Revision of Halisiphonia Allman, 1888 (Cnidaria, Hydrozoa, Hebellidae), with comments on its taxonomic position

The deep‐water genus Halisiphonia is reviewed, based on redescriptions of all available type specimens of its species. The genus includes four valid species, H. arctica, H. galatheae, H. megalotheca, and H. nana, and one species inquirenda, H. spongicola, for which the type could not be located.

Halisiphonia is a genus of little known and rarely recorded species, and is chiefly characterized by an indistinct demarcation between pedicel and hydrotheca and by having relatively long pedicels in comparison with other Hebellidae. The inconspicuous diaphragm renders some Halisiphonia species superficially similar to stolonal colonies of the Lafoeidae genus Lafoea, whose members are usually characterized by erect colonies and gonothecae that are aggregated into coppinia.
The Halisiphonia species are inhabitants of deep waters, making it difficult to obtain intact specimens and to gather information on their life history. Scarce material also constrains the understanding on the taxonomy of the genus. Rees and Vervoort (1987) pointed out two better known species of Halisiphonia (H. megalotheca and H. galatheae) and ''three more, poorly known species in Halisiphonia'' (Rees and Vervoort 1987, p 34), namely H. arctica, H. nana, and H. spongicola. We have studied the type material of all known species of Halisiphonia, except H. spongicola, whose type material is presumably lost.
The goal of this study is to redescribe the holotypes of the known species of Halisiphonia, in order to clarify the taxonomy of this poorly known hebellid genus and to provide additional morphometric and morphological data (e.g. cnidome). A reliable evaluation of the intra-and interspecific variability is currently not possible and new material might require some of the species to be synonymized.

Material and methods
The material studied belongs to the collections of The Natural History Museum (London, UK), Zoological Museum of the University of Copenhagen (Denmark), Zoologische Staatssammlung Mü nchen (Germany), and Nationaal Natuurhistorisch Museum (NNM, Leiden, The Netherlands). Types and additional material were examined, measured, and photographed with a compound microscope and a stereomicroscope. The cnidome terminology follows Weill (1934) and Mariscal (1974); measurements of nematocysts were made on non-discharged capsules. Other study methods for Hebellidae and Lafoeidae are given in Peñ a and García-Carrascosa (1993) and Peñ a Cantero et al. (1998).

Diagnosis
Colonies stolonal with creeping hydrorhiza. Hydrothecae tubular or slightly conical, deep, borne on pedicels of varied length; pedicels arising singly from hydrorhiza and almost imperceptibly merging into hydrothecae; diaphragm present, though inconspicuous in some hydrothecae, thin and membranous. Operculum and nematophores absent.

Remarks
Allman (1888, p 30) established the genus Halisiphonia based on H. megalotheca (see Allman 1888, p 31, Plate 16, Figure 1, 1a), a species he thought lacking a diaphragm, and of which he stated the hydrothecal cavity was ''directly continuous with that of the peduncle or stolon''. Therefore, since its erection, the presence of a diaphragm is generally not mentioned in the diagnosis of Halisiphonia species. Halisiphonia nana Stechow, 1921 was also described as lacking a diaphragm (Stechow 1921, p 228;1925, p 452, Figure 22). In both cases, however, the diaphragm was originally overlooked: for H. megalotheca the presence of a diaphragm was confirmed by Billard (1910, p 5), who examined the holotype; for H. nana, we found a very thin, membranous diaphragm, although it was indistinct or even absent in some hydrothecae. Kramp (1932, p 40) comments: ''a diaphragm may be more or less distinctly developed or altogether lacking in this genus''. Indeed, Kramp (1937Kramp ( , 1956 described two other species of Halisiphonia, H. arctica and H. galatheae, respectively, in which he recognized a diaphragm. For the former, the diaphragm is stated as being ''a very delicate membrane with a central opening'' (Kramp 1937, p 38), whereas for the latter, it was said that ''a very slight internal thickening may sometimes indicate the base of the hydrotheca, and in a few cases an extremely delicate diaphragm may be discerned'' (Kramp 1956, p 17). Similarly, Vervoort (1966, p 121, for H. galatheae) states, ''in some thecae there is an extremely delicate membrane basally of the place of attachment, in some theca present as a hollowed meniscus, in others as a tight membrane. It may represent a very thin diaphragm''. Bouillon (1985) regarded the feature as present in only some species and Calder (1991, p 31) implied the existence of a diaphragm or annular thickening for Hebellinae (his rank), including Halisiphonia.
The inconspicuousness of the diaphragm makes some of the Halisiphonia species superficially resemble stolonal colonies of Lafoea, a genus usually characterized by erect colonies (occasionally stolonal, see Calder 1991, p 36) and gonothecae aggregated into coppinia. Lafoeids with coppinia are included within the subfamilies Lafoeinae A. Agassiz, 1865 and Zygophylacinae Quelch, 1885, although the genus Cryptolarella, with single gonothecae, is exceptionally included among the Eulafoeinae [sic] sensu Bouillon (1985) (cf. Marques et al. 2005). In the past, lafoeids with solitary gonophores were assigned to the subfamily Hebellinae Fraser, 1912. The subfamily Hebellinae has been raised to family level (e.g. Schuchert 2001Schuchert , 2003, and kept separate from the Lafoeidae, a hypothesis corroborated by the presence of medusa buds in the gonothecae of H. arctica (Schuchert 2001); an opinion with which we concur.
In H. arctica, H. galatheae, and H. megalotheca the gonotheca is spatulate, being round or pear-shaped in frontal view, strongly compressed in lateral view, truncated distally, and attached to the hydrorhiza by a short pedicel (see below). However, according to the original description and single record, H. spongicola (Haeckel 1889, p 77, Plate 4, Figure 9) has gonotheca ''not compressed or spatuliform, with a slit-shaped opening; their transverse section and the distal opening are circular''. Nonetheless, the frontal outline of its gonotheca seems similar to those of the other Halisiphonia.

Description of holotype
Colony stolonal, creeping on hydrocaulus of Eudendrium planum. Stolonal hydrorhiza-a network of branching and anastomosing tubes of thin perisarc-giving rise to numerous pedicellate hydrothecae and five gonothecae. Pedicels smooth, with three to six complete basal annuli, 0.36-4.85 mm long, almost cylindrical throughout (0.10-0.13 mm wide where walls are parallel), slightly and progressively widening to base of hydrothecae, merging into it almost imperceptibly. Hydrothecae deep conical to almost cylindrical, 0.67-1.13 mm high (from diaphragm up to distal renovation), 0.11-0.23 mm wide at diaphragm, 0.19-0.38 mm wide at aperture, with straight and smooth walls (sometimes with inconspicuous undulations) and thin perisarc; margin entire, slightly flaring, with up to 13 renovations; aperture perpendicular to long axis of hydrotheca. Diaphragm membranous, transversal; desmocytes small (ca 4 mm in diameter) and inconspicuous, irregularly distributed or forming one or two transversal rows above diaphragm. Hydranths 0.15-0.25 mm high, 0.16-0.22 mm wide at base of tentacles, with 12-16 tentacles, hypostome conical. Retracted hydranths lying over diaphragm. Hydranth regenerations leaving marks outside (margin renovations) and inside the hydrotheca; new diaphragm formed above the preceding one resulting in a fine thickened line around inner side of hydrotheca and corresponding cycles of desmocytes (not always seen); previous diaphragm may disappear. Hydranth base may be marked with several slight constrictions at the place of older diaphragms. Gonothecae spatulate, rounded basally, truncated apically, a narrow transverse slit as superior aperture, arising singly from hydrorhiza on short, annulated pedicels (two to three rings). Pedicel 0.10-0.13 mm high, 0.10-0.13 mm wide. Gonotheca 2.50-3.42 mm high, 1.45-1.73 mm wide at aperture, 0.40-0.53 mm wide at base. Two gonothecae containing medusa buds, clearly seen through the fine and transparent gonothecal perisarc. Each gonotheca with two buds in a row, occupying only a fraction of gonothecal inner space; distal bud larger and more developed, with recognizable tentacles, manubrium, and umbrella. Umbrella twice as high as wide, mesoglea thin; manubrium tubular, reaching about halfway to bell margin. In both gonothecae, buds enclosed by a mantle. Peduncle Table I. Morphometric data of the holotype specimen of Halisiphonia arctica. uniting blastostyle to stem coenosarc broken in both cases. Apparently four tentacles with large bulbs. No nematocysts on the exumbrella or on the mantle. Neither radial canal (at higher magnification, 4006) nor sensorial structures (ocelli, statocysts) seen. Absence of gonads indicating that buds possibly represent immature medusae. Nematocysts of two categories. Heterotrichous microbasic mastigophores (seen discharged), 7.0-8.062.0-3.0 mm, rice grain-shaped, common, ratio shaft/capsule51:1. Heterotrichous ?macrobasic euryteles (not seen discharged), 10.0-12.564.0-5.5 mm, bean-shaped, common.

Remarks
Halisiphonia arctica has not been recorded again since its original description from Greenland. The species was considered similar to H. megalotheca by Schuchert (2001), who notes that the only difference between them is the more elongate hydrotheca of H. arctica.
However, concerning gross morphology, H. arctica is distinguished from its congeners by the combination of two characters: everted margin and annulated pedicels. Halisiphonia megalotheca and H. nana have everted margins but both lack annuli in their pedicels. Halisiphonia arctica differs from H. galatheae, with which it shares the presence of annuli in the pedicel, by having everted hydrothecal margin. Halisiphonia arctica also shows twice (up to 13) as many renovations as H. galatheae (up to six) and H. nana (up to six), although this may be a variable character. The process of hydranth regeneration of H. arctica leaves the scars of the old diaphragms, as described and illustrated by Kramp (1932, p 39, Figures 18-20), a unique feature among the species of the genus.
The medusa of H. arctica was previously reported by Schuchert (2001, p 61) from the holotype, the same material being described here. Besides the presence of medusae suggesting affinities with Hebella (Schuchert 2001), the morphology of the medusa buds of H. arctica, in some aspects (umbrella tall, four tentacles with large bulbs, manubrium cylindrical) comparable to the newly liberated medusae of Hebella scandens (Bale, 1888) and Hebella furax Millard, 1957 (see Andrade andMigotto 1997;Migotto and Andrade 2000, respectively), indicates affinities between Halisiphonia and Hebella. Moreover, once this stage becomes better known, there could be a drastic modification on the classification of Halisiphonia, and the genus might even fall into synonymy with a medusa-based genus.

Distribution
The species is only known for Greenland, at the depth of 1200 m.

Description of holotype
Colony stolonal, with many hydrothecae and two gonothecae arising from hydrorhiza. Hydrorhiza 0.12-0.16 mm wide, forming a sparse network of branching tubes of thin perisarc. Pedicel straight, cylindrical, elongated, 3.96-11.00 mm long, 0.10-0.16 mm wide, smooth but with two to six complete basal annuli; slightly and progressively widening to base of hydrotheca, merging into it almost imperceptibly. Hydrotheca deep conical, 0.70-1.20 mm high (from diaphragm up to distal renovation), 0.16-0.36 mm wide at diaphragm, 0.28-0.80 mm wide at aperture, with straight and smooth walls, and thin perisarc; margin entire, not flaring, with up to six renovations; aperture perpendicular to long axis of hydrotheca. Diaphragm membraneous, transversal, not conspicuous and sometimes lacking; desmocytes not seen. Hydranths not present. Gonothecae spatulate, laterally compressed, rounded basally, truncated apically, with a narrow transverse slit as superior aperture, arising singly from hydrorhiza on short, annulated pedicels. Pedicel 0.40-0.50 mm high, 0.10-0.14 mm wide. Gonotheca 1.80-2.04 mm high, 1.44-1.48 mm wide at aperture, 0.16-0.26 mm wide at base.
Nematocysts of one category, heterotrichous ?microbasic mastigophores (not seen discharged), 9.0-10.062.0-3.0 mm, rice grain-shaped, common. Kramp's (1956) description of H. galatheae is brief, particularly with regard to colony dimensions; the range of variation or average values of important characters are not given. Kramp (1956, p 17-18) did not recognize gonothecae in the holotype and overlooked that the hydrothecal pedicels are annulated at their bases. He reported pedicels much longer (25 mm) than those found by us (11 mm), but the other measurements given by him are within the range of variation we obtained, except the width of the pedicel, which is slightly thinner than the ones we measured. Nonetheless, H. galatheae is a well-characterized species due to the straight hydrothecal margin (not everted) and longer pedicels. Rees and Vervoort (1987, p 34) regarded H. galatheae as conspecific with H. megalotheca, due to the existence of intermediate specimens, regarding the pedicel length, and the similarity of their gonothecae. Contrary to their argument, H. galatheae have much longer and more slender  Figure 17a) and Rees and Vervoort (1987, p 31, Figure 6a, b) are also distinct from H. galatheae in this aspect. On the contrary, H. galatheae assigned by Vervoort (1966, p 122, Figure 24), later considered as H. megalotheca by Rees and Vervoort (1987), agrees well with the holotype of H. galatheae, having comparable long pedicels and straight margins. The type specimens of H. galatheae and H. megalotheca also differ in the presence of annuli on the pedicel and non-flaring hydrothecal rim of the former.
Gonothecae spatulate, laterally compressed, rounded basally, truncated apically, with a narrow transverse slit as superior aperture, arising singly from hydrorhiza on short, smooth pedicels. Pedicel ca 0.20 mm long and 0.18 mm wide at base. Gonotheca 2.38 mm total height (including pedicel), 1.16 mm maximal width, ca 0.90 mm wide at apex, 0.61 mm wide at base.

Remarks
Halisiphonia megalotheca has the largest hydrothecae so far described for the genus (at least twice as long; see Table IV). The two hydrothecae present in the holotype are similar in dimensions with the values given by Allman (1888, p 31; ''hydrothecae measure about one-tenth of an inch in length''; see Table I), but his illustration (Allman 1888, Plate 16, Figure 1) depicts hydrothecae with a greater length/width ratio than those presently found in the holotype. Stechow (1925, p 452) reports the species for the Indian Ocean (38u409S, 77u38.69E, 672 m deep) creeping on Symplectoscyphus paulensis Stechow, 1923 andSertularella valdiviae Stechow, 1923, remarking on its somewhat thinner pedicels and absence of diaphragm, although the place where the hydranth base was attached to the hydrotheca could be determined. The material described by Stechow (1925) presents characteristics intermediate between H. galatheae and H. megalotheca, with hydrothecal length closer to the former and pedicel length closer to the latter. This possibly led Rees and Vervoort (1987, p 31-34, reporting H. megalotheca) to consider H. megalotheca conspecific with H. galatheae. Previous authors (e.g. Vervoort 1966Vervoort , 1972, primarily on the basis of the much longer pedicels of the former, recognized both as separate species. Rees and Vervoort (1987, p 34) justified their decision based on the apparent existence of intermediate specimens, varying from the ''short stalked H. megalotheca'' to the ''long stalked H. galatheae''. Yet, the margin of the hydrotheca of H. galatheae is straight while that of H. megalotheca is everted, although only slightly. Also, we could confirm that Kramp (1956) did not notice that the pedicels of H. galatheae are annulated basally (see above), contrasting with those of H. megalotheca that are completely smooth. As the specimens studied by Vervoort (1972) and Rees and Vervoort (1987) include hydrothecae with both straight and everted margins, but without annulated pedicels, we do not regard them as conspecific with H. galatheae, although some of them could be assigned to H. megalotheca. This species was originally described based on few hydrothecae only, certainly not representing the range of variation of morphometrical characters possibly exhibited by the species. The material identified by Vervoort (1966) as H. galatheae, but later considered conspecific with H. megalotheca by Rees and Vervoort (1987), has straight walls and long pedicels (up to 15 mm long) with ''some indistinct rings or wrinkles'' (Vervoort 1966, p 121). Vervoort's (1966, Figure 22) illustration and description of the gonotheca of H. galatheae appear to be similar in shape and size to those we found in the holotype of the species, suggesting his identification was possibly correct (see above).

Material examined
Holotype: Halisiphonia nana Stechow, 1921; colony with many hydrothecae and without gonothecae in four slides and alcohol (ZSM no number).

Description of holotype
Colony stolonal, with hydrorhiza creeping on spicules of sponges and other material aggregated on a polychaete tube, and on hydrorhiza and hydrocaulus of Eudendrium antarcticum Stechow, 1921. Hydrorhiza smooth, 0.037-0.075 mm in diameter. Pedicel smooth, with thin perisarc, without annulations (usually with a constriction at base), 0.040-0.062 mm wide at base, slightly and progressively widening to base of hydrothecae, merging into it almost imperceptibly. Base of hydrothecae either with or without a thin, almost undetectable membranous diaphragm; few desmocytes present above diaphragm in some hydrothecae. Distance between hydrorhiza and diaphragm 0.195-0.462 mm. Hydrotheca almost cylindrical, slightly widening towards aperture, 0.352-0.750 mm long, with thin perisarc and smooth walls; margin entire, slightly flaring, with up to six renovations (though usually without renovations); aperture round, 0.107-0.162 mm in diameter. Hydrotheca usually slightly curved to one side; aperture perpendicular or slightly inclined to concave side. Without operculum and nematothecae. Hydranth with about 10 filiform tentacles in one whorl; tentacles with rings of nematocysts; hypostome domeshaped. Gonotheca not present. Nematocysts apparently of one category, rice grain-shaped, on tentacles (6-762.0 mm).

Remarks
Halisiphonia nana was redescribed by Stechow (1925) on the same original material, asserting the absence of a diaphragm. Nevertheless, in the holotype of H. nana, which includes plenty of material with well-preserved hydrothecae and hydranths, we found hydrothecae with diaphragm clearly recognizable as a very thin, transversal membrane at the base of the hydrotheca, although it was indistinct or even absent in some. The diaphragm is better seen at its insertion with the hydrothecal wall. Millard (1977, p 14) doubtfully assigned material from off Crozet Island (Indian Ocean) to the species. We agree with Rees and Vervoort (1987, p 31-34) in considering Millard's record dubious. Besides the absence of ''diaphragm or annular thecal thickening'', the specimens described by Millard (1977) are larger, with the diameter of the hydrothecae at the margin twice as wide (0.14-0.23 diameter at margin) as H. nana (see above and Table IV). The general dimensions, the everted hydrothecal margin, and the absence of a diaphragm indicate that Millard's specimens are possibly part of a stolonal, young colony of Lafoea. The absence of gonophores, however, hinders any better conclusion. Blanco (1984) recorded the species from off South Georgia (54u089S, 36u029W, 180 m deep) and also remarked on the absence of a diaphragm or thecal thickening, though her drawing suggests, at least, the presence of desmocytes marking the base of the hydrotheca.
Type specimen Rees and Vervoort (1987) made no remarks on the type series of the species. The material is not in the museum collections that we consulted and in which it could have been deposited. We believe the type material is lost.