Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species

Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

Contents lists available at ScienceDirect

Deep-Sea Research II journal homepage: www.elsevier.com/locate/dsr2

Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species Melina Dressler-Allame a, Christian Göcke a, Daniel Kersken a, Alexander Plotkin b, Dorte Janussen a,n a b

Senckenberg Research Institute and Nature Museum, Senckenberganlage 25, D-60325 Frankfurt am Main, Germany Department of Biology, Postbox 7803, University of Bergen, 5020 Bergen, Norway

art ic l e i nf o

a b s t r a c t

Keywords: Antarctic Cladorhiza Asbestopluma Chondrocladia Lycopodina Porifera

This paper presents 29 sponges of the family Cladorhizidae Dendy, 1922 sampled at 18 different stations in the Weddell Sea, Antarctic during two expeditions of RV Polarstern, PS61 ANT-XIX/2 ANDEEP 2 in 2002 and PS67 ANT-XXII/3 ANDEEP 3 in 2005. Fourteen species from four genera have been registered – one species of Asbestopluma Topsent, 1901, five species of Chondrocladia Thomson, 1873, three species of Cladorhiza Sars, 1872 and five species of Lycopodina Lundbeck, 1905. Six species are endemics of the Southern Ocean. Four species were previously only known from the areas north of the Antarctic and our records of them are thereby new for this region. Two species of Lycopodina, Lycopodina rhabdostylophora sp. nov. and Lycopodina pediculifera sp. nov., are new to science. Our study has considerably expanded the data on diversity of Cladorhizidae in the Southern Ocean. About 27 cladorhizid species (18–19% of global cladorhizid diversity) are now recorded for this region, of which 56% are endemics. & 2016 Elsevier Ltd. All rights reserved.

1. Introduction According to the World Porifera Database (http://www.mar inespecies.org/porifera on 2016-05-24) currently 8731 valid species of Porifera exist. The phylum Porifera is divided into four classes, all of which are present in the Southern Ocean: Demospongiae, Hexactinellida, Calcarea, and Homoscleromorpha (Janussen and Downey, 2014; Van Soest et al., 2012). In Antarctic benthic shelf communities, Porifera are an important component in terms of species numbers (400 species), abundance and biomass (Dayton et al., 2016; Downey et al., 2012; Janussen and Downey, 2014; Janussen and Tendal, 2007; McClintock et al., 2005). Furthermore, sponges have manifold functional roles within benthic communities (Bell, 2008; Kersken et al., 2014) The diversity of sponges is believed to have been caused by several physical (e.g. ACC), geological (e.g. high age and large area) and ecological factors (e.g. tolerance of varied substrates) (Grey, 2001; Janussen and Downey, 2014; Starmans and Gutt, 2002). The Antarctic sponge fauna is largely endemic (44% of species) because of temporal and biogeographic isolation (Clarke and Crame, 2010; Janussen and Downey, 2014; McClintock et al., 2005). Other common features concerning the distribution of Antarctic sponges are supposed to be circumpolarity (35% of species) and eurybathy (wide n

Corresponding author. E-mail address: [email protected] (D. Janussen).

depth range: 425% of sponges) (Janussen and Downey, 2014). Furthermore, recent studies showed that species richness of Antarctic sponge communities is significantly influenced by changes in bottom water tempereature, whereas increasing temperature causes decreasing species numbers (Kersken et al., 2016). This paper focusses on Antarctic Cladorhizidae Dendy, 1922, which are one of the pivotal families in the class Demospongiae (Hestetun et al., 2016). Demospongiae are the largest class within the phylum Porifera, comprising 83% of all sponge species (Van Soest et al., 2012). The class consists of 15 orders, 88 families and 500 genera (Hooper and Van Soest, 2002). In the Southern Ocean, 75% of all sponge species are demosponges. Seventy Antarctic sponge families are known with 47 belonging to the Demospongiae and comprising a total of 293 species (Janussen and Downey, 2014). Cladorhizids are recorded worldwide and predominate in the deep-sea. Ten cladorhizid genera are currently described (http:// www.marinespecies.org/porifera on 2016-05-24). In general, Cladorhizidae are characterized by the carnivorous feeding mode as an adaptation to life in nutrient-poor deep-sea habitats and by the lack of an aquiferous system and choanocytes. A rudimentary aquiferous system occurs only in the genus Chondrocladia, where it is used for the inflation of the turgescent spheres (Van Soest et al., 2012). Cladorhizid sponges capture small prey passively with their numerous filaments that protrude from the head and extend into

http://dx.doi.org/10.1016/j.dsr2.2016.08.006 0967-0645/& 2016 Elsevier Ltd. All rights reserved.

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

2

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

the surrounding water. Hook-like microscleres are located on the surface of the filaments which function during the prey capture. The usual prey organisms are small crustaceans (Copepoda, Isopoda, Ostracoda, Mysidacea) and small free-living polychaete worms (Polychaeta) (Vacelet and Duport, 2004). Based on the material sampled during the ANDEEP I-III and SYSTCO I expeditions, Göcke and Janussen (2013a) presented an ecological and zoogeographic review of the sponge assemblages in the Weddell Sea. Of all species composing these assemblages, 5% were Calcarea, 20% were Hexactinellida and 75% were Demospongiae, including 21 species of Cladorhizidae, of which 15 deepwater species are thoroughly described in the present study. The distribution of the Cladorhizidae ranged from lower shelf regions to abyssal plains, with most of the species occurring in bathyal and abyssal depths. The genera Cladorhiza Sars, 1872 and Asbestopluma Topsent, 1901 were found to co-occur in the Weddell Sea. Cladorhiza spp. were also common in abyssal depths of the central Weddell Sea and Asbestopluma spp. were found at shallower near shore environments and seamounts. Chondrocladia occurred at the western shelf edge areas, the continental slope (Queen Maud Land) and the American-Antarctic Ridge. Due to their results, Göcke and Janussen (2013a) subdivided the sponge fauna into three communities: the Polymastia/Tentorium (shelf/slope fauna), the Bathydorus (continental slope/upper abyssal) and the Caulophacus (abyssal) community. Cladorhizids are especially part of the two latter communities. The aim of our study is the taxonomic description of the cladorhizid sponges sampled during the expeditions ANDEEP II and ANDEEP III in the Weddell Sea. The study is a part of the ANDEEP project, which was focused on the investigation of the biodiversity and distributional patterns as well as the colonization and

exchange processes of deep-sea species. Before the ANDEEP expeditions, data on sponges communities in the deep Weddell Sea were rare, because only few previous cruises had taken deepsea samples (Janussen and Tendal, 2007). Our results, based on novel material, considerably expand the knowledge about the taxonomy and biogeography of Cladorhizidae.

2. Material and methods Sponges analyzed in this study were sampled during two expeditions of RV Polarstern: PS61 ANT-XIX/2 ANDEEP II in 2002 and PS67 ANT-XXII/3 ANDEEP III in 2005. This material comprises 10 specimens from ANDEEP II and 19 specimens from ANDEEP III (Fig. 1). The sponge samples were collected by Agassiz trawl (AGT), Epibenthic sledge (EBS) and Box corer (BC). Samples were collected at depths between 800 and 5000 m (Table 1). On deck, all samples were washed with sea-water, pre-sorted, photographed and labeled. Samples were preserved in undenatured Ethanol (96%). Spicule preparations were done following the standard procedure (Boury-Esnault and Rützler, 1997): a sample of about 2 mm3 was dissolved in a test tube with nitric acid (HNO3, 53%) and heated using a Bunsen burner. In some cases, the whole specimen had to be used for preparation, because of its small size. Afterwards the spicules were washed three times with deionized water and two or three times with pure ethanol (96%). Remaining spicules were mounted on glass slides with Euparal or Canada balsam. For SEM-investigation, spicules were mounted on stubs and sputter coated. The spicule assortment of all sponges was determined and 30 spicules of each type were measured using a light microscope

Fig. 1. Sample stations of Cladorhizidae: Black dots represent the proportional number of specimens collected from the ANDEEP I-III expeditions.

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

3

Table 1 Species list, showing geographical coordinates, sample depths (m), date, number and gears of the two expeditions PS61 ANT-XIX/2 (ANDEEP II) and PS67 ANT-XXII/3 (ANDEEP III). Genus

Specie

Depth [m]

Latitude

Longitude

Date

Station

SMF

Expedition

Gear

Asbestopluma Chondrocladia

A. (A.) belgicae C. (C.) albatrossi C. (C.) antarctica

4658 4995 4075.3 3947.4 3947.4 4075.3 4995 839.6 839.6 3099

 67.506944°  63.774722°  65.329722°  58.251944°  58.251944°  65.329722°  63.774722°  58.731944°  58.731944°  70.658333°

 00.060833°  33.781667°  48.034722°  24.367500°  24.367500°  48.034722°  33.781667°  25.204444°  25.204444°  14.733889°

14.02.05 14.03.02 09.03.02 19.03.02 19.03.02 09.03.02 14.03.02 25.03.02 25.03.02 22.02.05

A3#059-5 A2#137-3 A2#134-3 A2#139-5 A2#139-5 A2#134-3 A2#137-3 A2#143-3 A2#143-3 A3#080-5

11485 11479 11477 11480 11432 11482 11483 11481 11481b 11472

ANT-XXII/3 ANT-XIX/2 ANT-XIX/2 ANT-XIX/2 ANT-XIX/2 ANT-XIX/2 ANT-XIX/2 ANT-XIX/2 ANT-XIX/2 ANT-XXII/3

EBS AGT AGT AGT AGT AGT AGT AGT AGT GKG

2620 4805 4704 4725

 63.574333°  65.576111°  65.014167°  41.138056°

 50.691333°  36.521667°  43.004167° 09.945278°

14.03.05 06.03.05 09.03.05 26.01.05

A3#121-7 A3#102-11 A3#110-2 A3#016-10

11473 11485 11486 11501

ANT-XXII/3 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3

EBS AGT AGT EBS

3683 1123 4725 4725 4575 1823 2186 2186 4895 2620 4427 4725 4658 4933 4895

 59.674722°  65.344444°  41.138056°  41.138056°  47.681389°  69.418611°  71.165556°  71.165556°  66.637778°  63.574333°  70.523611°  41.138056°  67.506944°  68.065000°  66.637778°

 57.595278°  54.236389° 09.945278° 09.945278° 04.274167°  05.336667°  14.018333°  14.018333°  27.089167°  50.691333°  14.593889° 09.945278°  00.060833°  20.642500°  27.089167°

27.01.02 07.03.02 26.01.05 26.01.05 29.01.05 10.02.05 21.02.05 21.02.05 02.03.05 14.03.05 24.02.05 26.01.05 14.02.05 27.02.05 02.03.05

A2#042-2-5 A2#133-3 A3#016-10 A3#016-10 A3#021-7 A3#057-3 A3#078-9 A3#078-9 A3#094-11 A3#121-7 A3#081-8 A3#016-10 A3#059-5 A3#088-11 A3#094-11

11484 11501 11502 11503 11504 11433 11433b 11434 11500 11506 11505 11486 11487 11488

ANT-XIX/2 ANT-XIX/2 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3 ANT-XXII/3

EBS EBS EBS EBS EBS AGT EBS EBS AGT EBS EBS EBS EBS AGT AGT

C. (C.) cf. burtoni C. (C.) clavata C. (M.) turbiformis Cladorhiza

C. cf. moruliformis C. tridentata

Lycopodina

L. callithrix

C. sp.

L. L. L. L.

calyx pediculifera sp. nov. rastrichela rhabdostylophora sp. nov.

(Axiolab, Carl Zeiss) and a SEM (REM CS24, CamScan). Measurements were usually taken with the highest possible magnification. The values were taken in the schema as shown in Fig. 2. All investigated specimens are stored in the Porifera collection of the Forschungsinstitut und Naturmuseum Senckenberg, Frankfurt am Main (SMF, SeSam database: http://sesam.senckenberg.de/ page/index.htm).

3. Results The twenty-nine cladorhizid sponges from the ANDEEP II and III expeditions represent 14 species of the family Cladorhizidae: Two of these are new to science while four are new records for the Southern Ocean. The species belong to four genera: Asbestopluma Topsent, 1901 (1 species), Chondrocladia Thomson, 1873 (5 species), Cladorhiza Sars, 1872 (3 species) and Lycopodina Lundbeck, 1905 (5 species). Taxonomy follows the World Porifera Database (http://www.marinespecies.org/porifera on 2016-05-24). Class Demospongiae Sollas, 1885. Subclass Heteroscleromorpha Cárdenas, Perez & BouryEsnault, 2012. Order Poecilosclerida Topsent, 1928. Family Cladorhizidae Dendy, 1922.

Material: One specimen from station 059-5 (ANDEEP III), 4,658 m, 67° 29.850 S and 0° 3.390 W, 14.02.2005. Description: External morphology: The specimen has a delicate, feather-shaped habitus (Fig. 3A) with 0.5–1.0 mm long filaments attached laterally in a more or less right angle without distinct order. The color is white-yellowish. The total length of the specimen is 8 mm. Spicules (Table 2): Megascleres – Mycalostyles (Fig. 3C) 940– 1320 mm long and 17–25 mm wide. Subtylostyles (Fig. 3B) 480– 650 mm long and 4–13 mm wide. At the blunt end or along the shaft, tyles are present. Microscleres – Palmate anisochelae of the typical form with a gently curved shaft, 8.0–12.8 mm long (Fig. 3 E and F). Sigmas or occasionally Sigmancistras are 19–24 mm long and differently curved and contorted (Fig. 3D). Remarks: Reports of A. (A.) belgicae exist from both shelf (370– 569 m) and deep sea habitats (3147–3896 m). The species has been found in the Antarctic as well as in areas close to the equator (western coast of Africa at Gabon-Congo) (Hestetun et al., 2015). The morphology of the investigated specimen and its spicules is in high accordance with previous reports. Strongyles as described by Hestetun et al. (2015) are absent, as well as acanthostyles described by Koltun (1964) and Topsent (1901). The collected specimen is only a fragmentary stalk without roots, which might be an explanation why some spicule types are missing.

3.1. Genus Asbestopluma Topsent, 1901 3.2. Genus Chondrocladia Thomson, 1873 3.1.1. Asbestopluma (Asbestopluma) belgicae (Topsent, 1901) Original description: Cladorhiza (Asbestopluma) belgicae Topsent, 1901: p. 23. pl. I Fig. 4, pl. III Fig. 8. Synonymy: Detailed synonym list in Hestetun et al. 2015, p. 1318. Type locality: Antarctic Peninsula, East Antarctic Wilkes Land, South Shetland Island, Southern Ocean.

3.2.1. Chondrocladia (Chondrocladia) albatrossi Tendal, 1973 Original description: Chondrocladia (Chondrocladia) albatrossi Tendal, 1973: pp. 35, 36. Figs. 3 and 4. Type locality: Northeastern Brazil. Material: One specimen from station 137-3 (ANDEEP II), 4,995 m, 63° 46.290 S and 33° 46.540 W, 14.03.2002.

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

4

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

Fig. 2. Parameters for spicule measurements.

Description: External morphology: Stipitate habit (Fig. 4F) with a 2.5 cm long stalk (broken) and 1.5  1.0 cm2 wide head. The head has long thick filaments which are 1–2 cm long and 0.75 mm thick. The color of the sponge is whitish-grey and the consistency is hard with a smooth surface. The skeleton of the stalk and the filaments is axial, built up by styles (Fig. 4G). In the surrounding tissue are free anchorate isochelae. Spicules (Table 3): Megascleres – One kind of style (Fig. 4D and E). The size of styles varies only slightly in different parts of the sponge. Styles in the stalk axis measure 1290–2622 mm in length. Styles in the central body are 1064–1900 mm long. Styles in the apical filaments have a length of 988–1824 mm. Microscleres – One kind of anchorate isochela occurring in three different size categories (Fig. 4A-C) with usually five and occasionally four free teeth at each end, the shaft is gently curved. Isochelae I are 120–145 mm long and 3.4–7.3 mm in diameter. Isochelae II are 50–110 mm long and 4.8–6.7 mm in diameter. Isochelae III measure 17–40 mm in length and 1.9–4.8 mm in width.

Remarks: The specimen matches the original description of C. (C.) albatrossi. There are only few differences: Tendal (1973) describes a low abundance of sigmas which are completely absent in the specimen from ANDEEP II. Furthermore, the large axial styles are missing while the alae number of the main isochelae is identical. So far, this is the only report of C. (C.) albatrossi from the Southern Ocean. The only previous report of the species is from the Swedish deep-sea expedition by the Albatross in 1948 from north-eastern Brazilian sector of the Atlantic Ocean (Tendal, 1973). 3.2.2. Chondrocladia (Chondrocladia) antarctica Hentschel, 1914 Original description: Chondrocladia (Chondrocladia) antarctica Hentschel, 1914: pp. 77–79. pl. IV Fig. 6, pl. VI Fig. 5. Type locality: East Antarctic Wilkes Land, Southern Ocean, Weddell Sea. Material: Three specimens sampled from two stations: One specimen from station 134-3 (ANDEEP II), 4,075.3 m, 65° 19.47' S

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

5

Table 2 Spicule sizes of Asbestopluma (Asbestopluma) belgicae (Topsent, 1901) (mm): Minimum-mean-maximum and number of measured spicules (in brackets). For comparison, the values of A. (A.) belgicae described by Topsent (1901a) and Hestetun et al. (2015) are given. Parameter

Mycalostyles Length Diameter Subtylostyles Length Diameter

SMF11485

Topsent (1901a)

Hestetun et al. (2015)

940.0–1090.8  1320.0 1400 (30) 17.0–20.0  25.0 (30) 23

1010–1449  2070 (90) 17.3–24.2 31.4 (90)

480.0–553.0  650.0 (30) 4.0–8.8  13.0 (30)

610–734  880 (60) 11.0–15.1 18.8 (60)

Acanthostyles Length

800 12–15

200 2.5–3

127–198  284 (60) 1.5 (60)

Diameter Palmate anisochelae Length

8.0–11.3  12.8 (30)

12

11–12.7  14.1 (90)

Sigmas Length

19.2–21.9  24.0 (30)

33

27–30.7  34.5 (90)

and 48° 2.05' W, 09.03.2002. Two specimen from station 139-5 (ANDEEP II), 3,947.4 m, 58° 13.64' S and 24° 29.50' W, 19.03.2002. Description: External morphology: The sponge has a stipitate habit (Fig. 5J and K) consisting of a stalk, which is about 4.0 cm long and a nearly round head (2  1 cm2) with thin filaments. The sponge has a hispid surface and a hard consistency, the color is yellow-white. The specimen SMF11480 is lacking filaments but they are probably just drawn-in. The head is covered with little swellings, which have a dark central spot. The very small specimen SMF11432 was completely used up for preparations, so no description of the habitus can be given. Spicules (Table 4): Megascleres – There are two size categories of styles (Fig. 5H and I). In both specimens styles I are considerably thinner than type II (difference: Ø 11.4 mm). Styles I for specimen SMF11480 measure 1444–4484 mm in length and 40.0–49.6 mm in width, styles II are 1140–4750 mm long and 22.4–37.6 mm wide. In specimen SMF11477 styles I measure 1406–2584 mm in length and 19.2–41.6 mm in width, styles II are 500–1368 mm long and 17.6– 32.0 mm wide. For specimen SMF11432 styles I measure 2508– 3914 mm in length and styles II 850–1862 mm. Microscleres – Tridentate isochelae with a gently curved shaft, subdivided into two size categories (Fig. 5A–D): Chelae I measure 60–105 mm by 5.3– 10.0 mm. Chelae II are 20–55 mm long and 2.2–7.8 mm wide. Contorted sigmas of two size categories (Fig. 5E,F and G): Type I is about 80–105 mm long and 3.0 mm in diameter, while type II has a length of 25–55 mm and a diameter of 1.8–2.8 mm. Type I can be Sor C-shaped, with curved ends while sigmas of type II are all cshaped. Remarks: Despite the lack of filaments in specimen SMF11480 and the missing habitus in SMF11432 the sampled specimens equal each other in morphology, spicule composition and are also very similar to the holotype described by Hentschel (1914). The dark spots on the head of specimen SMF11480 could be the point where filaments are drawn-in. Only two spicule types differ from the original description: sigmas II and styles II. Especially the styles II may represent juvenile forms from the first type as they show similar size but different diameter (Differences: SMF11480 Ø 14.0 mm; SMF11477 Ø 8.8 mm). Hentschel (1914) gives only one value for a smaller type of styles but no comparable values for the

Fig. 3. Asbestopluma (Asbestopluma) belgicae (Topsent, 1901), (A) habitus, (B) subtylostyle, (C) mycalostyle, (D) sigma, (E) anisochela front view, (F) anisochela side view.

diameter are given. Therefore it cannot be proven if both, type I and II, belong to the same category or represent two different types. So far only three detailed reports of the species have been published: Hentschel (1914), Koltun (1964) and Göcke and Janussen (2013b). 3.2.3. Chondrocladia (Chondrocladia) cf. burtoni Tendal, 1973 Original description: Chondrocladia (Chondrocladia) burtoni Tendal, 1973: p. 36. Figs. 5–6. Type locality: Strait of Gibraltar, North Atlantic Ocean, Saharan Upwelling, South European Atlantic Shelf. Material: Two specimens sampled from two stations: One specimen from station 134-3 (ANDEEP II), 4,075.3 m, 65° 19.470 S and 48° 2.050 W, 09.03.2002. One specimen from station 137-3 (ANDEEP II), 4,995 m, 63° 46.290 S and 33° 46.540 W, 14.03.2002. Description: External morphology: The fragmentary specimen SMF11482 has a feather shaped habitus (Fig. 6J) with 0.25 mm long processes and a white-yellow color. The sponge has a length of 1.7 cm, however, the stalk and roots are missing. Specimen SMF11483 has a slender stalk and an elongate body with filaments, protruding in different directions (Fig. 6K). Upper head and crossing section between head and stalk are free of processes. The remaining stalk is 0.5 cm long, processes are 0.7 cm long. Surface of the sponge is rough while consistency is rigid. Spicules (Table 5): Megascleres – One kind of style in both specimens (Fig. 6A and B). Specimen SMF11482: Length of styles is 810–2242 mm with a diameter of 10.0–38.3 mm. Specimen SMF11483: Styles are 590–1634 mm long and 16.0–38.8 mm in width. The styles show their maximum diameter in the middle of

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

6

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎ Table 3 Spicule sizes of Chondrocladia (Chondrocladia) albatrossi Tendal, 1973 (mm): Minimum-mean-maximum and number of measured spicules (in brackets). For comparison, values of C. (C.) albatrossi from Tendal (1973) are given. Parameter Styles I (axis) Length Diameter Styles II (axis) Length Diameter Proper body styles Length Diameter Branches styles Length Diameter Anchorate isochelae I Length Diameter Anchorate isochelae II Length Diameter Anchorate isochelae III Length Diameter Sigmas Length Diameter

Fig. 4. Chondrocladia (Chondrocladia) albatrossi Tendal, 1973, (A) isochela III, (B) isochela II, (C) isochela I, (D) head style, (E) stalk style, (F) habitus, (G) section through a head filament.

the shaft, gently decreasing towards the ends. Microscleres – Anchorate isochelae with four teeth (unguiferous) (Fig. 6C, D and H). On each end, two fimbriae are present. In specimen SMF11482 chelae measure 37.5–80.0 mm with a diameter of 3.3–6.4 mm. In specimen SMF11483 chelae are 55.0–76.8 mm long and 3.8–6.3 mm wide. Sigmas are slim and differently curved (Fig. 6E,F and I). Length of sigmas in specimen SMF11482 46.4–90.0 mm, diameter is 2.0–6.4 mm. Sigmas in specimen SMF11483 measure 80–125 mm in length and 3.0–3.5 mm in width. Remarks: The observed specimens both resemble the species Chondrocladia: C. (C.) burtoni Tendal, 1973 and C. (C.) virgata Thomson, 1873. Both species possess the same spicule-types, which differ only slightly in size. The main difference is the habitus. C. (C.) burtoni has a straight axis with several warts while C. (C.) virgata is feather shaped with long processes. The number of teeth, the depth and size of sigmas were the main reasons to determine the specimens to C. (C.) cf. burtoni. The sponges from ANDEEP II have isochelae with four teeth, like in C. (C.) burtoni, while the chelae of C. (C.) virgata have seven teeth. Isochelae in C. (C.) cf. burtoni are in average 17 mm larger than in C. (C.) burtoni. Further, C. (C.) burtoni Tendal, 1973 is described from material sampled during the Atlantic Swedish deep-sea expedition by the Albatross in 1948, in the vicinity of the eastern Mid-Atlantic at 4870 m. C. (C.) virgata Thomson, 1873 from the Strait of Gibraltar at 870 m. The record of C. (C.) cf. burtoni is the first for the Southern Ocean, sampled at 4075–4995 m.

SMF11479

Tendal (1973)

3200–3688  4000 32–44 1290.4–2221.9-2622.0 (30) 23.9–33.1  39.4 (30)

1440–1898  2560 32–44

1064.0–1356.6 1900.0 (10)

800–1744  2240 13–38

988.0–1327.8-1824.0 (17)

960–1744  2080 25–38

120.0–137.7  145.3 (42) 3.4–5.8  7.3 (26)

120–151  170

50.0–76.4  110.1 (21) 4.8–5.6  6.7 (6)

63–82  113

17.0–27.8  40.0 (30) 1.9–3.4  4.8 (24)

13–24 44

38–57

3.2.4. Chondrocladia (Chondrocladia) clavata Ridley and Dendy, 1886 Original description: Chondrocladia (Chondrocladia) clavata Ridley and Dendy, 1886: p. 345. Type locality: New Zealand, Fiji, Ross Sea, Seychelles, Southern Ocean. Material: Two specimens sampled at station 143-3 (ANDEEP II), 839.6 m, 58° 43.550 S and 25° 11.760 W, 25.03.2002. Description: External morphology: Specimen SMF11481 has a stipitate shape, a long stalk and a rounded head (0.8  0.8 cm2) with some processes (0.5 cm long) (Fig. 7F). The transition between stalk and head is 0.58 cm and the stalk is 1.39 cm (broken) long. The color is white-yellow and the surface rough. Specimen SMF11481b has a long stalk (1.5 cm long) with a globular head (1.5 cm) (Fig. 7G) and a white-yellow color. The top of the head is stretched with several processes (0.75 cm long). Spicules (Table 6): Megascleres – Two size categories of styles (Fig. 7A and B). Styles I measure 520–1975 mm in length and 16.0– 38.4 mm in width. Styles II are distinctly smaller in length (difference: Ø 22.9 mm) and occur only in specimen SMF11481. Size: 218– 455 mm long and 3.5–10.2 mm in width. Microscleres – Tridentate isochelae (Fig. 7C-E) with equal ends and three free standing teeth, the shaft is gently curved. Length of the tridentate isochelae is 42.7–70.0 mm with shaft diameter 4.0–8.9 mm. Typical Sigmas c- or s-shaped, C-shaped sigmas 32.0–57.6 mm, s-shaped sigmas 45–56. In specimen SMF11481b no sigmas are present. Remarks: Two major differences exist between the investigated sponges and the original description of C. (C.) clavata: (1) Ridley and Dendy (1886) do not differ between C- and S-shaped sigmas; (2) styles II are missing in the type. These may represent a juvenile form of the styles I. The species has been found quite regularly, reports are published by Kelly et al. (2009) from New Zealand, by Burton (1929a) from the Ross Sea and Southern Antarctic Ocean, by Lévi (1964) from the Seychelles, by Bergquist (1972) from New Zealand, and by Hooper and Van Soest (2002) from Fiji.

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

Fig. 5. Chondrocladia (Chondrocladia) antarctica Hentschel, 1914, (A/B) isochela II, (C/D) isochela I, (E/F) sigma II, (G) sigma I, (H) style I, (I) style II, (J) habitus SMF11480, (K) habitus SMF11477.

7

Fig. 6. Chondrocladia (Chondrocladia) cf. burtoni Tendal, 1973, (A/B) styles, (D) front view of isochela claws, (E/F/I) sigmas, (H/C) side view isochela, (J) habitus SMF11482, (K) habitus SMF11483.

Table 4 Spicule sizes of Chondrocladia (Chondrocladia) antarctica Hentschel, 1914 (mm): Minimum-mean-maximum and number of measured spicules (in brackets). For comparison, the values of C. (C.) antarctica described by Hentschel (1914) are given. Parameter Styles I Length Diameter Styles II Length Diameter Tridendate chelae I Length Diameter Tridendate chelae II Length Diameter Sigmas I Length Diameter Sigmas II Length Diameter

SMF11480

SMF11477

SMF11432

Hentschel (1914)

1444.0–2717.0  4484.0 (32) 40.0–45.0  49.6 (10)

1406.0–1993.7  2584.0 (30) 19.2–31.7  41.6 (23)

2508–3355-3914 (18)

(1100)  2000–2560 45–50

1140.0–2055.1  4750.0 (28) 22.4–31.0  37.6 (20)

500.0–950.9  1368.0 (17) 17.6–22.9  32.0 (7)

850–1319-1862 (16)

63.7–78.6  100.0 (29) 5.3–6.8  8.3 (17)

62.6–78.8  97.0 (30) 5.5–7.0  10.0 (30)

60.0–85.6  105.0 (32)

96–112

20.0–37.8  55.0 (35) 2.2–3.6  5.2 (13)

27.2–35.4  49.6 (26) 2.6–3.9  7.8 (9)

25.0–38.8  55.0 (23)

40–45

80.0–94.2  105.0 (30) 3.0 (30)

90.0 (1)

90–94-100 (5)

96–160

26.5–36.2  55.0 (9) 1.8–2.2  2.8 (9)

33.6 (1)

25.0–30.0-37.5 (5)

3.2.5. Chondrocladia (Meliiderma) turbiformis Vacelet et al., 2009 Original description: Chondrocladia (Meliiderma) turbiformis Vacelet et al., 2009: pp. 59–62. Figs. 2, 3. Type locality: New Zealand, Chatham Rise. Material: One specimen from station 080-5 (ANDEEP III), 3,099 m, 70° 39.300 S and 14° 43.620 W, 22.02.2005.

Description: External morphology: The sponge is of stipitate shape (Fig. 8F) consisting of a round head (4.3  3.6 mm2) supported by a broken stalk (Length: 7.0 mm, diameter: 0.4 mm). Surface of the sponge head is irregular in shape and covered with several short processes (0.5 mm long). Color in ethanol is whiteyellow.

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

8

Table 5 Spicule sizes of Chondrocladia (Chondrocladia) cf. burtoni Tendal, 1973 (mm): Minimum-mean-maximum and number of measured spicules (in brackets). For comparison, the values of C. (C.) virgata described by Thomson (1873) and C. (C.) burtoni described by Tendal (1973) are given. Parameter Styles Length Diameter Tissue styles Length Diameter Isochelae Length Diameter Sigmas Length Diameter

SMF11482

SMF11483

Chondrocladia (C.) virgate Thomson, 1873

Chondrocladia (C.) burtoni Tendal, 1973

810.0–1486.7  2242.0 (30) 10.0–28.2  38.3 (28)

590.0–1133.9 1634.0 (30) 16.0–24.8  38.8 (30)

1552 28.2

1920–2460 2880 25–38 480–1069  1600 13–25

37.5–52.6  80.0 (30) 3.3–4.7  6.4 (30)

55.0–69.2  76.8 (30) 3.8–4.8  6.3 (30)

67.7

40–44 48

46.4–66.2  90.0 (30) 2.0–4.9  6.4 (30)

80.0–107.1 125.0 (30) 3.0–3.1  3.5 (7)

25.4 2.1

44–85 113

Table 6 Spicule sizes of Chondrocladia (Chondrocladia) clavata Ridley and Dendy, 1886 (mm): Minimum-mean-maximum and number of measured spicules (in brackets). For comparison, the values of C. (C.) clavata described by Ridley and Dendy (1886) are given. Parameter

Styles I length Diameter Styles II Length Diameter Tridendate chelae Length Diameter C-sigmas Length S-sigmas Length

Fig. 7. Chondrocladia (Chondrocladia) clavata Ridley and Dendy, 1886, (A) style II, (B) style I, (C/E) side view isochela, (D) front view isochela, (F) habitus SMF11481, (G) habitus SMF11481b.

Spicules (Table 7): Megascleres – One kind of style (Fig. 8A), 874–1368 mm long and 11.5–32.0 mm wide. Microscleres  . Anchorate isochelae, commonly with five or six teeth at each end, occasionally only three or four (Fig. 8C and D). At each end lateral fimbriae are present. Isochelae length is 69–85 mm and shaft diameter 6.7–25.6 mm. Sigmas C- or S-shaped with a length of 32– 54 mm and a diameter of 7–12 mm. (Fig. 8B). Trochirhabds with three whorls (Fig. 8E). Length about 34–51 mm. The diameter of the different rings varies between 5 and 15 mm. Both terminal ends are rounded, whereas the bulge at the thinner end is smaller than the one at the apex. In the middle of a straight shaft are three whorls, with diameter decreasing towards the smaller end. The surface of

SMF11481

SMF11481b

Ridley and Dendy (1886)

600.0– 1167.0  1786.0 (30) 16.0–29.2  36.8 (24)

520.0– 1228.0  1976.0 (30) 17.6–27.8  38.4 (30)

1000 22

218.5–355.2 455.0 (21) 3.5–5.6  10.2 (21)

42.7–58.1  70.0 (30) 4.0–5.6  8.9 (30) 32.0–49.9  57.6 (10)

46.0–51.2  60.4 (24) 4.0–5.2  6.5 (24)

57

44

45.0–52.2  56.0 (9)

the bulges and whorls, with small irregular spines or buttons, whereas the shaft is nearly smooth (only a few buttons). Remarks: The sampled specimen is in general accordance with the species description as given by Vacelet et al. (2009). In contrast to that, the mycalostyles type II, substrongyles and the isochelae type II are missing. The substrongyles are also absent in the holotype of C. (M.) turbiformis and only found in the paratypes (Vacelet et al., 2009). Furthermore they occur in the basal part of the stalk, which is missing in the examined specimen. Mycalostyles of the second type were very rare in the specimens described by Vacelet et al. (2009). Vacelet et al. (2009) furthermore mentioned the possibility that they are juvenile or ill-formed which might be an explanation for their absence. The second type of isochelae is only described for the embryos of C. (M.) turbiformis which are absent in specimen SMF11472 (Vacelet et al., 2009). So far only one record was published by Vacelet et al. (2009). The species is new for the Southern Ocean. Previous records are from the Pyre Seamount and Chatham Rise, New Zealand.

3.3. Genus Cladorhiza Sars, 1872 3.3.1. Cladorhiza cf. moruliformis Ridley and Dendy, 1887 Original description: Cladorhiza moruliformis Ridley and Dendy, 1887: pp. 90–92. pl. XX Fig. 3, pl. XXI Figs. 1, 15 and 19.

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

9

Table 7 Spicule sizes of Chondrocladia (Meliiderma) turbiformis Vacelet et al., 2009 (mm): Minimum-mean-maximum and number of measured spicules (in brackets). For comparison, the values of C. (M.) turbiformis described by Vacelet et al. (2009) are given. Parameter

Styles I Length Diameter Styles II Length Diameter Substrongyles Length Diameter Isochelae I Length Diameter Isochelae II Length Diameter Sigmas Length Diameter Three whorl trochirhabds Length Rings diameter Small terminal end bulb diameter Large terminal end bulb diameter Central disk diameter Small end terminal disk diameter Large end terminal disk diameter

SMF11472

Vacelet et al. (2009)

874.0–1203.9  1368.0 (30) 1000–1700 11.5–25.7  32.0 (25) 15–40 340–1400 4–15 260–1288 12–30 68.8–78.9  84.8 (34) 6.7–20.0  25.6 (26)

68–95 5 32–50.5 2

32.0–40.0  54.4 (22) 7.0–9.9  12.0 (10)

30–50

33.6–43.3  51.2 (30) 5.0–15.0 6.0–7.4  9.0 (30)

30–50 7–20

8.0–11.0  15.0 (30) 5.5–7.0  8.0 (30) 2.0–3.5  6.0 (30) 5.0–7.9  11.0 (30)

Type locality: South West Australian Shelf, East Antarctic Wilkes Land, Southern Ocean. Material: One specimen from station 121-7 (ANDEEP III), 2,620 m, 63° 34.460 S and 50° 41.40 W, 14.03.2005. Description: External morphology: Sponge has a stipitate habitus (Fig. 9C), consisting of a globular body (1.0  0.5 mm2) with several processes (all about 0.5 mm long) and a supporting long stalk (broken: 3 mm). The surface is rough and the consistency hard. Spicules (Table 8): Megascleres – Styles (Fig. 9A and B) about 570–1775 mm in length and 11–26 mm in diameter. Microscleres – Anchorate anisochelae with four free alae and two lateral fimbriae at the large end and three alae at the small end (Fig. 9D). Total length is 16–24 mm and diameter measures 1.8–2.7 mm. C-shaped sigmas with quite small and short endings (Fig. 9E). Length is 43– 105 mm and diameter 3.4–4.9 mm. Remarks: The analyzed specimens resemble two species of Cladorhiza: C. moruliformis Ridley and Dendy, 1887 and C. nematophora Lévi, 1964. However, an absolute classification is not possible. The new specimens differ in morphology and spiculation from the previously described species. C. moruliformis and C. nematophora have larger spicules (Table 8) and the anisochelae are reported to have three alae at each end, while the specimen SMF11473 shows four teeth at the large end and only three at the small end. The reason to determine the specimen as C. cf. moruliformis, however was not the spiculation, but the habitus. C. moruliformis shows a stipitate habitus with the globular head having short rounded processes all of similar length, by what the sponge looks like a mulberry. The habitus of C. nematophora has a globular head as well, but with several long processes. The habitus of SMF11473 is quite similar, the head is globular with several processes but they are not rounded and quite short.

Fig. 8. Chondrocladia (Meliiderma) turbiformis Vacelet et al., 2009, (A) style, (B) sigma, (C/D) isochelae, (E) trochirhabds, (F) habitus.

3.3.2. Cladorhiza tridentata Ridley and Dendy, 1887 Original description: Cladorhiza tridentata Ridley and Dendy, 1887: pp. 95, 96. pl. XX Fig. 9,a, pl. XXI Figs. 16 and 20. Synonymy: Detailed synonymy list see the World Porifera Database (http://www.marinespecies.org/porifera on 2016-05-24). Type locality: Prince Edward Islands, Indian Ocean. Material: Two specimens sampled from two stations: One specimen from station 102-11 (ANDEEP III), 4805 m, 65° 34.340 S and 36° 31.180 W, 06.03.2005. One specimen from station 110-2 (ANDEEP III), 4704 m, 65° 0.85' S and 43° 0.250 W, 09.03.2005. Description: External morphology: Small encrusting sponges of circular shape, without stalk. The surface is smooth without any processes, in the center an osculum-like opening is present (Fig. 11A). The specimen is about 1.2 cm in diameter and very flat with a greyish-yellow color. Spicules (Table 9): Megascleres – One kind of slender subtylostyle (Fig. 10F and J). The tyle is either located at the very top of the style, or may be displaced along the shaft. Some are slightly bent towards the pointed end. Length is 912.0–1162.5 mm and diameter 9.5–17.0 mm. Microscleres – Tridentate anisochelae (Fig. 10B–D) with alae on the large side clearly separated from each other and rounded while alae of the small end possess distinct notches. The shaft is gently curved with lateral fimbriae at the large end of the chela. The chelae measure 51.9–80.0 mm in length and 3.6–12.0 mm in width. Besides the characteristic C. tridentata forms there are also several young anisochelae of the same size (Fig. 10G). They are unguiferous, thinner and without wings. Sigmas are C- or S-shaped with a length of 35.2–91.0 mm and a width of 2–3 mm (Fig. 10 H and I). Specimen SMF11485 has also 28.8– 36.8 mm long C-shaped sigmas with short ends (Fig. 10 E).

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

10

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎ Table 8 Spicule sizes of Cladorhiza cf. moruliformis Ridley and Dendy, 1887 (mm): Minimummean-maximum and number of measured spicules (in brackets). For comparison, the values of C. moruliformis described by Ridley and Dendy (1887) and C. abyssicola described by Lundbeck (1905) are given. Parameter

Styles I Length

Diameter Styles II Length Diameter Anisochelae Length

SMF11473

Cladorhiza moruliformis Ridley and Dendy, 1887

Cladorhiza nematophora Lévi, 1964

570.0– 1072.2  1775.0 (22) 11.0–18.8  26.0 (10)

2000

1800–2500

50

30–45

16.0–20.1  24.0 (33) Shaft Diameter 1.8–2.3  2.7 (8) Sigmas I Length 43.2–72.3  105.6 (38) Diameter 3.4–4.3  4.9 (6) Sigmas II Length Diameter

Fig. 9. Cladorhiza cf. moruliformis Ridley and Dendy 1887, (A) style, (B) blunt end of style, (C) habitus, (D) anisochela, (E) sigma.

Remarks: In general, morphology and spicule composition match C. tridentata as described by Ridley and Dendy (1887) while specimen SMF11486 shows the most similarities. Specimen SMF11485 seems to be a juvenile sponge or in a phase of strong growth, because of its high abundance of juvenile microscleres. Also the second type of C-shaped sigmas might be a juvenile stage of the larger type. The unusual habitus of this species seems to be unique for the genus Cladorhiza and is therefore a distinct feature for species determination. In addition, the species seems to be rather rare. To the date, only two comprehensive descriptions have been published by Ridley and Dendy (1887) and Koltun (1964), all reporting specimens found in the Southern Ocean. 3.3.3. Cladorhiza sp Material: One specimen from station 016-10 (ANDEEP III), 4725 m, 41° 7.770 S and 9° 56.430 E, 26.01.2005. Description: External morphology: Sponge with a globular body (1.25 mm) on top of a short stalk (5 mm) (Fig. 11 A). The stalk goes smoothly over to the underside of the body. The whole upper part of the body is covered by numerous filaments (2 mm). The color is yellowish-white and the surface consistency is both hispid and firm. Spicules (Table 10): Megascleres – Subtylostyles (Fig. 12B) with a tyle on the end of the spicule. Length is 440–830 mm. Microscleres – Anchorate anisochelae with three rounded dents at each end (Fig. 11C and D) and a length of 14.4–19.2 mm. The shaft is gently curved. Remarks: The observed specimen could not be identified to species level. The spicules are similar to those of C. tridentata (Ridley and Dendy, 1887) but the habitus looks completely

900–1400 15–20 63

50–60

350

195–200

14.5

5–6 125–150

different. Our specimen has a globular head with a supporting stalk whereas C. tridentate is dome-shaped, without any stalk or processes. Furthermore, the anisochelae are much larger (mean difference 59.3 mm) and differ in morphology: Chelae in the observed specimen show rounded alae at both ends, while in C. tridentata only the alae at the large end are slightly rounded. The small end shows bifurcated teeth, which seems to be present in this species only. Besides, C. tridentata has a second type of microscleres (sigmas), which are missing in SMF11474. 3.4. Genus Lycopodina Lundbeck, 1905 3.4.1. Lycopodina callithrix (Hentschel, 1914) Original description: Asbestopluma callithrix Hentschel, 1914: pp. 64–66. pl. IV Fig. 3, pl. V Fig. 10. Synonymy: Asbestopluma (Asbestopluma) callithrix Hentschel, 1914. Type locality: Antarctic, East Antarctic Wilkes Land. Material: Nine specimens from seven stations: One specimen from station 042-2-5 (ANDEEP II), 3683 m, 59° 40.290 S and 57° 35.430 W, 27.01.2002; one specimen from station 133-3 (ANDEEP II), 1,123 m, 65° 20.070 S and 54° 14.340 W, 07.03.2002; two specimens from station 016-10 (ANDEEP III), 4725 m, 41° 7.770 S and 9° 56.430 E, 26.01.2005; one specimen from station 021-7 (ANDEEP III), 4575 m, 47° 40.530 S and 4° 16.270 E, 29.01.2005; one specimen from station 057-3 (ANDEEP III), 1823 m, 69° 24.670 S and 5° 19.720 W, 10.02.2005; two specimens from station 078-9 (ANDEEP III), 2186 m, 71° 9.530 S and 14° 0.780 W, 21.02.2005; and one specimen from station 094-11 (ANDEEP III), 4895 m, 66° 38.160 S and 27° 4.810 W, 02.03.2005. Description: External morphology: The specimens have a stipitate habit (Fig. 12A–E) with an approximately 6 mm long stalk and 1–2 mm wide head (globular/oval) which has numerous long and thin filaments. Color is brown-yellowish or white-yellowish alive and in ethanol. The head is supported by a radiate skeleton (without dermal skeleton). The skeleton of the stalk consists of one axis. Some of the specimens are fragmentary with the stalk completely missing or broken. None of these sponges is still attached to its substrate, therefore the roots are missing as well.

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

11

Fig. 11. Cladorhiza sp., (A) habitus, (B) subtylostyle, (C/D) anisochelae. Fig. 10. Cladorhiza tridentata Ridley and Dendy, 1887, (A) habitus, (B) anisochela side view, (C) anisochela front view, (D) anisochela back view, (E) sigma with short ends, (F) subtylostyle, (G) side view of a “young” anisochela, (H) C-sigma, (I) Ssigma, (J) slight swelling on one end of the style.

Spicules (Table 11): Megascleres – One kind of style/subtylostyle (Fig. 12F and G), 180–1600 mm long and 7–18 mm wide. Occasionally small tyles occur at the blunt end (Fig. 12H) or below the blunt end. Microscleres – One kind of palmate anisochela (Fig. 12I–L) with a length of 9–22 mm and width of 4–9 mm (measured at the large alae end). Lateral alae of the small end have two tips while the central tooth has three. Remarks: In general, the investigated specimens match the original description of L. callithrix described by Hentschel (1914) in morphology, spicule size and shape. The specimens show a large individual range of spicule sizes. Most of the styles/subtylostyles from the specimens are quite small (average about 553 mm) and only a few (SMF11502, SMF 11484) have spicules larger than 1000 mm. Large styles of 2000–4000 mm as reported by Hentschel (1914) are missing. The species seems to be quite rare. Only Hentschel (1914) and Koltun (1964) have previously reported it. 3.4.2. Lycopodina calyx (Hentschel, 1914) Original description: Asbestopluma calyx Hentschel, 1914: pp. 66, 67. pl. IV Fig. 4, pl. V Fig. 11. Synonymy: Asbestopluma (Asbestopluma) calyx Hentschel, 1914. Type locality: Antarctic, East Antarctic Wilkes Land, South Georgia. Material: One specimen from station 121-7 (ANDEEP III), 2620 m, 63° 34.460 S and 50° 41.480 W, 14.03.2005. Description: External morphology: Sponge with a stipitate shape (Fig. 13I and J) and a white-yellowish color. It consists of a

Table 9 Spicule sizes of Cladorhiza tridentata Ridley and Dendy, 1887 (mm): Minimummean-maximum and number of measured spicules (in brackets). For comparison, the values of C. tridentata described by Ridley and Dendy (1887) are given. Parameter

Subtylostyles Length Diameter Tridendate anisochelae Length Shaft diameter Sigmas Length Diameter C-sigmas Length

SMF11485

SMF11486

Ridley and Dendy (1887)

950.0– 1054.2  1162.5 (30) 9.5–14.3  17.0 (30)

912.0– 1040.0  1102.0 (30) 11.0–14.2  17.0 (30)

700

51.9–67.3  78.0 (30)

65.0–75.8  80.0 (30) 6.1–9.2  12.0 (28)

3.6–8.5  12.0 (24) 35.2–61.3  91.0 (30)

15.5

76

60.0–74.5  90.0 (14) 90 2.0–2.3  3.0 (5) 3.2

28.8–33.4  36.8 (30)

globular head (3  2 mm2) without filaments and a long stalk. The specimen is complete and still attached to some remains of substrate. The stalk measures 15.3 mm in length and 0.5 mm in width. The surface of the sponge is rough and bears little knobs. The skeletal structure is radial in the head and axial in the stalk. Spicules (Table 12): Megascleres – Three kinds of subtylotyles (Fig. 13C–H), differing by size. Styles I 600–850 mm long and 15– 32 mm wide. Styles II 400–650 mm in length and 9–30 mm in width. Styles III are 150–340 mm long and 6–12 mm wide. The diameter of

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

12

Table 10 Spicule sizes of Cladorhiza sp. (mm): Minimum-mean-maximum and number of measured spicules (in brackets). For comparison, the values of C. tridentata described by Ridley and Dendy (1887) are given. Parameter

Subtylostyles Length Diameter Anchorate anisochelae Length Sigmas Length Diameter

SMF11474

Cladorhiza tridentate (Ridley and Dendy, 1887)

440.0–630.0  830.0 (20)

700 15.5

14.4–16.7  19.2 (30)

76 90 3.2

Fig. 12. Lycopodina callithrix (Hentschel, 1914), (A) habitus SMF 11501, (B) habitus SMF11503, (C) habitus SMF11433, (D) habitus SMF11504, (E) habitus SMF11433b, (F/ G) subtylostyles, (H) swelling at the blunt end from the subtylostyle, I/J: palmate anisochela side view, K: palmate anisochela front view, L: palmate anisochela back view.

the styles I decrease from the middle towards both ends while the diameter of styles II and III are constant along the whole shaft. Microscleres – One kind of anisochela with a length of 14–33 mm (Fig. 13 A and B). Lateral alae are partly connected with the shaft while the central tooth stands free. Alae of the large end have a smooth margin, those of the small end have several little jags. The size of the jags increases towards the shaft. The central tooth of the small end possesses three little jags while the median one is the largest.

Remarks: Morphology, spicule size and shape are in accordance with the original description of L. calyx by Hentschel (1914). Spicules of our newly sampled specimen are slightly larger (Subtylostyles I: Ø 209.3 mm longer; Subtylostyles II: Ø 156.7 mm longer) whereas the specimen itself is smaller (1.6 cm; Length of L. calyx Hentschel, 1914 5 cm). The species appears to be quite rare. Only two detailed reports are given by Hentschel (1914) and Koltun (1964). Previous records were sampled in shallow shelf and bathyal depths between 46 and 540 m (Hentschel, 1914; Koltun, 1964) while the ANDEEP IIIspecimen was sampled from more than 2000 m for the first time (2620 m). In 2014 Lopes and Hajdu described a similar specimen (Asbestopluma (A.) cf calyx) from deep sea coral mounds in the Campos Basin (SW Atlantic, Brazil; 1077 m). Their specimen differs from Lycopodina calyx by having a second type of styles, straight or slightly bent without an acerate point, and a different morphology of the habitus, as it shows a cup shaped apical body, processing several long sinuous peduncles. Lycopodina calyx consists of a globular head without any filaments. 3.4.3. Lycopodina pediculifera sp. nov Type locality: Antarctic Weddell Sea. Material: One specimen from station 081-8 (ANDEEP III), 4427 m, 70° 30.850 S and 14° 34.980 W, 24.02.2005. Diagnosis: White-yellow sponge formed like a calyx, stalked, surface densely covered with protruding spicules. Spicules: (Subtylo)Styles I: 1786–2774 mm. Subtylostyles II: 390–730 mm. Subtylostyles III: 160–355 mm. Styles I: 600–1080 mm. Styles II: 1615–1950 mm. Anisochelae I: 33.6–41.6 mm. Anisochelae II: 22.4–27.2 mm. Forceps: 52.8–83.2 mm (Table 13). Description: External morphology: L. pediculifera sp. nov. possesses a head which is formed like a calyx (Fig. 14 A). The whole surface of the head is densely covered by protruding spicules (up to 2 mm long). The stalk is fixed to a little piece of rock and has a length of 3 mm while the head measures 3  3 mm2. The color of the sponge is white-yellow. Spicules (Table 13): Megascleres – Styles and subtylostyles of different size categories. The (subtylo-)styles I are the largest megascleres (Fig. 14 I, K and L), very thin and slightly bend towards the pointed end. Their length is 1786–2774 mm with a maximum diameter of 8.0–11.2 mm. The second type are strait subtylostyles II with length 390–730 mm and diameter 8.0–14.4 mm. Subtylostyles III (Fig. 14D, G and H) are 160–355 mm long with a diameter of 6.4– 9.5 mm. Styles I are very thick (Fig. 14C) with diameter decreasing distinctly from the center towards both ends whereas the minimum diameter can be less than half of the maximum. Sizes: length 600–1080 mm; maximum diameter 25.6–36.8 mm. Styles II are simple styles (Fig. 14B). The diameter of the shaft is nearly constant and decreases only at the pointed end. The styles have a length of 1615–1950 mm and a diameter of 11.2–17.0 mm. Microscleres – Palmate anisochelae I (Fig. 14E and F) with a gently curved shaft. Lateral alae are only partly fused with the shaft. Alae of the large end have smooth margins, those of the small end have three to four (lateral) or six (median) little jags (sometimes more). Length: 33.6–41.6 mm. Diameter of the large ala end: 14–25 mm. Anisochelae II are of the same kind as anisochelae I but smaller in size. They measure 22.4–27.2 mm in length and 9.6–14.0 mm in diameter at the larger ala end. Forceps (Fig. 14J) are u-shaped and the shaft at the center of the curve is a bit thickened. The legs are parallel and each of them has a thickening at end. Their length is 52.8–83.2 mm, the diameter of the shaft swelling measures 2.5– 4.8 mm and the maximum leg diameter is 4–8 mm. Etymology: pediculifera (“tootsy-bearing”) for the tootsie-like small alae of the anisochelae. Remarks: The new species shows morphological similarity to five other species of the genus Lycopodina: L. infundibulum

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

13

Table 11 Spicule sizes of Lycopodina callithrix (Hentschel, 1914) (mm). Minimum-mean-maximum and number of measured spicules (in brackets). For comparison, the values of L. callithrix described by Hentschel (1914) are given. Parameter Styles/ subtylostyles Length Diameter Palmate anisochelae Length Width Parameter Styles/ subtylostyles Length Diameter Palmate anisochelae Length Width

SMF 11501

SMF11433

SMF11433b

SMF11503

Hentschel (1914)

250.0–591.2  1000.0 (30) 3.2–7.3  9.6 (30)

230.0–553.3  910.0 (30) 5.0–7.9  19.0 (30)

330.0–479.7  760.0 (30) 4.0–6.8  15.0 (30)

320.0–466.5  550.0 (30) 8.0–9.3  11.2 (30)

400–4000 16

12.1–16.6-22.3 (20) 5.2–7.7  9.3 (11)

11.2–13.1  14.4 (30) 6.4

9.6–12.4  14.4 (30)

11.2–15.3  19.2 (30) 4.3–6.6  8.0 (14)

11–12.5 5–6.5

SMF11504

SMF11502

SMF11434

SMF 11484

A2#042-2-5

all broken

540.0–1020.4  1368.0 (30) 2.4–11.8  22.4 (30)

396.9–532.3  610.0 (5) 14.4–18.1  21.0 (5)

180.0–726.0  1596.0 (30) 8.0–17.6  28.3 (30)

300.0–607.7  1010.0 (30) 4.8–9.3  12.8 (29)

11.2–12.1  14.4 (30) 4.9–5.4  5.8 (6)

11.2–12.3  14.4 (30) 5.5–5.8  6.2 (8)

11.5–12.7  14.4 (16) 5.4–5.6  5.9 (4)

11.2–12.5  14.4 (30) 5.2–6.0  7.3 (16)

12.8–23.0  27.3 (30) 6.6–10.5  20.0 (30)

Table 12 Spicule sizes of Lycopodina calyx (Hentschel, 1914) (mm): Minimum-mean-maximum and number of measured spicules (in brackets). For comparison, the values of L. calyx described by Hentschel (1914) are given. Parameter Subtylostyles I Length Diameter Subtylostyles II Length Diameter Subtylostyles III Length Diameter Anisochelae Length Width

SMF11500

Hentschel (1914)

600.0–733.3 850.0 (30) 15.0–26.0  32.0 (7)

456–592 8–9

400.0–500.7  650.0 (30) 9.0–13.4  30.0 (11)

296–392 10

150.0–226.0  340.0 (30) 6.0–8.5  12.0 (12)

200–256 6

13.9–22.3  33.3 (30)

14–21 7–8

stands free. The only species, which has a body shape similar to L. pediculifera sp. nov. is L. infundibulum as both have a calyx-shaped habit. L. infundibulum nonetheless is lacking protruding spicules at the body surface. Unique morphological features of the new species are a higher abundance of thick styles and the existence of anisochelae with small ends that have a characteristic look.

Fig. 13. Lycopodina calyx (Hentschel, 1914), (A) anisochela front view, (B) anisochela back view, (C/E/H) style III, (D) style II, (F) style I, (G) style II, (I) habitus, (J) sponge head.

(Levinsen, 1887), L. occidentalis (Lambe, 1893), L. lycopodium (Levinsen, 1887), L. cupressiformis (Carter, 1874) and L. calyx (Hentschel, 1914), but only the first four of the before mentioned species also possess forceps. L. infundibulum and L. calyx show the closest similarities to the new species as both have similar anisochelae and three kinds of subtylostyles. The anisochelae of L. occidentalis, L. lycopodium and L. cupressiformis are ovoid with two lateral wings, which are completely fused with the shaft while the central tooth

3.4.4. Lycopodina rastrichela (Hestetun et al., 2015) Original description: Asbestopluma (Asbestopluma) rastrichela Hestetun et al., 2015: pp. 16, 17. Fig. 9. Synonymy: Asbestopluma (Asbestopluma) rastrichela Hestetun et al., 2015. Type locality: North Atlantic Ocean. Material: One specimen from station 016-10 (ANDEEP III), 4725 m, 41° 7.770 S and 9° 56.430 E, 26.01.2005. Description: External morphology: The sponge has a stipitate shape (Fig. 15A and B) consisting of a globular head with several filaments (longest 5 mm) supported by a long slender stalk. Most of the filaments are wound around the white-yellowish head. The head measures about 4 mm in diameter. The stalk is broken and has a length of 1.1 cm. Spicules (Table 14): Megascleres – One kind of subtylostyle (Fig. 15C and D). They measure 440–530 mm in length and 7–10 mm in diameter (Table 14). The styles have one pointed and one blunt end. The little knob is on the very top of the blunt end or a few mm below. Sometimes, little swellings occur along the shaft. Microscleres – One kind of palmate, ovoid anisochela (Fig. 15E–I) in two

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

14

Table 13 Spicule sizes of Lycopodina pediculifera sp. nov. (mm): Minimum-mean-maximum and number of measured spicules (in brackets). For comparison, the values of L. infundibulum (Lundbeck, 1905) and L. calyx (Hentschel, 1914) are given. Parameter

holotype SMF11506

(Subtylo-)styles I Length 1786.0– 2250.9  2774.0 (30) Diameter 8.0–9.3  11.2 (30) Subtylostyles II Length 390.0–541.3  730.0 (30) Diameter 8.0–11.0  14.4 (30) Subtylostyles III Length 160.0–255.2  355.0 (30) Diameter 6.4–7.8  9.5 (30) Styles I Length 600.0– 898.8  1080.0 (30) Diameter 25.6–30.9  36.8 (30) Styles II Length 1615.0– 1750.7  1950.0 (8) Diameter 11.2–13.5  17.0 (8) Anisochelae I Length 33.6–37.4  41.6 (30) Diameter large 14.0–20.5  25.0 end (30) Diameter small 5.0–8.9  11.0 (30) end Diameter shaft 2.5–4.8  6.4 (30) Anisochelae II Length 22.4–24.5  27.2 (30) Diameter large 9.6–12.5  14.0 (30) end Diameter small 4.8–6.0  8.0 (30) end Diameter shaft 1.6–2.4  3.2 (30) Forceps Length 52.8–75.6  83.2 (24) Shaft diameter 2.5–3.4  4.8 (24) Leg diameter 4.0–5.5  8.0 (24) (middle)

L. infundibulum (Lundbeck, 1905)

L. calyx (Hentschel, 1914)

440–600

456–592

7

8–9

170–830

296–392

5.7–11

10

149–220

200–256

6

6

18–27

14–21

10–14

7–8

Fig. 14. Lycopodina pediculifera sp. nov., (A) habitus, (B) style II, (C) style I, (D) subtylostyle, (E/F) anisochelae, (G) blunt end of a subtylostyle with a slight swelling, (H) pointed end of a subtylostyle, (I) blunt end of a (subtylo-)style, (J) forceps, (K) (subtylo-)style I, (L) pointed end of a (subtylo-)style.

1–4 75

1

size categories: Anisochelae I 6.4–12.8 mm. Anisochelae II 13.6– 19.2 mm. The large lateral alae are completely fused with the shaft while the central tooth stands free and ranges until the small alae end. The small lateral alae have one half of the complete chelae size. They are grown together with four large processes. The small central tooth has one central process and one peak at each side of the process. Remarks: The species shows similarity to L. rhabdostylophora sp. nov. and L. parvula Hestetun et al., 2015. Spicule composition and size are quite similar, but subtylostrongyles are missing in both. In addition, anisochelae in L. rastrichela have an unusual shape that differs from all other species of the genus Lycopodina Lundbeck, 1905. So far, only one report was published by Hestetun et al. in 2015. Collection of type material took place during the cruises Epicea 2 (1988) and Bengal 2 (1996–1998) in the deep North Atlantic Ocean. This record of L. rastrichela is the first for the Southern Ocean. 3.4.5. Lycopodina rhabdostylophora sp. nov Type locality: Antarctic Weddell Sea.

Material: A total of three specimens from three stations: One specimen (holotype) from station 059-5 (ANDEEP III), 4658 m, 67° 29.850 S and 0° 3.390 W, 14.02.2005; one specimen (paratype) from station 088-11 (ANDEEP III), 4933 m, 68° 3.540 S and 20° 38.330 W, 27.02.2005 and one specimen (paratype) from station 094-11 (ANDEEP III), 4895 m, 66° 38.160 S and 27° 4.810 W, 02.03.2005. Diagnosis: Stipitate sponge (white-yellow) with an oval head and a long, thin stalk. Several filaments of differing length protrude mainly in apical direction from the head. Spiculation: Subtylostyles 420–1178  9–17 mm; Rhabdo-subtylostyles 300–400  4–8 mm; Anisochelae 24.0–28.8 mm (Table 15). Description: External morphology: The sponge has a stipitate shape (Fig. 16A–C) and a white-yellow color. It consists of an oval head (8 mm wide and 5 mm high), which has a radiate skeleton and several processes of different lengths, mostly about 8–10 mm long. The stalk has an axial skeleton. It is broken and has a length of 2.2 cm. The paratypes are distinctly smaller with a body size of ca. 1 mm. Spicules (Table 15): Megascleres – Subtylostyles (Fig. 16D) 420– 1178 mm in length and 9–17 mm at maximum width. Proximal diameter is 5–8 mm. Additional tyles occasionally occur along the shaft. Rhabdo-subtylostyles (Fig. 16E) are 300–450 mm in length. Their maximum diameter is 4–9 mm and their proximal diameter 3–4 mm. They are bent to a wide open angle with several tyles all along the shaft. Microscleres – Ovoid palmate anisochelae (Fig. 16F–H) in two size categories. Large lateral alae are completely fused with the shaft while the central tooth stands free and ranges until the small alae end. On the small side, lateral alae are

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

15

2015 and Lycopodina rastrichela (Hestetun et al., 2015). The new species is distinguished from the above mentioned by its rhabdosubtylostyles. The habit of L. parvula is spherical or elongate with shorter filaments. It shows a similar spicule assortment, but with two main differences: (1) It possesses a second subtylostyle size category while rhabdo-subtylostyles are missing; (2) Morphology of the anisochelae is different: The central tooth in L. parvula does not reach the small end. Lateral alae have two little peaks of the same size and the central tooth has three little peaks of the same size, while the anisochelae in Lycopodina rhabdostylophora sp. nov. are egg-shaped. Lateral and central alae are of same size and in close contact with the small alae end. Furthermore, lateral alae show slight swellings while the central ones have five peaks of which the median one is the largest. In L. rastrichela the rhabdo-subtylostyles are missing and another type of styles (subtylostrongyle) is present. Here, the anisochelae are ovoid as well but the small alae end morphology differs clearly: One long central tooth with one long process and two little peaks is present and lateral alae are fused, having four long processes. Moreover, Hestetun et al. (2015) described a specimen fragment (Asbestopluma sp.) also having bent tylostyles/subtylostyles (rhabdostyles). They recognized five types of megascleres, while in L. rhabdostylophora sp. nov. only two types are present. Unfortunately no SEM images are available for a better comparison of the anisochelae, but the size categories are similar. Because of the differences in megascleres types and the incomplete description by Hestetun et al. (2015), due to specimen fragment, an absolute determination as both specimens represent the same species, is not possible. Further, all three species described by Hestetun et al. (2015) (L. parvula, L. rastrichela and Asbestopluma sp.) are from the North Atlantic Deep. Fig. 15. Lycopodina rastrichela (Hestetun et al., 2015), (A/B) habitus, (C) blunt end of a subtylostyle, (D) Subtylostyle, (E/F/G) palmate anisochelae front view, (H) palmate anisochelae front view, median large ala is missing, free view on the lateral small alae, (I) palmate anisochelae back view.

Table 14 Spicule sizes of Lycopodina rastrichela (Hestetun et al., 2015) (mm): Minimummean-maximum and number of measured spicules (in brackets). For comparison, the values of L. rastrichela described by Hestetun et al. (2015) are given. Parameter Subtylostrongyles Length Diameter Subtylostyles Length Diameter Palmate anisochelae I Length Palmate anisochelae II Length

SMF11505

Hestetun et al. (2015)

4950.0 (5) (broken)

710–890  990 11–13.8  17.3

440.0–487.7  530.0 (30) 7.0–9.0  10.0 (30)

340–397  450 6.3–7.9  9.4

6.4–9.0  12.8 (30)

11–12 12.6

13.6–16.2  19.2 (30)

14.1–16  18.8

fused as well, whereas the central tooth covers the lateral ones only partly. Sizes: Anisochelae I measure 24.0–28.8 mm in length. The large alae end has a diameter of 15–18 mm, the small alae end is 6–9 mm wide. Anisochelae II measure 9.6–20.8 mm in length. Diameter of the large alae end is 9–10 mm, the small alae end is 4– 7 mm wide. Etymology: rhabdostylophora (“rhabdostyle-bearing”) for the possession of characteristic rhabdostyles. Remarks: Two species reported from the Atlantic show some similarities to our new species: Lycopodina parvula Hestetun et al.,

4. Discussion The final taxonomic identification of sponges from the family Cladorhizidae verifies the records in the preliminary ANDEEP I-III taxa list given by Göcke and Janussen (2013a, see also discussion). The family is species-rich in the Weddell Sea, with most of the Antarctic species occurring in deep sea habitats. According to the results by Göcke and Janussen (2013a), the investigated sponges can be assigned to the three communities (Caulophacus, Polymastia/Tentorium and Bathydorus community) as follows: most records of the four investigated genera (Asbestopluma, Chondrocladia, Cladorhiza and Lycopodina) belong to the Caulophacus community. Only one species (Chondrocladia (Chondrocladia) clavata Ridley and Dendy, 1886) occurs as part of the Polymastia/ Tentorium community and another species (Lycopodina callithrix (Hentschel, 1914)) is part of the Bathydorus community. The Caulophacus community is an abyssal fauna dominated by Caulophacus spp. characterized by soft substrates and few stones in the deepest regions of the Weddell Sea abyssal plains. The Polymastia/ Tentorium community is a shelf/slope fauna characterized by Rosella-dominated associations and rock- or stone-rich bottom types. The third community, the Bathydorus community occurs on the lower continental slope and abyssal characterized by soft substrates with dropstones and rocks (Göcke and Janussen, 2013a). Data of this study and other ANDEEP studies before show that even with a small amount of sampling a considerable number of new species and species rarely recorded before can be found (Brandt et al., 2007; Göcke and Janussen, 2013a, 2013b; Janussen and Tendal, 2007). Before this study, 21 species of cladorhizid sponges were known from the Southern Ocean, which is 15% of all known species (144 species globally) (http://www.marinespecies. org/porifera on 2016-05-24). Results of this study expand the

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

16

Table 15 Spicule sizes of Lycopodina rhabdostylophora sp. nov. (mm): Minimum-mean-maximum and number of measured spicules (in brackets). For comparison, the values of L. parvula and L. rastrichela, both described by Hestetun et al. (2015) are given. Parameter

Subtylostyles I Length Diameter max. Diameter prox. Subtylostyles II Length Diameter Rhabdostylessubtylostyles Length Diameter max. Diameter prox. Palmate anisochelae I Length Diameter large alae Diameter small alae Palmate anisochelae II Length Diameter large alae Diameter small alae

holotype SMF11486

paratype 1 SMF11487

paratype 2 SMF11488 Lycopodina parvula Hestetun et al., 2015

Lycopodina rastrichela (Hestetun et al., 2015)

420.0–664.9  1178.0 (30) 9.0–14.5-17.0 (30) 5.0–6.3  8.0 (30)

400.0–620.0  760.0 (30) 8.0–12.1 16.0 (30) 4.0–6.3  8.0 (30)

330.0–437.4  500.0 (30) 7.0–9.1  12.9 (20) 3.5–4.4  6.5 (20)

220–358  580

340–397 450

4.7–7.7  12.6

6.3–7.9  9.4

600–806  1030 4.7–7.3  7.9

subtylostrongyles 710–890  990 11–13.8  17.3

17.3–18.5-20.4

14.1–16 18.8

11–13.9  15.7

11–12  12.6

300.0–382.0  450.0 (30) 4.0–5.3  8.0 (30) 3.0–3.7  4.0 (30)

280.0–363.0  410.0 (30) 3.0–4.9  8.0 (15) 2.5–3.5  4.0 (15)

24.0–26.0  28.8 (30) 15.0–16.6  18.0 (30) 6.0–8.2  9.0 (30)

22.4–25.0  27.2 (30) 14.2–15.9  17.3 (30) 6.2–7.8  9.4 (30)

9.6–15.4  20.8 (30) 9.0–9.7  10.0 (30) 4–5.47 7 (30)

14.4–18.7  20.8 (30) 9.8–10.4-11.0 (16) 5–5.78  7 (16)

260.0–277.5  290.0 (4) 3.0–4.5  7.0 (4) 2.0–2.6  3.5 (4)

9.6–14.9  17.6 (30) 9.3–10.3  11.4 (14) 4.51–5.33 6.66 (14)

current knowledge as two new species are described for the Southern Ocean and three are found in this region for the first time. There are now 26 species known from the Southern Ocean (18–19%) and 146 species globally. This shows that the Southern Ocean is an area with a species-rich cladorhizid community. Antarctic sponge species can show quite different distributional patterns with many species showing an allegedly circumpolar distribution (35%) (Göcke et al., 2015; Janussen and Downey, 2014). Furthermore, the occurrence of cryptic species may lead to an overestimation of the dispersal range of single species. To determine whether the ANDEEP II and III-material contains cryptic species (possibly the specimens determined as Chondrocladia (Chondrocladia) clavata Ridley and Dendy, 1886) further research and more material is needed. The most important factors for longitudinal dispersal of deep sea species through abyssal basins and plains are bottom-near deep-water currents like parts of the ACC or the NADW (North Atlantic Deep Water) and the AABW (Antarctic Bottom Water) of which about 60% are formed in the Weddell Sea (Janussen and Downey, 2014; McClintock et al., 2005). Other potential factors for circum-Antarctic species dispersal include coastal gyres, lecithotrophic larvae, stable environmental conditions or floating propagules (Janussen and Downey, 2014; McClintock et al., 2005). Furthermore, in the Southern Ocean 13 cladorhizid species were previously known to be endemic (44% of all species) (Janussen and Downey, 2014; http://www.marinespecies.org/por ifera on 2016-05-24). With the two new species from this study now 15 species are endemic, that is 56% of all Cladorhizidae found in the Southern Ocean. Possible reasons for the high numbers of endemic species are geographical long-term isolation (e.g. Gondwana break-up) or physical barriers (e.g. the ACC) (Janussen and Downey, 2014). However, some of these endemic species are described only once for one specimen. Thus, they have to be seen as “presumably endemic” due to the fact that the Antarctic deep sea is generally under-investigated. In this study, eight endemic species are reported: Asbestopluma (Asbestopluma) belgicae (Topsent, 1901), Chondrocladia (Chondrocladia) antarctica Hentschel, 1914, Cladorhiza cf. moruliformis Ridley and Dendy, 1887, Cladorhiza tridentata Ridley and Dendy, 1887, Lycopodina

rhabdostylophora sp. nov, Lycopodina pediculifera sp. nov, Lycopodina callithrix (Hentschel, 1914) and Lycopodina calyx (Hentschel, 1914). All other species are assumed to have a broader distribution. The investigated sponges mainly occur in depths between 1000 and 5000 m, only one species (C. (C.) clavata) was sampled at 840 m. The sponges which are new records for the Southern Ocean were sampled in depths between 3000 and 5000 m, which are influenced by the global conveyor belt. The global ocean conveyor system (thermohaline circulation) comprises northwards directed deep-water currents within the Pacific Ocean and southwards directed deep-water currents, like the before mentioned NADW, in the Atlantic Ocean (Broecker, 1991). Along the Antarctic the NADW encounter the AABW as the AABW mixes with the NADW and deep currents encircling the Antarctic (Broecker, 1991). These bottom-near currents might have supported dispersal of sponge species over geological time periods.

5. Conclusion Twenty-seven species of the family Cladorhizidae (ca. 20%) are known to occur in the Southern Ocean and more than half are endemic (ca. 55%). In this study, eight endemic species, four Atlantic species and two cosmopolitan species are included. New distribution records of the species Chondrocladia (Chondrocladia) cf. butoni Tendal, 1973, Chondrocladia (Meliiderma) turbiformis Vacelet et al., 2009, Lycopodina pediculifera sp. nov, Lycopodina rastrichela (Hestetun et al., 2015) and Lycopodina rhabdostylophora sp. nov were achieved by deep-sea sampling. Collecting undescribed species and expanding distribution ranges of known species were previously expected because sample collections of Antarctic deep-sea sponges are scarce. The biogeography and biodiversity of Southern Ocean Cladorhizidae are also poorly known although results of this study expand the current knowledge considerably. Further studies on morphology and phylogeny of the family Cladorhizidae are necessary in future studies.

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i

M. Dressler-Allame et al. / Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

Fig. 16. Lycopodina rhabdostylophora sp. nov., (A) habitus SMF11488, (B) habitus SMF11486, (C) habitus SMF11487, (D) subtylostyle, (E) rhabdo-subtylostyle, (F) anisochela back view, (G) anisochela front view, (H) anisochela lateral view.

Acknowledgments We acknowledge the Deutsche Forschungsgemeinschaft (DFGProject JA-1063/14, 1–3; JA-1063/17-1) for financial support to our research of Antarctic sponges by Dr. Dorte Janussen, the scientific leader Dr. Angelika Brandt (univ. Hamburg) and the captain and crew of RV Polarstern. Thanks to Ole S. Tendal for valuable discussions. Further thanks are to Tim Bollinger, Saskia Dimter and Heike Szmutka (Senckenberg Frankfurt) for spicule measurements and preparation. This is ANDEEP publication No. 212.

References Bell, J.B., 2008. The functional roles of marine sponges. Est. , Coast. Shelf Sci. 79 (3), 341–353. Bergquist, P.R., 1972. Deep water Demospongiae from New Zealand. Micronesic 8 (1–2), 125–136. Boury-Esnault, N., Rützler, K., 1997. Thesaurus of Sponge Morphology. Smithsonian Institution Press, Washington, D.C., p. 596. Brandt, A., Gooday, A.J., Brandao, S.N., Brix, S., Brökeland, W., Cedhagen, T., Choudhury, M., Cornelius, N., Danis, B., De Mesel, I., Diaz, R.J., Gillan, D.C., Ebbe, B., Howe, J.A., Janussen, D., Kaiser, S., Linse, K., Malyutina, M., Pawlowski, J., Raupach, M., Vanreusel, A., 2007. First insights into the biodiversity and biogeography of the Southern Ocean deep sea. Nat 447, 307–311. Broecker, W.S., 1991. The Great Ocean Conveyor. Oceanography 4 (2), 79–89. Burton, M., 1929a. Porifera. Part II. Antarctic sponges. British Antarctic (‘Terra Nova’) Expedition, 1910 Natural History Report. 6. British Museum (Natural History). Zoology, London, pp. 393–458, pls I–V. Carter, H.J., 1874. Descriptions and Figures of Deep-sea Sponges and their Spicules from the Atlantic Ocean, dredged up on board H.M.S.‘Porcupine’, chiefly in 1869; with Figures and Descriptions of some remarkable Spicules from the

17

Agulhas Shoal and Colon, Panama. Ann. Mag. Nat. Hist. 4 (14), 207-221–245257, pls. XIII–XV. Clarke, A., Crame, J.A., 2010. Evolutionary dynamics at high latitudes: speciation and extinction in polar marine faunas. Philos. Trans. R. Soc. B 365 (1558), 3655–3666. Dayton, P., Jarrell, S., Kim, S., Thrush, S., Hammerstorm, K., Slattery, M., Parnell, E., 2016. Surprising episodic recruitment and growth of Antarctic sponges: implications for ecological resilience. J. Exp. Mar. Biol. Ecol. 482, 38–55. Downey, R.V., Griffiths, H.J., Linse, K., Janussen, D., 2012. Diversity and distribution patterns in high southern latitude sponges. PlosOne 7 (7), 1–16. Grey, J.S., 2001. Antarctic marine benthic biodiversity in a world-wide latitudinal context. Polar Biol. 24, 633–641. Göcke, C., Janussen, D., 2013a. Sponge assemblages of the deep Weddell Sea: ecological and zoogeographic results of ANDEEP I-III and SYSTCO I expeditions. Polar Biol. 36, 1059–1068. Göcke, C., Janussen, D., 2013b. Demospongiae of ANT XXIV/2 (SYSTCO I) Expedition – Antarctic Eastern Weddell Sea. Zootaxa 3692 (1), 28–101. Göcke, C., Janussen, D., Reiswig, H.M., Jarrell, S.C., Dayton, P.K., 2015. Rosella podagrosa Krikpatrick, 1907 – a valid species after all. Zootaxa 4021 (1), 169–177. Hentschel, E., 1914. Monaxone Kieselschwämme und Hornschwämme der Deutschen Südpolar-Expedition 1901-1903. Dtsch. Südpolar-Exp. 1901–03 (15), 35–141, pls IV–VIII. Hestetun, J.T., Fourt, M., Vacelet, J., Boury-Esnault, N., Rapp, H.T., 2015. Cladorhizidae (Porifera, Demospongiae, Poecilosclerida) of the deep Atlantic collected during Ifremer cruises, with a biogeographic overview of the Atlantic species. J. Mar. Biol. Assoc. U. K. 95 (7), 1311–1342. Hestetun, J.T., Vacelet, J., Boury-Esnault, N., Borchiellini, C., Kelly, M., Ríos, P., Cristobo, J., Rapp, H.T., 2016. The systematics of carnivorous sponges. Mol. Phylogen. Evol. 94, 327–345. Hooper, J.N.A., Van Soest, R.W.M., 2002. Class Demospongiae Sollas, 1885. In: Hooper, J.N.A., Van Soest, R.W.M. (Eds.), Systema Porifera: A Guide to the Classification of Sponges. Kluwer Academic/Plenum Publishers, New York, pp. 15–51. Janussen, D., Downey, R., 2014. Porifera. In: De Broyer, C., Koubbi, P. (Eds.), Biogeographic atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, pp. 94–102, Chapter 5.5. Janussen, D., Tendal, O.S., 2007. Diversity and distribution of Porifera in the bathyal and abyssal Weddell Sea and adjacent areas. Deep-sea Res. Part II 54 (16–17), 1865–1875. Kelly, M., Edwards, A.R., Wilkinson, M.R., Alvarez, B., Cook, S., de, C., Bergquist, P.R., Buckeridge, St. J., Campbell, H.J., Reiswig, H.M., Valentine, C., Vacelet, J., 2009. Phylum Porifera: sponges. In: Gordon, D.P. (Ed.), New Zealand Inventory of Biodiversity: 1. Kingdom Animalia: Radiata. Lophotrochozoa, Deuterostomia, Canterburry University Press, pp. 23–46. Kersken, D., Feldmeyer, B., Janussen, D., 2016. Sponge communities of the Antarctic Peninsula: influence of environmental variables on species composition and richness. Polar Biology, 39. Springer, pp. 851–862. Kersken, D., Göcke, C., Brandt, A., Lejzerowicz, F., Schwabe, E., Seefeldt, M.A., VeitKöhler, G., Janussen, D., 2014. The infauna of three widely distributed sponge species (Hexactinellida and Demospongiae) from the deep Ekström Shelf in the Weddell Sea, Antarctica. Deep-Sea Res. Part II 108, 101–112. Koltun, V.M., 1964. Sponges of the Antarctic. 1 Tetraxonida and Cornacuspongida. In: Pavlovskii, E.P., Andriyashev, A.P., Ushakov, P.V. (Eds.), Biological Reports of the Soviet Antarctic Expedition (1955–1958), 6–133. Akademya Nauk SSSR, pp. 443–448. Lambe, L.M., 1893. Sponges from the Pacific coast of Canada. Proc. Trans. R. Soc. Can., 11; , pp. 25–43, pls. II–IV. Lévi, C., 1964. Spongiaires des zones bathyale, abyssale et hadale. Galathea Report. Scientific Results of The Danish Deep-Sea Expedition Round the World. 1950– 52. 7, 63–112, pls II–XI. Levinsen, G.M.R., 1887. Kara-Havets Svampe (Porifera). Dijmphna-Togtets zoologiskbotaniske Udbytte. 1, 339–372, pls XXIX–XXXI. Lundbeck, W., 1905. The Danish Ingolf-Expedition. 6(2). 68-72. BiancoLuno, Copenhagen, pp. 78–83, pls XI–XII. McClintock, J.B., Amsler, C.D., Baker, B.J., Van Soest, R.W.M., 2005. Ecology of Antarctic marine sponges: an overview. Integr. Comp. Biol. 45, 359–368. Ridley, S.O., Dendy, A., 1886. Preliminary report on the monaxonida collected by H. M.S. ‘challenger’. Ann. Mag. Nat. Hist. 5 (18), 325-351–470-493. Ridley, S.O., Dendy, A., 1887. Report on the Monaxonida collected by H.M.S. ‘Challenger’ during the years 1873–1876. Zool. 20 (59), i-lxviii, 1-275, pls. I-LI, 1 map. Starmans, A., Gutt, J., 2002. Mega-epibenthic diversity: a polar comparison. Mar. Ecol. Prog. Ser. 225, 45–52. Tendal, O.S., 1973. Sponges collected by the Swedish Deep Sea Expedition. Zool. Scr. 2, 33–38. Thomson, C.W., 1873. The Depths of the Sea. Macmillan and Co., London, pp. 1–527. Topsent, E., 1901a. Notice préliminaire sur les éponges recueuillies par l'Expédition Antarctique Belge. Arch. De. Zool. expérimentale Et. générale 3 (9), v–xvi. Vacelet, J., Duport, E., 2004. Prey capture and digestion in the carnivorous sponge Asbestopluma hypogea (Porifera: Demospongiae). Zoomorph 123, 179–190. Vacelet, J., Kelly, M., Schlacher-Hoenlinger, M., 2009. Two new species of Chondrocladia (Demospongiae: Cladorhizidae) with a new spicule type from the deep south Pacific, and a discussion of the genus Meliiderma. Zootaxa 2073, 57–68. Van Soest, R.W.M., Boury-Esnault, N., Vacelet, J., Dohrmann, M., Erpenbeck, D., De Voogd, N.J., Santodomingo, N., Vanhoorne, B., Kelly, M., Hooper, J.N.A., 2012. Global diversity of sponges (Porifera). PlosOne 7 (4), 1–23.

Please cite this article as: Dressler-Allame, M., et al., Carnivorous sponges (Cladorhizidae) of the deep Weddell Sea, with descriptions of two new species. Deep-Sea Res. II (2016), http://dx.doi.org/10.1016/j.dsr2.2016.08.006i