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Calcareous Sponges from the French Polynesia (Porifera: Calcarea)

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Calcareous Sponges from the French Polynesia (Porifera: Calcarea) Zootaxa 4748 (2): 261–295 ISSN 1175-5326 (print edition) https://www.mapress.com/j/zt/ Article ZOOTAXA Copyright © 2020 Magnolia Press ISSN 1175-5334 (online edition) https://doi.org/10.11646/zootaxa.4748.2.3 http://zoobank.org/urn:lsid:zoobank.org:pub:661CD94A-130B-4BD8-B201-28B079815618 Calcareous sponges from the French Polynesia (Porifera: Calcarea) MICHELLE KLAUTAU1,5, MATHEUS VIEIRA LOPES1, BRUNA GUARABYRA1, ERIC FOLCHER2, MERRICK EKINS3 & CÉCILE DEBITUS4 1Universidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Zoologia, Av. Carlos Chagas Filho, 373, CEP 21941- 902, Rio de Janeiro, RJ, Brasil. 2IRD, centre de Nouméa, SEOH, BPA5, 98713 Nouméa cedex, New Caledonia 3Queensland museum, PO Box 3300, South Brisbane BC, Queensland 4101, Australia 4IRD-CNRS-UBO-IFREMER, UMR6539 LEMAR, IUEM, rue Dumont d’Urville, F29280 Plouzané, France 5Corresponding author. E-mail: [email protected] Abstract Although the French Polynesian reefs are among the most well studied reefs of the world, sponges are still poorly known, with only 199 species or OTUs of sponges having been described from French Polynesia, 167 at an OTU level and 32 at a species level. From those 199 species, just five are calcareous sponges. As it is possible that this number is underestimated, the aim of the present work was to study the diversity of calcareous sponges from French Polynesia. Hence, different French Polynesian archipelagos were surveyed by SCUBA from 3 to 60 m of depth. Identifications were performed using morphological and molecular (ITS and C-LSU) tools. We found a total of nine species of Calcarea, comprising five different genera. Five species are new to science: Clathrina fakaravae sp. nov., Clathrina huahineae sp. nov., Ernstia variabilis sp. nov., Leucascus digitiformis sp. nov., and Leucandra tahuatae sp. nov. With the present work, the number of identified sponges from French Polynesia at a species level increased from 32 to 41. The only calcareous sponge previously known from French Polynesia that was recollected by our group was Leucetta chagosensis. Our results suggest that the Eastern Indo-Pacific Realm shows more affinity with the Central and the Western Indo-Pacific Realms. Four species supported these affinities: Ascandra cf. crewsi, previously known only from Papua New Guinea, Leucascus simplex from South Australia, and Leucetta chagosensis and L. microraphis, both widespread species in the Indo-Pacific. These two Leucetta species, however, most likely represent species complexes. Once again the molecular markers ITS and C-LSU helped in the identification of calcareous sponges, showing how important is an integrative taxonomy. Although our work has increased in 250% (6 spp to 15 spp) the diversity of calcareous sponges in French Polynesia, it is most possible that this number is still underestimated. Key words: biodiversity, Clathrina fakaravae sp. nov., Clathrina huahineae sp. nov., Ernstia variabilis sp. nov., Leucascus digitiformis sp. nov., Leucandra tahuatae sp. nov., ITS, C-LSU Introduction French Polynesia is a group of 118 islands and several islets and motus around atolls in the Pacific Ocean, occupy- ing a marine area of 2,500 km2. The islands are grouped in six archipelagos: Marquesas Islands, Society Islands, Tuamotu Archipelago, Gambier Islands, and Austral Islands.These archipelagos are part of two provinces of the Eastern Indo-Pacific Realm, the Southeast Polynesia Province and the Marquesas Province. The French Polynesia reefs are among the most well studied reefs of the world (Salvat et al. 2008), nonethe- less, sponges are still poorly known (Kelly-Borges & Valentine 1995; Hall et al. 2013). Currently, only 26 species or OTUs of sponges are known from French Polynesia, five of them being calcareous sponges, i.e., sponges whose skeleton has calcium carbonate spicules: Lelapiella sphaerulifera Vacelet, 1977, Lepidoleucon inflatum Vacelet, 1967, Plectroninia radiata Vacelet, 1967, and Murrayona phanolepis Kirkpatrick, 1910 from Moorea (Society Is- lands Archipelago) and Takapoto (Tuamotu Archipelago) (Vacelet 1977), and Leucetta cf. chagosensis Dendy, 1913 from Moorea (Society Islands Archipelago) (Wörheide et al. 2002; Hall et al. 2013) and Rangiroa (Tuamotu Archi- pelago) (Wörheide et al. 2002). It is possible that this number is underestimated, as no expeditions were dedicated Accepted by J. Hooper: 24 Jan. 2020; published: 6 Mar. 2020 261 to study calcareous sponges before. Therefore, the aim of the present work was to study the diversity of calcareous sponges from French Polynesia. Materials and methods Specimens collection In the present study, calcareous sponges collected during the surveys of the different French Polynesian archi- pelagos: Society Islands (Mehetia, Tahiti, Moorea, Tetiaroa, Huahine, Raiatea and Bora-Bora), Marquesas Islands (Nuku Hiva, Ua Pou, Ua Huka, Tahuata, Hiva Oa, Fatu Hiva), Tuamotu-Gambier Islands (Anuanuraro, Hereher- etue, Tematangi, Tureia, Nukutavake, Tureia, Hao, Amanu, Marokau, Raroia, Makemo, Fakarava, Toau, Takaroa, Rangiroa, Tikehau, Makatea), and Austral Islands (Marotiri, Rapa, Raivavae, Tubuai, Rurutu, Rimatara and Maria Islands) (Debitus, 2009, 2011, 2013a, b) (Fig 1). The collections were performed by SCUBA from 3 to 60 m of depth. When possible, the sponges were photographed in situ and then fixed and preserved in ethanol 93%. All the specimens are deposited at the Museum National d’Histoire naturelle (Paris). FIGURE 1. Map of the study area. A—French Polynesia. B—Studied islands. Morphological analysis The sponges were analysed under a stereomicroscope and slides to analyse skeletal organisation and spicules fol- lowed standard procedures (Wörheide & Hooper 1999; Klautau & Valentine 2003). Spicule measurements were taken with an ocular micrometer and are presented in tabular form, featuring length and width (minimum [min], mean, standard deviation [SD] and maximum [max]). We measured a total of 20 spicules of each category, always searching for the apparent smallest and the biggest spicules and measuring randomly 18 spicules. Skeleton and spicule photographs were taken with a digital Canon camera coupled to a Zeiss Axioscop mi- croscope. Scanning electron microscopy (SEM) micrographs were taken at the Biology Institute of the UFRJ on a JSM-6510 SEM equipment. Spicule preparations for SEM followed Azevedo et al. (2015). Molecular analysis The genomic DNA was extracted by the guanidine/phenol-chloroform method (Sambrook, Fritsch & Maniatis 1989) or with a QIAamp DNA MiniKit (Qiagen) and stored at –20°C until amplification. For Calcinea, primers situated in the adjacent 18S and 28S regions were used to amplify and sequence the internal transcribed spacer (ITS) region, containing ITS1, the 5.8S rDNA and ITS2. The primers used were: fwd: 5’-TCATTTAGAGGAAGTAAAAGTCG- 3’ and rv: 5’-GTTAGTTTCTTTTCCTCCGCTT-3’ (Lôbo-Hajdu et al. 2004). For Calcaronea, we amplified the C- LSU region (Voigt & Wörheide 2016), using the primers fwd: 5′-GAAAAGCACTTTGAAAAGAGA-3′ (Voigt & Wörheide 2016) and rv: 5′-TCCGTGTTTCAAGACGGG-3′ (Chombard, Boury-Esnault & Tillier 1998). The PCR mix included 1X buffer (5X GoTaq Green Reaction Buffer Flexi, PROMEGA), 0.2 mM dNTP, 0.5 262 · Zootaxa 4748 (2) © 2020 Magnolia Press Klautau ET AL. μg/μL bovine serum albumin (BSA), 2.5 mM MgCl2, 0.33 μM of each primer, one unit of Taq DNA polymerase (Fermentas or PROMEGA) and 1 μL of DNA in a final volume of 15 μL. The PCR amplification consisted of one cycle of 4 min at 94 °C, 35 cycles of 1 min at 92 °C, 1 min at 48° or 50 °C and 1 min at 72 °C, followed by a final cycle of 6 min at 72 °C. Forward and reverse strands were sequenced in an ABI 3500 (Applied Biosystems) at the Biology Institute of the Universidade Federal do Riode Janeiro (UFRJ). All the sequences obtained were analysed and edited in the program GeneStudio and BLAST searches (http://www.ncbi.nlm.nih.gov/blast/) were performed to confirm their biological source. Sequences retrieved from the Genbank database were also used and are listed in Table 1 with those generated in this study. Sequences were aligned through the MAFFT v.7 online platform (Katoh & Standley 2013) with the strategy Q-INS-i (Katoh & Toh 2008), taking into consideration the secondary structure of ribosomal DNA. For the other parameters we chose the default option. The final alignment of the ITS sequences was 1230 bp, including gaps. A total of 480 conserved sites, 571 variable sites, and 138 singletons were retrieved. For the C-LSU of Calcinea, the final alignment presented 427 bp, including gaps, and we retrived 287 conserved sites, 139 variable sites, and 29 singletons. The alignment of the C-LSU of Calcaronea had 404 bp, including gaps. A total of 271 conserved sites, 129 variable sites, and 31 singletons were retrieved. When a sequence from GenBank was longer than the final alignments size mentioned above, it was shortened. The nucleotide substitution model that best fit each alignment was indicated by the Bayesian Information Cri- terion in MEGA 6 (Nei & Kumar 2000; Tamura et al. 2013): GTR + G + I for Calcinea (ITS), T92 + G for Calcinea (LSU), and TN93 + G for Calcaronea. A Maximum Likelihood (ML) tree was built in MEGA 6 using an initial NJ tree (BIONJ) and 1000 pseudo-replicates bootstrap. Bayesian analises were performed in MrBayes 3.1.2. (Huelsen- beck & Ronquist 2001; Ronquist & Huelsenbeck 2003) under 106 generations and a 25% burn in, resulting in a consensus tree of majority. The posterior probability values are shown in the ML tree. The trees of Calcinea
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