A reassessment of Halopteris polymorpha (Billard, 1913) (Cnidaria: Hydrozoa), with descriptions of three new species Author Galea, Horia R. Hydrozoan Research Laboratory, 405 Chemin des Gatiers, F- 83170 Tourves, France horia.galea@gmail.com Author Gioia Di Camillo, Cristina Dipartimento di Scienze della Vita e dell'Ambiente, Università Politecnica delle Marche, I- 60121 Ancona, Italy Author Maggioni, Davide Marine Research and High Education (MaRHE) Center, Università degli Studi di Milano-Bicocca, 12030 Magoodhoo Island, Faafu Atoll, Maldives Author Montano, Simone Marine Research and High Education (MaRHE) Center, Università degli Studi di Milano-Bicocca, 12030 Magoodhoo Island, Faafu Atoll, Maldives Author Schuchert, Peter Muséum d’histoire naturelle, C. P. 6434, CH- 1211 Genève 6, Switzerland text Revue suisse de Zoologie 2018 2018-03-31 125 1 21 59 journal article 10.5281/zenodo.1196007 9f6a1d45-f725-42d1-a64c-b6ffaaae23d7 0035-418 1196007 Halopteris sibogae ( Billard, 1913 ) Figs 1 B-C, 2B, 4; Table 1 ; Appendix 1 Plumularia polymorpha var. sibogae Billard, 1913: 25 , fig. 16. – Van Soest, 1976: 89 . Thecocaulus polymorphus var. sibogae – Bedot, 1921: 9 . – Stechow, 1925: 497 . Halopteris polymorpha var. sibogae – Millard & Bouillon, 1973: 84 , fig. 10K. – (?) Hirohito, 1983: 62 ; 1995: 244 . Halopteris polymorpha – Schuchert, 1997 ( pro parte ): 66, 69, fig. 22E [non Halopteris polymorpha ( Billard, 1913 ) ]. Material examined: MHNG-INVE-97926; Indonesia , Bali , Tulamben , Liberty shipwreck, -8.27417° 115.59265°, 22 m , coll. H. R . Galea ; 29.09.2016 ; numerous plumes up to 23 mm high, of which many bear male gonothecae; 16S sequence MF784526 . – MHNG-INVE-97938; Indonesia , Bali , Padangbai, Jepun shipwreck, -8.52812° 115.51478°, 20 m , coll. H. R . Galea ; 06.10.2016 ; numerous plumes up to 25 mm high, of which 2 bear female gonothecae; 16S sequence MF784531 . – HRG-0991; Indonesia , Tukang Besi Archipelago , reef north off Hoga I. , -5.44633° 123.76417°, 20 m , coll. G. Allard ; 27.09.2011 ; several infertile plumes up to 20 mm high . Diagnosis: Halopteris with cormoids reaching heights of up to 2.5 cm , with monosiphonic, unbranched stems, divided homomerously into short internodes bearing a hydrotheca, a lateral apophysis, and up to 8 nematothecae (1 mesial, a pair of laterals, 1-2 axillary ones, and commonly 2-3 above hydrotheca). Cladia alternately arranged along stem, heteromerously divided into internodes; hydrothecate internodes longer than their ahydrothecate counterparts, carrying a hydrotheca and its up to 5 associated nematothecae (1 mesial, a pair of laterals, and 1-2 axillary ones); ahydrothecate internodes short, provided with 1-2 nematothecae. Hydrothecae deep, almost tubular. Lateral nematothecae borne on well-developed apophyses; basal chamber tall, whole nematotheca greatly surpassing hydrothecal margin; rim of upper chamber with adaxial emargination. Female gonotheca broadly ovoid, with large, rounded, apical aperture perpendicular to long axis of the theca, and closed by glass-watch-shaped operculum; 3 basal nematothecae. Male gonotheca smaller than female, ovoid, without noticeable aperture, with 2 basal nematothecae. In life, cauline polyps yellow, contrasting with their purely white cladial counterparts. Description: Colonies composed of numerous cormoids arising from tubular, creeping, branching hydrorhiza lacking nematothecae. Cormoids erect (though flaccid when out of liquid), up to 2.5 cm high. Cauli simple, monosiphonic ( Figs 1 B-C, 2B), from straight in their lower halves to distinctly geniculate in their upper halves; basal parts of varied length ( 1-11 mm long), rarely entire, generally subdivided into segments by a number of transverse nodes (up to 4 observed); segments ahydrothecate, but carrying a total of 0-43 nematothecae arranged in two distinct, longitudinal, closely-set rows; distal end of last segment marked by deeply-cut, oblique node. Remainder of stem longer, with strict homomerous segmentation; each cauline internode ( Fig. 4A ) moderately-long, bearing a hydrotheca in its lower half, a number of nematothecae, as well as at least a short, lateral apophysis supporting a cladium; up to 33 successive internodes observed. The proximal most internode bears always two opposite apophyses supporting a pair of cladia, but there may be up to 3 consecutive segments displaying this feature; all are demarcated by deeply-incised, oblique nodes, both proximally and distally. Above, the segments are separated by less-marked, oblique constrictions of the perisarc, and each bears but a single apophysis originating laterally next to the hydrotheca; apophyses alternate along the stem. There are 6-9 nematothecae per internode, of which 4-5 are associated to the hydrotheca: 1 mesial, a pair of laterals, 1-2 axillar, as well as 2-4 superior ones arranged in two parallel rows ( Fig. 4A ); all cauline nematothecae, exclusive of those associated to the hydrothecae, tightly and backwardly appressed against stem (turned posteriad), at least in preserved material. Cladia up to 3 mm long; composed of a very short, proximal, quadrangular, athecate segment, followed by a succession of alternating ahydrothecate and hydrothecate internodes ( Fig. 4A, C ); ahydrothecate internodes with proximal transverse node and oblique distal node; the reverse in hydrothecate internodes. First ahydrothecate internode comparatively longer than following counterparts, and always carrying 2 nematothecae in a row; remaining internodes with either 1 or 2 nematothecae in a row. Hydrothecate internodes, up to 8 per cladium, relatively short, accommodating a hydrotheca in their lower 3/4th and its 4-5 associated nematothecae: 1 mesial, a pair of laterals, and 1-2 axillar ( Fig. 4B, D ). Hydrothecae cup-shaped and relatively deep, adnate for half their length to corresponding internode, free adaxial and abaxial walls parallel, flaring slightly to margin; the latter circular in apical view, and slightly sigmoid laterally, with imperceptible scoop between side facing the lateral nematothecae and abaxial wall ( Fig. 4C, E ). All nematothecae, including the axillar ones, bithalamic and movable. Mesial ones triangular in frontal view, upper chamber with conspicuously lowered margin on adaxial side ( Fig. 4F 5 , 6 ). Lateral nematothecae mounted on well-developed apophyses ( Fig. 4F 7 ); long, greatly surpassing the hydrothecal rim ( Fig. 4C, E ), lower chamber high, upper one relatively shallow, and with adaxial emargination. Axillar nematothecae cornucopiashaped, adaxial wall of upper chamber with significant emargination ( Fig. 4F 8 , 9 ). Remaining nematothecae from both caulus (not shown) and cladia ( Fig. 4F 1-4 ) similar to the lateral ones, though comparatively shorter. Hydranths with 13-15 filiform tentacles; in life, all belonging to the stem characteristically yellow, contrasting with those from the cladia that are uniformly white ( Fig. 1C ). Colonies dioecious. Gonothecae arising laterally from below the stem hydrothecae through a short, lateral apophysis; mounted on short, quadrangular pedicel, broadly ovoid, though sexually dimorphic, with the males comparatively smaller than females; the latter provided basally with 3 nematothecae similar to the laterals of the hydrotheca, and a large, watchglass-shaped apical lid closing a rounded aperture with conspicuously thickened perisarc at margin ( Fig. 4G ); male gonothecae bearing two basal nematothecae and no noticeable aperture; a globular mass of sperm cells encircles a central, digitiform blastostyle ( Fig. 4H ); all female gonothecae observed ripe and empty, with the exception of basal remains of the blastostyle. Cnidome ( Fig. 4I ) composed of 3 types of microbasic mastigophores: large, elongated-ovoid [(18.1-19.8) × (6.6-7.3) μm, in nematophores, as well as scattered in the coenosarc]; small, banana-shaped [(6.1-6.6) × (2.1- 2.3) μm, in tentacles]; small, ovoid capsules [(5.1-5.4) × (2.9-3.1) μm, scattered in the coenosarc]. Fig. 4. Halopteris sibogae ( Billard, 1913 ) . Portion of stem and proximal part of a cladium in frontal (B) and lateral (C) aspects. Hydrotheca in frontal (D) and lateral (E) views. Cladial nematothecae (F): from ahydrothecate internodes (F 1-4 ), mesial (F 5, 6 ), lateral (F 7 ), single (F 8 ) and paired (F 9 ) axillar ones. Female (G) and male (H) gonothecae. Cnidome (I). Specimens MHNG- INVE-97938 (A-G, I), MHNG-INVE-97926 (H). Scale bars: 10 μm (F), 100 μm (D, E, I), 200 μm (G, H), 300 μm (A-C). Dimensions: See Table 1 . Remarks: In most stems, the proximal most hydrothecate internode gives rise to a pair of cladia; occasionally, two successive internodes are involved; in one instance, three proximal pairs occurred, followed by an internode provided with a single apophysis, and by another one giving rise to a pair of cladia. In such internodes, there are always 3 or even 4 nematothecae above the hydrotheca. The remaining stem internodes are randomly provided with either 2 or 3 nematothecae in two parallel rows. Both cauline and cladial hydrothecae bear either one (70% and 80% of cases, respectively, n=50 examined hydrothecae) or two (30% and 20% of cases, respectively) axillar nematothecae. Terminal stolonization occurs occasionally from the distal ends of both stems and cladia. Rarely, aberrant branching of cladia occurs: a short apophysis is given off laterally from either one or both apophyses supporting the lateral nematothecae; the structure of these 2nd order branchlets (not exceeding two hydrothecate internodes) is similar to that of a normal cladia, and begins with a short, quadrangular, athecate segment, followed by the first ahydrothecate intersegment carrying but a single nematotheca, instead of two as in the 1st order cladia. Sterile cormoids, similar to the present ones, with hydrothecae provided with exceedingly long lateral nematothecae were already reported notably from Indonesia by Billard (1913) and the Seychelles by Millard & Bouillon (1973) (both as Halopteris polymorpha var. sibogae ). According to the former author, this character mainly distinguishes his so-called variety from the nominal species. Similarly to the present observations, Millard & Bouillon indicate that “Intermediate athecate internodes [are] absent on stem but invariably present on hydrocladia”, although Billard observed that, on cladia, the ahydrothecate internodes may be occasionally fused to their preceding hydrothecate counterparts. Among the quite rich material studied here, only one case of fusion ( Fig. 4B , after the proximal most hydrotheca) was noted upon the careful examination of 10 cormoids from sample MHNG-INVE-97938. As noted above, the most prominent morphological difference between H. polymorpha and its so-called variety sibogae is to be found in the shape and size of their lateral nematothecae, including their corresponding apophyses (compare Fig. 3 D-F and 4B-E). Another noteworthy difference relies in the comparatively shallower hydrothecae (compare Fig. 3D & E and 4C & E ), and shorter cauline (compare Fig. 4A and 3 A-B) and cladial ahydrothecate (compare Fig. 4C and 3B ) internodes in the former. Moreover, only noticeable in living material, the bicolor aspect of the cormoids of the latter is striking ( Fig. 1B, C ), compared to the wholly yellow tinge observed in the former ( Fig. 1A ), especially when both species occur in sympatry. Other morphological and morphometrical differences observed in the material studied herein are listed in Table 1 . In light of these differences, we advocate here that the so-called variety sibogae must be recognized as a full species, different from H. polymorpha . The 16S data clearly corroborated this ( Fig. 9 ). Raising Plumularia polymorpha var. sibogae Billard, 1913 to full species is not threatened by Plumularia sibogae Billard, 1911 , because the former is to be correctly placed in the genus Halopteris Allman, 1877 [as H. sibogae ( Billard, 1913 ) ], while the latter is accommodated in Antennella Allman, 1877 . Halopteris sibogae differs from its congeners through a series of characters. A number of species with “peculiarities” (see under H. polymorpha ) should be excluded from the comparison, while the remaining ones are compared in Appendix 1. Among them, and in accordance with the phylogenetic tree, H. sibogae comes close to H. vervoorti Galea, 2008 (see below an account on the latter). Besides its exceedingly long, and thus very distinctive, lateral nematothecae, H. sibogae shares the following features with H. vervoorti : 1) their cauline internodes are rather short and bear 1-2 nematothecae distal to each hydrotheca; 2) there are 1-2 axillar nematothecae associated to both cauline and cladial hydrothecae; 3) their cladia are heteromerously-segmented, their ahydrothecate internodes are short compared to their hydrothecate counterparts, and bear single nematothecae; 4) their female gonothecae are indistinguishable morphologically (compare Fig. 4G and 5H, I, P ). Distribution: Indonesia [between Misool I. and West Papua ( Billard, 1913 ), Bali (present study), Tukang Besi Archipelago (present study)], Seychelles ( Millard & Bouillon, 1973 ), and questionably Japan ( Hirohito, 1983 ).