Rhabderemia forcipula ( Lévi & Lévi, 1989 )

Ise, Yuji, Tajiri, Rie, Mizuyama, Masaru & Fujita, Yoshihisa, 2025, Submarine cave sponges of the genus Rhabderemia (Demospongiae, Biemnida, Rhabderemiidae) from the Ryukyu Islands, southwestern Japan: rediscovery of R. forcipula and description of a new species, Zootaxa 5569 (2), pp. 365-382 : 371-377

Rhabderemia forcipula ( Lévi & Lévi, 1989)

Figs. 4–10 ; Table 2

Rhabdosigma forcipula Lévi & Lévi, 1989: 75–76 , text-fig. 43, pl VII, fig. 8.

Rhabderemia forcipula : Van Soest & Hooper, 1993: 335–336, Figs. 22–23, 33, 35, 40.

Type material examined. Holotype: MNHN-IP- 2015-384 (previously registered as MNHN D CL 3242), off Lubang Island , Philippines, 13º55′N, 120º20′E, 85–90 m depth, MUSORSTOM2 stat. 8, coll. by Philippe Bouchet, 12 November 1980 ( Lévi & Lévi, 1989).

Other materials examined. All new materials came from “Akuma-no-Yakata” cave on Shimoji Island (Miyako Island Group, the Ryukyu Islands, Japan) and were collected by Y. Ise, M. Mizuyama and Y. Fujita, using SCUBA. NSMT-Po- 2504, 20 m depth, 2 November 2014. NSMT-Po-2505, 16 m depth, 16 March 2013. NSMT-Po-2506, 20 m depth, 15 March 2013. NSMT-Po-2507, 20 m depth, 4 February 2017. NSMT-Po-2508, 20 m depth, 4 February 2017.

Description of holotype. External morphology can be seen on website of Muséum National D’Hisoire Naturelle (http://mediaphoto.mnhn.fr/media/1446200223006kuXFc7dh3aWahWDI). Sponge with three to four digitate branches. Each branch almost straight or curved, tapering to a blunt tip. Surface finely hispid due to protruding megascleres. Color reddish brown in alcohol. Maximum branch diameter 8–10 mm.

Skeleton. Exact morphology of skeletal arrangement in ectosome not clearly observed due to fine debris covered on fragment of holotype. The overall choanosomal skeleton plumo-reticulate.

Spicules ( Figs. 4 , 5 ). Rhabdostyles ( Fig. 4A ), shaft straight or slightly curved, surface smooth, sharply pointed. Size, 270.4–(325.1)–371.6 µm in length, 7.3–(15.4)–19.6 µm in shaft width. Rugose microstyles ( Fig. 4B ), thin, slender, slightly curved, covered with sharp spines, densely distributed at the base ( Fig. 4C ), sparsely around the sharp tip ( Fig. 4D ). Spines ca. 0.4–0.5 µm long, sharply pointed and disposed up right at base. Size, 143–(166.1)–178 µm in length, 1.5–(2.3)–3.0 in base width, 1.2–(1.8)–2.4 µm in shaft width. Some microstyles lack spines, forming a smooth, slender, and slightly curved shaft with a sharply pointed tip ( Figs. 4E, F ). Thraustosigmas ( Fig. 5A ), Cshaped, shaft smooth around midpoint and microspined near both apices. Size, 26–(29.6)–37 µm in total length, 2.3–(3.1)–4.3 µm in shaft width. Spirosigmas ( Fig. 5B ), irregular S-shaped, shaft contorted, slightly centrotylote, covered with minute spines. Spines relatively larger near both apices. Size, 13–(16.1)–22 µm in total length, 0.8– (1.3)–2.0 µm in shaft width.

Description of submarine cave specimens. External morphology ( Fig. 6 ). Multiple short lobes or finely divided branches, connected at the base or laterally, forming a fragmented mass about 33–48 mm high and 40–50 cm wide ( Fig. 6A )). Each branch 4.0–10.0 mm in diameter, slightly undulated, sometimes dichotomous, tapering to a blunt or subspherical tip ( Figs. 6B–D ). Color pale lemon yellow to cream in life, and cream in ethanol. Texture corky and compressible in preserved state. Surface semi-transparent in life due to the presence of a thin membrane and an inflated subdermal canal ( Figs. 6C–D ), which assembles into oscula ( Fig. 6B ) that shrinks when disturbed or on fixation. Surface of preserved specimen finely hispid due to vertically protruding rhabdostyles ( Figs. 7A, B ).

Skeleton ( Fig. 7 ). Ectosomal and choanosomal skeleton indistinguishable and plumo-reticulate ( Fig. 7A ). Plumose rhabdosyle tracts ascending to the surface ( Figs. 7A, B ), vertically penetrating up to one spicule long ( Fig. 7B ). Ascending rhabdostyle tracts usually connected by radially arranged spicules of one spicule long. Rhabdosyles roughly arranged radially and connected by the spiral blunt end of the spicule. A unit of such radially arranged rhabdostyles connected to other units by one spicule long, forming an isodictyal mesh-like structure ( Figs. 7C–D ).

Spicules ( Figs. 8–10 ). Rhabdostyles ( Fig. 8A ), shaft straight, surface smooth around base, number of spines gradually increasing from base to sharp tip. Size variable, 154.2–(287.4)–408.5 µm in length, 8.3–(12.8)–19.3 µm in shaft width. Rugose microstyles ( Fig. 8B ), thin, slender, slightly curved near base, shaft covered with tiny spines about 0.4–0.5 µm long ( Figs. 8C–E ). Spines sharply pointed and densely distributed at base ( Fig. 8C ), almost densely distributed asround axis ( Fig. 8D ) and sparsely distributed around sharp tip ( Fig. 8E ). Size, 124.0–(147.8)–174.5 µm in length, 1.2–(1.8)–2.3 µm in base width, 1.2–(1.4)–1.6 µm in shaft width. Smooth microstyles rarely present. Sigmoid microscleres in two size classes ( Figs. 9A, B ). Larger sigmoid microscleres ( Fig. 9A ), thraustosigmas and spirosigmas of similar size, rough surface, covered with tiny spines, spines larger near apices. Size, 19.6–(24.8)– 30.5 µm in total length. 1.6–(2.2)–2.7 µm in shaft width. The number of spirosigmas varies between submarine cave specimens; rare in specimens NSMT-Po-2506 and NSMT-Po-2508 with abundant thraustosigmas, and abundant in specimen NSMT-Po-2504 without thraustosigmas ( Fig. 10A ). Undeveloped young spirosigmas with thin and smooth shaft also present ( Fig. 9A ). Smaller sigmoid microscleres ( Figs. 9B , 10B ), spirosigmas, contorted, slightly centrotylote, surface rough, covered with tiny spines except at centrotylote part. Size, 14.3–(17.6)–22.1 µm in total length, less than 1 µm in shaft width. Spicule measurements of all analyzed specimens given in Table 2 .

Origin of Japanese name. A new Japanese vernacular name: “Kurayami-kiseru-kaimen” is proposed here. “Kurayami” is darkness in Japanese, referring to its habitat. “Kiseru” is a smoking pipe in Japanese, derived from the shape of the rhabdostyle. “Kaimen” is sponge in Japanese.

Ecology. Type specimens were collected from off Lubang Island, southwest of Manila, Philippines, at a depth of 85–90 m ( Lévi & Lévi, 1989). Newly collected specimens were found in the submarine cave “Akuma-no-Yakata”, located on the west side of Shimoji Island (Miyako Island Group, the Ryukyu Islands, Japan). It opens the entrance in the edge of the island and then extends into the underground of the island for about 110 m ( Osawa & Fujita, 2019). The inner part of the cave is under anchialine habitat. This species lives exclusively in total darkness at the depth of 15–32 m in the studied submarine cave and has not been found so far in other submarine caves around Okinawa.

Remarks. Hooper (2002) divided Rhabderemia species into two groups based on their skeletal structure. Our specimens belong to the group of species bearing plumo-reticulate skeletal structure. Among these, the newly collected sponges resemble R. forcipula in spicule categories present and their measurements ( Table 2 ).

After examining the holotype of R. forcipula for the first time in this study and redescription of the paratypes by Van Soest & Hooper (1993), we found some differences or variations between type specimens and submarine cave specimens, which are (1) color in ethanol: reddish brown in type specimens ( Lévi & Lévi, 1989; Van Soest & Hooper, 1993) vs cream in submarine cave specimens; (2) surface of rhabdostyles: smooth or slightly spined in type specimens ( Lévi & Lévi, 1989; Van Soest & Hooper, 1993) vs. spined in submarine cave specimens ( Fig. 8A ). An important variation is the presence of thraustosigmas, which is always observed in all type specimens ( Van Soest & Hooper, 1993; Fig. 5A in this study), but is rare or absent in some submarine cave specimens. In such cases, larger spirosigmas ( Fig. 10A ) appear to be an alternative to thraustosigmas. In specimens of NSMT-Po-2506 and NSMT- Po-2508, both thraustosigmas and larger spirosigmas were present, with the majority being thraustosigmas ( Fig. 10A ). The definition of spicule morphology is crucial for sponge identification, however, as for thraustosigmas and spirosigmas in the case of R. forcipula , the two spicule types may have same origin.

Morphological variation in spicules has been noted in sponges found from both shallow submarine caves and the deep-sea or mesophotic zone. According to Cárdenas & Rapp (2013), lower silica concentrations in shallow waters are expected to affect mainly on immature sterrasters of sponges belonging to the family Geodiidae . Cárdenas et al. (2018) expected that the difference in silica concentration would also affect the morphological variation of spicules in shallow-water submarine caves. Furthermore, even in the same submarine cave, there was a report of high frequency of malformations affecting on siliceous spicules of sponges depending on each part of the cave ( Harmelin et al., 2003). This type of spicule malformation has been reported for R. toxigera Topsent, 1892 , although the exact character of the malformation was not mentioned ( Harmelin et al., 2003). Pisera & Vacelet (2011) reported variation in both external morphology and spicule characters for Discodermia polymorpha Pisera & Vacelet, 2011 , and suggested that polymorphism could be related to differences in cave environment: between caves or between different parts of caves.

In this study, we could not find clear morphological features to distinguish our submarine cave specimens from the type specimens of R. forcipula , considering the morphological variation of the spicules: rhabdostyles and spirosigmas/thraustorigmas. In spite of our inability to spot any clear malformation in the spicules of our submarine cave specimens ( Figs 9 , 10 ), the unique environment of the submarine cave may have some influence on the morphological variation of the microscleres, as suggested by Pisera & Vacelet (2011) and Cárdenas et al. (2018). Thus, we decided to consider our submarine cave specimens as a phenotype of R. forcipula , the species once collected from the mesophotic zone of the Philippines ( Lévi & Lévi, 1989), assuming that the species has a morphological variation of spicules: rhabdostyles and spirosigmas/thraustorigmas.

Considering the morphological variation of microscleres, Rhabderemia mammiliata (Whitelegee, 1907) from southern Australia is comparable to our submarine cave specimens by the presence of thraustosigmas as the larger sigmoid microscleres and the size of rhabdostyles. However, R. mammilata lacks microstyles and has much smaller spirosigmas of the smaller categories (9–13 µm) (Whitelegee, 1907; Hallmann, 1916, 1917; Van Soest & Hooper, 1993).

Figures

FIGURE 4. Spicules of Rhabderemia forcipula, holotype (MNHN-IP-2015-384). A, rhabdostyles. B, rugose microstyle. C, magnified view of the base of the rugose microstyle with sharp spines distributed on the surface. D, magnified view of tip of rugose microstyle. E, smooth microstyle. F, magnified view of base of smooth microstyle. Scale bars: A, 50 µm; B, E, 20 µm; C, D, F, 2 µm.

FIGURE 5. Sigmoid microscleres of Rhabderemia forcipula, holotype (MNHN-IP-2015-384).A, thraustosigma. B, spirosigma. Scale bars: A, 10 µm; B, 5 µm.

FIGURE 6. Rhabderemia forcipula from a submarine cave of Shimoji Island. A, external morphology in alive (NSMT-Po- 2506). B–D. magnified view of the surface shows relatively large semitransparent subdermal canals. Arrowheads indicate the position of oscula that shrinks when disturbed.

FIGURE 7. Skeletal structure of Rhabderemia forcipula (NSMT-Po-2504) from a submarine cave of Shimoji Island. A, perpendicular section of the axis from a branch shows a plumo-reticulate skeletal structure. B, magnified view of the section close to the surface shows rhabdostyles perpendicularly upright and with tips outwardly protruding. C, D, magnified view of the choanosomal skeleton shows rhabdostyles roughly arranged radially and connected by the spiral blunt ends: C, section perpendicular to the branch axis; D, section parallel to the branch axis. Scale bars: A, 500 µm; B–D, 200 µm.

FIGURE 8. Spicules of Rhabderemia forcipula (NSMT-Po-2504), from a submarine cave of Shimoji Island. A, rhabdostyles. B, microstyle. C–E, magnified view of microstyle shows spines on the surface of the base (C), axis (D), and tip (E). Scale bars: A, 50 µm; B, 20 µm; C–E, 1 µm.

FIGURE 9. Sigmoid microscleres of Rhabderemia forcipula, (NSMT-Po-2508), from a submarine cave of Shimoji Island. A, thraustosigma and larger spirosigma show the variable shape. B, smaller spirosigma. Scale bars: A–B, 10 µm.

FIGURE 10. Sigmoid microscleres of Rhabderemia forcipula, (NSMT-Po-2504), from a submarine cave of Shimoji Island. A, larger spirosigma. B, smaller spirosigma. Scale bars: A–B, 5 µm.