Oscarella zoranja, Perez & Ruiz, 2018

Perez, Thierry & Ruiz, Cesar, 2018, Description of the first Caribbean Oscarellidae (Porifera: Homoscleromorpha), Zootaxa 4369 (4), pp. 501-514 : 507-509

Oscarella zoranja sp. nov.

Holotype: Muséum National d’Histoire Naturelle de Paris , MNHN—DJV196 : Martinique, Anses d’Arlet, Caribbean Sea. Site « Grotte Couleur » (14°29.752´N, 61°05.407´W), 7 m depth, under an overhang, date 11/06/ 2011. Sample code: 110611 -MT3TP5, collector T. Pérez ( Fig.5 ). GenBank accession number: KX3482266.

Paratype 1: Muséum National d’Histoire Naturelle de Paris , MNHN—DJV197 : Guadeloupe, Caribbean Sea. Site “ Grotte aux Barracudas ”, (16°27.301'N, 61° 32.253'W), 19 m depth, under an overhang, date 15/02/2012. Sample code: GR26HOM1, collector A. Ereskovsky.

Paratype 2: Muséum National d’Histoire Naturelle de Paris , MNHN—DJV198 : Martinique, Le Diamant, Caribbean Sea. Site « Grotte Zeb » (14°27.832' N, 61°01.065' W), 19 m depth, on a vertical wall at the entrance of the cave, date 15/05/2016. Sample code: 150516 -MT4CR13, collector C. Ruiz.

Other material examined: Martinique, 131203 -MT3CR2, Anses d'Arlet, Grotte Couleur at 8 m depth. collector C. Ruiz ; 150516 -MT4CR4, 150516 -MT4CR13, 150516 -MT4CR8 Le Diamant, Grotte Zeb at 19 m depth, collector C. Ruiz; 110611 -MT4TP12, 110611 -MT4TP5, Le Diamant, Grotte Zeb at 19 m depth, collector T. Pérez; 110613 - MT1TP7 Le Diamant , tunnel du Diamant at 15 m depth, collector T, Pérez. Guadeloupe, 150516 - MT8CR4, GR26HOM9, GR27HOM16, GR26HOM4, Grotte aux Barracudas at 19 m depth, collector A. Ereskovsky ; GR34HOM29, GR30HOM29, GR26HOM1, GR26HOM8, GR27HOM20 Grotte la Cathédrale at 18 m depth, collector A. Ereskovsky. This material is kept in the collection of the Station Marine d’Endoume (Marseille—France).

Etymology: From the creole zoranj (orange), the species name thus refers to the color of the new species. Diagnosis: Oscarella inhabiting shaded habitats. Orange color. Smooth, regularly lobate surface and rather cartilaginous consistency. Ovoid to spherical eurypylous choanocyte chambers. A single type of vacuolar cell, containing up to 10 vacuoles, and one type of spherulous cell.

Description. External morphology: A sponge with regular lobate surface which can be up to 15 to 20 cm large and 1 to 3 cm thick. The consistency is soft, and the sponge is easily removed from the substrate. The color in vivo is always a nuance of orange. The sponge does not exude any substance in contact with air, nor does its color change in alcohol. Its surface is smooth, and it presents between 1 and 3 oscula of about 12 mm in diameter. The lobes are small, rounded and regular, and only a few of them have inhalant ostia with a flared-out margin.

Soft tissue organization: No spicule or fibers. The ectosome is thick, from 30 to 83 µm. The inhalant canals (13 to 19 µm) run perpendicular to the surface. Exhalant canals run towards a well-developed system of irregular basal cavities leading to the oscula. The eurypylous choanocyte chambers are ovoid to spherical, with diameters between 30 and 72 µm ( Fig. 6 and 7 ). The apopyle is surrounded by apopylar cells.

Cytology: Choanocytes are ovoid to pyramidal, 2.2 to 5 µm large and 4 to 6 µm high. ( Fig.7B ). Their collar averages 3 µm wide and is composed of about 30 microvilli. Their nucleus, 1.5 to 2.5 µm in diameter, is in central to basal position. The cytoplasm usually contains 1 to 3 phagosomes, 0.6 to 1.7 µm in diameter, osmiophilic inclusions and mitochondria. Apopylar cells are ovoid to pyramidal in shape and of the same size as the choanocytes ( Fig. 7 ). Their nucleus is centrally positioned and 1.5 to 2.5 µm in diameter. Small vacuoles up to 2 µm wide are present in their cytoplasm. Pinacocytes are flat and flagellated, 7 to 12 µm large and 1 to 3 µm high. Their ovoid nucleus is up to 2 µm in diameter. Several osmiophilic inclusions between 0.4 and 0.7 µm were observed only in the cytoplasm of endopinacocytes. No archaeocyte was observed, although two types of cells with vacuoles were recorded in the mesohyl and in the ectosome. Both types are ovoid to irregular, from 8 to 16 µm in diameter, with a cytoplasm containing between 2 and 10 vacuoles of 3.5–10 µm in diameter ( Fig.7 ). The only difference between the two types lies in the content of the vacuoles: the first type can be defined as a vacuolar cell, with almost empty vacuoles ( Fig. 7 ), whereas the second type is a spherulous cell with vacuoles occupied by electron- dense materials. Prokaryotic cells are quite abundant in the mesohyl. The main morphotype is a bacilluslike shape, 1 to 1.5 µm long and 0.5 µm in diameter ( Fig. 7 ). The cell wall consists of many layers of dense filaments, and the cytoplasm can be dense to electrons. Each bacterium is surrounded by a layer devoid of collagen fibrils. No reproductive element was observed.

Ecology. Oscarella zoranja sp. nov. can be found in the same habitats as O. filipoi , on vertical walls of semidark caves, tunnels, overhangs and small crevices. This species was found from shallow waters down to 50 m depth in a cave off the Rocher du Diamant in Martinique. This species is never subject to epibiosis and no sign of predation was observed.

Taxonomic remarks. Oscarella zoranja sp. nov. has very classic Oscarella external morphology, lobate and with a rather cartilaginous consistency compared to O. filipoi sp. nov., again removing any possibility for confusion with the previous aspiculate Homoscleromorpha described in the Caribbean Sea (Ruiz et al. 2017). This species has the same external morphology and consistency as O. tuberculata , but the new species differs in color and in its mesohylar cells. Unlike both O. tuberculata and O. filipoi sp. nov., this new species does not present clusters of vacuolar cells.

DNA analysis. The positioning of the two new Oscarellidae within the Homoscleromorpha phylogeny was achieved after sequencing all examined individuals and downloading some GenBank sequences ( Fig. 8 ). The two families of Homoscleromorpha ( Gazave et al. 2010) are well supported in the phylogenetic reconstruction. Oscarellidae is composed of two main clades, and both new species clearly belong to the clade containing the type species of the family Oscarella lobularis . Oscarella filipoi sp. nov. is the closest to the type species, its sequences of the I3 -M11 CO1 fragment differing by 25 and 26 base-pairs from O. lobularis and O. tuberculata , respectively. Oscarella zoranja sp. nov. is not included in the O. filipoi sp. nov. clade and the type species of the family, because its sequences differ by 32 to 35 base-pairs on average from the previous group of species. Oscarella zoranja sp. nov. presents the highest genetic variability recorded among the Homoscleromorpha with this molecular marker, with up to 8 different base pairs between the sequenced individuals, compared with the single base-pair that differs between Oscarella tuberculata ( Schmidt, 1868) and O. lobularis . However, our analyses of the morphology of a great number of individuals of O. zoranja sp. nov. failed to reveal any trait which might support this variability.

Figures

FIGURE 6. General soft tissue organization of Oscarella zoranja sp. nov.. cc: Choanocyte chamber; pi: pinacoderm.

FIGURE 7. TEM micrographs of Oscarella zoranja sp. nov. A) Detailed view of a choanocyte chamber. B) Detailed view of choanocytes. C) Flagellated endopinacocyte. D, E) Detailed views of vacuolar cell type 1. F) Detailed view of the spherulous cell of O. zoranja.G) General view of the prokaryotes in the mesohyl.apo: Apopylar cells; cc:Choanocyte chamber.

FIGURE 8. Phylogenetic reconstruction positioning the two new Oscarellidae among Homoscleromorpha on the basis of the I3-M11 fragment of the CO1 mitochondrial gene using neighbor-joining analysis, and indicating maximum-likelihood. Bootstrap valuesare given for both analyses, with ML values in parenthesis.

FIGURE5. In situ picture of Oscarella zoranja sp. nov.. A) The orange chromotype is the most common color of this species. B) Pale yellow specimen mostly found in semi-dark habitats.