[en] Here, we report a new broad approach to investigating the presence and density of Symbiodiniaceae cells in corals of the order Antipatharia subclass Hexacorallia, commonly known as black corals. Antipatharians are understudied ecosystem engineers of shallow (<30 m depth), mesophotic (30–150 m) and deep-sea (>200 m) reefs. They provide habitat to numerous organisms, enhancing and supporting coral reef biodiversity globally. Nonetheless, little biological and ecological information exists on antipatharians, including the extent to which global change disturbances are threatening their health. The previous assumption that they were exempted from threats related to the phenomenon known as bleaching was challenged by the recent findings of high densities of dinoflagellates within three antipatharian colonies. Further studies were thus necessary to investigate the broader uniformity of these findings. Here we report results of an integrated methodology combining microscopy and molecular techniques to investigate the presence and estimate the density of Symbiodiniaceae cells within two antipatharians species—Cupressopathes abies and Stichopathes maldivensis—from both shallow and mesophotic reefs of SW Madagascar. We found that Symbiodiniaceae-like cells were present within samples of both species collected from both shallow and mesophotic reefs, although the overall cell density was very low (0–4 cell mm−3). These findings suggest that presence or high abundance of Symbiodiniaceae is not characteristic of all antipatharians, which is relevant considering the bleaching phenomenon affecting other corals. However, the possibility of higher densities of dinoflagellates in other antipatharians or in colonies exposed to higher light irradiance deserves further investigation.
Research Center/Unit :
Biology of Marine Organisms and Biomimetics, University of Mons; Marine Biology Laboratory, Université Libre de Bruxelles
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Gress, Erika
Eeckhaut, Igor
Godefroid, Mathilde
Dubois, Philippe
Richir, Jonathan ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (COU)
Terrana, Lucas
Language :
English
Title :
Investigating densities of Symbiodiniaceae in two species of Antipatharians (black corals) from Madagascar
Publication date :
25 November 2021
Journal title :
Oceans
eISSN :
2673-1924
Publisher :
MDPI
Volume :
2
Pages :
772–784
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
Fonds National de la Recherche Scientifique, Belgium: PDR T0083.18
Pyle R.L. Copus J.M. Mesophotic Coral Ecosystems: Introduction and Overview Coral Reefs World 2019 39 1469 1482
Baker E.K. Puglise K.A. Harris P.T. Mesophotic Coral Ecosystems—A Lifeboat for Coral Reefs? The United Nations Environment Programme and GRID-Arendal Arendal, Norway 2016
Gress E. Arroyo-Gerez M.J. Wright G. Andradi-Brown D.A. Assessing mesophotic coral ecosystems inside and outside a Caribbean marine protected area R. Soc. Open Sci. 2018 5 180835 10.1098/rsos.180835
Brugler M.R. Opresko D.M. France S.C. The evolutionary history of the order Antipatharia (Cnidaria: Anthozoa: Hexacorallia) as inferred from mitochondrial and nuclear DNA: Implications for black coral taxonomy and systematics Zool. J. Linn. Soc. 2013 169 312 361 10.1111/zoj.12060
Opresko D.M. New species of black corals (Cnidaria: Anthozoa: Antipatharia) from the New Zealand region, part 2 N. Z. J. Zool. 2019 47 149 186 10.1080/03014223.2019.1650783
Grigg R.W. Ecological studies of Black Coral in Hawaii Pac. Sci. 1965 19 244 260
Wagner D. Luck D.G. Toonen R.J. The Biology and Ecology of Black Corals (Cnidaria: Anthozoa: Hexacorallia: Antipatharia) Adv. Mar. Biol. 2012 63 67 132 10.1016/b978-0-12-394282-1.00002-8
Goldberg W.M. Chemical changes accompanying maturation of the connective tissue skeletons of gorgonian and antipatharian corals Mar. Biol. 1978 49 203 210 10.1007/BF00391132
Goldberg W.M. Hopkins T.L. Holl S.M. Schaefer J. Kramer K.J. Morgan T.D. Kim K. Chemical composition of the sclerotized black coral skeleton (Coelenterata: Antipatharia): A comparison of two species Comp. Biochem. Physiol. Part B Biochem. 1994 107 633 643 10.1016/0305-0491(94)90197-X
Bo M. Montgomery A.D. Opresko D.M. Wagner D. Bavestrello G. Antipatharians of the Mesophotic Zone: Four Case Studies Coral Reefs of the World Springer Singapore 2019 683 708
Tazioli S. Bo M. Boyer M. Boyer M. Rotinsulu H. Bavestrello G. Ecological observations of some common antipatharian corals in the marine park of Bunaken (North Sulawesi, Indonesia) Zool. Stud. 2007 46 227 241
Suarez H.N. Dy D.T. Violanda R.R. Density of associated macrofauna of black corals (Anthozoa: Antipatharia) in Jagna, Bohol, central Philippines Philipp. J. Sci. 2015 144 107 115
Parrish F.A. Abernathy K. Marshall G.J. Buhleier B.M. Hawaiian monk seals (Monachus schauinslandi) foraging in deep-water coral beds Mar. Mammal. Sci. 2002 18 244 258 10.1111/j.1748-7692.2002.tb01031.x
Boland R.C. Parrish F.A. Description of Fish Assemblages in the Black Coral Beds off Lahaina, Maui, Hawai‘i Pac. Sci 2005 59 411 420 10.1353/psc.2005.0032
Bruckner A.W. Advances in Management of Precious Corals to Address Unsustainable and Destructive Harvest Techniques The Cnidaria, Past, Present and Future 1st ed. Goffredo S. Dubinsky Z. Springer International Publishing Cham, Switzerland 2016 747 786
Terrana L. Lepoint G. Eeckhaut I. Assessing trophic relationships between shallow-water black corals (Antipatharia) and their symbionts using stable isotopes Belg. J. Zool. 2019 149 107 121 10.26496/bjz.2019.33
Baker A.C. Glynn P.W. Riegl B. Climate change and coral reef bleaching: An ecological assessment of long-term impacts, recovery trends and future outlook Estuar. Coast Shelf. Sci. 2008 80 435 471 10.1016/j.ecss.2008.09.003
Hughes T.P. Kerry J.T. Simpson T. Large-scale bleaching of corals on the Great Barrier Reef Ecology 2018 99 501 10.1002/ecy.2092
Bongaerts P. Smith T.B. Beyond the “Deep Reef Refuge” Hypothesis: A Conceptual Framework to Characterize Persistence at Depth Springer Cham, Switzerland 2019 881 895
Fisher R. Bessell-Browne P. Jones R. Synergistic and antagonistic impacts of suspended sediments and thermal stress on corals Nat. Commun. 2019 10 2346 10.1038/s41467-019-10288-9
Lajeunesse T.C. Parkinson J. Gabrielson P.W. Jeong H.J. Reimer J.D. Voolstra C.R. Santos S.R. Systematic Revision of Symbiodiniaceae Highlights the Antiquity and Diversity of Coral Endosymbionts Curr. Biol. 2018 28 2570 2580.e6 10.1016/j.cub.2018.07.008
Meistertzheim A.-L. Pochon X. Wood S.A. Ghiglione J.-F. Hédouin L. Development of a quantitative PCR–high-resolution melting assay for absolute measurement of coral-Symbiodiniaceae associations and its application to investigating variability at three spatial scales Mar. Biol. 2019 166 13 10.1007/s00227-018-3458-0
Davy S.K. Allemand D. Weis V. Cell Biology of Cnidarian-Dinoflagellate Symbiosis Microbiol. Mol. Biol Rev. 2012 76 229 261 10.1128/MMBR.05014-11
Brodersen K.E. Lichtenberg M. Ralph P. Kühl M. Wangpraseurt D. Radiative energy budget reveals high photosynthetic efficiency in symbiont-bearing corals J. R. Soc. Interface 2014 11 20130997 10.1098/rsif.2013.0997
Roth M.S. The engine of the reef: Photobiology of the coral-algal symbiosis Front. Microbiol. 2014 5 422 10.3389/fmicb.2014.00422
Roth M. Padilla-Gamiño J. Pochon X. Bidigare R. Gates R. Smith C. Spalding H. Fluorescent proteins in dominant mesophotic reef-building corals Mar. Ecol. Prog. Ser. 2015 521 63 79 10.3354/meps11108
Weis V.M. Cellular mechanisms of Cnidarian bleaching: Stress causes the collapse of symbiosis J. Exp. Biol. 2008 211 3059 3066 10.1242/jeb.009597
Lesser M.P. Oxidative stress in marine environments: Biochemistry and physiological ecology Annu. Rev. Physiol. 2006 68 253 278 10.1146/annurev.physiol.68.040104.110001
Barott K.L. Venn A.A. Perez S.O. Tambutté S. Tresguerres M. Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis Proc. Natl. Acad. Sci. USA 2015 112 607 612 10.1073/pnas.1413483112
Brook G. Report on the Antipatharia collected by HMS Challenger during the years 1873–1876. Report on the Scientific Results of the Voyage of HMS Challenger During the Years 1873–76 Zoology 1889 32 1 222 10.5962/bhl.title.6513
van Pesch A.J. The Antipatharia of the Siboga Expedition Siboga Exped. Monogr. 1914 17 1 258
Wagner D. Pochon X. Irwin L. Toonen R. Gates R.D. Azooxanthellate? Most Hawaiian black corals contain Symbiodinium Proc. R. Soc. B Biol. Sci. 2010 278 1323 1328 10.1098/rspb.2010.1681
Grigg R.W. A Contribution to the Biology and Ecology of the Black Coral, Antipathes grandis in Hawai‘i. MS Thesis in Zoology, 1964, p. 74. Hawai‘i., Honolulu Available online: http://cn.deziderkostrec.xyz/read/?id=Qv7PHAAACAAJ&format=pdf&server=1 (accessed on 2 April 2019)
Santiago-Vázquez L.Z. Brück T.B. Brück W.M. Duque-Alarcón A.P. McCarthy P.J. Kerr R.G. Br T.B. The diversity of the bacterial communities associated with the azooxanthellate hexacoral Cirrhipathes lutkeni ISME J. 2007 1 654 659 10.1038/ismej.2007.77
Bo M. Baker A. Gaino E. Wirshing H. Scoccia F. Bavestrello G. First description of algal mutualistic endosymbiosis in a black coral (Anthozoa: Antipatharia) Mar. Ecol. Prog. Ser. 2011 435 1 11 10.3354/meps09228
McFadden C.S. Quattrini A.M. Brugler M.R. Cowman P.F. Dueñas L.F. Kitahara M.V. A. Paz-García D. Reimer J.D. Pichon M. Recherches sur les peuplements à dominance d’anthozoaires dans les récifs coralliens de Tuléar (Madagascar) Atoll Res. Bull. 1978 222 1 490
Harris A. Manahira G. Sheppard A. Gouch C. Sheppard C. Demise of Madagascar’s once great barrier reef: Changes in coral reef conditions over 40 years Atoll Res. Bull. 2010 574 1 16 10.5479/si.00775630.574.16
Todinanahary G. Terrana L. Lavitra T. First records of illegal harvesting and trading of black corals (Antipatharia) in Madagascar Madag. Conserv. Dev. 2016 11 1 6 10.4314/mcd.v11i1.5
Todinanahary G.G. Refoty M.E. Terrana L. Lavitra T. Eeckhaut I. Previously unlisted scleractinian species recorded from the Great Reef of Toliara, southwest Madagascar West. Indian Ocean J. Mar. Sci. 2018 17 67 10.4314/wiojms.v17i2.6
Gudka M. Obura D. Mwaura J. Porter S. Yahya S. Mabwa R. Impact of the 3rd Global Coral Bleaching Event on the Western Indian Ocean in 2016 Global Coral Reef Monitoring Network (GCRMN)/Indian Ocean Commission Port Louis, Mauritius 2016 67
Zhang T. Fell F. An empirical algorithm for determining the diffuse attenuation coefficient Kd in clear and turbid waters from spectral remote sensing reflectance Limnol. Oceanogr. Methods 2007 5 457 462 10.4319/lom.2007.5.457
Zamoum T. Furla P. Symbiodinium isolation by NaOH treatment J. Exp. Biol. 2012 215 3875 3880 10.1242/jeb.074955
R Core Team R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing Vienna, Austria 2019 Available online: https://www.R-project.org/ (accessed on 2 April 2019)
Stat M. Pochon X. Cowie R. Gates R. Specificity in communities of Symbiodinium in corals from Johnston Atoll Mar. Ecol. Prog. Ser. 2009 386 83 96 10.3354/meps08080
Hume B.C. Ziegler M. Poulain J. Pochon X. Romac S. Boissin E. De Vargas C. Planes S. Wincker P. Voolstra C.R. An improved primer set and amplification protocol with increased specificity and sensitivity targeting the Symbiodinium ITS2 region PeerJ 2018 6 e4816 10.7717/peerj.4816
Mutahir Z. Mekasha S. Loose J.S.M. Abbas F. Vaaje-Kolstad G. Eijsink V.G.H. Forsberg Z. Characterization and synergistic action of a tetra-modular lytic polysaccharide monooxygenase from Bacillus cereus FEBS Lett. 2018 592 2562 2571 10.1002/1873-3468.13189
Pettay D.T. Wham D.C. Smith R.T. Iglesias-Prieto R. LaJeunesse T.C. Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella Proc. Natl. Acad. Sci. USA 2015 112 7513 7518 10.1073/pnas.1502283112 26034268
Holden H. Characterisation of Optical Water Quality in Bunaken National Marine Park, Indonesia Singap. J. Trop. Geogr. 2002 23 23 36 10.1111/1467-9493.00116