Chondrocladia, THOMPSON, 1873

Vacelet, Jean, 2006, New carnivorous sponges (Porifera, Poecilosclerida) collected from manned submersibles in the deep Pacific, Zoological Journal of the Linnean Society 148 (4), pp. 553-584 : 557-562

CHONDROCLADIA THOMPSON, 1873

Type species: Chondrocladia virgata Thompson, 1873 (by monotypy).

Diagnosis, modified from Hajdu & Vacelet (2002): Cladorhizidae with anchorate isochelae.

The diagnosis has been slightly modified by adding ‘anchorate’ to isochelae in order to avoid confusion with Abyssocladia Lévi, 1964 .

CHONDROCLADIA KOLTUNI SP. NOV.

( FIG. 3 )

Type material

Holotype: IORAS 5 /2/1 (Institute of Oceanology of Russian Academy of Sciences , Moscow). St. 2298 of submersible MIR-2, 26/07/1990, near Bering Island , 54°59.25′N, 165°42.50′E, 5249 m.

Etymology

Dedicated to the memory of the late Professor V. Koltun, in honour of his contribution to the knowledge of deep Pacific sponges.

Locality and habitat

Near Bering Island in the north part of Kuril Trench, 54°59.25′N, 165°42.50′E, 5249 m. Cruise 22 of R / V ‘Akademic Mstislav Keldysh’, dive of MIR-2, St. 2298, 26/07/1990. The sponge was rooted in muddy sediment .

Description

Large stalked sponge ( Fig. 3A, B ), 40 cm high, composed of a rooting system, a cylindrical stalk ending in an enlarged body from which radiate in all directions 15 secondary branches, each ending in a translucent sphere in the living animal, in an irregular swelling when preserved. Rhizoids anchoring the sponge in the mud, more than 60 mm long, richly ramified, composed of thick fibres of fusiform styles, very thin at their end. Stalk 30 cm high and 5–7 mm in diameter, rigid, made of thick fibres of longitudinally arranged fusiform styles with a less dense central part and a coating of smaller styles. Secondary axis similar to the main stalk, rigid, with two internal canals approximately 1 mm in diameter, straight and ending in a translucent sphere, 30–38 mm in diameter in life according to in situ photograph, slightly curved and ending in an irregular, shrunken bulge 5–10 mm in diameter after preservation. Long, thin appendages of most probably bathypelagic crustaceans present on the shrunken bulges, sometimes included in the bulges. Apertures not visible. Consistency fleshy, rather hard. Colour yellowish white to clear brown in life and in alcohol, root system brownish.

Skeleton: rhizoids made of thick fibres of large fusiform styles linked by spongin. Stalk made of similar fibres of spicules, spirally twisted, and covered by a 300–400-µm-thick coating of smaller styles irregularly arranged, forming an irregular hispidation in which some sediment is included. Secondary branches with a coating of small styles forming an irregular palisade, with an axis made of fibres similar to those of the main stalk ending at the extremity of the bulge. Bulges with irregularly radiating fascicles of relatively small styles and a thick cover of extremely numerous isochelae 1 perpendicular to surface, lining the surface and the internal folds.

Spicules:

1. Styles of the stalk ( Fig. 3G, I ), secondary axis, body and rhizoids, strongly fusiform, sometimes nearly oxea (for instance in a spicule 500 µm long, head 10 µm and middle part 30 µm in diameter, or in a spicule 4500 µm long, head 25 µm and middle part 50 µm in diameter), with an abrupt shrinking near the head and a short acerate tip. Overall size 420–5000 × 14– 50 µm, possibly longer. Longest spicules found in the main stalk, those of the body and of the rhizoids being usually less than 2000 µm. Styles of the inflatable bulges more regular and smaller, usually 630– 800 × 14–17 µm.

2. Styles or subtylostyles ( Fig. 3H ) from an external layer of the body and of the stalk, absent in the rhizoids and in the inflatable bulges, generally smooth, sometimes with very faint rare spines. Size 500– 750 × 6–10 µm.

3. Anchorate isochelae 1 ( Fig. 3C, E ), rare or absent from the stalk and rhizoids, common in the body and very abundant in the inflatable bulges, with six alae, more rarely five, at each end, curved shaft with fimbriae. Size 98–105 µm, shaft 7.5–8 µm thick.

4. Anchorate isochelae 2 ( Fig. 3D ), rare in the stalk, common in the rhizoids, absent in the body and the inflatable bulges. Same shape as isochelae 1, with six or five alae, but smaller. Size 55–70 µm, shaft 3.5–4.2 µm thick.

5. Sigma 1, rare in body and stalk. Size 92–110 µm.

6. Sigma 2 ( Fig. 3F ). Size 40–46 µm, some in the rhizoids only 30 µm.

Remarks

This large specimen of Chondrocladia has been figured and commented on without specific assignation several times since its observation and collection by the manned submarine MIR-2 ( Tendal, Barthel & Tabachnik, 1993; Tendal & Sahling, 1997; Hajdu & Vacelet, 2002). Being the first to be observed in situ and collected at the same time, it resolved the problem of a deep-sea organism whose nature long remained enigmatic owing to the striking difference in morphology between the in situ observations and the collected animals ( Tendal et al., 1993). The presence of several long, thin appendages of crustaceans on the shrunken bulges, with some of the setae trapped in the alae of the isochelae 1, and of crustacean debris within the bulges, illustrates the carnivorous feeding habit of the sponge, clearly demonstrated in other species of Chondrocladia ( Kübler & Barthel, 1999) .

The species evidently belongs to the concrescens group ( Topsent, 1930). It differs from the specimens of north-west Pacific identified as C. concrescens Schmidt, 1880 by Koltun (1970), a species first described from the Caribbean and whose records from the Pacific are doubtful (see Remarks for the following species). It also differs from C. lampadiglobus sp. nov. in the styles of the cover, which are nearly smooth here, and the size and characters of the isochelae.

Another specimen with the same external morphology, possibly belonging to the same species, has been photographed in situ by Tendal & Sahling (1997), from 4900 m depth, in a nearby area of the North Pacific, 550 km apart.

CHONDROCLADIA LAMPADIGLOBUS SP. NOV.

( FIGS 4 , 17A–D )

Type material

Holotype: NAUDUR ND 06 (9-1B), 11/12/1993, East Pacific Rise , 17°24.10′S, 113°13.75′W, 2714 m, Muséum National d’Histoire Naturelle, Paris, no. MNHN D JV 81.

Etymology

From lampas, lampadis, Latin, noun fem. lamp, lantern, and globus, globi, Latin, noun masc. ball, sphere. Referring to the resemblance of the sponge to a streetlight with several spherical glass globes.

Locality and habitat

East Pacific Rise , 17°24.10′S, 113°13.75′W, 2714 m, 11/ 12/1993, 16:30, near the thermal site ‘Rehu’. The holotype was rooted in sediment between pillow lava, near active hydrothermal sites, but in an area still with low density of animal life. Several other specimens possibly belonging to the same species have been observed from submersibles during several cruises on the East Pacific Rise under similar conditions, approximately 2600–3000 m depth, either rooted in a thick sediment layer or directly attached to pillow lava with a thin sediment cover ( Fig. 17C, D ), always at some distance from the rich animal communities of the active hydrothermal sites. These observations, which have been made over a large area of the East Pacific Rise extending from 23°32S to 13°N, are presented and discussed in the Remarks below .

Description

Large stalked sponge ( Figs 4A , 17A–D ), 27 cm high after preservation and loss of the basal part, approximately 50 cm high in life, composed of a rhizoid fixation system, a cylindrical stalk ending in an enlarged, ovoid body from which radiate in all directions secondary branches, each ending in an irregular swelling on the preserved specimen, a translucent sphere in the living animal. Fixation base not preserved, owing to the breakage of the lower part of the stalk, estimated at 6 cm long from Fig. 17A, B . Stalk 24.5 cm high and 5–6 mm in diameter, rigid, smooth near the base, rugose to the fingers near the body, made of longitudinally arranged fusiform styles and a coating of rugose tylostyles. Body ovoid, 30 × 20 mm, with a rugose surface, from which radiate 13 secondary axes, 2–4 mm in diameter. Five of the secondary axes broken more or less near the base, the other, 50 mm maximum length, somewhat curved, ending in an irregular bulge, which often coalesces with one or two of the bulges of the nearby extensions, sometimes forming a veil between the axes. Translucent spheres of variable diameter, estimated at 3–5 cm from the underwater pictures. Apertures not visible. Consistency rigid but easily broken. Colour yellowish white to clear brown in alcohol. Several unidentifiable crustacean debris fragments, up to 4 mm long, present on the surface of the body and more frequently on the surface of the bulges. Stalk bearing a comatulid crinoid, probably Thaumatometra sp. (M. Eleaume, MNHN, pers. comm.), and an unidentified ophiuroid. An unidentified worm, possibly a polychaete, gliding on one of the spheres visible on underwater pictures ( Fig. 17A ).

Skeleton: Stalk made of large fusiform styles arranged in parallel without any twisting, with a thick cover of rugose tylostyles arranged in a dense irregular feltwork. Cover devoid of microscleres in the most basal part of the stalk, with a few isochelae 1 near the body. Body and secondary branches with a rugose coating of styles smaller than those of the axis, including numerous microscleres. Bulges with a confused skeleton of fusiform styles, smaller than in the axis, and an outer cover of extremely numerous microscleres, especially isochelae 1.

Spicules:

1. Styles of the fibres in the body and the stalk ( Fig. 4C ), straight, strongly fusiform (for instance in a spicule 4750 µm long, head 20 µm and middle part 75 µm in diameter), with a head abruptly shrunken to 20 µm long and an acerate tip. Size 700–4750 × 15– 75 µm.

2. Styles of the terminal swellings, fusiform, similar to those of stalk and body ( Fig. 4D ), but smaller. Size 510–580 × 17–30 µm.

3. Subtylostyles or tylostyles of the outer cover of stalk and of swellings ( Fig. 4B ), slightly curved or flexuous, often with a marked oval head, rugose with numerous short spines. Size 300–535 × 5–6 µm.

4. Anchorate isochelae 1 ( Fig. 4E, F ), rare or absent from the stalk, common in the body and very abundant in the swellings, with six alae at each end. Alae relatively short, lanceolate, sharp, with a well-marked hull on the underside. Shaft curved, with narrow fimbriae. Size 123–140 µm, shaft 6–7 µm thick, alae 25 µm long.

5. Anchorate isochelae 2 ( Fig. 4G ), rare in the stalk, moderately abundant in the body and the bulges, with six alae. Alae rather thick, lanceolate with a sharp point. Size 20–32 µm, shaft 2 µm thick, alae 10–11 µm long.

6. Sigmas ( Fig. 4H ), rare in the body and in the stalk, not seen in the bulges. Size 45–120 × 2–3 µm, possibly in two size categories, but with numerous intermediary forms.

Remarks

The identification of species of Chondrocladia of the ‘ concrescens type’ is difficult, especially for the Pacific representatives, which are generally known from single or few specimens, giving no indication on specific variations. Furthermore, several specimens of Pacific Chondrocladia have been tentatively identified, probably incorrectly, either to C. concrescens Schmidt, 1880 or to C. gigantea (Hansen, 1885) , originally described, respectively, from the Gulf of Mexico and the northeast Atlantic.

This species from the East Pacific Rise is very similar in external morphology to Chondrocladia koltuni sp. nov. Both have the same aspect with inflated spheres in life. The holotypes of the two species differ in the styles of the coating, which are rugose tylostyles in C. lampadiglobus and nearly smooth styles in C. koltuni , in the size and characters of the isochelae, and the thickness of the main styles. Both differ in several important spicule characters from the sponge from the deep north Pacific identified as C. gigantea by Koltun (1958). However, C. lampadiglobus appears very similar to the sponge identified as C. concrescens by Koltun (1970), who gathered under this name specimens from the Gulf of Mexico, north Atlantic and north Pacific, while admitting extensive polymorphy. This ‘species’ appears to be common in the Okhotsk Sea and the South Kuril Islands, at 300–8860 m depth. Koltun did not comment on the variability of his numerous specimens, but according to his description they appear to differ from the type of C. concrescens from the Gulf of Mexico ( Schmidt, 1880; Topsent, 1920) and probably belong to an undescribed species. The specimen here described as C. lampadiglobus has a rather similar spiculation, differing only in larger rough tylostyles, a clearer distinction between the two types of isochelae, and in the isochelae 2 with longer alae. (These isochelae 2 are reminiscent of those that characterize C. concrescens , with very long alae, although here the opposite alae are far from being in contact, as described by Schmidt, 1880 and Topsent, 1920.) The possibility that C. lampadiglobus belongs to the same species as Koltun’s specimens from the north-west Pacific cannot be excluded, although the difference in the shape of anisochelae 2 and the large geographical distance make it rather unlikely. This will need to be confirmed when more is known of the variability of the spiculation of C. lampadiglobus , as discussed below.

The other species of Chondrocladia originally described from the Pacific, namely C. asigmata Lévi, 1964 , C. challengeri Topsent, 1920 , C. clavata Ridley & Dendy, 1886 , C. crinita Ridley & Dendy, 1886 , C. pulvinata Lévi, 1993 , C. scoloniema Lévi, 1993 and C. yatsui Topsent, 1930 , differ in spicule characters, which are admittedly rather subtle and whose constancy remains to be examined.

Specimens of Chondrocladia sp. with a similar morphology are rather common on the East Pacific Rise from 23°S to 13°N, but only one has been collected and it is at present unclear whether they all actually belong to the same species ( Fig. 17C, D ). During the NAUDUR cruise, the sponge was observed at the same depth in nearby areas of the type location or was recognized in the videos or photographs during PL04 , PL16 , PL17 and PL18 . Observations were also made during BIOSPEEDO dive PL 1579 , 19/04/2004, 17°24.86′S, 113°11.96′W, 2590 m (Jollivet et al., 2004), during PARS5 cruise of the R / Atlantis (dive 4095 of submersible Alvin, 23°32.06′S, 115°34.17′W, 2596 m) and during GEOCYARISE 1 and 3 cruises also on the East Pacific Rise but at a location more than 3000 km distant to the north (around 13°N). Only one specimen has been collected very recently during cruise PARS5 , from the southernmost location. A preliminary study of a single bulge and its axis was made during this work, with rather uncertain results for the specific identification. The spicules are rather similar to those of the holotype, although with a few significant differences. The rugose subtylostyles of the coat were not observed, possibly because they are located only on the main stalk, not studied, and there are numerous sigmancistras 40–65 µm long, not found in the holotype. It is likely that these differences come under specific variability, especially given the geographically rather distant location of the holotype and the PARS 5 specimen (725 km), implying a wide distribution of C. lampadiglobus on the East Pacific Rise. However , these differences are of the same order as those found between the holotype and the specimens from the North Pacific identified as C. concrescens by Koltun (1970). Accordingly, the identification of the PAR 5 specimen and the uncollected specimens to the new species is made with reservation, pending collection of more individuals .

The collected pictures indicate that the sponge could have up to 16 spheres, and that it could be rooted either on patches of thick sediment between pillow lava or directly attached to lava. During the NAUDUR cruise, the sponge was reported by the observers, mostly geologists, as the ‘arbre à boules’ (‘tree with spheres’). The number of ‘arbres à boules’ seen during dive PL06 (when the holotype was collected), and during PL17 (from 18°12.40′S, 113°22.10′W to 18°10.20′S, 113°20.90′W) has been reported by the observer ( V. Ballu, unpubl. report of NAUDUR cruise, Ifremer), allowing a rough estimation of the abundance of the sponge. Seven individuals were observed in PL06 over a distance of 6 km, and 12 individuals including a small one during PL17 over a distance of 4.5 km, between 2586 and 2684 m depth. The sponge is never directly associated with the dense animal fauna of the active sites, but occurs at least several tens of metres from the active smokers, in areas with poor and highly dispersed macrofauna. It has never been observed in the zones where the increasing abundance of the sea anemone Chondrophellia introduces the ‘oasis’ of life surrounding the active smokers ( Geistdoerfer et al., 1995) .

The video made before and during collection of the holotype shows that, contrary to what has been suspected from in situ photographs of a Chondrocladia sp. ( Tendal & Sahling, 1997), there was no fast reaction of the sponges, such as contraction of the spheres, during the few minutes of observation and the spheres are still fully expanded during collection by the arm of the submarine ( Fig. 17B ).

The in situ observation of an unidentified worm, possibly a polychaete, on a sphere of the holotype of C. lampadiglobus is interesting in this carnivorous sponge. The worm is not a prey item trapped by the sponge spicules because it moved significantly during the video sequence. It is possible that it is a commensal feeding on the crustacean debris in the process of digestion observed at the surface of the contracted sphere. Commensalism by polynoid polychaetes has been reported in deep-sea hexactinellid sponges ( Martín, Rosell & Uriz, 1992).

Figures

Figure 3. Chondrocladia koltuni sp. nov. A, sampling of the holotype by the manned submersible MIR, 5249 m depth, photo J. Volodin. B, holotype after preservation (scale bar: 13 mm). C, anchorate isochela 1 (scale bar: 12.3 µm). D, anchorate isochelae 2 (scale bar: 12.3 µm). E, anchorate isochelae 1, back view (scale bar: 7.6 µm). F, sigma 2 (scale bar: 7.3 µm). G, two styles from rhizoid (scale bar: 170 µm). H, head of a style from the cover of the stalk (scale bar: 93 µm). I, style of the stalk (scale bar: 106 µm).

Figure 4. Chondrocladia lampadiglobus sp. nov. A, holotype (scale bar: 17 mm). B, tylostyle of the cover of the stalk (scale bars: 42 µm and 4.2 µm). C, style of the stalk (scale bar: 30 µm). D, style of the body surface (scale bar: 63 µm). E, anchorate isochelae 1 (scale bar: 14 µm). F, anchorate isochelae 1 (scale bar: 9.6 µm). G, two anchorate isochelae 2 (scale bar: 7 µm). H, sigma (scale bar: 10 µm).

Figure 17. A, Chondrocladia lampadiglobus sp. nov., holotype, 2714 m (Ifremer/Naudur). Inset: unidentified worm gliding on the lower left sphere of A, changing position during the video sequence. B, C. lampadiglobus, collection of the holotype by the arm of ‘Nautile’ submersible (Ifremer/Naudur). C, presumed C. lampadiglobus, GEOCYARISE 3 (CY 30), 2622 m, 12°54′N, 103°58′W (Ifremer/Geocyarize 3). D, presumed C. lampadiglobus, GEOCYARISE 1 (CY 07), 2623 m (Ifremer/Geocyarize 1). E, collection of Abyssocladia formosa sp. nov. by the arm of ‘Nautile’ submersible, 1997 m (Ifremer/ Starmer 1). F, three presumed Cladorhiza segonzaci sp. nov. on a dead chimney on the tip of which was attached C. segonzaci and Abyssocladia naudur sp. nov. (Ifremer/Naudur).