Abstract
Mesophotic coral-reef ecosystems (MCEs), which comprise the light-dependent communities of corals and other organisms found at depths between 30 and ~ 150 m, have received very little study to date. However, current technological advances, such as remotely operated vehicles and closed-circuit rebreather diving, now enable their thorough investigation. Following the reef-building stony corals, octocorals are the second most common benthic component on many shallow reefs and a major component on deep reefs, the Red Sea included. This study is the first to examine octocoral community features on upper MCEs based on species-level identification and to compare them with the shallower reef zones. The study was carried out at Eilat (Gulf of Aqaba, northern Red Sea), comparing octocoral communities at two mesophotic reefs (30–45 m) and two shallow reef zones (reef flat and upper fore-reef) by belt transects. A total of 30 octocoral species were identified, with higher species richness on the upper MCEs compared to the shallower reefs. Although the MCEs were found to host a higher number of species than the shallower reefs, both featured a similar diversity. Each reef zone revealed a unique octocoral species composition and distinct community structure, with only 16% of the species shared by both the MCEs and the shallower reefs. This study has revealed an almost exclusive dominance of zooxanthellate species at the studied upper MCE reefs, thus indicating an adequate light regime for photosynthesis there. The findings should encourage similar studies on other reefs, aimed at understanding the spatiotemporal features and ecological role of octocorals in reef ecosystems down to the deepest limit of the MCEs.
References
Alderslade P (2000) Four new genera of soft corals (Coelenterata: Octocorallia), with notes on the classification of some established taxa. Zoologische Mededelingen 74:237–249
Appeldoorn R, Ballantine D, Bejarano I, Carlo M, Nemeth M, Otero E, Pagan F, Ruiz H, Schizas N, Sherman C, Weil E (2016) Mesophotic coral ecosystems under anthropogenic stress: a case study at Ponce, Puerto Rico. Coral Reefs 35:63–75
Bare AY, Grimshaw KL, Rooney JJ, Sabater MG, Fenner D, Carroll B (2010) Mesophotic communities of the insular shelf at Tutuila, American Samoa. Coral Reefs 29:369–377
Barneah O, Weis VM, Perez S, Benayahu Y (2004) Diversity of dinoflagellate symbionts in Red Sea soft corals: mode of symbiont acquisition matters. Mar Ecol Prog Ser 275:89–95
Benayahu Y (1989) Reproductive cycle and developmental processes during embryogenesis of Clavularia hamra (Cnidaria: Octocorallia). Acta Zool 70:29–36
Benayahu Y, Loya Y (1977) Space partitioning by stony corals, soft corals and benthic algae on the coral reefs of the northern Gulf of Eilat (Red Sea). Helgol Wiss Meeresunters 30:362–382
Benayahu Y, Loya Y (1981) Competition for space among coral-reef organisms at Eilat, Red Sea. Bull Mar Sci 31:514–522
Benayahu Y, Loya Y (1983) Surface brooding in the Red Sea soft coral Parerythropodium fulvum fulvum (Forskål, 1775). Biol Bull 165:353–369
Benayahu Y, Loya Y (1984a) Life history studies on the Red Sea soft coral Xenia macrospiculata Gohar, 1940. I. Annual dynamics of gonadal development. Biol Bull 166:32–43
Benayahu Y, Loya Y (1984b) Substratum preferences and planulae settling of two red sea alcyonaceans: Xenia macrospiculata Gohar and Parerythropodium fulvum fulvum (Forskl). J Exp Mar Bio Ecol 83:249–260
Benayahu Y, Loya Y (1985) Settlement and recruitment of a soft coral: why is Xenia macrospiculata a successful colonizer? Bull Mar Sci 36:177–188
Benayahu Y, Loya Y (1986) Sexual reproduction of a soft coral: synchronous and brief annual spawning of Sarcophyton glaucum (Quoy & Gaimard, 1833). Biol Bull 170:32–42
Benayahu Y, Loya Y (1987) Long-term recruitment of soft corals (Octocorallia: Alcyonacea) on artificial substrata at Eilat (Red Sea). Mar Ecol Prog Ser 38:161–167
Benayahu Y, Shlagman A, Schleyer MH (2003) Corals of the south-west Indian Ocean: VI. The Alcyonacea (Octocorallia) of Mozambique, with a discussion on soft coral distribution on south equatorial East African reefs. Zoologische Verhandelingen 345:49–58
Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327
Bongaerts P, Bridge TCL, Kline DI, Muir PR, Wallace CC, Beaman RJ, Hoegh-Guldberg O (2011) Mesophotic coral ecosystems on the walls of Coral Sea atolls. Coral Reefs 30:335
Bridge TC, Hughes TP, Guinotte JM, Bongaerts P (2013) Call to protect all coral reefs. Nat Clim Chang 3:528–530
Bridge TC, Fabricius KE, Bongaerts P, Wallace CC, Muir PR, Done TJ, Webster JM (2012) Diversity of Scleractinia and Octocorallia in the mesophotic zone of the Great Barrier Reef, Australia. Coral Reefs 31:179–189
Carlon DB, Olson RR (1993) Larval dispersal distance as an explanation for adult spatial pattern in two Caribbean reef corals. J Exp Mar Bio Ecol 173:247–263
Chao A, Chiu CH, Jost L (2014) Unifying species diversity, phylogenetic diversity, functional diversity, and related similarity and differentiation measures through Hill numbers. Annu Rev Ecol Evol Syst 45:297–324
Dahan M, Benayahu Y (1997) Reproduction of Dendronephthya hemprichi (Cnidaria: Octocorallia): year-round spawning in an azooxanthellate soft coral. Mar Biol 129:573–579
Etnoyer PJ, Wickes LN, Silva M, Dubick JD, Balthis L, Salgado E, MacDonald IR (2016) Decline in condition of gorgonian octocorals on mesophotic reefs in the northern Gulf of Mexico: before and after the Deepwater Horizon oil spill. Coral Reefs 35:77–90
Eyal (2014) Ecology and taxonomy of mesophotic communities in Israel (Red Sea and Mediterranean). M.Sc. thesis, Tel-Aviv University, Tel Aviv, Israel
Fabricius KK, Alderslade PP (2001) Soft corals and sea fans: a comprehensive guide to the tropical shallow water genera of the central-west Pacific, the Indian Ocean and the Red Sea. Australian Institute of Marine Science, Townsville, Australia
Fabricius K, De’Ath G (2008) Photosynthetic symbionts and energy supply determine octocoral biodiversity in coral reefs. Ecology 89:3163–3173
Garcia-Sais JR (2010) Reef habitats and associated sessile-benthic and fish assemblages across a euphotic–mesophotic depth gradient in Isla Desecheo, Puerto Rico. Coral Reefs 29:277–288
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391
Halàsz A, Reynolds AM, McFadden CS, Toonen RJ, Benayahu Y (2014) Could polyp pulsation be the key to species boundaries in the genus Ovabunda (Octocorallia: Alcyonacea: Xeniidae)? Hydrobiologia 759:95–107
Haverkort-Yeh RD, McFadden CS, Benayahu Y, Berumen M, Halász A, Toonen RJ (2013) A taxonomic survey of Saudi Arabian Red Sea octocorals (Cnidaria: Alcyonacea). Mar Biodivers 43:279–291
Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432
Holstein DM, Smith TB, Gyory J, Paris CB (2015) Fertile fathoms: deep reproductive refugia for threatened shallow corals. Sci Rep 5:12407
Holstein DM, Paris CB, Vaz AC, Smith TB (2016) Modeling vertical coral connectivity and mesophotic refugia. Coral Reefs 35:23–37
Kahng SE, Kelley CD (2007) Vertical zonation of megabenthic taxa on a deep photosynthetic reef (50–140 m) in the Au’au Channel, Hawaii. Coral Reefs 26:679–687
Kahng SE, Benayahu Y, Lasker HR (2011) Sexual reproduction in octocorals. Mar Ecol Prog Ser 443:265–283
Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein L, Toonen RJ (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29:255–275
Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Bio Ecol 375:1–8
Lloyd M (1967) Mean crowding. J Anim Ecol 36:1–30
Loya Y (1972) Community structure and species diversity of hermatypic corals at Eilat, Red Sea. Mar Biol 13:100–123
Loya Y, Eyal G, Treibitz T, Lesser MP, Appeldoorn R (2016) Theme section on mesophotic coral ecosystems: advances in knowledge and future perspectives. Coral Reefs 35:1–9
Mandelberg-Aharon Y, Benayahu Y (2015) Reproductive features of the Red Sea octocoral Sarcophyton auritum are uniform within generic boundaries across wide biogeographical regions. Hydrobiologia 759:119–132
McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297
McFadden CS, Benayahu Y, Pante E, Thoma JN, Nevarez PA, France SC (2011) Limitations of mitochondrial gene barcoding in Octocorallia. Mol Ecol Resour 11:19–31
Menza C, Kendall M, Hile S (2008) The deeper we go the less we know. Rev Biol Trop 56:11–24
Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens MH, Wagner H (2013) Vegan: community ecology package. R package version 2.0-10
Pandolfi JM, Connolly SR, Marshall DJ, Cohen AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422
Perkol-Finkel S, Benayahu Y (2004) Community structure of stony and soft corals on artificial and natural reefs in Eilat (Red Sea): comparative aspects and implications. Coral Reefs 23:195–205
Perkol-Finkel S, Benayahu Y (2005) Recruitment of benthic organisms onto a planned artificial reef: shifts in community structure one decade post-deployment. Mar Environ Res 59:79–99
Pielou EC (1969) An introduction to mathematical ecology. Wiley Interscience, New York, p 286
Pittman SJ, Christensen JD, Caldow C, Menza C, Monaco ME (2007) Predictive mapping of fish species richness across shallow-water seascapes in the Caribbean. Ecol Model 204:9–21
Puglise KA, Hinderstein LM, Marr JCA, Dowgiallo MJ, Martinez FA (2009) Mesophotic coral ecosystems research strategy: international workshop to prioritize research and management needs for mesophotic coral ecosystems, Jupiter, Florida, 12–15 July 2008. NOAA Technical Memorandum NOS NCCOS 98 and OAR OER 2. NOAA National Centers for Coastal Ocean Science, Silver Spring, MD, 24 pp
Reece JB, Urry LA, Cain ML, Wasserman SA, Minorsky PV, Jackson R, Campbell NA (2013) Campbell biology, 10th edn. Pearson, Boston
R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rényi A (1960) On the central limit theorem for the sum of a random number of independent random variables. Acta Mathematica Hungarica 11:97–102
Rosenberg E, Loya Y (2004) The coral reefs of Eilat—past, present and future: three decades of coral community structure studies. Coral reef health and disease. Springer, Heidelberg, pp 1–34
Sade AR, Hall JK, Tibor G, Niemi TM, Ben-Avraham Z, Al-Zoubi AA, Hartman G, Akawwi E, Abueladas AR, Amitc G (2008) The Israel national bathymetric survey: Northern Gulf of Aqaba/Eilat Poster. Israel Journal of Earth Sciences 57:139–144
Schleyer MH, Benayahu Y (in press) A checklist of the soft corals (Octocorallia: Alcyonacea) of Mayotte. Mar Biodivers
Shannon CE, Weaver W (1949) The mathematical theory of information. University of Illinois Urbana, Champaign, IL
Slattery M, Lesser MP, Brazeau D, Stokes MD, Leichter JJ (2011) Connectivity and stability of mesophotic coral reefs. J Exp Mar Bio Ecol 408:32–41
Spalding MD, Brown BE (2015) Warm-water coral reefs and climate change. Science 350:769–771
Van Ofwegen LP (2002) Status of knowledge of the Indo-Pacific soft coral genus Sinularia May, 1898 (Anthozoa: Octocorallia). Proc 9th Int Coral Reef Symp Vol 1
Van Ofwegen LP, Benayahu Y, McFadden CS (2013) Sinularia leptoclados (Ehrenberg, 1834) (Cnidaria, Octocorallia) re-examined. Zookeys 272:29
Van Ofwegen LP, McFadden CS, Benayahu Y (2016) Sinularia polydactyla (Ehrenberg, 1834) (Cnidaria, Octocorallia) re-examined. Zookeys 581:71
Van Oppen MJH, Bongaerts P, Underwood JN, Peplow LM, Cooper TF (2011) The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia. Mol Ecol 20:1647–1660
Verseveldt J (1980) A revision of the genus Sinularia May (Octocorallia, Alcyonacea). Zoologische Verhandelingen 179:1–28
Verseveldt J (1983) A revision of the genus Lobophytum von Marenzeller (Octocorallia: Alcyonacea). Zoologische Verhandelingen 200:1–103
Verseveldt J, Benayahu Y (1978) Descriptions of one old and five new species of Alcyonacea (Coelenterata: Octocorallia) from the Red Sea. Zoologische Mededelingen 53:57–74
Verseveldt J, Benayahu Y (1983) On two old and fourteen new species of Alcyonacea (Coelenterata, Octocorallia) from the Red Sea. Zoologische Verhandelingen 208:1–33
Zakai D, Chadwick-Furman NE (2002) Impacts of intensive recreational diving on reef corals at Eilat, northern Red Sea. Biol Conserv 105:179–187
Acknowledgements
We are indebted to the constructive comments of S.E. Kahng, Y. Belmaker, and the anonymous reviewers, which have greatly improved the manuscript. We thank the Interuniversity Institute for Marine Sciences in Eilat (IUI) for assistance and use of facilities. We acknowledge M. Weis, E. Gilad, and other diving buddies for help in the field work, A. Shlagman for curatorial skills, and N. Paz for editorial assistance. This research was in part supported by the Israel Cohen Chair in Environmental Zoology to YB. Collection of animals complied with a permit issued by the Israel Nature and National Parks Protection Authority.
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Shoham, E., Benayahu, Y. Higher species richness of octocorals in the upper mesophotic zone in Eilat (Gulf of Aqaba) compared to shallower reef zones. Coral Reefs 36, 71–81 (2017). https://doi.org/10.1007/s00338-016-1528-7
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DOI: https://doi.org/10.1007/s00338-016-1528-7