ZOOLOGIA 35: e24573

ISSN 1984-4689 (online)

zoologia.pensoft.net

RESEARCH ARTICLE

Ypsilothuria bitentaculata bitentaculata (Echinodermata: Holothuroidea)

from the southwestern Atlantic, with comments on its morphology
Luciana Martins1, Marcos Tavares1

1
Museu de Zoologia, Universidade de São Paulo. 04263-000 São Paulo, SP, Brazil.
Corresponding author: Luciana Martins ([email protected])
http://zoobank.org/6BEEC534-C983-4817-8799-FC8F89A1A9BE

ABSTRACT. Ypsilothuria bitentaculata bitentaculata (Ludwig, 1893), previously known from several localities in the Pacific Ocean,
is recorded herein for the first time from the southwestern Atlantic Ocean based on eight specimens caught off the coast of
southeastern Brazil, between 505–511 m deep. Several morphological details are added to the description of Y. b. bitentacu-
lata, including photographs of specimens and calcareous ring plates, as well as scanning electron microscope images of the
ossicles from the body wall, oral and anal siphons and introvert. Additionally, Y. b. bitentaculata is compared to its congeners.
KEY WORDS. Sea cucumber, Dendrochirotida, Ypsilothuriidae, Brazil, deep-sea, REVIZEE.

INTRODUCTION strait to Senegal], Y. b. virginiensis Heding, 1942 [West Indies]

and Y. talismani talismani Perrier, 1886 [Atlantic coasts of France,
Historically, the southwestern Atlantic deep-water benthic Spain, Morocco, Senegal and also the Caribbean Sea], and Y.
fauna has been poorly sampled and poorly understood (Manning talismani elegans Heding, 1942 [West Indies]. The recognition of
et al. 1989, Tavares 1999). In recent years, however, there has two subspecies by Heding (1942) within Ypsilothuria bitentaculata
been a proliferation of monitoring oceanographic cruises carried Ludwig, 1893 (namely Y. bitentaculata attenuata E. Perrier, 1886
out by oil and gas companies as well as survey expeditions con- and Y. bitentaculata virginiensis Heding, 1942) actually compul-
ducted by research institutions and the deep-sea fishing industry. sorily creates three subspecies (ICZN 1999: Art.47.1), with the
As a result, knowledge of Brazil’s deep-water benthic species, nominotypical subspecies Ypsilothuria bitentaculata bitentaculata
although very fragmentary, has been gradually increased. Ludwig, 1893 being the third one (regardless of the name of
Likewise, only recently more progress has been made on the nominotypical subspecies not appearing in Heding 1942).
the discovery of deep-sea holothuroids (e.g. Moura et al. 2010, Here we present a detailed morphological description of
Campos et al. 2010, Moura et al. 2015). the poorly known Y. b. bitentaculata, including color photo-
Among the recent efforts undertaken to explore Brazil’s graphs of full specimens and of the calcareous ring plates, as well
deep-sea benthic habitats are a number of deep-water oceano- as scanning electron microscope images of the ossicles from the
graphic investigations conducted in southeastern Brazil as part body wall, oral and anal siphons and introvert. Additionally, Y.
of the REVIZEE Program (Living Resources in the Exclusive b. bitentaculata is compared to its congeners.
Economic Zone) (Amaral and Rossi-Wongtschowski 2004). The
REVIZEE cruises in southeastern Brazil yielded eight specimens MATERIAL AND METHODS
of Ypsilothuria bitentaculata bitentaculata (Ludwig, 1893) (Ypsi-
lothuriidae), a species new to the southwestern Atlantic fauna. Specimens of Ypsilothuria bitentaculata bitentaculata were
As currently understood, the genus Ypsilothuria comprises collected from infaunal assemblages with the aid of a Van
two species: Y. bitentaculata (Ludwig, 1893) and Y. talismani Per- Veen grab and a rectangular dredge, sieved onboard through a
rier, 1886. These two species were questionably divided into five 1 mm mesh. Measurements were obtained from ethanol fixed
subspecies (Heding 1942, Paulay and Hansson 2013): Y. b. biten- specimens and correspond to the maximum lengths of the
taculata (Ludwig, 1893) [Pacific, South Africa and southwestern smallest and the largest specimens, respectively. Holothuroid
Atlantic – present record], Y. b. attenuata E. Perrier, 1886 [Davis morphological techniques and terminology followed Rowe and

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 L. Martins and M. Tavares

Doty (1977) and Samyn et al. (2006); the taxonomic classifica- with knobbed perforated plates, elongated, irregular in outline
tion followed Miller et al. (2017). Ossicles were sampled from (160–180 μm, Figs 10, 11). Plates of base of oral siphon with
different body regions (i.e. introvert, tentacles, body wall, oral undeveloped spires (400–800 μm, Fig. 15). Oral and anal siphons
and anal regions) using household bleach, washed five times with similar rods, anal rods smaller, strongly arched (40–70
in distilled water and then, five times in absolute ethanol. A μm, Figs 12–14). Anal siphon with irregularly perforated plates
number of ossicle samples were mounted on slides with Entellan (300–600 μm, Fig. 16).
Merck for permanent storage and then examined and measured Material examined. MZUSP 1306, Brazil, REVIZEE, off
under optical microscope. Other ossicle samples were dried coast of São Paulo, (25°43’S, 45°09’W), 13/Jan./1998, 511m, 6
and mounted on metal stubs with double-sided tape, coated spms. Ibidem, (24°20’S, 43°46’W), 9/Jan./1998, 505m, 2 spms.
with gold and observed with a LEO 440 Scanning Electron Comparative material examined. MNHN-IE-2005 6332,
Microscope (SEM). Slides of the type [body wall tables] Pacific, (6°35’S, 81°44 W),
Abbreviations and acronyms: specimen (spm); Museu de 24/Feb./1891, 782m. MNHN 3693, Pacific, (34°6’S, 119°8’W),
Zoologia, Universidade de São Paulo (MZUSP); Muséum national 1301m: 20 mm long [all originally labeled S. bitentaculata
d’Histoire naturelle, Paris (MNHN); National Museum of Natural Ludwig, 1893]. USNM 15689, United States, northwestern At-
History, Smithsonian Institution, Washington D.C. (USNM). lantic, Virginia, RV Albatross, stn 2723, (36°46’N, 73°09’W), 23/
Oct./1886, 3082m: 10 spms 3–10 mm long [originally labeled
TAXONOMY Y. bitentaculata (Ludwig, 1893)].
Distribution. Ypsilothuria b. bitentaculata has been re-
Ypsilothuriidae Heding, 1942 garded as a Pacific species (Oshima 1915, Pawson 1965, Gage
Ypsilothuria E. Perrier, 1886 et al. 1985). This is the first record of Y. b. bitentaculata from
the southwestern Atlantic. According to Thandar (1999) Y. b.
Ypsilothuria bitentaculata bitentaculata
bitentaculata (as Y. bitentaculata) occurs in green mud sediments
(Ludwig, 1893) and between 225 and 4440 m (Cherbonnier and Feral 1978).
Figs 1–19 Off the coast of São Paulo, Y. b. bitentaculata was found in silty
Sphaerothuria bitentaculata Ludwig, 1893:141, pl. XII, figs 16–17, sand bottoms around 500 m deep, within the previously known
pl. XIV, figs 5–14. bathymetric distribution of the species. In southwestern Brazil Y.
Sphaerothuria talismani – Deichmann 1930: 154, pl. 9, fig. 3 [not bitentaculata bitentaculata is so far lower bathyal in distribution
Ypsilothuria talismani Perrier, 1886] possibly owing to the influence of the colder waters from the
Ypsilothuria bitentaculata – Panning 1949: 455, Pawson 1965: 6–7,
South Atlantic Central Water (SACW) over the southwestern
text fig. 1, figs 1–5; Thandar 1999: 373–375, fig. 3 d–f; Massin
and Hendrix 2011: 422, fig. 7; Mecho et al. 2014: 294, 295, Brazilian shelf. It is not uncommon for deep-water species to
fig. 13. occur in depths shallower than usual owing to colder upwelling
waters (Kowalewski et al. 2002).
Diagnosis. Body strongly U-shapped. Tentacles crown of Remarks. Heding (1942: 26) split Ypsilothuria talismani E.
eight digitiform tentacles, the two lateral ones longest. Calcar- Perrier, 1886, Y. bitentaculata (Ludwig, 1893) and Y. attenuata
eous ring simple, radial and interradial plates deeply notched, E. Perrier, 1886 into two subspecies complexes, in which he
without posterior projections. Plates of body wall forming a test, included two additional subspecies: Y. talismani talismani E.
arched rods in tentacles. Knobbed plates in introvert. Perrier, 1886, Y. talismani elegans Heding, 1942, Y. bitentaculata
Description. Body strongly U-shaped (Fig. 1), length bitentaculata (Ludwig, 1893), Y. bitentaculata attenuata E. Perri-
5–10mm. Tentacles crown of eight digitiform tentacles, the er,1886, and Y. bitentaculata virginiensis Heding, 1942.
two lateral ones longest (Fig. 2). Oral and anal siphons short, Some authors have suggested that the morphological
opposite to each other, oral siphon wider than anal (Fig. 3). differences between the subspecies of Ypsilothuria are due to
Body wall thorny due to presence of intricate tables, visible with ontogeny only (Gage et al. 1985, Billet 1988). The shape of
naked eye (Fig. 4). Calcareous ring simple. Radial and interradial the calcareous ring, for example, changes with growth and the
plates with curved base, without projections on the posterior notches in the calcareous ring may not always be present, es-
surface, bifurcated anteriorly, the radial slightly higher than the pecially in juveniles. However, in the four specimens dissected
interradial (Figs 5, 18). for this study (maximal length: 6.0 mm; 7.9 mm; 8.2 mm and
Body wall tables with circular disc perforated, irregular in 10.0 mm), the shape of the calcareous ring was constant and the
outline. Each disc consisting of a laminar stereom with holes notches in the calcareous ring were always present.
ranging between 20 and 50 μm all over the disc plate (plate Recent observations are not consistent with Billet’s (1998)
size between 500 and 1400 μm; Figs 6–7). High spire strong claim that the average size of the dermal plates varies with the
(400–500 μm; Fig. 8), placed near edge of disc. Tentacles with size of the specimens. Specimens from the Indian Ocean with
arched rods (80–150 μm, Fig. 9), with one central perforation, about 20 mm had two-spired dermal plates ranging between
one central apophysis and perforated edge (2–4 holes). Introvert 1500 and 3000 μm (Samyn and Van den Spiegel 2016), whereas

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 Ypsilothuria b. bitentaculata from the southwestern Atlantic

Figures 1–5. Ypsilothuria bitentaculata bitentaculata (MZUSP 1306): (1) lateral view of the body; (2) detail of one of the two elongated
lateral tentacles detail of the tentacle (white arrow); (3) dorsal view of a specimen preserved in ethanol (note oral and anal siphons, white
and red arrows, respectively); (4) detail of the ossicles from the body wall (the red arrow indicates the spire); (5) calcareous ring. R, radial
plate. IR, interradial plate. Scale bars: 1–3 = 5 mm, 4 = 1 mm, 5 = 0.5 mm.

in the southwestern Atlantic a half-sized specimen (10 mm) tentacles). The plates of the introvert cannot be found neither
had single-spired dermal plates ranging from 500 to 1400 μm. in the type specimen of Y. bitentaculata (MNHN 6332) – since
Contrary, specimens from South Africa, although more than all that remains of it is a slide with the body wall plates –, nor
twice as large as the southwestern Atlantic specimens (25 mm), in the in the specimen MNHN 3693 which is incomplete. In
had single-spired, unexpectedly small dermal plates from 700 the specimen MNHN 3693 (20 mm) the size of the anal plates
to 1270 μm (Thandar 1999). ranged from 400 to 600 μm, whereas in the Brazilian specimens
Several authors (e.g. Ludwig 1893, Deichmann 1930, (5–10mm) the anal plates ranged from 300–600 μm. The north-
Heding 1942, Pawson 1965, Massin 1996) have referred to the western Atlantic (USNM 15689; 3–10 mm) and the southwestern
shape of the plates at the base of the tentacles to differentiate Atlantic specimens from Brazil agree well with each other.
between Y. t. talismani and Y. b. bitentaculata. However, as not- Ypsilothuria t. talismani actually differs from Y. b. bitentac-
ed by Thandar (1999) and in agreement with our results, the ulata in the morphology of the lateral interradial plates of the
knobbed plates are in fact present in the introvert (not in the calcareous ring, whose anterior ends are entire in Y. t. talismani

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 L. Martins and M. Tavares

Figures 6–16. SEM photomicrographs of the ossicles from Ypsilothuria bitentaculata bitentaculata (MZUSP 1306). (6–7) tables from body
wall in dorsal and lateral views, respectively; (8) detail of the spire; (9) rod from tentacles; (10–11) knobbed plates from introvert (12–14);
arched rods from anal and oral siphon. (15–16) plates from oral and anal siphons, respectively. Scale bars: 6 = 500 μm, 7–8 = 200 μm,
9–11 = 50 μm, 12–16 = 20 μm.

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 Ypsilothuria b. bitentaculata from the southwestern Atlantic

Figures 17–19. Outlines of the calcareous rings: (17) Ypsilothuria bitentaculata attenuata (after Heding, 1942); (18) Ypsilothuria bitentaculata
bitentaculata (MZUSP 1306); (19) Ypsilothuria bitentaculata virginiensis (after Heding, 1942). Note in 18 radials and interradials narrow
and the anterior end of both radials and interradials deeply notched. R, radial plate. IR, interradial plate.

and deeply notched in Y. b. bitentaculata. Additionally, the ten- the morphology of their tentacle rods and the size of the holes
tacle rods are straight and have few perforations at the ends in on their body wall plates.
Y. t. talismani (viz. Heding 1942), whereas the rods are arched
and have one central perforation and one central apophysis in ACKNOWLEDGEMENTS
Y. b. bitentaculata. Of noteworthy is that Billett’s (1988: fig. 16B)
illustration shows curved tentacle rods in Y. talismani similar to We are grateful to Jon Norenburg (USNM) and Marc Eleau-
Y. bitentaculata bitentaculata (Fig. 9). me (MNHN) for granting access to the collections under their
Ypsilothuria b. bitentaculata can be separated from Y. b. atten- responsibility and for providing working space to LM. Thanks
uata sensu Heding (1942) from the Northern Atlantic in having: also to Wagner Magalhães (University of Hawai’i at Mānoa) for his
(i) the calcareous ring with narrow radial and interradial plates helpful comments on a first draft of the manuscript and to Lara
(versus broad radial and interradial plates in Y. b. attenuata), (ii) Guimarães (MZUSP) for technical support with SEM images. LM
the anterior end of the radial and interradial plates deeply notched thanks Fundação de Amparo à Pesquisa do Estado de São Paulo
in the radial and interradial plates (Figs 5, 17, 18) (versus notched for providing financial support by way of a doctoral fellowship
only in the interradial plates in Y. b. attenuata) and (iii) arched (FAPESP process number 201318202-9). MT thanks Conselho
tentacle rods (versus irregular tentacle rods in Y. b. attenuata). Nacional de Desenvolvimento Científico e Tecnológico (CNPq
However, the differences between Y. b. bitentaculata and process 301806/2010-1) and Petróleo Brasileiro S.A. (PETROBRAS
Y. b. attenuata sensu Billett (1988) are subtler. In Y. b. attenuata process 4600224970) for supporting studies on the systematics
from South Africa both the radial and interradial plates of the of marine invertebrates. This manuscript greatly benefited from
calcareous ring are narrow and notched just as in the southwest- the comments of Y. Samyn and one anonymous reviewer.
ern Atlantic specimens of Y. b. bitentaculata (Figs 5, 18). In the
southwestern Atlantic, however, the size of plate holes range LITERATURE CITED
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Moura RB, Campos LS, Esteves AM (2015) Hooked from the deep: manuscript.
a rare new species of Taeniogyrus (Holothuroidea, Chiridoti- Competing Interests: The authors have declared that no competing
dae) from the continental slope of Brazil, southwestern Atlan- interests exist.

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