First Record of Psolid Sea Cucumber Psolidium (Holothuroidea: Dendrochirotida: Psolidae) from the Brazilian Coast, with the Description of Two New Species

© 2020 Academia Sinica, Taiwan Open Access First Record of Psolid Sea Cucumber Psolidium (Holothuroidea: Dendrochirotida: Psolidae) from the Brazilian Coast, with the Description of Two New Species Luciana Martins1,* and Marcos Tavares1 1Museu de Zoologia, Universidade de São Paulo, São Paulo-SP, 04263-000, Brazil. *Correspondence: E-mail: [email protected] (Martins). E-mail: [email protected] (Tavares). Received 20 August 2019 / Accepted 5 January 2020 / Published 4 February 2020 Communicated by James D. Reimer Two new species, Psolidium nanoplax and Psolidium lonchostinum, are described from the southeastern Brazilian coast, from 44 and 200–258 meters deep, respectively. This is the first record of the genus Psolidium from Brazil. Psolidium nanoplax sp. nov. superficially resembles its Atlantic and Magellanic congeners, P. disciformis (Théel, 1886), P. dorsipes Ludwig, 1886, and P. prostratum Pawson & Valentine, 1981, but it can be readily distinguished from these by a combination of characters of the sole ossicles and by the absence of midventral tube feet. Psolidium lonchostinum n. sp. stands apart from all Atlantic and Southern Ocean species (Atlantic sector), including Psolidium nanoplax sp. nov., in having branched rods (thorn ossicles) and knobbed plates in the sole. A key and a synoptic table to all Atlantic and Southern Ocean (Atlantic sector) species of Psolidium is provided. Key words: Echinodermata, Sea cucumber, Biodiversity, Atlantic Ocean, Southern Ocean. Citation: Martins L, Tavares M. 2020. First record of psolid sea cucumber Psolidium (Holothuroidea: Dendrochirotida: Psolidae) from the Brazilian coast, with the description of two new species. Zool Stud 59:2. doi:10.6620/ZS.2020.59-02. BACKGROUND The Holothuroidea fauna from the Brazilian coast is still poorly know, but efforts over the last 18 years have improved our knowledge of the holothuroid biodiversity (Martins et al. 2012a b 2016; Martins and Souto 2015 2018; Souto et al. 2017; Martins 2018; Martins and Tavares 2018a b c 2019a b). In a continued effort to broaden the current knowledge of Brazil’s Holothuroidea, we describe herein two new species of Psolidium Ludwig, 1886, from São Paulo and Rio Grande do Sul. This is the first record of the genus from the Brazilian coast. Psolidium now includes 13 species in the regions comprising the Atlantic Ocean and the Atlantic sector of the Southern Ocean. In addition to a species descriptions, we provide a dichotomous key for the Psolidium species occurring in these regions. Additionally, a synoptic table of all Atlantic and Southern Ocean (Atlantic sector) Psolidium is provided. MATERIALS AND METHODS The specimens of Psolidium lonchostinum sp. nov. were collected from infaunal assemblages during the REVIZEE Program (Living Resources in the Exclusive Economic Zone), with the aid of a Van Veen grab and a rectangular dredge. Psolidium nanoplax sp. nov. was obtained from infaunal assemblages during the Campos Basin Monitoring Program with the aid of an ELOS dredge (Tommasi 1994). The infaunal samples were sieved onboard through a 1 mm mesh. Measurements (in millimeters, mm) were taken from ethanol fixed specimens and refer to the maximum length of the smallest and of the largest specimens, Zoological Studies 59: 2 (2020) doi:10.6620/ZS.2020.59-02 1 © 2020 Academia Sinica, Taiwan ethanol-fixed specimens and the maximum length was recorded of the smallest and largest specimens, unless otherwise stated. Dates are written in the format day.month.year, with months in lower-case Roman numerals. Labels on the calcareous ring follow Ludwig’s (1889–1892) scheme. Ossicles were extracted from the dorsal and lateral scales, tube feet and sole using household bleach, washed five times in distilled water, and then five times in absolute ethanol according to Samyn et al. (2006). Ossicle samples were mounted on slides with Entellan Merck® for permanent storage and then examined and measured under optical microscope. Micrometric data were obtained from 30 measurements for each ossicle category. Other ossicle samples were dried and mounted on metal stubs with double-sided tape, coated with gold and observed with a LEO 440 Scanning Electron Microscope (SEM). The studied specimens were deposited in the collections of the Museu de Zoologia, Universidade de São Paulo (MZUSP): AsSO (Atlantic section of the Southern Ocean), NEA (northeastern Atlantic), SEA (southeastern Atlantic), and SWA (southwestern Atlantic). RESULTS TAXONOMY Order Dendrochirotida Grube, 1840 Family PSOLIDAE Burmeister, 1837 Genus Psolidium Ludwig, 1886 Type species. Psolidium dorsipes Ludwig, 1886 [by monotypy] Atlantic and Southern Ocean Species (Atlantic Sector): Psolidium prostratum Pawson & Valentine, 1981 (NWA); P. complanatum Cherbonnier, 1969 (NEA); Psolidium lonchostimum sp. nov. (SWA); Psolidium nanoplax sp. nov. (SWA); Psolidium disciformis (Théel, 1886) (AsSO - Strait of Magellan); Psolidium dorsipes Ludwig, 1886 (AsSO - Argentine, Strait of Magellan); Psolidium gaini* Vaney, 1914 (AsSO); Psolidium incubans* Ekman, 1925 (AsSO); Psolidium pawsoni* O’Loughlin & Ahearn, 2008 (AsSO); Psolidium tenue* Mortensen, 1925 (AsSO); Psolidium whittakeri* O’Loughlin & Ahearn, 2008 (AsSO); Psolidium pulcherrimum Thandar, 2008 (SEA); Psolidium pseudopulcherrimum Thandar, 2008 (SEA). (*) Species also known from outside the AsSO. Psolidium lonchostinum sp. nov. Martins and Tavares (Figs. 1–3) urn:lsid:zoobank.org:act:C2B17FCD-41FE-4D98-BB758EA7348EFDC9 Holotype: 8.3 mm (MZUSP 744), Brazil, REVIZEE, off coast of Rio Grande do Sul, 33°41'S–51°32'W, 02.iv.1998, 200 m. Paratypes:7 specimens, 7–7.5 mm (MZUSP 743), 8 specimens, 6–8.2 mm (MZUSP 591), Brazil, REVIZEE, off coast of São Paulo, 24°20'S, 44°09'W, 258 m, 10. i.1998. Etymology: The specific epithet is formed by the combination of two Greek words, lonche (spear) and ostinos (bony, Latinized to ostinum), and refers to the thorn-shaped ossicles (branched rods) found in the sole. Diagnosis: Body flat, oval in outline, mouth and anus covered by a variable number of small and irregular scales, lacking oral and anal valves. Dorsal and lateral body with conspicuous imbricating scales covered by inconspicuous small tube feet (up to two per scale). Calcareous ring notched only in radial plates. Tube feet arranged in two rows, lacking midventral tube feet. Dorso-lateral ossicles are smooth multiperforated plates and branched rods (thorn ossicles). Sole ossicles are knobbed and perforated plate and smooth plates with slightly knobbed in edges. Dorso-lateral tube feet with perforated rods. Description: Body flat, oval in outline, 6–8.3 mm long and 4–5.9 mm wide (Fig. 1A). Mouth and anus covered by a variable number of small and irregular scales (0.8–1 mm wide), up to two tube feet penetrate each scale dorsally and laterally (Fig. 1B), lacking oral and anal valves. Marginal dorsolateral scales (0.1–0.3 mm) smaller than dorsal scales (Fig. 1C). Thin sole, lacking scales, tube feet arranged in a double series: inner series of large tube feet and outer peripheral series of smaller tube feet close to the ventral margin (Fig. 1D), lacking mid-ventral (sole) radial series of tube feet, except for a cluster (up to 5) posteriorly and anteriorly (Fig. 1E). Calcareous ring simple, lacking posterior processes; radial and interradial plates united only at the base, notched only at the radial plate (Fig. 1F). Dorsal/lateral ossicles are smooth and perforated plates, irregular in outline, with undulating margins (100–120 μm long) and round holes (5–20 μm in diameter) (Fig. 2B) and branched rods (thorn ossicles) (40–60 μm long, Fig. 2C). Dorsal tube feet with perforated rods (70–130 μm long), with undulating in margins (Fig. 2D). Sole with single-layered and elongated plates (130–150 μm long), perforated at their entire length and knobbed at center and margins (Fig. 2E–F) and smooth plate (Fig. 3A–E), slightly knobbed in the margin (70–100 μm long). Ventral tube feet with perforated rods with irregular, curved and undulating margins (80–160 μm long) (Fig. 3F) and end-plate. Distribution: Brazil: São Paulo (~24°S) and Rio Grande do Sul (~30°S), between 200 and 258 m. page 2 of 11Zoological Studies 59: 2 (2020) © 2020 Academia Sinica, Taiwan Fig. 1. (A–F) Psolidium lonchostinum sp. nov. (A–D) holotype (MZUSP 744). (A) upper view; (B) detail of dorsal tube feet (black arrow); (C) detail of lateral scales (white arrow); (D) ventral view; detail of ambulacral feet (note the inner and outer rows of tube feet: black and white circles, respectively); (E) paratype (MZUSP 591)) detail of ventral tube feet (black arrow); (F) outline of the calcareous ring [holotype] R, radial plate. IR, interradial plate. Note in F interradial plate entire and radial plate notched. Scale bars: A = 4 mm; D = 2 mm; E = 3 mm; F = 500 μm. (A) (C) (E) (B) (D) (F) page 3 of 11Zoological Studies 59: 2 (2020) © 2020 Academia Sinica, Taiwan Fig. 2. (A–F) Psolidium lonchostinum sp. nov., holotype (MZUSP 744). SEM photomicrographs of the ossicles. (A) scale from dorsal body wall, showing canals for tube feet (white arrow); (B) smooth plate from dorsal body; (C) branched rods (thorn ossicle) (black arrow); (D) rod from dorsal tube feet; (E–F) knobbed plates from sole. Scale bars: A–B = 50 μm; C = 40 μm; D–F = 50 μm. (A) (C) (E) (B) (D) (F) page 4 of 11Zoological Studies 59: 2 (2020) © 2020 Academia Sinica, Taiwan Fig. 3. (A–F) Psolidium lonchostinum sp. nov., holotype (MZUSP 744). SEM photomicrographs of the ossicles. (A) four-holed smooth plate from sole, ventral view; (B) four-holed smooth plate from sole, dorsal view; (C–D) multiperforated smooth plate from sole, dorsal view; (E) four-holed smooth plate from sole, lateral view; (F) rod from ventral tube feet, dorsal view. Scale bars: A–B = 30 μm; C = 40 μm; D–E = 50 μm; F = 80 μm. (A) (C) (E) (B) (D) (F) page 5 of 11Zoological Studies 59: 2 (2020) © 2020 Academia Sinica, Taiwan Psolidium nanoplax sp. nov. Martins and Tavares (Figs. 4–5) urn:lsid:zoobank.org:act:AC75BF38-07B5-4013-B197DBDCDB1B6E3F Holotype:11 mm (MZUSP 589), Campos Basin, southeastern Brazil, 21°41'S–40°20'W, Campos Basin, Monitoring Program coll., xii.1991 to i.1992, 44 m. Paratype: 1 specimen 8.5 mm (MZUSP 592), same data as the holotype. Etymology: The specific name is formed by the Greek words, nano (little) and plax (plate), in reference to the reduced length of the sole plates. Diagnosis: Body elongate in large forms (8–10 mm long; 5.5–5.9 mm wide), small forms ventrally and dorsally flattened. Dorso-lateral body covered by multilayered imbricating scales without granules or tubercles. Lacking oral and anal valves. Calcareous ring notched only in the radial plates. Tube feet arranged in two rows, lacking mid-ventral tube feet. Dorso-lateral ossicles are knobbed multiperforated plates. Sole ossicles are knobbed perforated plates and “cup-like” perforated plates. Tube feet with perforated plates and end plate. Description: Body elongate in large forms (10 mm long) (Fig. 4A); small forms ventrally and dorsally flattened (8 mm) (Fig. 4B). Mouth and anus lacking valves (Fig. 4B); anal cone slightly raised (Fig. 4C). Dorsal and lateral body with conspicuous imbricating scales (0.8–1 mm) and without granules or tubercles at the surface. One inconspicuous tube foot present at each scale (Fig. 4D). Marginal dorsolateral (Fig. 4E) scales smaller than dorsal scales (0.1–0.3 mm). Ventral sole lacking scales, tube feet arranged in a double series: inner series of large tube feet and outer peripheral series of smaller tube feet close to ventral margin (Fig. 4F), midventral tube feet absent. Calcareous ring simple, lacking posterior processes, radial and interradial plates united only at the base; radial plate notched (Fig. 4G–I). Dorso-lateral ossicles are knobbed and multiperforated single plates, flat, oval in outline, heavily knobbed on one side, smooth on the other surface, knobbed edges (150–170 μm long) and rounded holes 10–20 μm in diameter (Fig. 5A). Sole with knobbed and multiperforated single plates, strongly concave, oval in outline, heavily knobbed on one side, smooth on the other surface, knobbed edges (70–100 μm long), and round holes 15–20 μm in diameter (Fig. 5G) and “cup-like” multiperforated plates, concave, oval in outline (50–70 μm long) 10–15 μm in diameter (Fig. 5C–F). Dorsal tube feet with supporting rods (Fig. 5B), curved with one central perforation and one central apophysis (80–150 μm). Ventral tube feet with knobbed and multiperforated plates (Fig. 5H–I; (120–150 μm). Distribution: Campos Basin, southeastern Brazil, between 20.5° and 23°S. DISCUSSION Psolidium lonchostinum sp. nov. can be distinguished from its congeners (except P. ramum Davey and Whitfield 2013, from New Zealand; Psolidium parmatum (Sluiter, 1901) and Psolidium nigrescens Clark, 1938, both from northwest Australia) in having branched rods (thorn ossicles) in the sole. In this regard, P. lonchostinum sp. nov. P. parmatum, P. nigrescens and P. ramum resemble one another. However, P. lonchostinum sp. nov. differs from P. ramum in having the midventral tube feet restricted to the anterior and posterior parts of the body (Fig. 1E), whereas the midventral row of tube feet is complete across the body in P. ramum (see also Davey and Whitfield 2013. Psolidium lonchostinum sp. nov. stands apart from both P. parmatum and P. nigrescens in the absence of bulbous pillars on the dorsal and lateral scales and the absence of cups in the sole, respectively versus bulbous pillars present in P. parmatum and cups present in P. nigrescens). Psolidium lonchostinum sp. nov. additionally, differs from its southwestern Atlantic and Magellanic congeners, P. prostratum, P. disciformis and P. dorsipes, as follows: 1) from P. prostratum in having smooth and knobbed plates in the sole and about 50 dorsal tube feet (versus knobbed plates only and about 100 dorsal tube feet in P. prostratum); 2) from both P. dorsipes and P. disciformis in having no cups in the sole (versus presence of cups in P. dorsipes and P. disciformis). Psolidium nanoplax sp. nov. differs from P. lonchostinum sp. nov. in the absence of branched rods (thorn ossicles) in the sole, which are present in the latter species, and in having both knobbed and “cuplike” plates in the sole, whereas P. lonchostinum sp. nov. has knobbed and smooth plates in the sole. Psolidium nanoplax sp. nov can be readily differentiated from its southwestern Atlantic and Magellanic congeners P. prostratum, P. disciformis and P. dorsipes, by the characters of the sole ossicles and the absence of midventral tube feet. It differs from P. prostratum in having both knobbed and “cup-like” plates in the sole, whereas the latter species only has knobbed plates. The knobbed and “cup-like” plates in the sole of P. nanoplax sp. nov. also allow for its distinction from P. dorsipes, which has cups and knobbed buttons, and P. disciformis, which has cups and disc like-plates. Psolidium nanoplax sp. nov. further stands apart in having no midventral page 6 of 11Zoological Studies 59: 2 (2020) © 2020 Academia Sinica, Taiwan tube feet, whereas P. dorsipes and P. disciformis have midventral tube feet. Key to the Atlantic and Southern Ocean (Atlantic sector) species of Psolidium 1. Mid-ventral line of tube feet complete ......................................... 2 - Mid-ventral line of tube feet restricted to the anterior and posterior parts of the body ............................................................ 3 2. Sole ossicles include cups and perforated disc-like plates ............ ...................................................................................P. disciformis - Sole ossicles include cups and knobbed buttons ...........P. dorsipes 3. Cups absent .................................................................................. 4 - Cups present ................................................................................. 7 4. Dorsal region includes plates and branched rods ........................... ................................................... Psolidium lonchostinum sp. nov. - Dorsal region includes plates; branched rods absent ................... 5 5. Sole ossicles include only smooth and perforated plates ............... ...............................................................................P. complanatum - Sole ossicles include “cup-like” perforated plates and knobbed plates ............................................................................................. 6 6. Sole ossicles include perforated plates “cup-like” (up to 70 μm) and knobbed plates .........................................P. nanoplax sp. nov. - Sole ossicles include only knobbed plates; “cup-like” plates absent ......................................................................... P. prostratum 7. Brood-protection present .............................................................. 8 - Brood-protection absent ............................................................. 10 Fig. 4. (A–F) Psolus nanoplax sp. nov. (MZUSP 589, 592). (A) lateral view of holotype preserved in ethanol (note anal cone in white arrow); (B) upper view of [paratype-MZUSP 592] preserved in ethanol (note mouth and anus in black and red arrows, respectively); (C) detail of anal cone [holotype-MZUSP 592] (note anal cone and papillae, in white and red arrows, respectively); (D) detail of dorsal tube feet [holotype-MZUSP 592] (red arrow); (E) detail of lateral scales [paratype-MZUSP 592]; (F) ventral view detail of ambulacral feet [paratype-MZUSP 592], (note the inner and outer rows of tube feet: black and white arrows, respectively); (G) calcareous ring (H) detail of retractor muscle (white arrow) and (I) outline of the calcareous ring [paratype-MZUSP 592]; R, radial plate. IR, interradial plate. Note, only radial plate notched. Scale bars: A = 5 mm; B = 4 mm; C = 500 μm, D = 500 μm, E = 0.5 mm; F = 2 mm; G–I = 500 μm. (A) (C) (G) (H) (I) (B) (C) (E) (F) page 7 of 11Zoological Studies 59: 2 (2020) © 2020 Academia Sinica, Taiwan 8. Young brooded in folds of sole ....................................P. incubans - Young brooded in coelomic pouches ........................................... 9 9. Dorsal ossicles include cups and smooth plates ...P. pulcherrimum - Dorsal ossicles absent ............................... P. pseudopulcherrimum 10. Dorsal and lateral tube feet lacking support plates .................... 11 - Dorsal and lateral tube feet with support plates ......................... 12 11. Dorsal scales frequently with smooth white thickening; perforations reduced, many almost closed ....................P. pawsoni - Dorsal scales with irregular lumpy or reticulate thickening, rarely with smooth white thickening and almost closed perforations ...... ....................................................................................P. whittakeri 12. Sole ossicles include knobbed buttons and smooth perforated plates ...................................................................................P. gaini - Sole ossicles include knobbed plates and smooth perforated plates ................................................................................... P. tenue CONCLUSIONS The genus Psolidium comprises about 50 species distributed world-wide (WoRMS 2019), most of which found in the Southern Hemisphere (SH) (n = 40), especially in the Antarctic region (n = 10). The IndoPacific harbors 26 Psolidium species, the Pacific NH harbors 8 species, and the Atlantic Ocean harbors 13 species (Table 1). The distribution of tube feet along the midventral surface of the sole and the type of sole ossicles are diagnostic to the species level in Psolidium. Interestingly enough, the species with complete midventral row of tube feet across the body are confined Fig. 5. (A–I) Psolus nanoplax sp. nov. Martins & Tavares (MZUSP 589). SEM photomicrographs of the ossicles. (A) knobbed plate from dorsal body (B) supporting rod from dorsal tube feet; (C) “cup-like” plates from sole in dorsal view; (D) “cup-like” multiperforated plates from sole in ventral view; (E) “cup-like” four-holed plates from sole in dorsal view; (F) “cup-like” plates from sole in lateral view (G) knobbed plates from sole and (H–I) knobbed plates from ventral tube feet. Scale bars: A–B = 50 μm; C = 20 μm; D–I =, 30 μm. (A) (C) (G) (H) (I) (B) (C) (E) (F) page 8 of 11Zoological Studies 59: 2 (2020) © 2020 Academia Sinica, Taiwan Table 1. Synoptic table of the gross geographic and bathymetric distributions, and main morphological characters of the Atlantic and Southern Ocean (Atlantic sector) species of Psolidium. ANT, Antarctic region. NEA, northeastern Atlantic. NWA, northwestern Atlantic. SEA, southeastern Atlantic. SWA, southwestern Atlantic (including the Strait of Magellan and the Falklands/Malvinas Is.). TF, tube feet. (*) Type species of Psolidium. Bioecorregions follow Spalding et al. (2007) Character/species P. complanatum P. prostratum Psolidium nanoplax sp. nov P. lonchostinum sp. nov P. disciformis P. dorsipes* Distribution NEA Mediterranean NWA North Carolina to Florida SWA Brazil SWA Brazil SWA Strait of Magellan SWA Argentina, Chile; Strait of Magellan, Tierra del Fuego Deep (m) 480-1200 380-450 44 200-258 8-448 10-483 Complete Midventral radial TF No No No No Yes Yes Dorsal/lateral ossicles “Cup-like plates”; arched plates Smooth plates; knobbed plates Knobbed plates; supporting rods Smooth perforated plates; perforated rods ? Knobbed plates; smooth perforated plates; cups Ventral TF ossicles Smooth perforated plates Endplate Knobbed plates end plate Rods end plate Rod “like plates” ? Sole ossicles Smooth perforated plates Knobbbed perforated plates "Cup-like plates" Knobbbed perforated plates Knobbbed perforated plates; Smooth perforated plates Perforated disc-like smooth plates, cups; X shaped bodies Cups, Knobbed buttons; Knobbed perforated plates Number of TF by scale 1-2 1-3 1 1-2 1-2 1-2 Branched rods (thorn ossicles) Absent Absent Absent Present Absent Absent Reference(s) Cherbonnier (1969); FernándezRodríguez et al. (2019) Pawson & Valentine (1981) Present paper Present paper Théel, 1886; Pawson (1969) O'loughlin & Ahearn (2008) Ludwig, 1886; Pawson (1969) O'loughlin & Ahearn (2008) Character/species P. pulcherrimum Thandar, 2008 P. pseudopulcherrimum Thandar, 2008 P. gaini Vaney, 1914 P. incubans Ekman, 1925 P. pawsoni O'loughlin & Ahearn, 2008 P. tenue Mortensen, 1925 P. whittakeri O'loughlin & Ahearn, 2008 Distribu tion SEA South Africa SEA South Africa ANT South Georgia, Weddell Sea, Antarctic Peninsula ANT South Georgia ANT Weddell Sea ANT Antarctic Peninsula, ANT South Sandwich, South Shetland Islands Deep (m) 200 200 19-795 12-38 137-920 90-2100 146-759 Complet e Midvent ral radial TF No No ? No No No No Dorsal/ lateral ossicles Cups; smooth plates Absent Curved tube foot support plates Cups Smooth plates Tube foot support plates; endplates Absent Ventral TF ossicles Perforated plates Rods plates ? ? Perforated rod plates Perforated rod plates Irregular rods and elongate perforated rodplates Sole ossicles Knobbed plates; cups Knobbed plates; cups; end plate Knobbed buttons; smooth perforated plates Cups; perforated plates Smooth plates Smooth perforated plates; knobbed plates Shaped rods and perforated plates Number of TF by scale ? ? 1-3 1-2 1-4 1-3 1-4 Branche drods (thorn ossicles) Absent Absent Absent Absent Absent Absent Absent Reference(s) Thandar (2008) Thandar (2008) Vaney, 1914; O'loughlin & Ahearn (2008) Ekman, 1925; O'loughlin & Ahearn (2008) O'loughlin & Ahearn (2008) Mortensen (1925); O'loughlin & Ahearn (2008) O'loughlin & Ahearn (2008) page 9 of 11Zoological Studies 59: 2 (2020)