Abstract
In this study, a zoantharian specimen was found associated with a gorgonian colony of the genus Nicella (Anthozoa, Octocorallia), representing the first zoantharian-octocoral association reported from the southwestern Atlantic. Unexpectedly, phylogenetic analyses of mitochondrial (COI and mt 16S rDNA) and nuclear (ITS-rDNA) markers assigned the specimen to the widely distributed species Parazoanthus cf. swiftii, known until now to associate exclusively with sponges (Porifera). In the sampled locality (Alcatrazes Archipelago, São Paulo State), P. cf. swiftii has been observed to associate with both sponges and octocoral. We review the literature and discuss the specificity of biotic substrate associations in Zoantharia and suggest that many interactions may not be as host-specific as previously thought. Such flexibility in habitat choice may provide the mechanisms that have allowed zoantharians to adapt and associate with a wide range of invertebrate hosts across evolutionary time scales.
References
Aued AW, Smith F, Quimbayo JP, Candido DV, Longo GO, Ferreira CEL, Witman JD, Floeter SR, Segal B (2018) Large-scale patterns of benthic marine communities in the Brazilian Province. PLoS ONE 13:1–15
Bayer FM, Grasshoff M (1995) Two new species of the gorgonacean genus Ctenocella (Coelenterata: Anthozoa, Octocorallia) from deep reefs in the western Atlantic. Bull Mar Sci 56:625–652
Bertoloni A (1819) Amoenitates Italicae, Sistentes Opuscula ad Rem Herbariam et Zoologiam Italiae Spectantia. Bononiae
Bo M, Lavorato A, Di Camillo CG, Poliseno A, Baquero A, Bavestrello G, Irei Y, Reimer JD (2012) Black coral assemblages from Machalilla National Park (Ecuador). Pac Sci 66:63–82
Burnett WJ, Benzie JAH, Beardmore JA, Ryland JS (1997) Zoanthids (Anthozoa, Hexacorallia) from the great barrier reef and Torres Strait, Australia: systematics, evolution and a key to species. Coral Reefs 16:55–68
Cairns SD (2007) Studies on western Atlantic Octocorallia (Gorgonacea: Ellisellidae). Part 7: the genera Riisea Duchassaing & Michelotti, 1860 and Nicella Gray, 1870. Proc Biol Soc Wash 120:1–38
Carlgren O (1913) Zoantharia. Dan Ingolf-Exp 5(4):1–64
Carlgren O (1945) Polypdyr (Coelenterata). III. Koraldyr. Danamarks Fauna, 51 BD. Kobenhavn. pp 168
Carreiro-Silva M, Braga-Henriques A, Sampaio I, de Matos V, Porteiro FM, Ocaña O (2010) Isozoanthus primnoidus, a new species of zoanthid (Cnidaria: Zoantharia) associated with the gorgonian Callogorgia verticillata (Cnidaria: Alcyonacea). ICES J Mar Sci 68:408–415
Carreiro-Silva M, Ocaña O, Stanković D, Sampaio Í, Porteiro FM, Fabri MC, Stefanni S (2017) Zoantharians (Hexacorallia: Zoantharia) associated with cold-water corals in the Azores region: new species and associations in the deep sea. Front Mar Sci 4:88
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
Cerrano C, Danovaro R, Gambi C, Pusceddu A, Riva A, Schiaparelli S (2010) Gold coral (Savalia savaglia) and gorgonian forests enhance benthic biodiversity and ecosystem functioning in the mesophotic zone. Biodivers Conserv 19:153–167
Cutress C, Pequegnat W (1960) Three new Zoantharia from California. Pac Sci 14:89–100
Danielssen DC (1890) Actinida. Grøndahl & Søns Bogtrykkeri, Kristiana
Darriba D, Taboada GL, Doallo R, Posada D (2012) JModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772
Dons C (1944) Norges korallrev. Det K Norske Vidensk Selsk Forhandl 16:37–82
Duchassaing de Fonbressin P, Michelotti G (1860) Memoir sur les corralliares des Antilles. Imprimerie Royale, Turin
Duerden JE (1898) Jamaican Actiniaria. Part I.—Zoantheae. Sci Trans R Dublin Soc 6:329–384
Duerden JE (1903) West Indian sponge incrusting actinians. Bull Am Mus Nat Hist 19:495–503 pls. 44–47
Francini-filho RB, De Moura RL (2010) Predation on the toxic zoanthid Palythoa caribaeorum by reef fishes in the Abrolhos Bank, eastern Brazil. Braz J Oceanogr 58:77–79
González-Muñoz R, Simões N, Guerra-Castro EJ, Hernández-Ortíz C, Carrasquel G, Mendez E, Lira C, Rada M, Hernández I, Pauls SM, Croquer A, Cruz-Motta JJ (2016) Sea anemones (Cnidaria: Actiniaria, Corallimorpharia, Ceriantharia, Zoanthidea) from marine shallow-water environments in Venezuela: new records and an updated inventory. Mar Biodivers Rec 9:18
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321
Haddon AC, Shackleton AM (1891) A revision of the British Actiniæ. Part II. Zoantheæ. Sci Trans R Dublin Soc 4:609–672
Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Hoeksema BW, Butôt R, García-Hernández JE (2018) A new host and range record for the gall crab Fungicola fagei as symbiont of the mushroom coral Lobactis scutaria at Hawai’i. Pac Sci 72:251–261
Katoh K, Rozewicki J, Yamada K (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166
Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649
Kise H, Maeda T, Reimer JD (2019) A phylogeny and the evolution of epizoism within the family Hydrozoanthidae with description of a new genus and two new species. Mol Phylogenet Evol 130:304–314
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Low MEY, Sinniger F, Reimer JD (2016) The order Zoantharia Rafinesque, 1815 (Cnidaria, Anthozoa: Hexacorallia): supraspecific classification and nomenclature. ZooKeys 641:1–80
Montenegro J, Acosta A (2010) Habitat preference of Zoantharia genera depends on host sponge morphology. Univ Sci 15:110–121
Montenegro J, Sinniger F, Reimer JD (2015) Unexpected diversity and new species in the sponge-Parazoanthidae association in southern Japan. Mol Phylogenet Evol 89:73–90
Montenegro J, Low MEY, Reimer JD (2016) The resurrection of the genus Bergia (Anthozoa, Zoantharia, Parazoanthidae). Syst Biodivers 14:63–73
Muirhead A, Tyler PA, Thurston MH (1986) Reproductive biology and growth of the genus Epizoanthus (Zoanthidea) from the north-East Atlantic. J Mar Biol Assoc UK 66:131–143
Ocaña O, Brito A (2004) A review of Gerardiidae (Anthozoa: Zoantharia) from the Macaronesian islands and the Mediterranean Sea with the description of a new species. Rev Acad CanarCienc 15:159–189
Ocaña O, Brito A, Núñez J, Bacallado JJ (1995) Redescripción de Geradia savaglia (Bertoloni, 1819) (Anthozoa: Zoantharia: Gerardiidae). Vieraea 24:153–164
Oigman-Pszczol SS, Figueiredo MADO, Creed JC (2004) Distribution of benthic communities on the tropical rocky subtidal of Armação dos Búzios, southeastern Brazil. Mar Ecol 25:173–190
Ong CW, Reimer JD, Todd PA (2013) Morphologically plastic responses to shading in the zoanthids Zoanthus sansibaricus and Palythoa tuberculosa. Mar Biol 160:1053–1064
Pérez CD, Vila-Nova DA, Santos AM (2005) Associated community with the zoanthid Palythoa caribaeorum (Duchassaing & Michelotti, 1860) (Cnidaria, Anthozoa) from littoral of Pernambuco, Brazil. Hydrobiologia 548:207–215
Reimer JD, Fujii T (2010) Four new species and one new genus of zoanthids (Cnidaria, Hexacorallia) from the Galápagos Islands. ZooKeys 42:1–36
Reimer JD, Takishita K, Ono S, Tsukahara J, Maruyama T (2007) Molecular evidence suggesting interspecific hybridization in Zoanthus spp. (Anthozoa: Hexacorallia). Zool Sci 24:346–359
Reimer JD, Nonaka M, Sinniger F, Iwase F (2008a) Morphological and molecular characterization of a new genus and new species of parazoanthid (Anthozoa: Hexacorallia: Zoantharia) associated with Japanese red coral. Coral Reefs 27:935–949
Reimer JD, Sinniger F, Hickman CP Jr (2008b) Zoanthid diversity (Anthozoa: Hexacorallia) in the Galapagos Islands: a molecular examination. Coral Reefs 27:641–654
Reimer JD, Lorion J, Irei Y, Hoeksema BW, Wirtz P (2014) Ascension Island shallow-water Zoantharia (Hexacorallia: Cnidaria) and their zooxanthellae (Symbiodinium). J Mar Biol Assoc UK 97(4):695–703
Reimer JD, Wee HB, García-Hernández JE, Hoeksema BW (2018) Zoantharia (Anthozoa: Hexacorallia) abundance and associations with Porifera and Hydrozoa across a depth gradient on the west coast of Curaçao. Syst Biodivers 16:820–830
Reimer JD, Kise H, Santos MEA et al (2019) Exploring the biodiversity of understudied benthic taxa at mesophotic and deeper depths: examples from the order Zoantharia (Anthozoa: Hexacorallia). Front Mar Sci 6:305
Risi M, Macdonald AH (2016) Molecular examination of rocky shore brachycnemic zoantharians (Anthozoa: Hexacorallia) and their Symbiodiniun symbionts (Dinophyceae) in the Southwest Indian Ocean. Mar Biodivers 46:113–127
Rodríguez F, Oliver JL, Marín A, Medina JR (1990) The general stochastic model of nucleotide substitution. J Theor Biol 142:485–501
Ronquist F, Teslenko M, Van Der Mark P et al (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542
Santana EFC, Alves AL, Santos ADM, Maria Da Gloria GS, Perez CD, Gomes PB (2015) Trophic ecology of the zoanthid Palythoa caribaeorum (Cnidaria: Anthozoa) on tropical reefs. J Mar Biol Assoc UK 95:301–309
Santos MEA, Kitahara MV, Lindner A, Reimer JD (2016) Overview of the order Zoantharia (Cnidaria: Anthozoa) in Brazil. Mar Biodivers 46:547–559
Sinniger F, Montoya-Burgos JI, Chevaldonné P, Pawlowski J (2005) Phylogeny of the order Zoantharia (Anthozoa, Hexacorallia) based on the mitochondrial ribosomal genes. Mar Biol 147:1121–1128
Sinniger F, Reimer JD, Pawlowski J (2010) The Parazoanthidae (Hexacorallia: Zoantharia) DNA taxonomy: description of two new genera. Mar Biodivers 40:57–70
Sinniger F, Ocaña OV, Baco AR (2013) Diversity of zoanthids (Anthozoa: Hexacorallia) on Hawaiian seamounts: description of the Hawaiian gold coral and additional zoanthids. PLoS ONE 8:e52607
Stampar SN, Francisco P, Luiz OJ Jr (2007) Predation on the zoanthid Palythoa caribaeorum (Anthozoa, Cnidaria) by a hawksbill turtle (Eretmochelys imbricata) (Reptilia, Vertebrata) in southeastern Brazil. Mar Turtle Newsl 117:3–5
Swain TD (2009) Phylogeny-based species delimitations and the evolution of host associations in symbiotic zoanthids (Anthozoa, Zoanthidea) of the wider Caribbean region. Zool J Linnean Soc 156:223–238
Swain TD (2010) Evolutionary transitions in symbioses: dramatic reductions in bathymetric and geographic ranges of Zoanthidea coincide with loss of symbioses with invertebrates. Mol Ecol 19:2587–2598
Swain TD, Wulff JL (2007) Diversity and specificity of Caribbean sponge – zoanthid symbioses: a foundation for understanding the adaptive significance of symbioses and generating hypotheses about higher-order systematics. Biol J Linn Soc 92:695–711
Swain TD, Strimaitis AM, Reuter KE, Boudreau W (2017) Towards integrative systematics of Anthozoa (Cnidaria): evolution of form in the order Zoanthidea. Zool Scr 46:227–244
West DA (1979) Symbiotic zoanthids (Anthozoa: Cnidaria) of Puerto Rico. Bull Mar Sci 29:253–271
Acknowledgments
We thank Ralf Cordeiro for his help in the analyses and generic assignment of the octocoral. MVK thanks the support of FAPESP (2014/01332-0) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (301436/2018-5). The first author was supported by a PhD scholarship from Conselho Nacional de Desenvolvimento Científico e Tecnológico (142149/2018-7). CFV, AEM, and MVK are grateful for the support from Kelen Leite and Silvia Godoy (ICMBio). The editor and two anonymous reviewers are thankful for comments that improved an earlier version of this manuscript.
Funding
This study was funded by Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP) (grant number 2014/01332-0 to MVK) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (grant number 301436/2018-5 to MVK and grant number 142149/2018-7 to CVF).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for animal testing, animal care, and use of animals were followed by the authors.
Sampling and field studies
All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities (ICMBio) and are mentioned in the acknowledgements.
Data availability
New sequences determined in the present study were deposited in the GenBank repository (accession numbers: MN545904, MN545740, MN563139). Accession numbers of already published and deposited in GenBank sequences used to build the alignments are listed in Online Resources 1.
Author Contribution
CFV and MVK conceived and designed research. CFV and AEM conducted the analyses. All authors contributed to the writing of the manuscript.
Additional information
Communicated by B. W. Hoeksema
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Vaga, C.F., Santos, M.E.A., Migotto, A.E. et al. Octocoral-associated Parazoanthus cf. swiftii from the southwestern Atlantic. Mar. Biodivers. 50, 17 (2020). https://doi.org/10.1007/s12526-020-01041-3
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12526-020-01041-3