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Unravelling the taxonomic identity of Ophiothela Verrill, 1867 (Ophiuroidea) along the Brazilian coast

Published online by Cambridge University Press:  24 April 2020

Renata A. S. Alitto Open the ORCID record for Renata A. S. Alitto [Opens in a new window] ,
Gabriela Granadier ,
Ana B. Christensen ,
Timothy O'Hara ,
Maikon Di Domenico  and
Michela Borges
Renata A. S. Alitto*
Affiliation:
Departamento de Biologia Animal, Universidade Estadual de Campinas, 13083-863, Campinas, Brazil
Gabriela Granadier
Affiliation:
Departamento de Biologia Animal, Universidade Estadual de Campinas, 13083-863, Campinas, Brazil
Ana B. Christensen
Affiliation:
Biology Department, Lamar University, 10037, Beaumont, USA
Timothy O'Hara
Affiliation:
Museum Victoria, GPO Box 666 Melbourne, Victoria, Australia
Maikon Di Domenico
Affiliation:
Centro de Estudos do Mar, Universidade Federal do Paraná, 83255976, Pontal do Paraná, Brazil
Michela Borges
Affiliation:
Museu de Zoologia da Universidade Estadual de Campinas, 13083-863, Campinas, Brazil
*
Author for correspondence: Renata A. S. Alitto, E-mail: renataalitto@gmail.com
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Abstract

Since 2012, when Ophiothela was first described in the Atlantic, there has been no consensus regarding its identification. It has been described as O. mirabilis, O. cf. mirabilis, O. danae, or only Ophiothela sp. In order to fill these gaps, our aim was to test if specimens from Brazil are Ophiothela mirabilis and/or Ophiothela danae. Syntypes from the Museum of Comparative Zoology and United States National Museum, Smithsonian Institution, were used. We examined species boundaries of the small six-rayed brittle star Ophiothela using independent character sets utilizing morphology (external morphology and morphometry) and molecular data (16S and COI). Concordance was found between the analyses indicating that Ophiothela sp. from Brazil (BR), Ophiothela mirabilis and Ophiothela danae are closely related. We suggest that O. danae should be considered as a junior synonym of O. mirabilis. A detailed description of O. mirabilis BR is presented using external morphology and microstructural ossicles (arm plates, vertebra, dental and oral plates). This description includes new diagnostic features, particularly regarding its microstructures: (i) transspondylous articulation (first record in Ophiotrichidae); (ii) eight smooth knobs on the dorsal surface of the vertebrae (to date only in Ophiothela); (iii) vertebrae with distal keel divided into two separate end processes matching the two large dorsal grooves proximally (first time in the literature); and (iv) an opening on both sides of the oral plate (as seen in other fissiparous species Ophiactis savignyi and Ophiocomella ophiactoides).

Keywords

Biodiversitybrittle starsfissiparousophiuroidstaxonomytransspondylous joint
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 100 , Issue 3 , May 2020 , pp. 413 - 426
Copyright
Copyright © Marine Biological Association of the United Kingdom 2020

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References

Alitto, RAS, Bueno, ML, Di Domenico, M and Borges, M (2016) Annotated checklist of echinoderms from Araçá Bay, Southeastern Brazil. Check List 12, 1–15.CrossRefGoogle Scholar
Alitto, RAS, Bueno, ML, Guilherme, PDB, Di Domenico, M, Christensen, AB and Borges, M (2018) Shallow-water brittle stars (Echinodermata: Ophiuroidea) from Araçá Bay (Southeastern Brazil), with spatial distribution considerations. Zootaxa 4405, 1–66.CrossRefGoogle Scholar
Alitto, RAS, Amaral, ACZ, Oliveira, LD, Serrano, H, Seger, KR, Guilherme, PDB, Di Domenico, M, Christensen, AB, Lourenço, LB, Tavares, M and Borges, M (2019) Atlantic West Ophiothrix spp. in the scope of integrative taxonomy: confirming the existence of Ophiothrix trindadensis Tommasi, 1970. PLoS ONE 14, e0210331.CrossRefGoogle ScholarPubMed
Araújo, JT, Soares, MdO, Matthews-Cascon, H and Monteiro, FAC (2018) The invasive brittle star Ophiothela mirabilis Verrill, 1867 (Echinodermata, Ophiuroidea) in the southwestern Atlantic: filling gaps of distribution, with comments on an octocoral host. Latin American Journal of Aquatic Research 46, 1123–1127.Google Scholar
Arribas, P, Andújar, C, Sánchez-Fernández, D, Abellán, P and Millán, A (2013) Integrative taxonomy and conservation of cryptic beetles in the Mediterranean region (Hydrophilidae). Zoologica Scripta 42, 182–200.CrossRefGoogle Scholar
Bumbeer, J and Rocha, RM (2016) Invading the natural marine substrates: a case study with invertebrates in South Brazil. Zoologia 33, 1–7.CrossRefGoogle Scholar
Clark, AM (1966) Notes on the family Ophiotrichidae (Ophiuroidea). Journal of Natural History 9, 637–655.CrossRefGoogle Scholar
Clark, AM (1976) Tropical epizoic echinoderms and their distribution. Micronesica 12, 111–117.Google Scholar
Clark, EG, Hutchinson, JR, Darroch, SAF, Mongiardino Koch, N, Brady, TR, Smith, SA and Briggs, DEG (2018) Integrating morphology and in vivo skeletal mobility with digital models to infer function in brittle star arms. Journal of Anatomy 233, 696–714.CrossRefGoogle ScholarPubMed
de Loriol, P (1900) Notes pour servir à l'étude des Echinodermes. VIII. Revue Suisse de Zoologie 1–686.Google Scholar
Devaney, DM (1970) Studies on Ophiocomid brittlestars. I. A new genus (Clarkcoma) of Ophiocominae with reevaluation of the genus Ophiocoma. Smithsonian Contributions to Zoology 51, 1–41.CrossRefGoogle Scholar
Di Camillo, CG, Gravulli, C, De Vito, D, Pica, D, Piraino, S, Puce, S and Cerrano, C (2018) The importance of applying Standardised Integrative Taxonomy when describing marine benthic organisms and collecting ecological data. Invertebrate Systematics 32, 794–802.CrossRefGoogle Scholar
Excoffier, L, Smouse, PE and Quattro, JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.Google ScholarPubMed
Felsenstein, J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle ScholarPubMed
Glynn, PW, Coffman, B, Primov, K, Renegar, DA, Gross, J, Blackwelder, P, Martinez, N, Dominguez, J, Vanderwoude, J and Riegl, BM (2019) Benthic ctenophore (Order Platyctenida) reproduction, recruitment, and seasonality in south Florida. Invertebrate Biology 138, e12256.CrossRefGoogle Scholar
Goloboff, PA and Catalano, SA (2016) TNT Version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics 32, 221–238.CrossRefGoogle Scholar
Granja-Fernández, R, Herrero-Pérezrul, MD, López-Pérez, RA, Hernández, L, Rodríguez-Zaragoza, FA, Jones, RW and Pineda-López, R (2014) Ophiuroidea (Echinodermata) from coral reefs in the Mexican pacific. ZooKeys 406, 101–145.CrossRefGoogle Scholar
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95⁄98⁄NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hart, MW and Podolsky, RD (2005) Mitochondrial DNA phylogeny and rates of larval evolution in Macrophiothrix brittlestars. Molecular Phylogenetics and Evolution 34, 438–447.CrossRefGoogle ScholarPubMed
Hendler, G (2005) Two new brittle star species of the genus Ophiothrix (Echinodermata: Ophiuroidea: Ophiotrichidae) from coral reefs in the southern Caribbean Sea, with notes on their biology. Caribbean Journal of Science 41, 583–599.Google Scholar
Hendler, G (2018) Armed to the teeth: a new paradigm for the buccal skeleton of brittle stars (Echinodermata: Ophiuroidea). Contributions in Science 526, 189–311.Google Scholar
Hendler, G and Brugneaux, SJ (2013) New records of brittle stars from French Guiana: Ophiactis savignyi and the alien species Ophiothela mirabilis (Echinodermata: Ophiuroidea). Marine Biodiversity Records 6, e113.CrossRefGoogle Scholar
Hendler, G, Migotto, ÁE, Ventura, CRR and Wilk, L (2012) Epizoic Ophiothela Brittle stars have invaded the Atlantic. Coral Reefs 31, 1005.CrossRefGoogle Scholar
Hoareau, TB and Boissin, E (2010) Design of phylum-specific hybrid primers for DNA barcoding: addressing the need for efficient COI amplification in the Echinodermata. Molecular Ecology Resources 10, 960–967.CrossRefGoogle ScholarPubMed
Hotchkiss, FHC and Glass, A (2012) Observations on Onychaster Meek & Worthen, 1868 (Ophiuroidea: Onychasteridae) (Famennian–Visean age). In Kroh, A and Reich, M (eds), Echinoderm Research 2010: Proceedings of the Seventh European Conference on Echinoderms, Göttingen, Germany 2–9 October 2010. Auckland: Magnolia Press, Zoosymposia, pp. 121–138.Google Scholar
Hotchkiss, FHC, Prokop, RJ and Petr, V (2007) Isolated ossicles of the family Eospondylidae Spencer et Wright, 1966, in the Lower Devonian of Bohemia (Czech Republic) and correction of the systematic position of Eospondylid brittle-stars (Echinodermata: Ophiuroidea: Oegophiurida). Acta Musei Nationalis Pragae 63, 3–18.Google Scholar
Koehler, R (1905) Ophiures de l'expédition du Siboga. Leiden: Librairie et imprimerie ci-devant E. J. Brill.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Lawley, JW, Fonseca, AC, Júnior, EF and Lindner, A (2018) Occurrence of the non-indigenous brittle star Ophiothela cf. mirabilis Verrill, 1867 (Echinodermata, Ophiuroidea) in natural and anthropogenic habitats off Santa Catarina, Brazil. Check List (Luis Felipe Toledo) 14, 453–459.CrossRefGoogle Scholar
Leigh, JW and Bryant, D (2015) Popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.CrossRefGoogle Scholar
Litvinova, NM (1994) The life forms of Ophiuroidea (based on the morphological structures of their arms). In David, B, Guille, A and Feral, JP (eds), Echinoderms Through Time. Rotterdam: Balkema, pp. 449–454.Google Scholar
Lyman, T (1871) Supplement to the Ophiuridae and Astrophytidae Illustrated Catalogue of the Museum of Comparative Zoology at Harvard College 6, 1–17.Google Scholar
Mantelatto, MC, Vidon, LF, Silveira, SB, Menegola, C, Rocha, RM and Creed, JC (2016) Host species of the non-indigenous brittle star Ophiothela mirabilis (Echinodermata: Ophiuroidea): an invasive generalist in Brazil? Marine Biodiversity Records 9, 1–7.CrossRefGoogle Scholar
Marinho, CF, Cônsoli, FL, Penteado-Dias, AM and Zucchi, RA (2017) Description of two new species closely related to Doryctobracon areolatus (Szépligeti, 1911) (Hymenoptera, Braconidae), based on morphometric and molecular analyses. Zootaxa 4353, 467–484.CrossRefGoogle Scholar
Martynov, A (2010) Reassessment of the classification of the Ophiuroidea (Echinodermata), based on morphological characters. I. General character evaluation and delineation of the families Ophiomyxidae and Ophiacanthidae. Zootaxa 2697, 1–154.CrossRefGoogle Scholar
Matsumoto, H (1917) A monograph of Japanese Ophiuroidea, arranged according to a new classification. Journal of the College Science, Imperial University Tokyo 38, 1–408.Google Scholar
Mladenov, PV (1996) Environmental factors influencing asexual reproductive processes in echinoderms. Oceanologica Acta 19, 227–235.Google Scholar
Mortensen, T (1913) On the alleged primitive ophiuroid Ophioteresis elegans Bell, with description of a new species of Ophiothela. Mindeskrift for Japetus Steenstrup. Bianco Lunos Bogtrykkeri: Copenhagen 1, 1–26.Google Scholar
Nielsen, E (1932) Papers from Dr Th. Mortensen's Pacific Expedition 1914–1916 - 59. - Ophiurans from the Gulf of Panama, California, and the Strait of Georgia. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening 91, 241–346.Google Scholar
Nylander, JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.Google Scholar
O'Hara, TD, Hugall, AF, Thuy, B, Stöhr, S and Martynov, AV (2017) Restructuring higher taxonomy using broad-scale phylogenomics: the living Ophiuroidea. Molecular Phylogenetics and Evolution 107, 415–430.CrossRefGoogle ScholarPubMed
O'Hara, TD, Stöhr, S, Hugall, AF, Thuy, B and Martynov, A (2018) Morphological diagnoses of higher taxa in Ophiuroidea (Echinodermata) in support of a new classification. European Journal of Taxonomy 416, 1–35.Google Scholar
O'Hara, TD, Hugall, AF, Cisternas, PA, Boissin, E, Bribiesca-Contreras, G, Sellanes, J, Paulay, G and Byrne, M (2019) Phylogenomics, life history and morphological evolution of ophiocomid brittlestars. Molecular Phylogenetics and Evolution 130, 67–80.CrossRefGoogle ScholarPubMed
Padial, JM, Miralles, A, De la Riva, I and Vences, M (2010) The integrative future of taxonomy. Frontiers in Zoology 7, 1–14.CrossRefGoogle ScholarPubMed
Palumbi, S, Martin, A, Romano, S, McMillan, WO, Stice, L and Grabowski, G (1991) The simple fool's guide to PCR, version 2.0, privately published document compiled by S. Palumbi. Department of Zoology and Kewalo Marine Laboratory 96822, 1–45.Google Scholar
Pérez-Portela, R, Almada, V and Turon, X (2013) Cryptic speciation and genetic structure of widely distributed brittle stars (Ophiuroidea) in Europe. Zoologica Scripta 42, 151–169.CrossRefGoogle Scholar
R Development Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.CrossRefGoogle ScholarPubMed
Spalding, MD, Fox, HE, Allen, GR, Davidson, N, Ferdaña, ZA, Finlayson, M, Halpern, BS, Jorge, MA, Lombana, A and Lourie, SA (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. BioScience 57, 573–583.CrossRefGoogle Scholar
Stöhr, S, Conand, C and Boissin, E (2008) Brittle stars (Echinodermata: Ophiuroidea) from La Réunion and the systematic position of Ophiocanops Koehler, 1922. Zoological Journal of the Linnean Society 153, 545–560.CrossRefGoogle Scholar
Stöhr, S, O'Hara, TD and Thuy, B (2012) Global diversity of brittle stars (Echinodermata: Ophiuroidea). PLoS ONE 7, e31940.CrossRefGoogle Scholar
Stöhr, S, O'Hara, TD and Thuy, B (2019) World Ophiuroidea Database. http://www.marinespecies.org/ophiuroidea.Google Scholar
Taboada, S and Pérez-Portela, R (2016) Contrasted phylogeographic patterns on mitochondrial DNA of shallow and deep brittle stars across the Atlantic-Mediterranean area. Scientific Reports 6, 32425.CrossRefGoogle ScholarPubMed
Thuy, B and Stöhr, S (2011) Lateral arm plate morphology in brittle stars (Echinodermata: Ophiuroidea): new perspectives for ophiuroid micropalaeontology and classification. Zootaxa 3013, 1–47.CrossRefGoogle Scholar
Thuy, B and Stöhr, S (2016) A new morphological phylogeny of the Ophiuroidea (Echinodermata) accords with molecular evidence and renders microfossils accessible for cladistics. PLoS ONE 11, e0156140.CrossRefGoogle ScholarPubMed
Venables, WN and Ripley, BD (2002) Random and mixed effects. In Modern Applied Statistics with S. New York, NY: Springer, pp. 271–300.CrossRefGoogle Scholar
Verrill, AE (1867) Notes on the Radiata in the Museum of Yale College, with descriptions of new genera and species. Transactions of the Connecticut Academy of Arts and Sciences 1, 247–351.Google Scholar
Verrill, AE (1869) On new and imperfectly known echinoderms and corals. Proceedings of the Boston Society of Natural History 12, 381–391.Google Scholar
Viana, FS (2010) Taxonomia das Famílias Ophiotrichidae, Ophiocomidae e Ophionereididae (Echinodermata: Ophiuroidea) presentes na região entre Salvador/BA (13°S) e o Cabo de São Tomé/RJ(22°S). (Master dissertation), Universidade Federal do Rio de Janeiro, Rio de Janeiro.Google Scholar
Weber, AA-T, Stöhr, S and Chenuil, A (2019) Species delimitation in the presence of strong incomplete lineage sorting and hybridization: lessons from Ophioderma (Ophiuroidea: Echinodermata). Molecular Phylogenetics and Evolution 131, 138–148.CrossRefGoogle Scholar
Wickham, H (2009) Elegant Graphics for Data Analysis (ggplot2). New York, NY: Springer-Verlag.Google Scholar
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