Hemieuryale pustulata
Creators: name: Gondim, Anne Isabelley
name: Dias, Thelma Lúcia Pereira
name: Christoffersen, Martin Lindsey
name: Stöhr, Sabine
Publisher: name: Zenodo
Year: 2015
Subjects: Biodiversity
Taxonomy
Animalia
Echinodermata
Ophiuroidea
Ophiurida
Hemieuryalidae
Hemieuryale
Hemieuryale pustulata

description: Hemieuryale pustulata von Martens, 1867
Figures 2 A–F; 3A–G; 4A–J; 5A–E
Hemieuryale pustulata von Martens 1867: 179, 484–486, fig. 2a–c.― Lyman 1869: 313; 1883: 277.― Verrill 1899b: 363 –364.― H.L. Clark 1915: 192.— Matsumoto 1917: 140. ― A.H. Clark 1921: 52.― Fell 1960: 12.― Emson & Woodley 1987: 33.― Martynov 2010: 48, fig. 36a.― Alvarado 2011: 270.― Alvarado & Solís-Marín 2013: 624.
Type material. Museum of Natural History of Berlin (Museum für Naturkunde). Two syntypes, MZB 1739. (Examined on photographs, provided by C. Lüter).
Type locality. 18° N; 70° W, Antilles, Caribbean Sea.
Material examined. Continental shelf in front of Municipality off Macau, of Rio Grande do Norte, 100 m: 1 spm, 17 Oct 2010 [UFPB. ECH.2159], 9 spms, 14 Sep 2012 [UFPB. ECH.2171], 13 spms, 0 6 Nov 2010 [UFPB. ECH.2169], 16 spms, 16 Feb 2011 [UFPB. ECH.2172], 23 spms, 17 Oct 2010 [UFPB. ECH.2173], 7 spms 0 4 Jul 2010 [UFPB. ECH.2175], 120 m: 25 spms, 24 Sep 2011 [UFPB. ECH.2170], continental shelf in front of Diogo Lopes, Macau, Rio Grande do Norte, 4º40’31,05”S 36º28’30,01”W, 130 m: 17 spms, 0 4 Jun 2012 [UFPB. ECH.2167], 5 spms, 15 Mar 2012 [UFPB. ECH.2168], 10 spms, 0 8 Dec 2012 [UFPB. ECH.2174], 4º42’09,9”S 36º28’08,22”W, 100 m: 7 spms, 23 Sep 2010 [UFPB. ECH.2163], 3 spms, 16 Aug 2012 [UFPB. ECH.2164], 4 spms, 0 9 Mar 2010 [UFPB. ECH.2166], 4º47’56,47”S 36º27’33,59”W, 130 m: 2 spms, 12 Dec 2011 [UFPB. ECH.2162], 8 spms, 18 Aug 2011 [UFPB. ECH.2165], 1 spm., 8 July 2010, [UFPB. ECH.212176], 2 spms., 04º44,8945’S, 36º25,4571, Potiguar Basin, 23 May 2011 [UFPB. ECH.2177], REVIZEE Central, col. N. Oc. Almirante Saldanha, 22º12’56”S, 250–500 m, calcareous bottom: 1 spm, 12 Jun 2002 [EQMN 2955], REVIZEE Central, 22º22’56”S 37º35’15”W, 240–300 m, bottom of rhodoliths: 2 spms, 12 Jun 2002 [EQMN 2953], Potiguar Basin, Rio Grande do Norte: 172 spms, Universidade Federal de Pernambuco, without registration number.
Diagnosis. Same as for genus.
Redescription (UFPB.ECH.2175). Disc pentagonal (dd = 5.62 mm), covered by strongly calcified, imbricated scales, of variable size and shape (Fig. 2 A, C, 3A, D). Radial shields large, approximately half length of dd, triangular, with tuberculous stereom, separated along their full length by a row of small plates that extend to arm (Fig. 2 C, E, 3A, E). Interradius covered by strongly calcified imbricated scales, slightly larger than those in center of disc. Central primary plate circular, flat and bulging (Fig. 2 A, C, 3A, B). Scales of variable size and shape, some strongly swollen, others flattened, are found surrounding the central primary plate (Fig. 2 A, C, 3A, B). Radial primary plates oval, strongly swollen on distal half (Fig. 2 A, C, 3A, B), almost forming a tubercle between each radial shield pair. Ventral interradius short, with scales similar to dorsal ones in shapes and sizes (Fig. 2 D), but more flattened and less imbricated. Bursal slits short and broad (Fig. 2 D, E, 3D, F), located on lateral margins of oral shields. Oral shields large and flabelliform (Fig. 2 D, 3D, F), stereom weakly tuberculous, occupying most of the ventral disc. Madreporic oral shield with large pore offset near lateral edge, stereom not tuberculous (Fig. 2 D, 3D, F). Adoral shields slightly smaller than oral shields, swollen with tuberculous stereom (Fig. 2 D, 3D, F). Small triangular extraoral plate, present on all or only some jaws (Fig. 2 D, 3D, F). Three to five lateral oral papillae (Fig. 2 D, 3D, F), the distal one largest and operculous, proximalmost papillae pointed and slightly infradental, middle papillae intermediate in size, rounded. One triangular pointed apical papilla (Fig. 2 D, 3D, F).
Arms. Five arms, approximately 4 to 7 times disc diameter long, and thick (Fig. 2 A, B). A mosaic of small plates on dorsal arm, variable in size and shape (Fig. 2 A, E, 3C). Accessory dorsal arm plate swollen and rounded (Fig. 2 A, C, E, 3A, C, E). The first accessory dorsal arm plate is the largest and most swollen (Fig. 2 E, 3A, E). Dorsal and accessory plates with simple stereom. Lateral arm plate visible dorsally and ventrally, with tuberculous stereom (Fig. 4 A, C), pairs dorsally and ventrally widely separated. Isolated plate from proximal arm about as high as long, outer surface on distal two thirds strongly tuberculous, flatter, proximal band with simple stereom. Inner side of lateral plate with vertical ridge, almost for entire plate height, slightly slanting proximalwards, with round flat "knob" on lower proximal part; a single perforation almost in center of inner surface. Arm spine articulations two parallel ridges, of equal length, separated at both ends, nerve opening perforating, muscle opening shallow depression (Fig. 4 C). Ventral arm plate axe-shaped, widest distally, with slightly convex distal edge, strongly concave lateral edges, obtuse proximal angle (Fig. 2 F, 3G), tuberculous stereom. Consecutive plates just touching on proximalmost arm, further out separated. One oval, operculiform tentacle scale (Fig. 2 F, 3G), longer than wide. Two thick round arm spines (Fig. 2 F, 3G), slightly longer than half an arm segment, ventral spine shorter than dorsal, both with a crown of thorns at tip (Fig. 4 E). Arm spines visible only on ventral side, absent on first two arm segments, two arm spines from third segment. Vertebrae streptospondylous (Fig. 4 F, J).
Dental plate. Entire, non–perforated, with five shallow tooth sockets, three times longer than wide, widest ventrally with largest socket (Fig. 5 C).
Oral plate. Approximately 1.5 times as long as high (Fig. 5 A, B). Abradial muscular area small (approximately 300 µm in diameter), elliptical, positioned transversally (Fig. 5 B). Adradial articular area slightly comma-shaped (Fig. 5 A).
Genital plates and radial shields. Adradial genital plate small (approximately as long as 3 arm segments) (Fig. 5 D), positioned laterally from second to fourth vertebrae. Abradial genital plate may be absent or is extremely reduced and possibly similar to a disc scale that we were unable to identify. Articulation surface of adradial genital plate is a long curved distal band (Fig. 5 D). Articulation surface of radial shield formed by two circular depressions, the distal one larger and deeper, and a narrow band corresponding to the band on the genital plate (Fig. 5 E). Radial shield slightly comma-shaped, convex abradial edge, almost straight adradial edge, distal end twice as wide as proximal end.
Variations. The observed variation with respect to general morphology was small in the studied specimens. A small extraoral triangular plate (Fig. 2 F, 3D, F) is present in most specimens. However, in some specimens, this plate was found absent on one or several jaws, or was even completely absent. This variation was observed both in juvenile and adult individuals. The extraoral plates are sometimes large, corresponding to about 1/3 of the length of the oral shield. The jaw plates (oral and adoral shields) are flattened in some specimens, differing from the typical pattern for this species (swollen plates). One specimen had one of the pairs of adoral shields fused, forming a single, slightly pentagonal plate, approximately of the same size as the oral shield. The ventral arm plate is be fragmented into two in few specimens. The primary plates are sometimes flattened and well developed or not evident, in which case the center of the disc is occupied by small scales of variable size and shape. In only one individual we observed the presence of one or two swollen scales (almost circular) between the radial shields. We observed five individuals with four- and two with six-fold symmetry (Fig. 9 A–H) in the 325 studied specimens.
Color. Hemieuryale pustulata has a color similar to that of its host Nicella guadalupensis (Duchassaing & Michelotti, 1860), being reddish-brown (Fig. 6). The color pattern may vary from uniformly reddish-brown, reddish brown with white spots, to almost completely white with reddish-brown areas (Fig. 6 A–F). This spotted pattern is extremely variable. Von Martens (1867) observed this same color pattern in the type specimens (Fig. 6 C, D, E). Individuals of H. pustulata found associated with the octocoral Verrucella Milne Edwards & Haime, 1857 are reddish-brown or yellowish with white spots of variable shape and distribution (Verrill 1899b). Frequently some of the plates of the oral region are white.
Description of the juveniles (up to 3 mm dd). (UFPB.ECH.2175) Disc pentagonal (Fig. 10 A, C) (dd = 1.5 mm), inflated, covered with strongly calcified and juxtaposed scales (Fig. 9 A, C). Radial shields large (approximately half length of dd), triangular (Fig. 10 A, C), largely separated by a row of scales which extend to the arm. Primary plates well developed, central and radials circular (Fig. 10 A, C). These are the largest plates found on the disc. Interradius occupied by 3 or 4 scales (Fig. 10 C). Bursal slits short and broad. One triangular apical papilla on tip of jaw. Four lateral oral papillae. Oral shield fan-shaped. Adoral shield large, slightly smaller than oral shields. Extraoral plate absent. Dorsal arm plate replaced by a mosaic of small plates (Fig. 10 D). Dorsal plate on distal arm small, triangular. Lateral arm plate large, and tuberculous. Ventral arm plate pentagonal, distal margin wider. One arm spine with a crown of thorns at tip. Arm spines absent on two first arms segments. One large and rectangular tentacle scale.
Main differences between juveniles and adults. In general, juveniles are very similar to adults. The difference is that juvenile specimens (≤ 3 mm dd) have flattened scales on the disc and the accessory dorsal arm plate has not differentiated (Fig. 10). Usually juveniles are completely reddish-brown (as their octocoral host), the characteristic white spots observed in most adults being rare. Specimens larger than 2 mm dd already have accessory dorsal arm plates, but these are still not swollen. In these individuals only the first accessory dorsal arm plate becomes slightly hemispherical. Unfortunately, no postlarval stages were observed in this study.
Differentiation of the dorsal and accessory dorsal arm plates. In the beginning the dorsal and ventral surfaces of the arm are almost completely covered by the lateral arm plate (Fig. 11 A). The lateral arm plate is large (corresponding to the full length of the arm segment) and they touch each other both dorsally and ventrally. Only in the distalmost portion do the two lateral arm plates become separate, forming a triangular opening in which the dorsal arm plate is inserted, forming a small triangular plate (Fig. 11 A).Subsequently the dorsal arm plate fragments into three plates (pc, pl I, and pl II) (Fig. 11 B). Plates I and II (pl I-II) will differentiate into the accessory dorsal arm plate. After the first fragmentation, the central plate (pc) divides into four plates (pc1, pc2, pc3, and pc4) (Fig. 11 C). Subsequently the plates formed from the first divisions continue to subdivide, giving rise to several plates of irregular shape and size (Fig. 11 D). As the central plate divides into several other plates, the accessory dorsal arm plate is displaced to more lateral areas, becoming swollen posteriorly. At the end of the process of plate fragmentation the dorsal arm plate is replaced by a mosaic of small plates (Fig. 2 E, 11E). In the adult arm segments it becomes impossible (without further experimental manipulation and more sophisticated topological marking techniques) to determine the central plate from which the final plates originated.
Distribution. Caribbean Sea (The Bahama Islands, Cuba, Jamaica, Dominican Republic, Martinique, Saint Lucia, Barbados, Grenada, Belize, Saba Bank – Netherlands Antilles, and Panama), Colombia (Emson & Woodley 1987; Alvarado 2011; Alvarado & Solís-Marín 2012), and Brazil (Fig. 7). In Brazil from Pará, Ceará, Rio Grande do Norte, Bahia, and Rio de Janeiro (Fig. 7). This study provides the first records for the Brazilian littoral.
Depth range. From 18 to 330 m (Smithsonian Database; Verrill 1899b).
Remarks. Von Martens (1867) described this species on the basis of two specimens collected in the Antilles with a dd of 5 mm (Fig. 8). According to Verrill (1899b), H. pustulata is common in waters of moderate depth throughout the West Indies (Caribbean Sea), wherever Verrucella (as Gorgonella Nielsen) lives. Although this study represents the first record for Brazil, H. pustulata appears to be an abundant species across the littoral, at least in northeastern Brazil.
Insights on the ecology of Hemieuryale pustulata. Fifty-three gorgonians were observed, all belonging to the species Nicella guadalupensis. Their maximum length and width was 495 mm and 580 mm, respectively. Ophiuroids (Hemieuryalidae) were found on all collected gorgonians. A total of 251 specimens of Hemieuryale pustulata were recorded in association with these gorgonians, having a mean disc diameter of 2.91 mm (varying from 0.55 to 7.41 mm) (Table 1). Some individuals are clearly juveniles, strongly camouflaged and difficult to perceive on the gorgonian. Only 2.15% (n = 7) of the analyzed individuals had scars, suggesting predation attempts. The largest and smallest specimens with regenerated parts measured had 4.53 mm and 1.35 mm in dd, respectively.
Gorgonian (Nicella guadalupensis) Ophiuroid (Hemieuryale pustulata)
No H (mm) W (mm) dd (mm) of specimens Mean (±SD) Tsp ......continued on the next page Hemieuryale pustulata was present on 100% of the collected gorgonians, varying from one to 30 individuals on the same colony (mean of 5.9 individuals/gorgonian). Table 1 provides size data for the studied hemieuryalid individuals found on the analyzed gorgonians. In three colonies of N. guadalupensis, the presence of bivalves (family Pteriidae) and another species of ophiuroid (an unidentified Ophiacanthidae) were observed, in addition to H. pustulata. Comparing the studied gorgonians, we observed a significant difference in the abundance of H. pustulata among them (Pseudo-F1-52 = 1.1614; p = 0.0016). Pearson’s correlation showed a moderate relation between the number of individuals and the gorgonian area (p = 0.009; r = 0.351) (Fig. 10 A). The majority of individuals were found on gorgonians with an area ranging from 0.004 and 0.2 m 2. However, there was no difference in the use of quadrants by individuals (Pseudo-F1-52 = 1.8849; p = 0.3271), indicating no clear pattern of distribution regarding the place of occupation in the habitat (Fig. 1 B).
Regarding size, individuals did not differ among the quadrants (Pseudo-F1-52 = 1.088; p = 0.0327), suggesting the absence of distinct distribution patterns for juvenile and adult individuals across the host gorgonian. This result was similar to that found in another euryalid species, Astrobrachion constrictum (Farquhar, 1900) (Stewart & Mladenov, 1997). There was no correlation between the size of individuals and the area of the gorgonians (p = 0.09; r = 0.235) (Fig. 12 B).
description: Published as part of Gondim, Anne Isabelley, Dias, Thelma Lúcia Pereira, Christoffersen, Martin Lindsey & Stöhr, Sabine, 2015, Redescription of Hemieuryale pustulata von Martens, 1867 (Echinodermata, Ophiuroidea) based on Brazilian specimens, with notes on systematics and habitat association, pp. 341-360 in Zootaxa 3925 (3) on pages 344-356, DOI: 10.11646/zootaxa.3925.3.2, http://zenodo.org/record/238248