Geodia parva, HANSEN, 1885

Cárdenas, Paco, Rapp, Hans Tore, Klitgaard, Anne Birgitte, Best, Megan, Thollesson, Mikael & Tendal, Ole Secher, 2013, Taxonomy, biogeography and DNA barcodes of Geodia species (Porifera, Demospongiae, Tetractinellida) in the Atlantic boreo-arctic region, Zoological Journal of the Linnean Society 169 (2), pp. 251-311 : 293-298

GEODIA PARVA HANSEN, 1885

GEODIINAE P PARVA (PhyloCode SPECIES NAME)

( FIGS 21–23 , TABLE 5)

Geodia parva, Hansen, 1885, p. 17 .

Isops phlegraei pyriformis, Klitgaard & Tendal, 2004: p. 57 (synonymy by this study).

Misidentifications: Isops pyriformis, Hentschel, 1929: p. 865 . Geodia phlegraei, Koltun, 1964 (in part?): p. 148; Koltun, 1966 (in part): p. 55; Cárdenas et al., 2011 (in part): table S1; Murillo et al., 2012 (in part?): p. 842. Geodia cf. phlegraei, Wagoner et al., 1989: p. 2344 .

Type material examined

Geodia parva , unknown station, Norwegian North Sea Exp. 1876–78, ZMBN 100 (wet specimen) .

External morphology and cortex: It seems there are two morphotypes for this species. The first morphotype can be found in true Arctic waters (Norwegian Sea, Greenland Sea, Davis Strait) – it is very characteristic and different from G. phlegraei ; this morphotype is the one described below. The second morphotype, henceforth called the mixed-water mor- photype, is found in areas where Arctic and Atlantic waters mix ( Denmark Strait, Flemish Cap) and has a mix of characters of the Arctic morphotype and G. phlegraei (cf. Discussion for its description). Arctic morphotype: Juveniles are spherical. Larger specimens are more or less spherical, flattened and cupshaped ( Fig. 21A–C ); the largest specimens are 26 cm in diameter ( Klitgaard & Tendal, 2004), so G. parva reaches smaller sizes than G. phlegraei . Specimens from the Schultz Massive Seamount (Biodeep and H2deep Expeditions) can be fairly irregular ( Fig. 21D ). Root-like structures at the base are fairly common. Budding is commonly observed, and the buds are string like ( Fig. 21D ) to more massive (e.g. club-shaped). Most specimens have a dense fur covering the whole body, even the top surface where the oscules are found ( Fig. 21A, B ). In dredged specimens, this fur is often lost except in sheltered folds ( Fig. 21E ). Colour alive is whitish to light brownish. With the openings usually lighter-coloured this gives the sponge a characteristic mottled appearance. The cortex is very thin to thin (0.15–0.7 mm thick) ( Fig. 21G, H ), flexible, and easily cut (no breakage in large pieces as in G. phlegraei ). Many epibionts (e.g. sponges) are present in this hispid part ( Fig. 21B ). Uniporal oscular openings are up to 1 mm in diameter, and are found mainly on the upper surface ( Fig. 21E ). Oscular openings are often wide and surrounded by a white rim (more rarely conical elevations), as in many specimens of G. phlegraei . Uniporal pores (up to 1 mm in diameter) ( Fig. 21F ) are scattered on the sides and partly on the underside of the body. Pores can be very slightly elevated and are usually surrounded by a white margin.

Description of holotype: The type material of G. parva is composed of one very small spherical sponge (4 mm in diameter) and a small piece of cortex of another specimen (3 mm). This explains the name given to this species: ‘parva’ means ‘small’ in Latin. The small piece of cortex has been completely used for spicule and SEM preparation ( Fig. 22E, F ), and the resulting slides and SEM stub are now stored at the ZMBN under the same number.

Spicules ( Fig. 22 , Table 5): Megascleres: (a) oxeas, sometimes modified to styles, length: 773–7935 Mm; width: 14–102 Mm. (b) Orthotriaenes, dichotriaenes are fairly rare, rhabdome length: 360–5395 Mm; width: 20–108 Mm; orthotriaene clad length: 102– 1008 Mm; protoclad length: 56–405 Mm; deuteroclad length: 44–521 Mm. (c) Anatriaenes are fairly rare, rhabdome length: 1–16 mm (minimum length measured by Hentschel, 1929); width: 15–34 Mm; clad length: 29–78 Mm. (d) Meso/protriaenes, very rare, clades are slightly forward or even slightly backward, with or without a central clad, rhabdome length: 840–8371 Mm; width: 9–68 Mm; clad length: 36– 161 Mm; central clad length: 60–334 Mm. Microscleres: (e) sterrasters, spherical with a ‘bumpy’ appearance and commonly irregular (Arctic morphotype), usually spherical, but also sometimes elongated, similar to the sterrasters of G. phlegraei (mixed-water morphotype), 56–104 Mm in diameter (Arctic morphotype); length: 68–124 Mm (mixed-water morphotype); thickness: 52–56 Mm; shallow and large hilum: 16–25 Mm. Rosettes are made of 10–15 piled smooth rays. Rosette diameter: 6–8 Mm. (f) Spherasters with fairly spiny actines which look almost blunt under an optical microscope and commonly irregular (Arctic morphotype), spherasters with less spiny actines, which look more conical and pointy under an optical microscope as in G. phlegraei (mixed-water morphotype), 10–30 Mm in diameter. (g) Oxyasters, smooth or more rarely slightly rough actines, 10–72 Mm in diameter.

DNA barcodes: GenBank accession no. HM 592690 (Folmer COI). We have sequenced COI from specimens from Spitsbergen (1), the Schultz Massive Seamount in the Greenland Sea (3), the Davis Strait (1), the Flemish Cap (2), and Orphan Knoll (1): the Folmer COI is identical in all these specimens. No. KC481223 (18S), obtained from ZMBN 85210 (Schultz Massive Seamount).

Distribution ( Fig. 23 ): Arctic distribution. It has been found at depths from 100 m [Canadian Ice Island ( Wagoner et al., 1989)] to 2747 m (Orphan Knoll), at temperatures of –1.5 °C ( Wagoner et al., 1989) to 4.4 °C (Ingolf Exp. st. 90).

Biology: Associated fauna has never been closely investigated but, as in G. phlegraei , our observations suggest that many macrosymbionts grow on its fur, especially sponges ( Fig. 20B ): Hexactinellida, Hexadella dedritifera , Asbestopluma (A.) lycopodium ( Levinsen, 1887) , Craniella infrequens ( Carter, 1876) , etc. H. nagelfar (chiton) and the parasitic foraminiferan H. sarcophaga have not been observed on G. parva , but these two species do not actually thrive in cold waters.

Distinctive characters: External morphology (Arctic morphotype): bumpy/wrinkled surface and thin flexible cortex (c. 0.5 mm). Budding. Hispidity all over the sponge and overgrown with other sponges, etc. Spicules: spherical small sterrasters (56–92 Mm), some irregular sterrasters.

Remarks: Koltun (1966) noted a different G. phlegraei morphotype of the Norwegian Sea, the Greenland Sea, and the central part of the Arctic Ocean. They are smaller, brighter in colour, with a thinner cortex (0.5–0.9 mm) and their spherasters have blunt rays (instead of being pointy). Klitgaard & Tendal (2004) also recognize this morph and consider the boreal and arctic form to be subspecies by calling them Isops phlegraei phlegraei and I. phlegraei pyriformis (arctic subspecies). They in fact sometimes occur in the same catch, in the hydrographically mixed regions of the Denmark Strait (Stations 78, 90, and 92 of Ingolf Exp.), the south-western Barents Sea, and at Orphan Knoll ( Fig. 23 ). As we have shown above, I. pyriformis is a synonym of I. phlegraei and is therefore not an available name. On the other hand, a re-examination of the type material of G. parva ( Table 5, Fig. 22 ) showed that it belonged to the arctic population.

The most obvious differences between G. phlegraei and G. parva are that G. parva show budding and have a thin flexible cortex which gives a characteristic bumpy wrinkled surface appearance. We have never seen buds in G. phlegraei , and its cortex is thick and stiff. Koltun (1966) also notes that oxeas are often modified to styles in G. phlegraei ; we have observed this, but only in G. parva . The presence of irregular sterrasters is fairly common in G. parva ( Fig. 22F ) but never observed in G. phlegraei . Furthermore, the 1-bp difference (position 370, A in G. phlegraei , C in G. parva ) between the COI of the two species is consistent. It reflects the close phylogenetic relationship of these species but also suggests that they may have completely diverged. 18S being far more conserved than the Folmer COI marker, we observed no differences between the 18S of G. phlegraei and G. parva . We therefore gather here enough morphological and molecular evidence to upgrade these two subspecies to two sister species: G. phlegraei and G. parva (here officially resurrected).

We remain troubled by the specimens collected in areas where Atlantic and Arctic waters mix ( Denmark Strait, Flemish Cap), which essentially includes specimens from St. 90 (Ingolf Exp.) and from the NEREIDA campaign off Newfoundland. Using the COI marker, specimens from the Flemish Cap were identified as G. parva . However, their external morphology may in some occasions be closer to G. phlegraei [thicker cortex, up to 1.8 mm ( UPSZMC 78279), oscules with conical elevations, smooth surface]. Their spicules make us also think of G. phlegraei (larger sterrasters and regular less spiny spherasters). Without a molecular marker they are almost impossible to identify for some of them. The status of these populations is therefore questioned: these could be G. parva populations in different environmental conditions (mixing of waters) or G. phlegraei / parva hybrids. Faster evolving genetic markers are clearly needed to settle this matter.

The specimens identified by Hentschel (1929) as I. pyriformis were collected in arctic deep waters (1000 m depth) along with typical arctic species (e.g. G. hentscheli , Stelletta rhaphidiophora Hentschel, 1929 ). Furthermore, sterraster measurements (81– 91 Mm) fit well with those of G. parva ( Table 5). Pictures of the specimens described by Hentschel ( ZMB Por 7542, 7543, 7544, and 8420, courtesy of C. Lueter) confirm that these are G. parva . Also, Koltun (1964) records G. phlegraei from the Greenland Sea (Obb, 1956, st. 7, 1441 m, -0.4 °C), south-west of Spitsbergen (Lena, 1958, st. 2, 759 m, ca 0.65 °C) and north-west of Franz Josef Land (F. Litke, 1955, st. 26, 415 m, 0.4 °C). We suppose that G. phlegraei specimens from station 7 (Obb, 1956) are G. parva because only typical Arctic species were collected at this deep station with negative temperature: Craniella infrequens , Stelletta rhaphidiophora , and Thenea abyssorum Koltun, 1964 . Concerning stations 26 and 2, we cannot be sure.

The phylogenetic position of the G. phlegraei + G. parva clade in the Geodiinae is still very uncertain, except that it does not belong to the three wellsupported clades Cydoniump, Depressiogeodiap, or Geodiap ( Fig. 2 ). Contrary to the Cydoniump and Depressiogeodiap clades which, for the time being, only include Atlantic species, the G. phlegraei + G. parva clade forms a well-supported clade with Geodia intermedia ( Wiedenmayer, 1989) from Southern Australia.

Figures

Figure 2. Molecular phylogeny of the Geodia genus, modified from Cárdenas et al. (2011: figure 2). Maximum-likelihood tree made from concatenated sequences of COI (Folmer fragment) and 28S (C1-D2 domains). Bootstrap nodal support values are given above the nodes: *, ± 75%; +, ±99% (2000 replicates).

Figure 20. Spicules of the holotype (BMNH 1910.1.1.840) of Geodia phlegraei Sollas, 1880b. A, oxyasters. B, spherasters. A and B have the same scale. C, orthotriaene. D, sterrasters. E, close-up on the hilum of a sterraster. Note the smooth rosettes. Scale bar: 3 Mm.

Figure 21. External morphology and thick sections of Geodia parva Hansen, 1885. A, specimens from Canadian Ice Island at 81°N, 130 m depth (Wagoner et al., 1989). B, specimen collected on the Schultz Massive Seamount (H2DEEP Exp. 2008). The three arrows point to other sponges living on the specimen: Hexadella dedritifera, Asbestopluma (A.) lycopodium and a large white hexactinellid. C, UPSZMC 76801 (left) and 76802 (right) from eastern Greenland, 1900 m depth (Swedish Polar Exp. 1900). D, specimen ZMBN 85210, budding (arrows point to the buds), from the lower slope of the Schultz Massive Seamount, 1997 m depth (BIODEEP Exp. 2007). E, uniporal oscules (UPSZMC 76802). F, uniporal pores (UPSZMC 76802). G, thick section (ZMBN 85210, Schultz Massive Seamount, 1997 m depth). H, thick section (PC553, Schultz Massive Seamount, 688 m depth). Scale bars: B: 10 cm; E and F: 1 cm; G and H: 1 mm.

Figure 22. Spicules of Geodia parva Hansen, 1885. A, orthotriaene (UPSZMC 76801, eastern Greenland). B, oxyaster (UPSZMC 78273, Flemish Cap). C, oxyaster and spheraster (UPSZMC 76801). D, two spherasters (UPSZMC 76801). E, spheraster (ZMBN 100, holotype). F, sterraster (ZMBN 100, holotype). G, sterraster (ZMBN 85210, Schultz Massive seamount). H, close-up on the hilum of a sterraster. Note the smooth rosettes (UPSZMC 76801). Scale bar: 3 Mm. I, sterrasters (regular and irregular) (UPSZMC 76801). All sterrasters of this plate are at the same scale (10 Mm). C and D are at the same scale (3 Mm).

Figure 23. Distribution of Geodia phlegraei Sollas, 1880b (dark dots) and Geodia parva Hansen, 1885 (light dots). White dots represent specimens of G. phlegraei or G. parva but that we could not assign to the proper species for various reasons (map made with GeoMapApp, http://www.geomapapp.org). T, type locality.