Aspiculophora papillata, Ruiz & Ereskovsky & Perez, 2022

Ruiz, Cesar, Ereskovsky, Alexander & Perez, Thierry, 2022, New Skeleton-Less Homoscleromorphs (Porifera, Homoscleromorpha) From The Caribbean Sea: Exceptions To Rules Are Definitely Common In Sponge Taxonomy, Zootaxa 5200 (2), pp. 128-148 : 136-137

Aspiculophora papillata sp. nov.

Etymology: the species name refers to the papillate surface of this Plakinidae , papilla = nipple in Latin.

Diagnosis: encrusting Aspiculophora with papillate surface. Collagen layer (<1µm thick) separating the exopinacoderm and ectosome. Well-developed mesohyl with sub-ectosomal cavities. Leuconoid aquiferous system with aphodal choanocyte chambers. One type of vacuolar cell. High abundance of prokaryotic symbionts in the mesohyl.

Examined material: Holotype: Muséum National d’Histoire Naturelle de Paris , France MNHN DJV204 Bequia, The Grenadines, “Full Moon Cave” (12°59.525’ N, 61°16.731’ W), 10-12 m depth, beneath an overhang, date 19/05/2015, sample code: 150519LG1-CR13, collector: C. Ruiz. Genbank accession number: MK 949486

Paratype: Muséum National d’Histoire Naturelle de Paris , France MNHN DJV205 Guadeloupe, “Grotte Cathédrale” (16°27.740’ N, 61°31.837’ W), 18 m depth, on a vertical wall in the dark part of the cave, date 29/05/2015, sample code: 150529GU3-CR1, collector: C. Ruiz.

Other material examined: Martinique, “Grotte Zeb” (14°27.832’N, 61°01.065’W), 19 m depth, on a vertical wall in the semi-dark part of the cave, dates 15 and 16/05/2015, sample codes: 150515 MT4 -CR3, 150515 MT4 - CR6, 160515 MT4 -CR14, collector: C. Ruiz.

Bequia , The Grenadines “Full Moon Cave” (12°59.525’ N, 61°16.731’ W), 10-12 m depth, beneath an overhang, date 19/05/2015, sample codes: 150519LG1-CR10, 150519LG1-CR13, 150519LG1-TP11, collectors: C. Ruiz & T. Pérez

Comparative material examined: Aspiculophora madinina MNHN DJV 180, Rocher du Diamant “Grotte Zeb”, Martinique (14°26.5´N, 61°03.083´W), 12 m depth, date 13/06/2011, sample code: 110613 MT4 -TP11 collector: T. Pérez,

Aspiculophora madinina , “ Grotte Amédien”, Guadeloupe (16°30.033’ N, 061°28.774’ W), 12 m depth, date 30/05/2015, sample code: 150530-GU6-TP07, collector: T. Pérez .

Plakina nathaliae MNHN DJV 179, Rocher du Diamant “Grotte Zeb”, La Martinique (14°26.5´N, 61°03.083´W), 17 m depth, date 13/06/2011, sample code: 110613 MT4 -TP2, collector: T. Pérez.

Description:

External morphology: Aspiculophora papillata sp. nov. is a thinly encrusting irregular sponge which is quite hard to collect because of its fragile consistency. Collected specimens measured up to 10 cm wide and 1 mm thick. The sponge has a papillate surface and its color varies from yellow to light brown in vivo, whereas it is light brown in ethanol. Papillae are cylindrical, up to 3 mm high and about 1 mm in diameter. The top of the papillae is often larger with an umbrella-like form of 2-3 mm in diameter. Oscula of about 1 mm in diameter are sometimes visible in the top of the papillae ( Figure 4A, B ).

Internal Anatomy: No spicule or fibrous skeleton. A collagen lager <1 µm separates the exopinacoderm from the ectosome. The ectosome is 20-25 µm thick ( Figure 4 C-E). The aquiferous system is leuconoid. The inhalant canals are 15-25 µm wide. The choanocyte chambers are aphodal, spherical to ovoid, 20 to 37 µm in diameter ( Figure 4C, E ). The proportion between mesohyl and choanocyte chambers is greater than 1.

Cytology: Choanocytes are cylindrical, 5 µm wide and 8 µm high. Their nuclei are spherical, about 2 µm in diameter and are located in apical position. Their cytoplasm usually contains osmiophilic inclusions of about 0.1 µm in diameter in basal position ( Figure 5A, B ). Apopylar cells have a trapezoid shape ( Figure 5A ). Exo- and endopinacocytes are flat and flagellated (5-15 µm long; 1-2 µm wide) with a nucleus of about 2.5 µm in diameter ( Figure 5C ). One type of abundant vacuolar cell was found randomly distributed in the mesohyl. This cell has an ovoid to spherical shape, is 12-20 µm in diameter, and generally harbors one to five vacuoles occupying most of the volume of the cytoplasm. Some heterogeneous to filamentous materials can be seen inside the vacuoles, and microorganisms can be found in their cytoplasm (see arrow in Figure 5C ). No archaeocyte was observed. The new species can be considered as an HMA sponge. At least four prokaryotic morphotypes seem to be dominant in the mesohyl ( Figure 5D ). The first morphotype is peanut-shaped, 2.5 µm long 0.5 µm wide, with a dense cytoplasm and a double membrane. The second morphotype is of similar size, is cylindrical in shape and has a translucent external membrane. The third morphotype has an irregular shape and is 2-4 µm long and 1 µm wide. The fourth morphotype is bean-shaped with a dense membrane and translucent cytoplasm.

Ecology: The new sponge species was found in the Caribbean islands of Guadeloupe, Martinique and Bequia (Lesser Antilles). It lives in sympatry (and sometimes in syntopy) with A. madinina , on walls and ceilings of dark marine caves, where it is always found between 10 and 20 m depth. No sign of predation was observed, but the new species usually lives in close association with other sponges and invertebrates such as Serpulidae and Sabellidae worms ( Figure 4A ).

Taxonomic remarks: Aspiculophora papillata sp. nov. is a skeleton-less Plakinidae like A. madinina . The new species mainly differs by its external morphology, the papillate surface being a trait observed for the first time among Homoscleromorpha. In contrast with A madinina , no dark exudate was recorded in contact with alcohol for A. papillata . The collagen layer between the exopinacoderm and the ectosome region in A. papillata sp. nov. is very thin in comparison with A. madinina . Another difference between these species is the presence of sub-ectosomal cavities in A. papillata sp. nov. that do not exist in A. madinina . Both species share the leuconoid aquiferous system with aphodal choanocyte chambers, only one type of vacuolar cell which is mostly concentrated in the ectosome and similar microbial compositions.

Figures

FIGURE 4. A, B. In situ photographs of two color morphotypes of Aspiculophora papillata sp. nov. showing the characteristic papillate surface. C. Light microscopy micrograph of the internal organization of A. papillata. D. Detailed view of the ectosome showing concentration of vacuolar cells and sub-ectosomal cavities: the arrow indicates the collagen layer between the region of exopinacocyte and ectosome. E. Detailed view of a choanosome. cha, choanocyte chambers; ec, ectosome; pin, pinacocytes; pk, prokaryotes; vc, vacuolar cell; Scav, sub-ectosomal cavities.

FIGURE 5. TEM micrograph of Aspiculophora papillata sp. nov. A. Detailed view of a choanocyte chamber: the choanocyte nucleus is inapical position.Arrows point toapopylarcells.B. Detailedview of choanocytes.C.Vacuolar cellandendopinacocytes bordering an exhalant canal in A. papillata: arrows point to prokaryotes inside vacuolar cells. D. morphological diversity of the prokaryote community associated to A. papillata: numbers correspond to morphotypes. apo, apopylar cells; cha, choanocyte chambers; cho, choanocyte; n, nucleus; pin, pinacocytes; pk, prokaryotes; vc, vacuolar cell.