Holothuroidea of the Charlie Gibbs Fracture Zone area, northern Mid-Atlantic Ridge

Abstract

Holothurians are among the most species-rich taxa in the megabenthos on the northern Mid-Atlantic Ridge at depths of 2200–3700 m. Extensive new collections of 32 holothurian species were made in 2007–2010 in the Charlie Gibbs Fracture Zone area as part of the ECOMAR project. New material includes samples taken using a trawl and the ROV Isis. Samples and in situ observations from the ROV were of particular value because the morphological details of a number of holothurian species could be clarified. Many of these species are gelatinous and fragile and were damaged in trawls. Three species of elasipodid holothurians are described as new to science. An annotated check-list of all species of deep-sea holothurians collected in the Charlie Gibbs Fracture Zone area is provided. The checklist includes synonyms, distribution data and morphological descriptions as well as photographs taken in situ and in vivo. Ecological remarks are given for some species.

Keywords:

• Deep-sea holothurians
• North Atlantic
• taxonomy
• diversity
• benthic fauna

Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory, University of Copenhagen, Denmark

Introduction

Over the last decade special attention has been given to the benthic fauna at the Mid-Atlantic Ridge (MAR). Several cruises were organized by the MAR-ECO project focusing on the ridge segment between Iceland and the Azores (Bergstad & Godø 2003, http://www.mar-eco.no/). These studies have resulted in a number of papers dealing with the ecology and the taxonomy of benthic fauna at the MAR (Dilman 2008; Mironov 2008; Tabachnik & Collins 2008; Gebruk et al. 2010, etc.). Between 2007 and 2010 the ECOMAR programme (http://www.oceanlab.abdn.ac.uk/ecomar/), a UK-funded field project contributing to MAR-ECO, conducted three cruises to the Charlie Gibbs Fracture Zone (CGFZ) area of the MAR onboard the RRS James Cook. Four target sites were investigated on either sides of the MAR north and south of the CGFZ and the sub-polar front, at a target depth of around 2500 m (Figure 1). The ECOMAR project is aimed at investigation of the MAR ecosystem and its controlling physical factors. The main goals of the cruises were to investigate the benthic megafauna – species composition, biomass and abundance and distribution of species and communities. The benthic fauna was sampled using a trawl while an ROV provided images and physical samples. Holothurians obtained formed the basis for the present work.

Figure 1.  Map of of four ECOMAR target sites.

Holothurians are one of the most species-rich megafaunal taxa at the northern MAR (Gebruk 2008; Gebruk et al. 2010). Within the ECOMAR they often dominated the trawl catches in numbers and biomass, and were very abundant in the video footage (C. Alt, unpubl. data). They were common on sedimented plains and slopes at all four ECOMAR sites.

Deep-sea holothurians are often very fragile and/or gelatinous and are therefore easily damaged by conventional sampling methods. Hence, characters of external morphology remain unknown in many species despite their importance for species identifications. Although underwater observation techniques are becoming more common in deep-sea research, video and photography surveys are rarely used to complement taxonomic work. Most deep-sea holothurians cannot be recognized to species or even generic level on photographs. Images and videos obtained using the ROV Isis on the ECOMAR cruises provided unique data on the external appearance and also the biology and ecology of deep-sea holothurians.

The present article reports on the taxonomic composition of holothurians of the CGFZ area of the MAR, with comments on their distribution, ecology and biology. Three new species are described.

Material and methods

Holothurian samples were obtained from a total of 13 trawls taken in 2007 (RRS James Cook cruise JC011), 2009 (RRS James Cook cruise JC037), and 2010 (RRS James Cook cruise JC048) (Table I). Samples were also obtained on the latter cruise using the ROV Isis. Additional samples were collected on test dive 158 of the ROV on JC048 west of the northwest ECOMAR site, at a depth of 3500 m. Full station data and a cruise report can be found on the ECOMAR website (see above). On cruises JC011 and JC037 benthic fauna were collected using a semi-balloon otter trawl (OTSB 14, 13.7 m headline, fished on a single wire). Trawl samples were preserved in 10% formalin and were transferred to 80% ethanol for long-term preservation. Selected specimens were preserved in 80% ethanol for genetics. Two species were obtained from the megacorer samples in JC048. The megacorer was deployed with eight larger core tubes (internal diameter 100 mm) that were used for sampling macrofauna. Individual cores were sliced at 0–2, 2–6 and 6–10 cm intervals. All cores from a megacorer drop were mixed into a single sample. Sediment from deeper than 10 cm below the surface was investigated for evidence of deep burrowing macrofauna and megafauna. All core slices were washed through a net of 500- and 300-µm mesh sieves with filtered sea water. The sieved sediment was washed into 500-ml Nalgene™ bottles, and fixed with 10% buffered formalin solution.

Table I. Data on stations of ECOMAR cruises

Cruise No./ Station No.	Dive No.	Gear	Latitude start–end, N	Longitude, start–end, W	Depth start–end, m	Date
JC011/17	–	OTSB	49°14.68′ 49°03.43′	27°42.31′ 27°53.86′	2687–2727	21 Jul 2007
JC011/23	–	OTSB	48°54.59′ 49°15.85′	27°50.00′	2631–2724	22 Jul 2007
JC011/75	–	OTSB	53°51.10′ 54°06.02′	36°11.36′ 36°07.20′	2605–2630	5 Aug 2007
JC011/101	–	OTSB	54°06.33′ 53°47.47′	33°58.27′ 34°02.89′	2405–2435	10 Aug 2007
JC011/106	–	OTSB	54°05.68′ 53°46.94′	33°58.54′ 34°03.02′	2410–2445	11 Aug 2007
JC011/111	–	OTSB	54°05.68′ 53°47.71′	33°58.54′ 34°02.83′	2404–2430	12 Aug 2007
JC037/15	–	OTSB	48°58.73′ 49°11.14′	27°51.01′ 27°49.17′	2630	10 Aug 2009
JC037/19	–	OTSB	48°58.05′ 49°14.36′	27°51.60′ 27°49.29′	2750	10–11 Aug 2009
JC037/27	–	OTSB	48°57.34′ 49°13.55′	27°49.83′ 27°50.92′	2700	18 Aug 2009
JC037/61	–	OTSB	54°19.62′ 54°04.96′	36°00.87′ 36°07.98′	2618	28 Aug 2009
JC037/67	–	OTSB	54°19.50′ 54°06.55′	36°01.11′ 36°07.14′	2620–2676	28–29 Aug 2009
JC037/70	–	OTSB	54°19.23′ 54°03.65′	36°01.17′ 36°08.42′	2621–2630	29–30 Aug 2009
JC037/79	–	OTSB	54°03.60′ 53°57.69′	33°58.84′ 34°00.55′	2452	31 Aug–1 Sep 2009
JC048/3	158	ROV	52°23.46′ 52°23.24′	41°03.70′ 41°03.75′	3500	29 May 2010
JC048/6	159C**	ROV	53°58.77′	36°11.50′	2538	1 Jun 2010
JC048/15	161T*	ROV	53°57.86′ 53°59.19′	36°12.49′ 36°08.26′	2173–2500	5–6 Jun 2010
JC048/16	162C	ROV	53°59.39′	36°11.66′	2450–2272	6 Jun 2010
JC048/17	163C	ROV	53°59.39′	36°11.66′	2450	7 Jun 2010
JC048/22	–	Megacorer	54°00.65′	34°10.42′	2510	8 Jun 2010
JC048/24	165C	ROV	54°01.08′	34°09.46′	2501–2398	9–10 Jun 2010
JC048/26	167T	ROV	54°02.41′ 53°59.72′	34°08.45′ 34°11.51′	2364–2404	10–11 Jun 2010
JC048/27	–	Megacorer	54°00.67′	34°10.42′	2508	11–12 Jun 2010
JC048/28	168C	ROV	54°01.47′	34°10.63′	2445–2435	12–13 Jun 2010
JC048/29	169T	ROV	52°40.86′ 52°41.30′	35°04.20′ 35°04.82′	3599–3670	14 Jun 2010
JC048/33	170T	ROV	48°43.63′ 48°43.97′	28°38.87′ 28°39.35′	2500–2641	16 Jun 2010
JC048/34	–	Megacorer	48°45.76′	28°38.50′	2564	16–17 Jun 2010
JC048/36	171T, C	ROV	48°43.83′	28°39.61′	2500	19 Jun 2010
JC048/38	172C	ROV	48°43.63′	28°28.83′	2600	19–20 Jun 2010
JC048/40	173C	ROV	48°44.12′	28°39.34′	2623–2428	21 Jun 2010
JC048/42	–	Megacorer	48°45.70′	28°38.56′	2563	21 Jun 2010
JC048/43	174C	ROV	48°43.87′ 48°44.23′	28°39.01′ 28°39.57′	2620–2547	22 Jun 2010
JC048/48	176T	ROV	49°07.47′ 49°05.03′	27°49.89′ 27°50.41′	2741	23–24 Jun 2010
JC048/49	–	Megacorer	49°05.34′	27°50.22′	2768	24 Jun 2010
JC048/50	–	Megacorer	49°05.40′	27°50.23′	2770	24 Jun 2010
JC048/51	177T	ROV	49°00.82′ 49°02.95′	27°40.49′ 27°44.47′	2951–2227	26–27 Jun 2010
JC048/52	–	Megacorer	49°05.41′	27°50.19′	2775	27 Jun 2010
JC048/53	178C	ROV	49°01.44′	27°41.26′	2442–2630	27 Jun 2010
JC048/54	179C	ROV	49°05.91′	27°50.33′	2700	28 Jun 2010
JC048/56	180C	ROV	49°01.18′	27°42.33′	2758	29 Jun 2010
*T, benthic line transects; **C, collection dives.

Individual specimens were collected by the ROV Isis. The ROV was equipped with two high-definition video cameras each hosting a pair (red and green) of laser lights for determining the size of viewed objects. The ROV also had four HMI lights and a Scorpio digital still camera with flash unit. Observations on benthic fauna were made during video transect dives and on dives dedicated to specimen collections (Table I). On collection dives each specimen was recorded on video and photographed prior to sampling. Sampling was conducted using a suction sampler (slurp-gun) flowing into a carousel with six transparent chambers with video control. Larger specimens were sampled using the two ROV manipulators. The samples were sorted and processed in a temperature controlled room at 4–6°C onboard and then preserved in 80% ethanol. Some specimens were photographed in the cold room prior to preservation.

Holothurians were identified after the cruise by examining external and internal taxonomic characteristics with a dissecting microscope. The morphology of calcareous elements (ossicles in the skin and internal organs and the structure of the calcareous ring) was studied on temporary and permanent preparations using a compound microscope. To extract ossicles, pieces of tissue were dissolved in chlorinated bleach solution.

Terms and abbreviations

C-shaped ossicles, small ossicles, less than 0.1 mm in size, occurring in the elpidiid genera Amperima, Ellipinion, Protelpidia and Scotoplanes. C-shaped ossicles are usually not taxonomically useful at the species level.

Deflection angle, the angle between the arm or apophysis and the vertical axis in ossicles (Figure 9A).

Mouth tube, that part of the body with tentacles anterior to the velum, present in many elpidiids.

NHM, Natural History Museum, London.

NOCS, National Oceanography Centre Southampton, UK

OTSB, semi-balloon Otter trawl

Peniagone-type ossicles, ossicles consisting of a central stem with four usually bent arms and 0–4 apophyses on the arms or stem.

Taxonomy

Order Dendrochirotida Grube, 1840

Family Cucumariidae Ludwig, 1894

Staurocucumis abyssorum (Théel, 1886)

(Figure 17A)

Cucumaria abyssorum Théel, 1886a: 66–67, plates 4(6), 16(6); von Marenzeller 1893: 14; Ludwig 1894: 122–125, plates 9(28–29), 13(1–5); Grieg 1921: 11, text figure 9; Ludwig & Heding 1935: 179; Cherbonnier 1941: 93–96, 101, figures 1, 3(j,n–p).

Staurocucumis abyssorum Ekman 1927: 385–387; Clark & Deichmann 1936: 566; Hansen 1988: 302–303, figure 1.

Abyssocucumis abyssorum Heding 1942: 33–35, text figures 34–36; Gage et al. 1985: 191.

Cucumaria abyssorum var. grandis Théel, 1886a: 67–68, plate 5(1).

Cucumaria abyssorum var. hyalina Théel, 1886a: 68–69, plate 4(7).

Cucumaria sluiteri Ohshima, 1915: 263, 263, plate 10(21a,b).

Cucumaria ingolfi Deichmann in Mortensen, 1927: 396.

Staurocucumis ingolfi Clark & Deichmann 1936: 567.

Cucumaria albatrossi Cherbonnier, 1941: 96–101, 103, figures 2, 3(a–i,k–m).

Material examined

St. JC011/17 (1 ind.), St. JC011/23 (60 ind.), St. JC037/15 (131 ind.), St. JC037/19 (127 ind.), St. JC037/27 (102 ind.). This species was observed in situ at stations JC048/33 Dive 170 (3 ind.), JC048/43 Dive 174 (1 ind.), JC048/48 Dive 176 (22 ind.), JC048/36 Dive 171 (4 ind.) and JC048/51 Dive 177 (1 ind.).

Distribution

Cosmopolitan species, known from all oceans except the Arctic. In the Atlantic Staurocucumis abyssorum occurs in the central and western parts. Depth 1210–4636 m.

Order Aspidochirotida Grube, 1840

Family Synallactidae Ludwig, 1894

Bathyplotes natans (M. Sars, 1868)

Holothuria natans M. Sars, 1868: 20.

Bathyplotes natans Östergren 1896: 352–353, plate 18(27–35); 1902: 6; Ludwig 1901: 137–138; Grieg 1921: 7; Mortensen 1927: 384–385, text figures 228(2), 229; Deichmann 1930: 100–102, plate 9(1–2, 9); 1954: 386; Heding 1942: 10–12, text figures 10, 11(1–10), 12(1–2); Pawson 1963b: 90–94, plate 7(1–7); 1965: 16–18, figure 4; 1970: 51; Gage et al. 1985: 194; Harvey et al. 1988: 183; Miller & Pawson 1990: 4; Madsen & Hansen 1994: 79–82, figures 48–50; Rowe & Gates 1995: 328; Liao 1997: 73–74, figure 39.

Stichopus natans G. O. Sars 1872: 30; M. Sars 1877: 58, plate 7(18–41); Théel 1886a: 193; Bell 1892: 51.

Stichopus tizardi Théel, 1882b: 696; 1886a: 193; Bell 1892: 51; Koehler 1896: 108–11, figures 33–35.

Bathyplotes tizardi Östergren 1896: 354; Ludwig 1901: 138; Perrier 1902: 350; Mitsukuri 1912: 35–39, text figure 8; Grieg 1921: 4.

Bathyplotes fallax Östergren, 1896: 355, plate 18(44).

Herpysidia reptans Perrier, 1898: 247–248.

Bathyplotes reptans Perrier 1902: 352–358, plates 12(3–4), 18(1–9); Mortensen 1927: 384.

Bathyplotes assimilis Koehler & Vaney, 1905: 25–26, plates 3(3), 10(1–3).

Bathyplotes papillosus Koehler & Vaney, 1905: 28–29, plate 10(21–24).

Bathyplotes patagiatus Fisher, 1907: 688–690, plate 72(1).

Bathyplotes östergreni Ohshima, 1915: 225–226, plate 8(3a–d).

Bathyplotes heterostylides Heding, 1942: 12–13, text figures 12(3–5), 13(1–15).

Material examined

St. JC011/23 (3 ind.), St. JC037/19 (1 ind.) and St. JC037/75 (3 ind.).

Distribution

North Atlantic: off Norway, Rockall Trough, Faroe-Shetland Channel, west off Ireland, south off Iceland, MAR south of the CGFZ, Gulf of Mexico. Also known from the Pacific (New Zealand and East China Sea). Depth 193–2750 m. Our new records are the deepest for this species.

Benthothuria funebris R. Perrier, 1898

(Figures 17B, 19B)

Benthothuria funebris Perrier, 1898: 1665; 1899: 248; 1902: 365–371; Deichmann 1930: 91; Heding 1940: 363–364; 1942: 6; Gage et al. 1985: 194–195; Harvey et al. 1988: 183.

Material examined

St. JC011/23 (8 ind.), St. JC011/75 (2 ind.), St. JC011/101 (12 ind.), St. JC037/15 (15 ind.), St. JC037/19 (26 ind.), St. JC037/27 (53 ind.) and St. JC037/61 (2 ind.). This species was observed in situ at stations JC048/15 Dive 161 (1 ind.), JC048/29 Dive 169 (1 ind.), JC048/36 Dive 171 (1 ind.), JC048/48 Dive 176 (4 ind.) and JC048/54 Dive 179 (1 ind.).

Distribution

North Atlantic. Depth 782–3757 m.

Remarks

Common species in the CGFZ area, both north and south from the fracture zone. Gelatinous consistency in this species suggests the ability to swim.

Hansenothuria sp.

(Figure 2, 17C)

Figure 2.  Hansenothuria sp. (A–C) Underwater photographs: (A) St. JC048/43 Dive 174; (B) St. JC048/40 Dive 173; (C) JC048/53 Dive 178. (D–G) Ossicles of papillae. (D) scale 0.1 mm; (E–G) scale 0.2 mm.

Material examined

St. JC048/43 Dive 174 (1 fragment). This species was observed in situ at stations JC048/40 Dive 173 (several ind.) and JC048/53 Dive 178 (1 ind.).

Remarks

The specimen was about 18 cm long and was referred to Hansenothuria based on the following characters: broad ventrolateral brim, two rows of dorsal papillae, absence of midventral tube feet, dorsal anus, absence of ossicles in the body wall skin, resemblance of ossicles in papillae to those of Hansenothuria benti Miller and Pawson, 1989. However, our specimen differs in its pinkish colour of the body wall and the papillae. In H. benti the body colour ranges from light blue to pale purple, and the papillae colouration ranges from translucent to black.

The skin was thick and very gelatinous with a lot of mucus. Ossicles were found only in the papillae (Figure 2D–G) and tube feet. They were rod-shaped, up to 0.5 mm long, ranging from almost straight to bent or curved forming a C or ring shape; ossicles spinous over most of its length; some ossicles with a central swelling, and some had additional processes or bifurcations at the ends. Tentacles were not preserved. Ossicles were absent in the gonad.

The specimen was observed swimming in the slurp-gun chamber after sampling. When the ROV was retrieved on deck, only fragments of this specimen were left. This species was observed on cliffs and talus slopes south of the CGFZ on JC048.

Mesothuria cathedralis Heding, 1940

Mesothuria (Allantis) cathedralis Heding, 1940: 336–338, text figure 5, figures 1–10.

Mesothuria (Penichrothuria) cathedralis Heding 1942: 8–9, text figure 8(1–5).

Mesothuria cathedralis Gage et al. 1985: 196; Gebruk et al. 2012: 284–289, figure 7.

Material examined

St. JC011/17 (6 ind.), St. JC011/23 (11 ind.), St. JC011/75 (4 ind.), St. JC011/101 (1 ind.), St. JC037/15 (8 ind.), St. JC037/19 (35 ind.), St. JC037/27 (30 ind.), St. JC037/70 (3 ind.) and St. JC048/16 Dive 162 (1 ind.).

Distribution

North Atlantic, including Porcupine Abyssal Plain, the Gulf of Guinea, off Morocco, Irminger Basin off southern Greenland to southeast of Iceland, MAR and the Gulf of Mexico. Depth 1292–4930 m.

Remarks

Epibenthic species. The skin is covered with globigerina shells, sponge ossicles and particles of sand and detritus.

Mesothuria maroccana R. Perrier, 1898

(Figure 17D)

Mesothuria maroccana Perrier, 1898: 1665; 1899: 245; 1902: 312–317, plate 16(32–35); Hérouard 1923: 17; Deichmann 1930: 97, plate 7(2–7); 1940: 191; 1954: 385; Grieg 1921: 4; Hansen 1956: 46, figure 14a; Gebruk et al. 2012: 301–303, figure 9(a–b).

Mesothuria (Mesothuria) maroccana Heding 1940: 333; 1942: 8.

Holothuria murrayi (var.?) Théel, 1886: 187, plate 9(3).

Holothuria intestinalis var. verrilli Hérouard, 1896: 163.

Material examined

St. JC011/17 (10 ind.), St. JC011/75 (5 ind.), St. JC037/15 (6 ind.), St. JC037/19 (1 ind.), St. JC037/27 (2 ind.) and St. JC048/40 Dive 173 (1 ind.).

Distribution

Common in the North Atlantic deep sea. Known from the Moroccan coast, the Azores, south of Iceland, Jamaica, eastern Gulf of Mexico, east of Florida, MAR. Depth 700–3120 m.

Remarks

This epibenthic species was observed on cliffs directly on hard rock substrate. Specimen was bright white in situ as a result of pteropod shells covering most of the body (Figure 17D). These shells were lost during sampling. The specimen collected by ROV was covered with scattered globigerina shells and mineral particles only. The body colour was brownish, changing to dark purple in the tentacles; the hind gut and the skin around anus were dark purple. The specimen had very long filiform dorsal tube feet attached to rock in situ.

Molpadiodemas violaceus (Théel, 1886)

Pseudostichopus villosus var. violaceus Théel, 1886a: 172, plate 10(6b).

Molpadiodemas violaceus O'Loughlin & Ahearn 2005: 165, figures 1(e,i), 2(f), 7(g–i), 8(u–x).

Pseudostichopus villosus Théel, 1886a: 170–171 (partim).

Material examined

St. JC011/75 (1 ind.).

Distribution

West and central North Atlantic, South Atlantic, Antarctic, South Indian Ocean, South Pacific. Depth 2196–6354 m.

Paelopatides grisea R. Perrier, 1899

(Figure 18A)

Paelopatides grisea Perrier, 1899: 248; 1902: 361–365; Mortensen 1927: 388; Heding 1940: 351; Billett et al. 1985: 407; Gage et al. 1985: 195–196; Harvey et al. 1988: 183; Miller & Pawson 1990: 5.

Paelopatides gigantea Deichmann 1930: 104–106 (partim); Sibuet 1977: 554; Miller & Pawson 1990: 35. (non Verrill, 1884)

Material examined

St. JC011/23 (1 ind.), St. JC011/101 (38 ind.), St. JC011/106 (13 ind.), St. JC011/111 (18 ind.), St. JC037/15 (1 ind.), St. JC037/19 (1 ind.) and St. JC037/61 (1 ind.). This species was observed in situ at stations JC048/6 Dive 159 (1 ind.) and JC048/15 Dive 161 (9 ind.).

Distribution

North Atlantic: Canary Islands, between the Azores and Portugal, Porcupine Abyssal Plain, Rockall Trough, Bahama Islands, Caribbean, MAR. Depth 1695–4060 m.

Pseudostichopus peripatus (Sluiter, 1901)

(Figure 18D)

Meseres peripatus Sluiter, 1901a: 10–11; 1901b: 48–49, plates 5(5), 8(7); Perrier 1902: 359; Rowe & Gates 1995: 285.

Pseudostichopus peripatus O'Loughlin & Ahearn 2005: 174–175, figure 1(10–12). (non Marenzeller, 1893 )

Pseudostichopus occultatus Hérouard 1902: 14–15, plate 2(4–14) (partim). (non von Marenzeller, 1893)

Pseudostichopus occultatus var. plicatus Koehler & Vaney, 1905: 9–10, plates 3(8), 9(1–3); Heding 1940: 353.

Plicastichopus plicatus Heding 1940: 354–359; 1942: 6.

Pseudostichopus propinquus Fisher, 1907: 691–693, plates 71(3), 72(2), 73(3), 74(1), 76(3); Imaoka 1978: 382.

Pseudostichopus (Trachostichopus) propinquus Heding 1940: 357; Imaoka 1978: table 1–1; 1990: 148, 152.

Meseres propinquus O'Loughlin 2002: 309.

Pseudostichopus aleutianus Ohshima, 1915: 228, plate 8(5a–c); Imaoka 1978: 380.

Pseudostichopus (Trachostichopus) aleutianus Heding 1940: 353–359; Imaoka 1978, table 1–2.

Pseudostichopus unguiculatus Ohshima, 1915: 230–231, plate 8(7a–c); Imaoka 1978: 384; Rowe & Gates 1995: 285.

Pseudostichopus (Pseudostichopus) unguiculatus Heding 1940: 353–360; Imaoka, 1978: table 1–1; 1990: 152; Thandar 1992: 167.

Pseudostichopus marenzelleri Hérouard, 1923: 25; Mortensen 1927: 287–288; Deichmann 1930: 90.

Pseudostichopus (Pseudostichopus) marenzelleri Heding 1940: 353–359; Imaoka 1978: table 1–1; Thandar 1992: 167.

Pseudostichopus lapidus Hérouard, 1923: 26–28, plate 4(5).

Pseudostichopus (Pseudostichopus) lapidus Heding 1940: 353–360.

Plicastichopus ingolfi Heding, 1942: 5–6, text figures 4–5, plate 1(4–5).

Meseres ingolfi Rowe & Gates 1995: 285.

Pseudostichopus (Trachostichopus) tuberculatus Imaoka, 1990: 149–152, figures pp. 149, 151.

Material examined

St. JC011/23 (7 ind.), St. JC011/75 (6 ind.), St. JC011/101, St. JC011/106, St. JC037/15 (23 ind.), St. JC037/19 (2 ind.), St. JC037/27 (11 ind.), St. JC037/61 (2 ind.), St. JC037/67 (10 ind.), St. JC037/70 (4 ind.) and St. JC048/24 Dive 165 (several ind.). Many specimens of this species were observed in situ at stations JC048/6 Dive 159, JC048/15 Dive 161, JC048/16 Dive 162, JC048/26 Dive 167, JC048/33 Dive 170, JC048/36 Dive 171 and JC048/51 Dive 177.

Distribution

Cosmopolitan eurybathic species known from the Indo-Pacific, North and South Pacific Ocean, North and South Atlantic Ocean, Southern Ocean. Depth 134–5453 m.

Remarks

In the ECOMAR area this species had a very characteristic in situ appearance: its dorsal side was covered with many of the large (up to 2 cm diameter) disc-like foraminiferan Discospirina tenuissima which were usually lost during sampling.

Synallactes aff . crucifera

(Figures 3, 18J)

Material examined

St. JC037/15 (3 ind.), St. JC011/23 (3 ind.) and St. JC048/16 Dive 162 (1 ind.). This species was observed in situ at the Station JC048/36 Dive 171 (3 ind.).

Description

Colour whitish, in situ light pink. Skin thick, non-transparent, rough owing to dense layer of ossicles. Body elongated (Figure 3A–C), up to 80 mm in length in fresh specimen, 60 mm in ethanol. Dorsal papillae in 6 rows, retractable. Tentacles 18. Ventrolateral tube feet about 25 pairs. Mid-ventral tube feet about 10 pairs, scarcely distributed. Anus dorsal. Ossicles spatulated crosses only, each with long spinous apophysis. Dorsal crosses (Figure 3D,E): arms up to 0.1 mm long, central apophysis ~0.15 mm with prominent spines; ends of arms spatulated, each with a large hole; 1–3 small holes sometimes present; small ossicles may have only one hole or lack holes completely. Apophyses not perforated. Ventrally very small crosses sparsely distributed; arms 0.03–0.05 mm (Figure 3F,G).

Figure 3.  Synallactes aff. crucifera, St. 48/16 Dive 162. (A–C) preserved specimen in dorsal, ventral, and lateral view; (D,E) dorsal ossicles, upper and side view; (F,G) ventral ossicles, upper and side view.

Remarks

Examined specimens resemble Synallactes crucifera R. Perrier, 1898 in external morphology: body shape, skin colour, arrangement of dorsal papillae, ventrolateral and midventral tube feet. Their ossicles are also similar in size, number of perforations on arms and spinous apophysis lacking projections. However, ossicles with perforated central apophyses described by Perrier were not found.

This species was frequently observed on steep slopes – on rocky outcrops and sediment pockets between them. It is likely that this species has the ability to swim.

Synallactidae gen. et sp. indet.

(Figures 4, 18C)

Figure 4.  Synallactidae gen. et sp. indet. (A,B) Underwater photographs: (A) St. JC048/40 Dive 173; (B) St. JC048/43 Dive 174. (C–E) St. JC048/43 Dive 174, ossicles of papillae, scale 0.05 mm; (F) St. JC048/43 Dive 174, tentacle ossicles, scale 0.2 mm; (G) St. JC048/43 Dive 174, gonad ossicles, scale 0.2 mm.

Material examined

St. JC048/43 Dive 174 (one very damaged specimen). This species was also observed in situ at the station JC048/40 Dive 173 (several specimens).

Description

Body about 20 cm in length, anterior end wide, posterior end tapered, ventral side flat, dorsal side convex. Skin thick, gelatinous, semi-transparent ranging in colour from light to deep purple; tentacles and skin around mouth the most pigmented. Dorsal papillae in 2 rows, longest papillae in the anterior one-third of dorsum, other papillae minute and slender, almost not visible. Mid-ventral tube feet in double row. Ventrolateral brim wide, widest in anterior half. Ossicles curved rods (Figure 4C–G), present in papillae, mid-ventral tube feet, tentacles and gonads; rods more or less of the same type; rods in papillae and tube feet up to 0.18 mm in length with enlarged ends covered by large spines; in tentacles rods up to 0.55 mm in length, more spinous and varying in shape compared to rods in papillae and tube feet; rods in gonad up to 0.5 mm in length, more slender than those in external skin.

Remarks

The specimen swam actively in the slurp-gun chamber soon after sampling. By the time the specimen could be preserved it had become badly damaged, owing to its very gelatinous consistency.

The species was observed on cliffs and talus slopes south of the CGFZ, often together with Hansenothuria sp.

Order Elasipodida Théel, 1882

Family Deimatidae Théel, 1879

Deima validum validum Théel, 1879

(Figure 18E)

Deima validum Théel, 1879: 5, figures 36–38; 1882a: 68–70, plates XVIII, XIX, XXXI(4–9), XXXVI(4), XXXVII(8), XLIII(7), XLIV(13), XLVI(5); Sluiter 1901b: 60.

Deima validum validum Hansen 1967: 488–490, figure 5.

Deima fastosum Théel, 1879: 5–6, figures 1–3; 1882a: 71–73, plates XX, XXI(1), XXXI(10–13), XXXV(7–10), XXXVI(7), XXXVII(3), XLIII(2–3, 5), XLVI(8).

Deima blakei Théel, 1886b: 1–2, figures 1–2; Koehler & Vaney 1905: 55–57, plate XI(13–15); Hérouard 1923: 40–41, plates V(7), VI(5); Deichmann 1930: 115–116, plates X(7–11), XI(1–3); 1936: 9; 1940: 198–199.

Deima atlanticum Hérouard, 1898: 88–89, figures 1–2; 1902: 32–35, plates III(3), IV(18), V(1–5), VIII(26–29); Grieg 1921: 4, plate I(2–3).

Deima mosaicum Ohshima, 1915: 233–234.

Material examined

St. JC011/23 (2 ind.). This species was observed in situ at stations JC048/36 Dive 171 (1 ind.) and JC048/43 Dive 174 (1 ind.).

Distribution

Cosmopolitan species, occurring from tropical to moderate latitudes. Depths 724–5424 m, in the North Atlantic 1049–4360 m.

Family Laetmogonidae Ekman, 1926

Laetmogone billetti sp. nov. Rogacheva & Gebruk

(Figures 5, 6, 17H, I, 18K, 19G—I)

Figure 5.  Laetmogone billetti sp. nov., paratype, St. JC048/16, dive 162. (A,B) Dorsal and ventral view, scale 2 cm; (C) tentacle disc magnified; (D–H) dorsal ossicles, scale 0.1 mm; (I,J) ventral ossicles, scale 0.1 mm.

Figure 6.  Laetmogone billetti sp. nov., paratype, St. JC048/16, dive 162. (A–G) Tube feet; (H–L) papillae; (M–V) tentacles; (U) magnified ossicle (T). (F,U) scale A; all others scale B.

Holotype

NHM 2012.3, RRS James Cook, St. JC048/24, ROV Isis Dive 165, 54°01.08′N, 34°09.46′W, 2501–2398 m, 9–10 June 2010, specimen 50 mm long in preserved state.

Paratypes

NHM 2012.4-5, RRS James Cook, St. JC048/16, ROV Isis Dive 162, 53°59.39′N, 36°11.66′W, 2450–2272 m, 6 June 2010, 2 ind., 80 and 40 mm in length in preserved state; NHM 2012.6, RRS James Cook, St. JC048/56, ROV Isis Dive 180, 49°01.18′N, 27°42.33′W, 2758 m, 29 June 2010, 1 ind., 25 mm long.

Additional material

This species was observed in situ at the Station JC048/6 Dive 159.

Type locality

North Atlantic, MAR, CGFZ area. Depth 2272–2758 m.

Diagnosis

Tentacles 15, large. Tube feet small and slender, up to 32 pairs. Dorsal papillae conspicuous, up to 12 pairs. Ossicles of the body wall wheels only; dorsal wheels of two types: large wheels (0.1–0.2 mm in diameter) with 5 or 4 central rays and central holes smaller than peripheral ones, and small wheels (0.05–0.1 mm) with central primary crosses and central holes larger than peripheral ones; ventral wheels small (0.05–0.06 mm) with 3 or 4 central rays.

Description

Colour in-vivo light purple (Figures 17H,I, 18K, 19G—I). Dorsal side convex, ventral flat. Skin semi-transparent. Body elongated, length up to 80 mm in fresh specimens, 50 mm in ethanol preserved specimens. Tentacles 15, large; tentacle discs with small knobs (Figure 5C). Number of papillae and tube feet increased with body size. Two rows of conspicuous dorsal papillae (Figure 5A); 12 dorsal papillae in one row in the largest specimen. Tube feet small in preserved specimens, long and slender in live specimens, up to 32 pairs. Ventrolateral brim absent.

Wheel-type ossicles numerous both on dorsum and ventrum. Dorsal wheels of two size types: large (>0.1 mm) and small (<0.1 mm). Large wheels predominant (Figure 5D,E), 0.10–0.22 mm in diameter, spokes 9–10 in most wheels, rarely 8 or 11 spokes; central rays usually 5, rarely 4 (primary crosses) or 6 rays. Stellate ossicles (ossicles with no rim) (Figure 5G) rarely occur, apparently these are undeveloped wheels. Small wheels (Figure 5F,H) 0.05–0.1 mm in diameter with central primary crosses and 4 central holes, central holes larger than peripheral ones. Small wheels may represent an early stage of development of wheel-type ossicles. Ventral ossicles (Figure 5I,J) small wheels 0.05–0.06 mm in diameter, centrally primary cross or 3 rays; ventral ossicles resemble dorsal wheels of small type. Wheels in tube feet small (Figure 6F), 0.04–0.06 mm in diameter, with central primary crosses and 4 central holes larger than peripheral ones. Slightly curved rods also present, up to 0.65 mm in length with small and large spines, large spines often bifurcated and bearing smaller spines (Figure 6A,B); small rods can bear few little spines; some rods with additional processes (Figure 6E,G). One more type of ossicles on ventrum flattened crosses with spinous arms (Figure 6D). In papillae wheels large (Figure 6K,L) and small, similar in size and shape to those in dorsal skin, however small wheels dominant; rods also present, up to 0.4 mm in length, slightly curved (Figure 6H,J) or with curved ends (Figure 6I); spines mainly on rod ends. Ossicles in tentacles very variable (Figure 6M–V): numerous small and large wheels as on dorsum, small wheels being more numerous, rods up to 1.1 mm long, from straight to curved or irregular, most of rods with numerous spines of different size, large spines sometime bifurcate and bear additional spines.

Remarks

Observed mainly on steep slopes with patches of detritus. Possibly able to swim.

Relationships

Laetmogone billetti sp. nov. is similar to species with two types of wheels and slender tube feet: L. fimbriata (Sluiter, 1901) and L. biserialis Fisher, 1907 . Laetmogone billetti differs from both these species by having large wheels with 5 central rays dominating on the dorsum. In L. fimbriata and L. biserialis large wheels have 6 central rays.

Distribution

Known only from the type locality.

Etymology

The species is named after Dr David S. M. Billett, renowned deep-sea biologist and expert on deep-sea holothurians.

Family Psychropotidae Théel, 1882

Benthodytes gosarsi Gebruk, 2008

(Figure 17E; online supplement 2)

Benthodytes gosarsi Gebruk, 2008: 49–50, 52, figures 1(a), 2, 3.

Material examined

St. JC011/23 (39 ind.), St. JC011/75 (21 ind.), St. JC011/101 (1 ind.), St. JC037/15 (15 ind.), St. JC037/19 (42 ind.), St. JC037/27 (40 ind.), St. JC037/61 (56 ind.), St. JC037/67 (23 ind.) and St. JC037/70 (23 ind.). This species was observed in situ at stations JC048/3 Dive 158 (1 ind.), JC048/6 Dive 159 (2 ind.), JC048/15 Dive 161 (9 ind.), JC048/26 Dive 167 (1 ind.), JC048/29 Dive 169 (1 ind.), JC048/33 Dive 170 (14 ind.), JC048/36 Dive 171 (7 ind.), JC048/48 Dive 176 (11 ind.) and JC048/51 Dive 177 (2 ind.).

Remarks

Benthodytes gosarsi was described based on material collected at two stations on the MAR: north of the Azores and south of the CGFZ. Later this species was found off Iceland and in the Whittard Canyon (original data): BIOICE (SBS) Sample Nr 2862, cruise B-13-95, St. 734, 30 August 1995, 61.168–61.170°N, 18.008–18.026°W, 2399 m; BIOICE (SBS) Sample Nr 3572, cruise B-4-03, St. 391, 5 September 2003, 63.502–63.500°N, 29.637–29.667°W, depth 2238–2242 m; RRS James Cook, Cruise JC36, St. JC36/005 ROV Isis Dive 99, 48°9.078′N, 10°34.607′W–48°8.590′N, 10°34.119′W, depth 3647–3680 m.

Benthodytes gosarsi was observed also on the Isis test dive (Dive 158), west from the ECOMAR northwest site (base of the MAR slope) at 3500 m depth.

Specimens were bright green in situ, which is the colour of their external skin layer. Specimens from trawl catches often lacked the external skin layer and their colour ranged from greenish-brown to purple.

Benthodytes gosarsi was one of the dominant holothurian species both in number and biomass at the northwest ECOMAR site and was also very abundant at the southeast site (original data, will be published separately). The species occurred only on flat areas. A young specimen of B. gosarsi was observed swimming on Dive 168 (online supplement 2).

Distribution

Eastern and central North Atlantic. Depth 2238–3680 m.

Benthodytes lingua R. Perrier, 1896

(Figure 18B)

Benthodytes lingua Perrier, 1896: 902; 1902: 456–461, plates XII(1–2), XXI(1–9); Deichmann 1930: 124–125; 1940: 200–201, plate XXXV(3–4); 1954: 384; Heding 1942: 15.

Benthodytes janthina Grieg 1921: 11; Heding 1942: 15. (non von Marenzeller, 1892)

Pannychia glutinosa Hérouard, 1902: 32, plate IV(17).

Material examined

St. JC037/27 (2 ind.), and St. JC048/43 Dive 174 (1 ind.). This species was observed in situ at stations JC048/33 Dive 170 (7 ind.), JC048/36 Dive 171 (2 ind.) and JC048/48 Dive 176 (1 ind.).

Remarks

Benthodytes lingua was common at the southern sites. This species is benthopelagic.

Distribution

North and South Atlantic. Depth 860–4700 m.

Benthodytes sanguinolenta Théel, 1882

Benthodytes sanguinolenta Théel, 1882a: 104–105, plates XXIII, XL(4–5), XLII(6); Ludwig 1894: 53–60, plate I(1–8); Koehler & Vaney 1905: 72; Clark 1913: 233; Ohshima 1915: 245; Clark 192: 142; Clark 1923a: 162; 1923b: 420; Heding 1940: p. 367; Hansen 1956: 44–45; 1975: 94–96, plates III–VI, IX(6–7), XII(4–5); Carney & Carey 1976: 69; Pawson 1982: 129–145; Bluhm & Gebruk 1999: 175, figure 3(d); Rogacheva et al. 2009: 463, figure 2.

Material examined

St. JC037/19 (1 ind.).

Distribution

Cosmopolitan eurybathic species. Recorded in the Atlantic (MAR, Peru Basin, off Bahama Islands), Pacific (Tasman Sea, Kermadec Trench, off Panama isthmus, Japan and Cascadia Basin), Indo-Pacific, South Africa and the Bay of Bengal and off the Crozet Islands. Depths 768–7250 m.

Psychropotes depressa (Théel, 1882)

(Figure 17F,G)

Euphronides depressa Théel, 1882a: 93–96, plates XXVI, XXX(5–6), XL(7), XLVI(4); Ohshima 1915: 244–245, figure 1.

Psychropotes depressa Hansen 1975: 106–111, figures 43–44.

Euphronides depressa var. minor Théel, 1886b: 2.

Euphronides cornuta Verrill, 1884: 217; 1885: 518, 538, figures 32–33; Deichmann 1930: 127–128; Heding 1940: 368.

Euphronides tanneri Ludwig, 1894: 39–44, plates III(7), IV, V(17–19).

Euphronides auriculata Perrier, 1896: 901–902; 1902: 434–438, plates XIII(1–2), XX(12–13); Grieg 1921: 8–9.

Euphronides violacea Perrier, 1896: 902; 1902: 438–441, plate XX(14), Deichmann 1930: 128–129; 1940: 201–202; 1954: 384; Heding 1942: 15–16; Madsen 1947: 16.

Euphronides talismani Perrier, 1896: 902; 1902: 441–444, plate XX(15); Hérouard 1902: 30–31, plate II(19–22); Deichmann 1930: 129; Heding 1942: 15, text figure 15.

Benthodytes assimilis Théel, 1886b: 2–3.

Material examined

St. JC011/23 (2 ind.), St. JC011/101 (5 ind.), St. JC037/15 (2 ind.), St. JC037/19 (2 ind.), St. JC037/27 (13 ind.), St. JC037/61 (10 ind.), St. JC037/67 (5 ind.) and St. JC037/70 (1 ind.). This species was observed in situ at stations JC048/15 Dive 161 (2 ind.), JC048/17 Dive 163 (1 ind.), JC048/24 Dive 165 (1 ind.), JC048/26 Dive 167 (8 ind.), JC048/33 Dive 170 (1 ind.), JC048/43 Dive 174 (1 ind.), JC048/48 Dive 176 (1 ind.), JC048/54 Dive 179 (2 ind.) and JC048/56 Dive 180 (1 ind.).

Distribution

Psychropotes depressa is known from the North and South Atlantic, and Pacific: off Japan, Gulf of Panama and Chile. One of the common species in the ECOMAR area. Depth 957–4200 m.

Family Elpidiidae Théel, 1879

Amperima furcata (Hérouard, 1899)

(Figures 7A–E, 17K, 18M,N, 19C)

Figure 7.  (A–E) Amperima furcata (Hérouard, 1899). (A,B) St. JC048/43 Dive 174, dorsal and ventral view, scale A; (C–E) dorsal ossicles, St. JC048/54, Dive 179: (C) scale B; (D,E) scale C. (F–N) Ellipinion delagei (Hérouard, 1896), St. JC048/24 Dive 165. (F,G) Dorsal and ventral view, scale D; (H) distal part of tube foot, magnified; (I) ventral C-shaped ossicle, scale E; (J,K) ventral rods, scale F; (L–N) tube foot ossicles, scale G.

Kolga furcata Hérouard, 1899: 171, figure 2; 1902: 40–41, plates III(7), VI(4–10), VIII(17).

Amperima furcata Hansen 1975: 159, figure 75; Gebruk 1990: 141–142, figure 61(7–9).

Periamma furcata Hérouard 1923: 91.

Material examined

St. JC011/23 (120 ind.); St. JC037/15 (90 ind.); St. JC048/43 Dive 174 (4 ind.) and St. JC048/54 Dive 179 (1 ind.). This species was observed in situ at stations: JC048/33 Dive 170 (88 ind.), JC048/36 Dive 171 (30 ind.) and JC048/56 Dive 180 (1 ind.).

The ECOMAR specimens collected by the ROV were in excellent condition, allowing the external morphological characters to be clarified.

Description

Colour in vivo pinkish, tentacle discs light pink; colour in ethanol whitish (Figures 17K, 18M,N, 19C). Skin semi-transparent, full of ossicles. Body ovoid. Length up to 65 mm in vivo, in preserved specimens up to 35 mm. Velum composed of two pairs of papillae fused almost over their whole length (Figure 7A–E). One pair of long papillae posteriorly to velum. Tube feet 8 pairs, located in the posterior two-thirds of the body, crowded posteriorly, forming a narrow brim.

Ossicle morphology corresponds well with the diagnosis. Dorsal ossicles (Figure 7C–E) with arms curved downwards, arms up to 0.35 mm in length. Apophyses bifurcated (rarely not); length of apophyses up to 0.12 mm. Ventral ossicles with arms straight or slightly curved downwards, arms up to 0.33 mm in length, distal one-third of arms may be curved upwards; apophyses bifurcated, up to 0.07 mm long.

Remarks

Very common species at the southern ECOMAR sites. Benthopelagic species.

Distribution

Northeast and central Atlantic (off the Azores, Bay of Biscay, MAR), northeast Pacific. Depth 1846–4700 m.

Ellipinion delagei (Hérouard, 1896)

(Figures 7F–N, 19K)

Scotoplanes delagei Hérouard, 1896: 167–168, figure 3; 1902: 39–40, plates VI(1–3), VIII(8–9).

Ellipinion delagei Hérouard 1923: 90–91; Hansen 1975: 163; Harvey et al. 1988: 185–186; Gebruk 1990: 133, figure 58.

Material examined

St. JC037/15 (20 ind.), St. JC037/19 (1 ind.) and St. JC048/24 Dive 165 (1 ind.).

Remarks

Occurred on flat areas and cliffs. Benthopelagic species. (Also see remarks for Ellipinion alani sp. nov.)

Distribution

Central and northeast Atlantic. Depth 1165–2750 m.

Ellipinion alani sp. nov. Rogacheva & Gebruk

(Figures 8, 17N, 19F)

Figure 8.  Ellipinion alani sp. nov., holotype. (A) Dorsal view, scale A; (B–F) ventral ossicles; (G–M) tube foot ossicles; (N–R) tentacle ossicles. (D–F,M) scale B; (B,C,G–L,N–R) scale C.

Holotype

NHM 2012.7, RRS James Cook, St. JC048/24, ROV Isis Dive 165, 54°01.08′N, 34°09.46′W, 2501–2398 m, 9–10 June 2010, specimen 70 mm long.

Paratypes

NHM 2012.8, RRS James Cook, St. JC048/24, ROV Isis Dive 165, 54°01.08′N, 34°09.46′ W, 2501–2398 m, 9–10 June 2010 (1 ind., 70 mm long) and NHM 2012.9, St. JC048/43, ROV Isis Dive 174, 48°43.87′–48°44.23′N, 28°39.01′–28°39.57′W, 2620–2547 m, 22 June 2010 (1 ind., 100 mm long).

In situ observations

This species was observed in situ at the Station JC048/33 Dive 170 (16 ind.).

Type locality

North Atlantic, MAR, CGFZ area. Depth 2398–2620 m.

Diagnosis

Skin semi-transparent, light orange. Velum consists of two pairs of papillae; one pair of papillae posteriorly from velum. Tube feet 11–12 pairs, posterior 6 pairs fused at the base. Ossicles absent in dorsal skin. Ventral ossicles rods up to 0.85 mm in length and C-shaped elements up to 0.05 mm.

Description

Body ovoid. Length in vivo 110–130 mm, in ethanol 65–100 mm. Skin semi-transparent, colour in vivo light orange (Figures 17N, 19F). Tentacles and tips of tube feet are more pigmented than the body skin. Velum consists of two pairs of papillae fused over half to two-thirds of their length. One pair of free papillae located posteriorly to velum. Tube feet 11–12 pairs; posterior 6 pairs of tube feet partly fused forming brim. Tentacles 10. Ossicles lacking in dorsum; in dorsal papillae numerous rods occur in tips. On ventrum sparsely distributed rods (Figure 8B,C), up to 0.85 mm long, straight or slightly curved, with spinous ends and rare C-shaped ossicles (Figure 8D–F) 0.03–0.05 mm in size, usually with central swelling; C-shaped ossicles more numerous than rods, or approximately in equal proportion with rods. In tube feet mostly rods (Figure 8G–L) up to 1.1 mm in length, curved or irregular, rarely straight, with spinous ends and usually smooth central part; C-shaped ossicles 0.04–0.07 mm in size also present (Figure 8M). In tentacles numerous rods of different size and shape (Figure 8N–R), curved, irregular or rarely straight, with pointed or blunt spinous ends; spines more numerous in distal parts of rods, on some rods spines present in the middle; large spines bear additional small spines, additional processes sometime develop; C-shaped ossicles about 0.04 mm also present, less numerous than in tube feet.

Remarks

Tips of tube feet are enlarged and form discs, their surface knobbed and variously pigmented. A similar feature was observed in E. delagei (Figure 7H). This character is not known in other elpidiids. The function of the discs is unclear.

Ellipinion alani is the second species of the genus occurring in the Atlantic (E. delagei also occurs in the Atlantic). Ellipinion alani is a benthopelagic species; it has been observed on flat areas and talluses. It was one of the most common species at the southwest site.

Relationships

Ellipinion alani is most closely related to E. delagei. Both species lack dorsal ossicles and have C-shaped ossicles and rods on the venter. Ellipinion alani differs from E. delagei in the form of C-shaped ossicles: these lack processes in the middle part in the new species.

Distribution

Known only from the type locality.

Etymology

The species is named after Dr J. Alan Hughes for his great help in this work and his contribution to benthic studies in the ECOMAR project.

Kolga nana (Théel, 1879)

(Figure 19J)

Elpidia nana Théel, 1879: 15–16, figures 20–22.

Kolga nana Théel 1882a: 39–42, plates II(3–4), XXXIII(1–2); XXXIV(5); XXXVI(25), XLII(5, 8); Rogacheva 2012: 1186–1190, figures 4–7.

Kolga hyalina Hansen 1975: 170–171 (partim); Billett & Hansen 1982: 804–806, figures 2(1–9), 4–6; Gage et al. 1985: 200; Harvey et al. 1988: 185; Gebruk 1990: 121–122 (partim). (non Danielssen & Koren, 1879)

Kolga sp. Gebruk 2008: 50, 51, 52, 58, figure 1(c).

Material examined

St. JC048/24 Dive 165 (5 ind.).

Remarks

Description of this material was published earlier (Rogacheva 2012).

Extensive aggregations of Kolga nana were observed at the northeast site. The density of the aggregations was in tens of specimens per m². A number of specimens were seen inside the CGFZ on the ROV Isis Dive 169. K. nana is a benthopelagic species.

Distribution

The North Atlantic and Antarctic. Depth 1484–6235 m.

Peniagone azorica von Marenzeller, 1893

(Figures 9, 12H,I, 17J, 19D)

Figure 9.  Peniagone azorica von Marenzeller, 1893, dorsal ossicles, side view, ha. (A–D) St. JC048/24 Dive 165; (E–G) St. JC011/101; (H–L) BIOICE Sample No. 2852. (da) Deflection angle.

Peniagone azorica von Marenzeller, 1893: 12–13, plates 1(4), 2(5); Hérouard 1902: 42–43, plate VI(21–26); 1923: 87–88; Grieg 1921: 8, figure 4; Heding 1942: 20; Hansen 1975: 138–142 [partim: figure 63(5–9)]; Gage et al. 1985: 199; Tyler et al. 1985: 71–81; Gebruk 1990: 110–111, figure 45 (partim).

Material examined

St. JC011/101 (33 ind.), St. JC011/106 (6 ind.), St. JC011/111 (64 ind.), St. JC037/79 (29 ind.) and St. JC048/24 Dive 165 (1 ind.). This species was observed in situ at stations JC048/15 Dive 161 (1 ind.) and JC048/26 Dive 167 (36 ind.).

Additional material

BIOICE, south of Iceland, the Reykjanes Ridge, Sample Nr 2862, Cruise B-13-95, St. 734, Agassiz trawl, 30 August 1995, 61.17°N, 18.01–18.03°W, 2399 m, 40 ind.; Sample Nr 2863, B-13-95, St. 734, Agassiz trawl, 30 August 1995, 61.17°N, 18.04–18.05°W, 2400 m, 27 ind. RV Akademik Kurchatov, St. 916, Scotia Sea, 56°29′S, 50°51′W, 4660–5380 m, 2 ind.

Remarks

Peniagone azorica was described from the northeast Atlantic based on the Princess-Alice (Hirondelle II) collection. Hansen (1975) refered P. vedeli Hansen, 1956 to this species as well as a number of specimens from the Kermadec Trench (South Pacific). Gebruk (1990) re-established P. vedeli and referred most of the Kermadec specimens of Hansen to P. vedeli and P. affinis Théel, 1882. Gebruk (1990) also reported P. azorica from the Antarctic.

In the ECOMAR material, Peniagone azorica was identified mainly based on the morphology of its dorsal ossicles. It was a common holothurian species in the ECOMAR area. A close similarity was found between specimens of P. azorica and P. islandica Deichmann, 1930, the latter another common ECOMAR species. Peniagone islandica was described originally from the Reykjanes Ridge in 1930 (Deichmann 1930) but had never been collected since. The two species have a very similar external morphology and are indistinguishable in situ. Differences were found in ossicle morphology, the most important taxonomic feature in Peniagone. However, ossicles intermediate between those typical for P. azorica and P. islandica were also present. This is an important aspect in support of synonymizing the two species, in which case P. islandica would be a younger synonym. However, we prefer to accept P. azorica and P. islandica as separate species until new evidence becomes available. The taxonomy of these species requires further investigation, including the examination of the type specimens and additional material from the Atlantic.

The following is a comparative description of taxonomic characters in P. azorica and P. islandica.

i.	External morphology: Body elongate, live specimens up to 110 mm long in P. azorica and up to 150 mm long in P. islandica. Skin semi-transparent, light orange in vivo, whitish in ethanol-preserved specimens. Velum about 1/3 of the body length, with 2 pairs of papillae, the anterior pair the largest, fused at the proximal 1/3, posterior pair minute. Two pairs of minute small papillae posteriorly from velum. Tube feet 9–10 pairs, arranged in posterior 3/4 of the body, 4 or 5 posteriormost pairs fused forming a wide brim.
ii.	Dorsal ossicles. In both species of the Peniagone-type, with curved arms and usually 4 (or 3, very rarely 2) apophyses rising from the arms; arms and apophyses with small serrations more conspicuous on apophyses (Figure 12C–E,H,I). In P. azorica (Figures 9, 12H,I) length of arms 0.10–0.24 mm, usually 0.17–0.22 mm; arms and apophyses approximately equal in length, sometimes arms longer than apophyses, rarely shorter. Deflection angle 13–28° in apophyses, 13–35° in arms. The most common type of dorsal ossicles in P. azorica (the ‘azorica’ type) with apophyses slightly shorter than arms or approximately equal in length; deflection angle in apophyses 15–25°, in arms 25–30° (Figure 9A,B,H–J). In P. islandica (Figures 10 and 11) dorsal ossicles are more variable, the arm length 0.15–0.42 mm, usually 0.17–0.25 mm; arms shorter than apophyses, rarely equal in length or longer. Deflection angle in apophyses 10–32°, in arms 30–78°. The most common type of dorsal ossicles in P. islandica (the ‘islandica’ type) with arms widely spaced, shorter than apophyses; distal part of arms curved downwards, deflection angle in arms 35–45°, in apophyses 20–23° (Figures 10A–D, 11A–C,F–H,L). However, many variations of the ‘islandica’ type were found, e.g. ossicles with widely spaced arms, deflection angle in arms >50° (Figure 10F–H), or ossicles with exceptionally long narowly spaced apophyses and arms (Figure 11J). Ossicles of the ‘azorica’ type prevail in P. azorica, while ossicles of the ‘islandica’ type dominate in P. islandica. However, in both P. azorica and P. islandica ossicles of both types can be mixed, or ossicles of intermediate types occur (Figures 9C–G,K,L and 11D,E,I). Overall the variability in the shape of dorsal ossicles in these two species is much higher than in other species of Peniagone.
iii.	Ventral ossicles. In both species flattened crosses with 4 short spinous apophyses and spinous enlarged arm ends (Figure 12F,G,J).

Figure 10.  Peniagone islandica Deichmann, 1930, dorsal ossicles, side view. (A–D) St. JC048/43 Dive 174; (E–G) St. JC037/15; (H,I) St. JC048/54 Dive 179.

Figure 11.  Peniagone islandica Deichmann, 1930, dorsal ossicles, side view. (A–E) St. JC048/53 Dive 178; (F–J,K–M) two specimens from St. JC037/15.

Figure 12.  (A–G) Peniagone islandica Deichmann, 1930, St. JC048/53 Dive 178. (A,B) Dorsal and ventral view, scale A; (C–E) dorsal ossicles, scale C; (F,G) ventral ossicles, scale B. (H–J) Peniagone azorica von Marenzeller, 1893, St. JC011/101. (H,I) Dorsal ossicles, scale C; (J) ventral ossicles, scale B. (K–M) Peniagone longipapillata Gebruk, 2008. (K) Dorsal view, St. JC048/16 Dive 162, scale A; (L) dorsal ossicle of Peniagone-type, St. JC048/24 Dive 165, scale D; (M) dorsal rods, St. JC048/24 Dive 165, scale E.

The genetic relationship between P. islandica and P. azorica was examined based on sequences of four gene segments isolated from the ECOMAR material: 16S mtDNA, 18S and 28S rRNA and histone 3 H3 (C. Alt unpubl. data). Only H3 showed a clear separation of these species. On the consensus tree P. islandica and P. azorica grouped in one clade, but with low support (0.86). This may indicate that they are diverging species. The high degree of variability and overlap in the morphology of the dorsal ossicles in the two species supports this hypothesis.

Records show P. azorica and P. islandica are separated by the sub-polar front at the ECOMAR study site: P. azorica occurred north of the front, while P. islandica to south of it. Both species were relatively common at the MAR and are benthopelagic.

Specimens from the Scotia Sea (Akademik Kurchatov, St. 916) referred to P. azorica by Gebruk (1990) were re-examined and found to belong to a separate species, possibly a new one.

Distribution

Reliable records come from the central and eastern North Atlantic. Depth 1385–4020 m.

Peniagone islandica Deichmann, 1930

(Figures 10, 11, 12A-G 17M, 18L)

Peniagone islandicus Deichmann, 1930: 137; Heding 1942: 20–21, text figure 19.

Peniagone islandica Hansen 1975: 150; Gebruk 1990: 95–96, figure 35.

Material examined

St. JC011/23 (103 ind.), St. JC037/15 (49 ind.), St. JC037/19 (20 ind.), St. JC037/27 (20 ind.), St. JC037/79 (1 ind.); St. JC048/43 Dive 174 (1 ind.) and St. JC048/54 Dive 179 (1 ind.). This species was observed in situ at stations JC048/33 Dive 170 (11 ind.), JC048/36 Dive 171 (10 ind.), JC048/40 Dive 173 (numerous), JC048/53 Dive 178 (numerous) and JC048/56 Dive 180 (numerous).

Remarks

An important character that distinguishes this species, and is contained in the original description, is the number of tentacles which totals 8. This number is unusual for Peniagone and the wider Elpidiidae family: most elpidiids have 10 tentacles, with the exception of the genus Achlyonice which has 10–12 tentacles. Eight tentacles were present in the two (and only) type specimens upon which the original description of P. islandica was based (Deichmann 1930). The 8 tentacles were later confirmed in the two type specimens by Heding (1942) and Hansen (1975).

All of the specimens of P. islandica and P. azorica examined in this study had 10 tentacles. Numerous specimens of Peniagone identified as P. azorica and collected in the type locality of P. islandica (south-west of Iceland) by the BIOICE programme were re-examined. In all these specimens the number of tentacles was also 10.

Also, see ‘Remarks’ for P. azorica.

Distribution

Northern MAR, from the CGFZ area to Iceland. Depth 2137–2758 m.

Peniagone longipapillata Gebruk, 2008

(Figures 12K–M, 17O, 18F,G,P)

Peniagone longipapillata Gebruk, 2008: 56–58, figures 1(b), 9, 10.

Material examined

St. JC011/111 (1 ind.), St. JC048/16 Dive 162 (1 ind. fixed in formalin) and St. JC048/24 Dive 165 (1 ind.).

Peniagone longipapillata was described based on incomplete damaged specimens that had been collected by the MAR-ECO cruise at several stations on the MAR between the Azores and the CGFZ. The description included one in situ image showing a dark red specimen with two very long papillae extending from the velum (Gebruk 2008, figure 1B). The ECOMAR specimens collected by the ROV were in excellent condition allowing the external morphological characters to be clarified, in particular the structure of the velum.

Diagnosis

(After Gebruk 2008, and clarified by the present material.) Body elongated and flattened. Colour reddish to dark pink. Skin gelatinous. Tube feet 10–13 pairs, in posterior half of the body; posteriormost tube feet fused forming wide lobe. Velum composed of 3 pairs of papillae; first anteriormost pair short, fully fused; second pair extremely long papillae fused proximally, exceeding body in length; third pair very short. One pair of short dorsal papillae posterior of velum. Ossicles dorsally with 4 curved arms, 0.3–0.4 mm long, and 4 apophyses 0.15–0.25 mm long; both arms and apophyses spinous; ossicles of deeper skin layers spinous rods up to 0.12 mm long. Ventral ossicles primary crosses, with arms 0.10–0.15 mm long, slightly bent; short apophysis on each arm.

Description

Body in vivo up to 160 mm in length (without long velum papillae). Skin thick, gelatinous, semi-transparent, reddish. Mouth tube long, comprising one third of the body length. Velum consists of three pairs of papillae (Figure 12K): the anteriormost papilae short, completely fused forming a lobe; papillae in the second pair exceptionally long, may exceeded twice the body length (Figure 18G); papillae of the third pair are the smallest, they have appearance of a small triangular lobe at the base of papillae of the second pair. One additional pair of short papillae posterior to the velum. Tube feet 10–13 pairs; 6 posteriormost pairs of tube feet fused forming posterior swimming lobe. Unlike the type specimens in the ECOMAR specimen the ossicles of the ‘Peniagone-type’ (Figure 12L) were very scarce in the skin. Ossicles in deeper skin layers numerous spinous rods up to 0.12 mm long (Figure 12M), not noted in the type specimens. Ventral ossicles only numerous rods in deeper skin layers, similar to those on dorsum, no primary crosses present in the type series.

Remarks

Despite some differences in the ossicle composition, we refer the specimens to Peniagone longipapilata, mainly because the main type of dorsal ossicles corresponds well to the original description. Also, this species has very characteristic unusually long papillae and a reddish colour, which are characters rarely found in Peniagone. Differences in ossicles may arise from natural variability or be the result of differences in preservation. More material is required to clarify this issue.

Peniagone longipapillata is a benthopelagic species.

Distribution

Central and northeast Atlantic. Apart from the ECOMAR study area this species was observed in situ in the Whittard Canyon, northeast Atlantic, at depths around 3500 m (RRS James Cook cruise JC036). It is also known from the Porcupine Seabight (D. Billett, pers. comm.). Depth 2272–3500 m.

Peniagone coccinea sp. nov. Rogacheva & Gebruk

(Figures 13, 14, 18H,I, O, 19E; online supplement 1)

Figure 13.  Peniagone coccinea sp. nov. (A) Paratype, St. JC048/43 Dive 174, dorsal view, scale 50 mm; (B,C) St. JC037/15, freshly caught specimen, scale 50 mm; (D–I) dorsal ossicles, scale 0.1 mm; (J–L) ventral ossicles scale 0.1 mm: (E,G,H,I,L) holotype; (D,F,J,K) St. JC037/15.

Figure 14.  Peniagone coccinea sp. nov., St. JC048/43 Dive 174. (A–G) Tube foot ossicles; (H–P) tentacle ossicles.

Holotype

NHM 2012.10, RRS James Cook, St. JC048/38, ROV Isis Dive 172, 48°43.63′N, 28°28.83′W, 2600 m, 19–20 June 2010, specimen 70 mm long.

Paratypes

NHM 2012.11, RRS James Cook, St. JC048/43, ROV Isis Dive 174, 48°43.87′–48°44.23′N, 28°39.01′–28°39.57′W, 2620–2547 m, 22 June 2010 (1 ind., 65 mm long) and NHM 2012.12, St. JC037/27, 48°57.34′–49°13.55′N, 27°49.83′–27°50.92′W, 2700 m, 18 August 2009 (1 ind., ~35 mm long, originally preserved in 10% formalin).

Additional material

St. JC037/15 (15 ind.), St. JC037/19 (14 ind.) and JC037/27 (10 ind.). This species was observed in situ at stations: JC048/33 Dive 170 (24 ind.), JC048/36 Dive 171 (9 ind.) and JC048/40 Dive 173 (numerous).

Type locality

North Atlantic, MAR, to south of the CGFZ. Depths 2600–2750 m.

Diagnosis

Body elongated, posterior end broad. Colour bright red, skin transparent. Velum with 2 pairs of long and wide papillae fused at the base. Tube feet 9 pairs, posterior pairs forming brim. Ossicles of Peniagone-type, scattered; dorsal ossicles with spinous curved arms up to 0.2 mm long, each arm with one spinous apophysis up to 0.07 mm long.

Description

Length 70–90 mm in vivo, reducing to 50 mm in ethanol preserved specimens. Body length about 2.5× the width. Posterior end wide (more round in specimens caught by trawls; Figure 13B,C). Colour from light red to scarlet (Figures 18H,I, 19E). Skin thick, transparent, consistency gelatinous; skin may be not transparent in specimens sampled by trawls or preserved in ethanol. Velum (Figure 13A) large, may reach in length 2/3 of the body length; 2 pairs of wide papillae fused at the very base; the first pair longer than the second. Velum almost lacking, reduced to small protrusion in specimens caught by trawls (Figure 13B). Two pairs of small papillae arranged posteriorly of velum, not preserved in specimens caught by trawl. Tube feet 9 pairs; posterior 2 pairs small; posterior 3 pairs fused forming narrow brim. Ossicles of Peniagone-type scarcely distributed in skin; some specimens from trawl catches lacked skin with ossicles. Dorsal ossicles (Figure 13 D–H) with arms up to 0.2 mm long, strongly curved downward, spinous; apophyses 4, up to 0.07 mm long, covered by small spines, pointed; ossicles of deeper skin layers on dorsum flattened crosses with spinous arms about 0.2 mm in length (Figure 13I). Ventral ossicles (Figure 13J–L) flattened crosses with highly spinous arms bearing 4, rarely 3, short blunt spinous apophyses; arms up to 0.15 mm, apophyses 0.05 mm, ossicles in deeper skin layers lacking. Tube feet ossicles flattened crosses with 0–2 apophyses (Figure 14A–C), crosses with arms curved downward with 1–2 apophyses (Figure 14D), and various rods up to 0.5 mm in length, often spinous (Figure 14E–G). In tentacles flattened crosses and crosses with arms curved downward, with 0–2 apophyses (Figure 14 H,M,O,P), usually apophyses absent; various rods (Figure 14J–L,N) and ossicles of irregular shape also present (Figure 14I).

Remarks

This benthopelagic species is common at both southern ECOMAR sites. Commensal polynoid polychaetes attached to the ventral side were found in one specimen (online supplement 1).

Relationships

Dorsal ossicles in Peniagone coccinea resemble those in P. porcella R. Perrier, 1896, but in the former they are smaller and less robust (dorsal ossicles in P. porcella have arms 0.2–0.3 mm long and apophyses of about 0.1 mm long). Peniagone coccinea has a very characteristic appearance, recognizable on in situ images and videos: the velum consists of 2 long and wide papillae that are free over almost their whole length, and bright red colour of body that is rare in Peniagone.

Distribution

Known only from the type locality.

Etymology

The species name coccinea means ‘scarlet’, corresponding to the colour of this holothurian.

Penilpidia midatlantica Gebruk, 2008

Penilpidia midatlantica Gebruk, 2008: 52–54, figures 4–6.

Material examined

St. JC037/19 (1 ind.).

Distribution

Penilpidia midatlantica is known only from the MAR: north of the Azores and to southeast of CGFZ. Depth 2078–2430 m.

Family Pelagothuriidae Ludwig, 1894

Enypniastes eximia Théel, 1882

Enypniastes eximia Théel, 1882a: 56–57, plate VIII(6–7); Sluiter 1901b: 77–79, plates II(8–9), V(5); Mitsukuri 1912: 215–218, plate VII(59–60); Heding 1950: 118; Pawson 1976: 289, plate I(a); 1982: 132, figure 3(a–c); Ohta 1985: 127–128; Gebruk 1989: 61–63, figure 2(6–7); Miller & Pawson 1990: 10–13, figures 1(c,d), 4; Bluhm & Gebruk 1999: 181, figure 6(d).

Enypniastes decipiens Koehler & Vaney, 1910: 95–96, plate III(1).

Enypniastes globosa Hansen & Madsen, 1956: 58–59, plate I(4–5).

Peniagone ecalcarea Sluiter, 1901a: 74–75, plate X(2).

Enypniastes ecalcarea Heding 1950: 118, figures 1–4.

Euryplastes obscura Koehler & Vaney, 1905: 71–72, plate IV(7–9).

Pelagothuria bouvieri Hérouard, 1906: 1–6, figure 2; 1923: 94–99, plate VI(1).

Planktothuria diaphana Gilchrist, 1920: 373–381, figures 1–4.

Enypniastes diaphana Billett et al. 1985: 400–403, figure 2.

Material examined

Only visual observation at station JC048/43 Dive 174 (1 ind.).

Distribution

Cosmopolitan species, occurring in tropical and moderate latitudes at depth range of 0–5433 m (Gebruk 1989).

Order Molpadiida Haeckel, 1896

Family Molpadiidae Müller, 1850

Molpadia musculus Risso, 1826

Molpadia musculus Risso, 1826: 293; Clark 1908: 165, plates 22(4–9), 23(4–7); Deichmann 1940: 225, plate 40(1–15); 1954: 405; Pawson 1965: 11, figure 3; 1977: 100, figures 1–4; Cherbonnier 1965: 17, plates 7(i–q), 8(a–j); Tortonese 1965: 98, figure 42; Pawson et al. 2001: 317–318, figure 2(a–c).

Molpadia violacea Studer, 1876: 464; Pawson 1963a: 15–16, plate 3(4–8); 1965: 12–13.

Trochostoma violaceum Théel 1886a: 42, plate 2(6); Lampert 1889: 842; Perrier 1905: 65.

Haplodactyla violacea Heding 1931: 280.

Eumolpadia violacea Heding 1935: 42, text figure 8(7–10), plates 5(10), 7(3), 8(4); Ludwig & Heding 1935: 144–145, text figure 11.

Eumolpadia asaphes Heding, 1935: 42–44, text figure 9, plates 5(9–10), 7(2).

Ankyroderma loricatum Perrier, 1898: 1666; 1902: 535, plate 22(23–28); Hérouard 1923: 133.

Ankyroderma danielsseni Théel, 1886a: 39, plate 2(6).

Material examined

St. JC011/17 (20 ind.), St. JC011/23 (39 ind.), St. JC011/101 (2 ind.), St. JC011/106 (1 ind.), St. JC011/111 (1 ind.), St. JC037/19 (66 ind.), St. JC037/27 (204 ind.) and St. JC037/61 (1 ind.).

Remarks

This infaunal species was common at all three ECOMAR sites that were trawled.

Distribution

Cosmopolitan species, unknown only from the Arctic. Depth 35–5205 m.

Molpadia aff. blakei (Théel, 1886)

(Figure 15)

Figure 15.  Molpadia aff. blakei (Théel, 1886), St. JC037/27. (A–H) Body wall ossicles; (I–L) tail ossicles.

Material examined

St. JC011/23 (11 ind.), St. JC011/75 (3 ind.), St. JC011/101 (3 ind.), St. JC011/106 (2 ind.), St. JC037/15 (2 ind.), St. JC037/19 (21 ind.), St. JC037/27 (32 ind.), St. JC037/61 (5 ind.), St. JC037/67 (5 ind.) and St. JC037/70 (4 ind.).

Description

Body length 9–38 mm. Skin brownish-light violet. Anterior part separated by constriction behind calcareous ring. Tentacles 15, discs with 2 processes. Body wall ossicles (Figure 15A–H) tables with three-pillared spires; most tables with 6 holes; tables with 3–5 holes also present. Phosphatic deposits absent. Tail with fusiform ossicles with three-pillared spire and few holes of different size (Figure 15I–L).

Remarks

In the ECOMAR specimens, discs in the body wall ossicles had mostly 6 holes that were different from prevailing discs with three holes in the original description and descriptions of Deichmann (1930, 1940) and Pawson et al. (2001). The ECOMAR specimens were referred to as Molpadia blakei based on the composition of ossicles. The variation of ossicles in M. blakei is not well known. Examination of the type material of M. blakei and additional material from the north Atlantic is required for more reliable identification.

This infaunal species was common in trawl catches at three ECOMAR sites: both northern sites and the southeast site.

Order Apodida Brandt, 1835

Family Myriotrochidae Théel, 1877

Myriotrochus clarki Gage & Billett, 1986

(Figure 17L)

Myriotrochus clarki Gage & Billett, 1986: 247, figures 7(d), 9(d), 13–17, 18(a); Harvey et al. 1988: 190; Smirnov 1999: 17.

Myriotrochus vitreus Cherbonnier 1970: 1269. (non M. Sars, 1866)

Myriotrochus sp. Gage et al. 1985: 203.

Material examined

St. JC011/075 (3 ind.), St. JC011/101 (2 ind.), St. JC037/15 (1 ind.), St. JC037/19 (6 ind.), St. JC037/27 (5 ind.), St. JC037/61 (4 ind.), St. JC037/67 (5 ind.), St. JC037/70 (6 ind.), St. JC048/49 (2 anterior fragments), St. JC048/50 (1 anterior fragment), St. JC048/52 (1 anterior fragment).

Remarks

Although this species is infaunal, it was observed in situ at the sediment surface at the station JC048/24 Dive 165. Skin in the specimen in vivo was transparent and light greenish in colour.

Distribution

The northeast Atlantic (Rockall Trough and the Bay of Biscay) and the Mid-Atlantic Ridge. Depth 480–2907 m.

Family Synaptidae Östergren, 1898

Labidoplax sp.

(Figure 16A,B)

Figure 16.  (A,B) Labidoplax sp., St. JC037/15, body wall ossicles. (C,D) Gephyrothuria alcocki Koehler & Vaney, 1905. St. JC037/19. (C) Dorsal view, scale 25 mm; (D) tentacle disc, magnified. ap, anal papilla; gp, genital papilla; eg, endgut; pp, posterior protuberance.

Material examined

St. JC011/75 (a fragment of body wall skin), St. JC048/34 (1 full ind., 1 anterior and 2 posterior fragments), St. JC048/22 (1 anterior fragment), St. JC048/27 (fragments), St. JC048/42 (1 ind.), St. JC048/49 (1 ind. and 1 anterior fragment), St. JC048/50 (1 anterior fragment), St. JC048/52 (1 ind.).

Description

Specimens 4–20 mm long. Skin whitish with dense layer of ossicles. Tentacles 11, each with 1 terminal and 2 lateral digits. Calcareous ring consists of 11 pieces. Ossicles anchors and anchor plates (Figure 16A,B). Anchors 0.13–0.20 mm long, narrower than anchor plates, outer margin of arms with few serrations; shaft swollen posteriorly. Anchor plates 0.15–0.20 mm in length, 0.12–0.18 mm wide; anterior part with 7 serrate holes, rarely serration absent; posterior hole bean-shaped, rarely rounded; handle tapered, with 2 smooth holes, the posteriormost hole the biggest, sometimes holes fused into long narrow hole.

Remarks

The morphology of the anchor and the anchor plate ossicles is the most characteristic feature in the taxonomy of Labidoplax. Labidoplax sp. from the ECOMAR area is similar to L. georgii Smirnov, 1997 in the number of tentacles and the ossicle morphology. There are some minor differences in the shape of the handle, which is not narrowed in L. georgii. Ossicles of our specimens also resemble L. media Östergren 1905, the species with 12 tentacles. Labidoplax georgii is known based on three records off New Caledonia from a depth range 570–1675 m. Labidoplax media is distributed at sublittoral depths at Norwegian, Scottish and Irish coasts and in the North and Mediterranean Seas.

Only two species of Labidoplax are known in the deep sea: L. southwardorum and L. similimedia. Both species were described by Gage (1985) from the Rockall Trough in the northeast Atlantic, from depths between 1000 and 2950 m.

Only a fragment of one specimen was found in OTSB catches. Other specimens were collected with a megacorer. Specimens of Labidoplax sp. were found mainly in the upper 0–2 cm sediment slices. However, two specimens also were found in 2–6 cm slices. At stations JC048/49, JC048/50 and JC048/52, Labidoplax sp. was found together with Myriotrochus clarki but in different sediment layers: 0–2 and 2–6 cm, respectively.

Incertae familiae

Family Gephyrothuriidae Koehler & Vaney, 1905

Gephyrothuria alcocki Koehler & Vaney, 1905

(Figures 16C,D, 19L)

Figure 17.  Underwater images. (A) Staurocucumis abyssorum, St. JC048/43 Dive 174; (B) Benthothuria funebris, St. JC048/29 Dive 169; (C) Hansenothuria sp., St. JC048/40 Dive 173; (D) Mesothuria maroccana, St. JC048/40 Dive 173; (E) Benthodytes gosarsi, St. JC048/3 Dive 158; (F) Psychropotes depressa, St. JC048/43 Dive 174; (G) Psychropotes depressa, St. JC048/54 Dive 179; (H) Laetmogone billetti sp. nov., St. JC048/24 Dive 165; (I) Laetmogone billetti sp. nov., St. JC048/16 Dive 162; (J) Peniagone azorica, St. JC048/24 Dive 165; (K) Amperima furcata, St. JC048/43 Dive 174; (L) Myriotrochus clarki, St. JC048/24 Dive 165; (M) Peniagone islandica and Amperima furcata, St. JC048/43 Dive 174; (N) Ellipinion alani sp. nov., St. JC048/24 Dive 165; (O) Peniagone longipapillata, St. JC048/24 Dive 165.

Figure 18.  (A–J) Underwater images; (K–P) freshly caught specimens from ROV, photos courtesy: David Shale. (A) Paelopatides grisea, St. JC048/6 Dive 159; (B) Benthodytes lingua, St. JC048/43 Dive 174; (C) Synallactidae gen. et sp. indet., St. JC048/40 Dive 173; (D) Pseudostichopus peripatus, St. JC048/24 Dive 165; (E) Deima validum validum, St. JC048/43 Dive 174; (F,G) Peniagone longipapillata, St. JC048/24 Dive 165; (H,I) Peniagone coccinea sp. nov., St. JC048/54 Dive 179; (J) Synallactes aff. crucifera, St. JC048/16 Dive 162; (K) Laetmogone billetti sp. nov., St. JC048/56, Dive 180; (L) Peniagone islandica, St. JC048/54 Dive 179; (M,N) Amperima furcata, St. JC048/54 Dive 179; (O) Peniagone coccinea sp. nov., St. JC048/54 Dive 179; (P) Peniagone longipapillata, St. JC048/16 Dive 162.

Figure 19.  Freshly caught specimens from trawls and ROV, photos courtesy: David Shale. (A) Abyssocucumis abyssorum, St. JC037/15; (B) Benthothuria funebris, St. JC037/15; (C) Amperima furcata, St. JC048/54 Dive 179; (D) Peniagone azorica, St. JC048/24 Dive 165; (E) Peniagone coccinea sp. nov., St. JC048/54 Dive 179; (F) Ellipinion alani sp. nov., St. JC048/24 Dive 165; (G) Laetmogone billetti sp. nov., St. JC048/56, Dive 180; (H,I) Laetmogone billetti, St. JC048/24 Dive 165; (J) Kolga nana, St. JC048/24 Dive 165; (K) Ellipinion delagei, St. JC048/24 Dive 165; (L) Gephyrothuria alcocki, St. JC037/61.

Gephyrothuria alcocki Koehler & Vaney, 1905: 78–80, figures 6–8; Clark 1908: 22, 186; Hérouard 1923: 33; Deichmann 1930: 202; 1940: 358; Heding 1935: 78; O'Loughlin 1998: 495–496, figure 1.

Himasthlephora glauca Clark, 1908: 22, 40–41, 185, plate XIII(1–4); Heding 1935: 78.

Gephyrothuria glauca Hérouard 1923: 33; Deichmann 1930: 202–203; 1940: 209–211; Heding 1940: 358; Hansen 1956: 48; Pawson et al. 2001: 315.

Gephyrothuria europeensis Hérouard, 1923: 30–33, plate IX(10).

Material examined

St. JC011/17 (1 ind.), St. JC011/23 (33 ind.), St. JC011/75 (34 ind.), St. JC011/101 (7 ind.), St. JC011/106 (6 ind.), St. JC011/111 (1 ind.), St. JC037/15 (4 ind.), St. JC037/19 (89 ind.), St. JC037/ 27 (118 ind.), St. JC037/61 (12 ind.), St. JC037/67 (9 ind.) and St. JC037/70 (7 ind.).

Description

Body cylindrical, posterior end narrowed (Figure 16C). Skin thin, smooth (in fresh specimens), whitish, non-transparent or semi-transparent, naked or completely covered with sand particles. Mouth terminal. Anus subdorsal, opened on tip of anal papillae, skin of anal papillae thin and damaged by intestine protruding out in all observed specimens; posterior end pointed upward. Papillae 6–9, filiform, paired and unpaired; paired papillae mainly arranged obliquely. Tentacles 15; tentacle discs with 2 short appendices on the outer margin (Figure 16D). Genital papillae if present located close to the anterior end of dorsal interradius. Gonad in single tuft.

Remarks

The ECOMAR specimens were referred to as G. alcocki according to the last revision of Gephyrothuriidae by O'Loughlin (1998). In that work, G. europeensis and G. glauca are considered as young synonyms of G. alcocki. However, Pawson et al. (2001) referred the northwest Atlantic Gephyrothuria to G. glauca, not commenting on its relationship to G. alcocki.

This infaunal species was common in trawl catches at the following three ECOMAR sites: both northern sites and the southeast site.

Distribution

Cosmopolitan in tropical and moderate latitudes. Depths 732–5379 m.

Faunal composition

In total, 32 species of Holothuroidea were identified in the ECOMAR area including the 3 species new to science: Laetmogone billetti sp. nov., Ellipinion alani sp. nov. and Peniagone coccinea sp. nov. The two species Hansenothuria sp. and Labidoplax sp., might also be new to science, but for their reliable identification more data are required on the variation of the ossicles. One species was identified only to family level (Synallactidae gen. sp.). The species belong to five orders: Dendrochirotida (1 species), Aspidochirotida (10 species), Elasipodida (16 species), Molpadiida (2 species) and Apodida (2 species). One species, Gephyrothuria alcocki, belongs to the family Gephyrothuriidae, a group for which the taxonomic position is uncertain (Solís-Marín 2003), currently placed within the Molpadiida (O'Loughlin 1998; Pawson et al. 2001). New data on the molecular phylogeny of Gephyrothuriidae suggest that it constitutes a separate order from the Molpadiida (C. Alt unpubl. data).

Elasipodida, in particular the family Elpidiidae, appeared the most species-rich taxon at the CGFZ area (Gebruk et al. 2010). This was expected, as elpidiids are very common in the deep sea at lower bathyal and especially abyssal depths.

The deep North Atlantic is one of the best-explored regions of the deep ocean. About 55 holothurian species are known from the northern MAR from 20°N to Iceland. All, with the exception of the three new species, were known from the North Atlantic. Many of these species were reported earlier by the MAR-ECO project (Gebruk 2008). The holothurians in MAR-ECO were sampled using the otter-trawl (the gear similar to that used in ECOMAR) at 9 stations: 5 southeast and 4 northwest of the CGFZ, in the depth range 1237–3527 m. At these stations 24 species were identified. From these species, 17 were found in the ECOMAR material and of those Peniagone longipapillata, Penilpidia midatlantica and Benthodytes gosarsi, are species that were described by the MAR-ECO expedition (Gebruk 2008). Twelve of the ECOMAR species were reported by MAR-ECO north of the Azores, while several species reported by MAR-ECO were not found by ECOMAR. Some of them, such as Psychropotes longicauda, probably occur at greater depth than was sampled within ECOMAR, and others occur at shallower depths (e.g. Thyone sp.). Paroriza pallens and Peniagone diaphana, reported by MAR-ECO northwest of the CGFZ, also were absent from the ECOMAR samples. Overall, despite the narrower depth range sampled in ECOMAR, more holothurian species were found in the CGFZ area compared to MAR-ECO: 32 and 24 species, respectively. This is a result of more intensive benthos sampling in ECOMAR together with the use of the ROV.

Sampling using ROV and trawl

In situ observations and selective targeted sampling using ROV Isis added the following seven species of holothurians that had not been collected by trawling within ECOMAR: Hansenothuria sp., Synallactidae gen. et sp. indet., Kolga nana, Peniagone longipapillata, Enypniastes eximia, Ellipinion alani sp. nov. and Laetmogone billetti sp. nov. Some of these species occur in habitats where trawling is impossible. For example, Hansenothuria sp. and the Synallactidae gen. et sp. indet. were observed only on steep slopes and cliffs. Laetmogone billetti sp. nov. was more common on slopes and cliffs than on flat sedimentary terrains. Other species, such as Enypniastes eximia, were also inaccessible through trawling because they are benthopelagic and rarely descend to the flat terrace. Finally, there is a group of species of gelatinous consistency. Even if sampled in trawls, they usually are badly damaged, rendering identification impossible. Among such species are Kolga nana, Peniagone longipapillata and Ellipinion alani sp. nov.

Equally, seven species found in ECOMAR were not observed in situ by the ROV video survey. Among them were infaunal species (Molpadia musculus, M. aff. blakei, Labidoplax sp. and Gephyrothuria sp.) and rare species (Bathyplotes natans, Molpadiodemas violaceus and Penilpidia midatlantica). Some holothurians, such as species of Mesothuria and Pseudostichopus, are difficult to identify in situ and their identification is only possible in the lab.

Our results demonstrate that significantly more information is obtained on deep-sea holothurians by combining data from trawl catches with observations and sampling from ROV video surveys. Many deep-sea holothurians are gelatinous and features of their external morphology are lost in specimens caught by trawls. Hence, the taxonomy of deep-sea holothurians is based mainly on ossicle morphology; characteristics of external morphology, although distinctive, are difficult to use.

Morphological adaptations

The external morphology in many genera of elpidiids is related to adaptations to a benthopelagic lifestyle, primarily swimming (Hansen 1975; Gebruk 1990, 1994, 1995). It has been suggested that swimming, drifting or moving with the current on the sea floor can reduce the energy costs for locomotion in holothurians (Miller & Pawson 1990; Gebruk 1995; Rogacheva et al. 2012). Swimming elpidiids have an enlarged mouth tube that is formed by a tentacle crown and the anterior part of the body. Expanded tentacles forming the anterior lobe are the most powerful and effective locomotory organ in swimming holothurians. The posterior swimming lobe is formed by fused posterior tube feet, and a flattened posterior part of the body. The role of the velum does not appear to be very important for swimming. The velum in elpidiid holothurians is more important for their positioning at the seafloor: with the aid of the velum and by using the currents holothurians can lift up (Figure 20B) or press down (Figure 20A) the tentacle crown relative to the substratum, resulting in optimal positioning for food collection (Gebruk 1995). Some species seem to use their velum as a sail – as an extra driving force when ‘walking on legs’. Another common feature in elasipodids are two lateral rows of large tube feet (legs) used for walking (Hansen 1975). Free tips of velum papillae, when stretched, can also act as tactile organs exploring the substrate, as suggested by Hansen (1975).

Figure 20.  The role of the velum in locomotion. (A) Pressing force; (B) lifting force.

Peniagone is the most species-rich genus in the family Elpidiidae, showing the highest diversity of external morphological features. In the ECOMAR area we observed in situ detailed morphology of the following species: P. diaphana, P. azorica, P. islandica, P. longipapillata and P. coccinea sp. nov. The combination of position and size of their tube feet, velum and tentacle crown is shown in Figure 21. The enlargement of tentacles (an important adaptation for swimming) correlates with major morphological transformations in the genus. Peniagone azorica and P. islandica (Figure 21A) have relatively well-developed tube feet in the anterior half of the body and a small velum, and their tentacles are not enlarged. The velum can be relatively larger, as in P. horrifer (Figure 21B), the species observed in situ at the abyssal plain around the Crozet Islands (Cross et al. 2012). In these three species, the anterior part of the body with tentacles used for food collection at the seafloor is balanced through the presence of large anterior tube feet and a velum. These species are more epibenthic, and they actively walk on their large lateral tube feet.

Figure 21.  Morphological diversification in Peniagone. Side view (left row) and shape of the velum (right row). (A) Peniagone azorica and Peniagone islandica; (B) Peniagone horrifer; (C) Peniagone coccinea sp. nov.; (D) Peniagone longipapillata; (E) Peniagone diaphana.

Peniagone coccinea (Figure 21C) and P. longipapillata (Figure 21D) have enlarged tentacles, which lift the anterior part of the body above the substrate. At this morphological stage anterior tube feet become inefficient, unless their size is much increased. The tube feet get displaced towards the posterior end and are partly fused. A large velum or long velum papillae in these species can be effective in balancing the anterior end when holothurians are on the substrate. Peniagone longipapillata was observed commonly with its papillae stretched frontwards into the current, with the size of its papillae exceeding that of body length. Peniagone coccinea has comparatively the largest velum, which is also commonly observed at the seafloor stretched frontwards into the current. This type of velum increases the buoyancy of the body and can be also effective as a parachuting lobe for drifting in the water column (online supplement 1).

In Peniagone diaphana the tube feet are almost reduced and the velum is weakly developed, forming the anterior skin fold (Figure 21E). According to in situ observations, P. diaphana spends most of its time drifting above the seabed with its anterior end oriented downward (Barnes et al. 1976). Lipps & Hickman (1982) used a term ‘big-bag construction’ for such a morphology and behaviour.

In other genera of Elpidiidae, the velum (if present) is usually rather simple: built of two or three pairs of relatively short papillae, fused to varying extent and forming the anterior dorsal lobe, similar to the morphology of some Peniagone species such as P. azorica and P. islandica. The variability of the velum in Peniagone illustrates one of its adaptations to the deep-sea environment and correlates with the success of this genus in the deep ocean.

Lifestyle and habitat

New observations in situ showed that swimming holothurians often empty their intestines before leaving the seabed. The intestine is long in many deep-sea holothurians (Roberts et al. 2000) and acts as ballast when filled with sediment and detrital material. The following phases of activity seem to be common in swimming holothurians: swimming/drifting with the current (i), arriving at a feeding spot at the seabed (ii), actively feeding at the seabed (iii), defecating (iv), and taking off for swimming (v). These activities on the examples of Peniagone coccinea sp. nov. and Benthodytes gosarsi can be seen in the video supplement (online supplements 1 and 2). Many of the holothurian species reported here had not been observed in situ before (Rogacheva et al. 2012).

Holothurians are one of the most successful megafaunal taxa in the ECOMAR area: they are species-rich and abundant in different habitats (Gebruk et al. 2010). Most epibenthic deep-sea holothurians are deposit-feeders, usually occurring in flat areas on sedimented surfaces. Sedimented terrains (terraces) are a common feature of the ridge in the studied area and are a suitable habitat for deposit-feeders. Holothurians in the ECOMAR area belong to the following ecological categories: infaunal, epibenthic and benthopelagic. Among the infaunal species, species of Molpadia and Gephyrothuria alcocki were the most abundant. Two small burrowing holothurians, Myriotrochus clarki and Labidoplax sp., were also common, but because of their rather macrofaunal size they were sampled less successfully with OTSB. Several specimens of both species occurred in megacorer samples. Eight out of 11 specimens of Labidoplax sp. were from the upper 2 cm sediment layer, two specimens were from the 2–6 cm layer and 1 specimen was from the 6–10 cm layer. All four specimens of M. clarki were from the 2–6 cm layer. At stations JC048/49, JC048/50 and JC048/52 these two species occurred together: Labidoplax sp. in the 0–2 cm layer, M. clarki in the 2–6 cm layer. Larger specimens of M. clarki are likely to borrow deeper into sediment.

Epibenthic forms were dominated by Pseudostichopus peripatus, Staurocucumis abyssorum and Mesothuria ssp. Among the benthopelagic forms, different species dominated in abundance at different ECOMAR sites. At the southern sites, the dominant species were Benthodytes gosarsi, Psychropotes depressa, Peniagone islandica and Amperima furcata. In the north, the most abundunt species included Paelopatides grisea, Peniagone azorica and Kolga nana. Benthothuria funebris was abundant both in the north and the south. Kolga nana was remarkably numerous at the northeast site: several tens of individuals per square metre occurred in aggregations of this species (Rogacheva 2012).

Holothurians were observed even on cliffs, which was an unexpected habitat for this taxon. They were recorded on rocks and in sediment pockets between rocky outcrops. Some species, such as Laetmogone billetti sp. nov., Synallactidae gen. et sp. indet. and Hansenothuria sp., could be specialized cliff forms: they were seen overwhelmingly in habitats only accessible to swimmers (Rogacheva et al. 2012). The data on the abundance and biogeography of the ECOMAR holothurians will be a subject of separate publications.

Editorial responsibility: John Zardus

Acknowledgements

We would like to thank David Billett, Alan Hughes, Pam Talbot, Tammy Horton, Ian Cross, Nataliya Budaeva, Holly Bik and Andrew Cabrinovic for their help during work at sea, NOCS and NHM. Thanks are also due to Alexander Mironov for identification of Myriotrochus clarki, Alexey Smirnov for valuable comments on Labidoplax taxonomy and Mark O'Loughlin and an anonymous reviewer for critical comments to the manuscript. Special thanks to David Shale for remarkable photographs of holothurians made on board RRS James Cook. We also thank Henry Ruhl and Chris Hauton for providing material and in situ images from the JC036 Cruise, Mark Shields and Raimundo Blanco-Perez for providing holothurians from the megafaunal samples, Andy Gooday for identification of Discospirina tenuissima and David Billett for the correction of English usage. We are grateful to the ROV Isis team and the crew of the RRS James Cook for their great assistance and cooperation on board, and Ben Boorman for having led the trawling at the MAR. The BIOICE material was kindly provided by Guðmundur Guðmundsson, Guðmundur Helgason and Olafur Asthorsson. The authors thank Imants Priede for his support of this work from field activities to the manuscript stage. This work was supported by the UK NERC-funded ECOMAR project (NE/C512961/1). AR is grateful for partial financial support from the Norwegian Ministry of Foreign Affairs granted to the Institute of Marine Research, Norway, the MAR-ECO project and RFBR reseach grant 12-05-33049. AR and AG were in part supported by the grant of Minobrnauki of Russian Federation Nr 8664.

Notes

Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory, University of Copenhagen, Denmark