealand’s endemic black corals. Water Atmos 4:18–19

    Google Scholar 

  • 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:353–363

  • Molodtsova TN (2006) New species of Hexapathes Kinoshita, 1910 (Anthozoa, Antipatharia, Cladopathidae) from the South-West Pacific. Zoosystema 28:597–606

    Google Scholar 

  • Molodtsova TN, Pasternak FA (2005) Redescription of Parantipathes euantha (Pasternak, 1958) (Anthozoa: Antipatharia) from Kurile-Kamchatka Trench. Invertebr Zool 2:169–179

    Google Scholar 

  • Moon HW, Song JI (2008) Taxonomy of the black coral family Myriopathidae (Anthozoa: Antipatharia) from Korea. Korean J Syst Zool 24:251–263

    Article  Google Scholar 

  • Noome C, Kristensen I (1976) Necessity of conservation of slow growing organisms like black coral. CCA Ecology Conference Bonaire 11:76–77

    Google Scholar 

  • Oishi FG (1990) Black coral harvesting and marketing activities in Hawai‘i - 1990. Division of Aquatic Resources, State of Hawai‘i

  • Oliver JK, Babcock RC (1992) Aspects of the fertilization ecology ofbroadcast spawning corals: sperm dilution effects and in situ measurements of fertilization. Biol Bull 183:409–417

    Article  Google Scholar 

  • 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 80-12

  • Opresko DM (1972) Redescriptions and reevaluations of the antipatharians described by L.F. de Pourtales. Bull Mar Sci 22:950–1017

    Google Scholar 

  • Opresko DM (2003) Revision of the Antipatharia (Cnidaria: Anthozoa). Part III. Cladopathidae. Zool Meded (Leiden) 77:495–536

    Google Scholar 

  • Opresko DM (2005) New genera and species of antipatharian corals (Cnidaria: Anthozoa) from the North Pacific. Zool Meded (Leiden) 79–2:129–165

    Google Scholar 

  • Opresko DM (2009) A new name for the Hawaiian antipatharian coral formerly known as Antipathes dichotoma (Cnidaria: Anthozoa: Antipatharia). Pac Sci 63: 277––291

    Article  Google Scholar 

  • Opresko DM, Genin A (1990) A new species of antipatharian (Cnidaria: Anthozoa) from seamounts in the eastern North Pacific. Bull Mar Sci 46:301–310

    Google Scholar 

  • Padilla C, Lara M (2003) Banco Chinchorro: the last shelter for black coral in the Mexican Caribbean. Bull Mar Sci 73:197–202

    Google Scholar 

  • Parker NR, Mladenov PV, Grange KR (1997) Reproductive biology of the antipatharian black coral Antipathes fiordensis in Doubtful Sound, Fiordland, New Zealand. Mar Biol 130:11–22

    Article  Google Scholar 

  • 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 159–194

  • Pax F (1918) Die Antipatharien. Zool Jahrb Abt Syst Ökol Geogr Tiere 41:419–479

    Google Scholar 

  • Pax F (1932) Beitrag zur Kenntnis der japanischen Dörnchenkorallen. Zool Jahrb Abt Syst Ökol Geogr Tiere 63:407–450

    Google Scholar 

  • 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, Paris

  • Pearse JS, Eernisse DJ (1982) Photoperiodic regulation of gametogenesis and gonadal growth in the sea star Pisaster ochraceus. Mar Biol 67:121–125

    Article  Google Scholar 

  • Pennington JT (1985) The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biol Bull 169:417–430

    Article  Google Scholar 

  • 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 77:267–296

    Google Scholar 

  • 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 60:185–203

    Article  Google Scholar 

  • Romero XM (1997) Ecuador’s vanishing black corals. Aquaticus: J Shedd Aquar 26:21–25

    Google Scholar 

  • 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, Monaco

  • Sakai K (1998) Effect of colony size, polyp size, and budding mode on egg production in a colonial coral. Biol Bull 195:319–325

    Article  Google Scholar 

  • Schmidt H (1972) Die Nesselkapseln der Anthozoen und ihre Bedeutung für die phylogenetische Systematik. Helgol Wiss Meeresunters 23:422–458

    Article  Google Scholar 

  • Schmidt H, Zissler D (1979) Die Spermien der Anthozoen und ihre phylogenetische Bedeutung. Zoologica (Stuttg) 44:1–97

    Google Scholar 

  • Schultze L (1896) Beitrag zur Systematik der Antipatharien. Abh Senckenb Natforsch Ges 23:1–39

    Google Scholar 

  • 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 87–100

    Google Scholar 

  • Stimson JS (1978) Mode and timing of reproduction in some common hermatypic corals of Hawai‘i and Enewetak. Mar Biol 48:173–184

    Article  Google Scholar 

  • Szmant AM (1986) Reproductive ecology of Caribbean reef corals. Coral Reefs 5:43–54

    Article  Google Scholar 

  • 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 358:39–45

    Article  Google Scholar 

  • 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 48:161–212

    Article  Google Scholar 

  • Van Pesch AJ (1914) The antipatharians of the Siboga Expedition. Siboga-Expeditie, 17. E.J. Bill, Leyden

  • Van Woesik R, Lacharmoise F, Köksal S (2006) Annual cycles of solar insolation predict spawning times of Caribbean corals. Ecol Lett 9:390–398

    Article  PubMed  Google Scholar 

  • 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 23:206–214

    Article  Google Scholar 

  • Von Koch G (1878) Zur Phylogenie der Antipatharia. Morphol Jahrb 4:74–86

    Google Scholar 

  • 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 24:271–290

    Article  Google Scholar 

  • 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 130:211–225

    Article  Google Scholar 

  • 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 65:249–255

    Article  Google Scholar 

  • Wallace CC (1985) Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Mar Biol 88:217–233

    Article  Google Scholar 

  • 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 81:533–542

    Google Scholar 

  • 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 24:594–602

    Article  Google Scholar 

  • Walton WH (1948) Feret’s statistical diameter as a measure of particle size. Nature 162:329–330

    Article  Google Scholar 

  • 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 187:193–206

  • 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 2:1123–1128

    Google Scholar 

  • WPRFMC (2006) 2006 black coral science and management workshop report. Western Pacific Regional Fishery Management Council, Honolulu, HI

    Google Scholar 

  • Zakai D, Levy O, Chadwick-Furman NE (2000) Experimental fragmentation reduces sexual reproductive output by the reef-building coral Pocillopora damicornis. Coral Reefs 19:185–188

    Article  Google Scholar 

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Acknowledgments

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.

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Wagner, D., Waller, R.G., Montgomery, A.D. et al. Sexual reproduction of the Hawaiian black coral Antipathes griggi (Cnidaria: Antipatharia). Coral Reefs 31, 795–806 (2012). https://doi.org/10.1007/s00338-012-0882-3

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