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Zoanthids of the Cape Verde Islands and Their Symbionts: Previously Unexamined Diversity in the Northeastern Atlantic

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Zoanthids of the Cape Verde Islands and Their Symbionts: Previously Unexamined Diversity in the Northeastern Atlantic Contributions to Zoology, 79 (4) 147-163 (2010) Zoanthids of the Cape Verde Islands and their symbionts: previously unexamined diversity in the Northeastern Atlantic James D. Reimer1, 2, 4, Mamiko Hirose1, Peter Wirtz3 1 Molecular Invertebrate Systematics and Ecology Laboratory, Rising Star Program, Transdisciplinary Research Organization for Subtropical Island Studies (TRO-SIS), University of the Ryukyus, Senbaru 1, Nishihara, Okinawa 903-0213, Japan 2 Marine Biodiversity Research Program, Institute of Biogeosciences, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), 2-15 Natsushima, Yokosuka, Kanagawa 237-0061, Japan 3 Centro de Ciências do Mar, Universidade do Algarve, Campus de Gambelas, PT 8005-139 Faro, Portugal 4 E-mail: [email protected] Key words: Cape Verde Islands, Cnidaria, Symbiodinium, undescribed species, zoanthid Abstract Symbiodinium ITS-rDNA ..................................................... 155 Discussion ...................................................................................... 155 The marine invertebrate fauna of the Cape Verde Islands con- Suborder Brachycnemina .................................................... 155 tains many endemic species due to their isolated location in the Suborder Macrocnemina ...................................................... 157 eastern Atlantic, yet research has not been conducted on most Conclusions ............................................................................. 158 taxa here. One such group are the zoanthids or mat anemones, Acknowledgements ...................................................................... 158 an order of benthic cnidarians (Hexacorallia: Zoantharia) com- References ...................................................................................... 158 mon in many marine environments. In this study, the diversity Appendix ......................................................................................... 161 of zoanthids in the Cape Verde Islands is specifically examined for the first time. Field images and sampling are combined with molecular phylogenetic analyses utilizing two mitochondrial Introduction DNA markers (cytochrome oxidase subunit I and 16S ribos- omal DNA) to determine the number of species present. Speci- mens from eight species (Palythoa caribaeorum, Palythoa sp. Zoanthids are an order of benthic anthozoans found in 265, Zoanthus aff. pulchellus, Isaurus tuberculatus, Parazoan- most marine environments. Despite their presence in thus sp. 269, Parazoanthus sp. 1401, Antipathozoanthus maca- most marine ecosystems, zoanthids remain a taxo- ronesicus, Terrazoanthus sp. 276) were identified, including nomically neglected group due to a relatively simple two to four species that are likely new to science. Additional body plan, a lack of proven species-level diagnostic examinations of Symbiodinium endosymbionts in zooxanthel- late species showed that clades A, B, and C were present; this is morphological characteristics, high levels of intraspe- the first report of clade B associating with a zoanthid species. cific variation (Burnett et al., 1997; Reimer et al., An appendix describing the eight zoanthid species found in the 2004), and encrustations of sand and detritus in their Cape Verde Islands is included to provide a base for future mesoglea (body walls) making internal examinations zoanthid research in this region. very problematic (discussed in Reimer et al., 2010). Thus, with a lack of information, overall levels of spe- cies diversity remain unknown (Burnett et al., 1997; Contents Reimer et al., 2004). However, recent examinations of zoanthids from Introduction ................................................................................... 147 many different locations such as Australia (Burnett Material and methods .................................................................. 151 Specimen collection and initial identification ................ 151 et al., 1997), the Galapagos Islands (Reimer et al., Specimen nomenclature ........................................................ 151 2008c; Reimer and Hickman, 2009), Japan (Reimer, DNA extraction, PCR Amplification, and sequencing .. 151 2007), New Caledonia (Sinniger, 2006), Singapore Phylogenetic analyses ........................................................... 151 (Reimer and Todd, 2009), and the Caribbean (Swain, Results ............................................................................................. 152 2009) have shown that a combination of careful in In situ morphological zoanthid identification ................. 152 DNA sequence and phylogenetic identification - situ observation of substrate and habitat along with mt 16S rDNA ............................................................................ 154 the utilization of molecular techniques can accurate- COI ............................................................................................ 154 ly ascertain taxonomic identifications and identify 148 ­­­Reimer et al. - Zoanthids of the Cape Verde Islands potential undescribed species. Furthermore, exami- and undescribed species are constantly being discov- nations from insular and more isolated oceanic re- ered (e.g. Opresko, 2003; Freitas and Castro, 2005; gions such as the Galapagos have demonstrated the Stokvis and van Ofwegen, 2006; Wirtz, 2009). Due to presence of potentially endemic or rarely known their isolated position about 600 km off the western zoanthids that were simply just in need of discovery tip of Africa, the Cape Verde Islands harbor numerous (Reimer and Fujii, 2010). endemic species (see the species lists mentioned The marine fauna and flora of the Cape Verde Is- above for examples). lands is much more tropical in character than the West Morri and Bianchi (1995), Morri et al. (2000), and African coast at the same latitude, where cold up- Monteiro et al. (2008) described epibenthic communi- welling occurs (Türkay, 1982). Morri et al. (2000) ties at Sal Island and recorded the depth distribution of gave a preliminary description of the marine zooge- Palythoa caribaeorum Duchassaing and Michelotti, ography of the Cape Verde Islands. As pointed out by 1864. There are two historical records of zoanthid spe- numerous authors (e.g. Laborel, 1974; Prud’homme cies in the Cape Verde Islands, which are mentioned van Reine and Van den Hoek, 1988; Wirtz, 2001 and later, in the discussion part of this manuscript. Other references therein), the marine fauna and flora of the recent records of zoanthids from the Cape Verde Is- Cape Verde Islands shows a strong amphi-atlantic lands include 1) xanthid crabs associated with Paly- component. The molluscs (Rolán, 2005), fish (Reiner, thoa (Den Hartog and Holthuis, 1984; Den Hartog and 1996; Brito et al., 1999) and some selected groups of Türkay, 1991), 2) a mention of Zoanthus and Palythoa Hexacorallia (Boekschoten and Borel Best, 1988) are in Van der Land (1993), 3) a photo of Isaurus tubercu- some marine groups reasonably well studied. Türkay latus Gray, 1828 by the third author, taken near Tar- (1982) and Wirtz and D'Udekem d'Acoz (2001) sum- rafal, Santiago Island (Wirtz and Debelius, 2003, page marized the state of knowledge on decapod crusta- 63, bottom left), and 4) several records discussing the ceans; Núñez et al. (2000) gave a preliminary list of presence of Antipathozoanthus macaronesicus Ocaña the polychaetes. Many other marine invertebrate and Brito, 2003 (Ocaña and Brito, 2003; Ocaña et al., groups lack comprehensive accounts and unrecorded 2007; Sinniger et al., 2010). W25° W20° W15° Nouakchott Ilhas de Barlavento Santo Antao Murdeira Sal Pedra de Lume Sao Vicente Sao Nicolau Santa Maria Cape Verde Tarrafal Boa Vista Islands locations Calheta de Sao Miguel Africa Santiago N15° Dakar to toven de So Ilhas North Atlantic Ocean Bissau 100 km Fig. 1. Map showing location of zoanthid specimen sampling sites in the Cape Verde Islands. Sampling location names in bold, island names in italics. Contributions to Zoology, Contributions79 (4) – 2010 to Zoology, Table 1. Zoanthid specimens from Cape Verde examined in this study, n/a = not available. specimen location collection habitat COI 16S Symbiodinium conclusion (identity) no. month accession no. accession no. clade 264 Tarrafal Bay, Santiago I. Aug. 07 tidal flat HM130482 HM130463 n/a Palythoa caribaeorum 265 Tarrafal Bay, Santiago I. Aug. 07 tidepool HM130481 HM130464 clade C HM130504 Palythoa sp. 265 266 Tarrafal Bay, Santiago I. Aug. 07 low tide line HM130486 HM130465 clade A HM130513 Zoanthus aff. pulchellus 267 Calheta de Sao Miguel, Santiago I. Aug. 07 tidepool HM130483 HM130466 clade C HM130503 Palythoa caribaeorum 268 Tarrafal Bay, Santiago I. Aug. 07 Tanacetipathes wirtzi HM130496 HM130467 n/a Antipathozoanthus macaronesicus (antipatharian) 269 Tarrafal Bay, Santiago I. Aug. 07 inside cave, on sponge HM130497 HM130468 n/a Parazoanthus sp. 269 270 Tarrafal Bay, Santiago I. Aug. 07 tidepool HM130492 HM130469 clade A HM130506 Zoanthus aff. pulchellus 271 Tarrafal Bay, Santiago I. Aug. 07 low tide line HM130487 n/a clade A HM130510 Zoanthus aff. pulchellus 272 Tarrafal Bay, Santiago I. Aug. 07 low tide line HM130488 n/a clade A HM130507 Zoanthus aff. pulchellus 273 Santa Maria, Sal I. Aug. 07 20 m HM130484 HM130470 clade A HM130502 Palythoa caribaeorum 274 Pedra de Lume, Sal I. Aug. 07 tidepool HM130489 HM130471 clade A HM130509 Zoanthus aff. pulchellus 275 Pedra de Lume, Sal I. Aug. 07 tidepool HM130490 HM130472 clade A HM130508 Zoanthus aff. pulchellus 276 Murdeira,
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