ANATOMY AND TAXONOMIC POSITION OF ELMA H. ADAMS, 1866: A HIGH-SPIRED SOUTHEAST-ASIAN GENUS OF STREPTAXIDAE

This paper describes the reproductive anatomy and the radula morphology of a Taiwanese species of Elma H. Adams, 1886, providing the first information on the anatomy of the genus. The species is provisionally identified as the type species of Elma, E. cf. swinhoei (H. Adams, 1866). Based on this and contrary to previous systematics, we suggest that Elma belongs to the subfamily Streptaxinae or Gibbinae, based on the presence of a well-developed penial sheath and the vas deferens which forms a loop under the penial sheath. Elma is the first high-spired, Southeast-Asian genus to be thus classified. We discuss possible relationships with other Streptaxoidea including the Elma-like genus Pseudelma Kobelt, 1904 and the highspired “Ennea” aliena Bavay et Dautzenberg, 1912.


INTRODUCTION
The Streptaxidae Gray, 1860 are carnivorous land snails which are widely distributed in the tropics (ZilcH 1960).ZilcH (1960) subdivided the family into Streptaxinae and Enneinae.scHileyKo (2000: 771) criticised Zilch's system, because the characters of the taxa overlapped between the two subfamilies, and classified the streptaxid genera into six subfamilies, partly based on the genital characters, especially the male part.The six subfamilies were Streptaxinae, Gibbinae Steenberg, 1936, Enneinae Bourguignat, 1883, Ptychotrematinae Pilsbry, 1919, Marconiinae Schileyko, 2000and Odontartemoninae Schileyko, 2000. Later, based 2010) published the results of an extensive molecular study primarily focusing on taxa from East Africa and the islands of the Indian Ocean and showed that the previously recognised subfamilies in the Streptaxidae were polyphyletic.
The genus Elma, introduced by adams (1886), was included in the Enneinae by both ZilcH (1960) and scHileyKo (2000), although its anatomy was unknown.Approximately ten species of Elma are known; they inhabit Taiwan, Northern Vietnam and mainland China (VarGa 2012).Their shells are high-spired, relatively large (7-24.5 mm), nearly smooth or regularly ribbed, with a pear-shaped, elongated, toothless aperture which has its upper mar-gin curved backwards.During a recent field trip to Taiwan, one of the authors (a.Hunyadi) collected a live specimen of Elma cf.swinhoei (H.Adams, 1866).Though only provisionally identified, the specimen is evidently very similar to E. swinhoei, the type species of the genus.The aim of this paper is to describe the anatomy, and to discuss the taxonomic position of the genus based on this information.

MATERIAL AND METHODS
Dissection of a single specimen was performed in ethanol under a Leica stereomicroscope, with a camera attached to provide photographs of the genital structures from which drawings were then produced.To describe the reproductive system, we used the terms "proximal" and "distal" in relation to the interior of the body.The buccal mass was removed and soaked in 2 molar KOH solution for 5 hours before extracting the radula which was preserved in 70% ethanol.The radula was directly examined without coating in a low vacuum SEM (Miniscope TM-1000, Hitachi High-Technologies, Tokyo).

ANATOMY
Genitalia (Figs 2-7): Atrium short; internally with numerous blunt papillae which became larger to-wards the vagina.Penis long, slender and cylindrical, nearly equally thick throughout; there is a very slight caecum-like thickening near the distal end, without any differentiation on the inner wall.Inner wall of penis with scattered papillae, with brown penial hooks in each papilla, except for some papillae in the apical (proximal) part.Hooks largest in the middle portion of penis and somewhat smaller towards the atrium and vas deferens.Hooks with sharp tips curved towards the atrium.Penial sheath present, covering approximately half of penis; end of penial sheath doubled back on itself with a very slender retractor muscle attaching to the atrium.No epiphallic differentiation observed.Vas deferens enters proximal end of penis slightly laterally (at an angle of ca.45°) after forming a loop under the penial sheath, with one side of the loop attached to the inner surface of sheath; loop ending approximately at the middle of penial sheath.Diameter of vas deferens is somewhat greater between the spermoviduct and the penial sheath than between the penis and the penial sheath.Penial retractor muscle long, inserting at the penis-vas deferens junction and attached to the diaphragm.Vagina very short, stout.Bursa copulatrix duct long, slender, with somewhat thickened reservoir, reaching the albumen gland.Free oviduct relatively long, thicker than penis; inner wall of the vagina and the free oviduct with elevated, conspicuous folds which converge towards the atrium; oviduct enlarged and folded.Talon small, thickened and curved.Pallial complex and salivary gland: Pallial complex typically streptaxid, similar to that of Discartemon Lateral and marginal teeth undifferentiated, unicuspid and lanceolate, some even mucronate; anterior laterals with much less pointed cusps; laterals gradually decreasing in length and size, outer laterals much smaller and shorter than the inner laterals.

SYSTEMATICS OF THE GENUS ELMA
The taxonomy of Taiwanese Elma needs revision.Altogether three species or subspecies have been reported from the island (Fig. 10), namely Elma swinhoei (type locality: "Tamsui"), E. swinhoei hotawana (Pilsbry et Hirase, 1905) (type locality: "Hotawa"), and Elma oblongata Yen, 1939 (type locality: "Lungso-tan, Kwangtung", China, see: yen 1939) (PilsBry & Hirase 1905, lee & cHen 2003, Hemmen & niederHöfer 2007).Examination of the types of the taxa described from Taiwan, and a number of specimens recently collected by a. Hunyadi and by K. oKuBo, suggests there is a range of variation with larger and more acute forms present in the south and east (Fig. 10, Appendix 1).No anatomical information was previously available on any of these taxa.Indeed, only one live adult was found, so live indi-Fig.1.Shell of the anatomically examined specimen of Elma cf.swinhoei (H.Adams, 1866).Scale bar 5 mm viduals may be scarce as seems to be the case with some other streptaxid genera (e.g.siriBoon et al. 2014).The anatomically examined specimen (Fig. 1) was provisionally identified as E. cf.swinhoei because it was collected approximately 37 km east of the type locality of E. swinhoei.However it was similar to the holotype of E. swinhoei hotawana, collected ca.250 km to the south (Fig. 10).We note that a revision is required and that shape variation in Taiwanese Elma could in some cases be continuous.

ATTRIBUTION OF ELMA TO STREPTAXID SUBFAMILY
The description of the anatomy of Elma makes it possible to discuss its relationship to other  Indoennea Kobelt, 1904, which is conchologically similar to Sinoennea, may also prove to belong to the Diapheridae once its anatomy is known, as may some other small-shelled genera.
Secondly, Elma has a well-developed penial sheath, and a vas deferens which forms a loop between the penis and the penial sheath (Fig. 3).The striking presence or absence of these features was considered important by scHileyKo (2000) for his subfamily classification.Indeed, the sheath is present throughout some of the major clades revealed in the molecular analysis of rowson et al. ( 2010) and absent throughout others.The additional presence of a loop formed by the vas deferens, however, cannot alone be used to distinguish subfamilies.For example, in the genus in the Ptychotrematinae.None of the other anatomically known genera in the Ptychotrematinae sensu Schileyko has a sheath.In addition, the small talon (Fig. 4) and the uniform penial hooks (Figs 6-7) of Elma contrast with the large talon and the differentiated hooks seen in some of these genera.Overall, we conclude that Elma is probably not a member of Ptychotrematinae sensu Schileyko, 2000.
In fact the presence of penial sheath and loop of the vas deferens is sufficient to classify Elma into another of the subfamilies used by scHileyKo (2000): Streptaxinae or Gibbinae.In scHileyKo's (2000) system, the main difference between the Streptaxinae and the Gibbinae is that the vas deferens does not pass under the penial sheath in the former, but does in the latter.According to rowson et al. ( 2010) species of the genera Indoartemon Forcart, 1946,  If correct, the name Gibbinae could be applied to this clade, and in turn Elma could be considered to belong in the Gibbinae.The slight reduction in diameter of the vas deferens would also support the placement in the Gibbinae according to scHileyKo (2000).This would be biogeographically notable, since the Asian Elma could be descended from the same lineage that gave rise to this Indian Ocean radiation.However, the fact that scHileyKo (2000) placed Stereostele in the Streptaxinae and Gonospira in the Gibbinae emphasises the problem of accurate classification of these genera at the subfamily level.This is partly a consequence of the great variation in shell morphology in such clades, and the occurrence of multiple clades in some biogeographical regions.The genus Pseudelma Kobelt, 1904 was introduced for shells en-  (2000).Elma, however, has a well-developed penial sheath, lacks a penial caecum, and has a small talon.Consequently, Elma and Pseudelma belong in different subfamilies according to scHileyKo's (2000) anatomical criteria, and probably even the opposite subfamily to that in which they were classified.Their strikingly similar shells can better be explained either by parallel evolution, or as ancestral character states pre-dating the origin of their respective subfamilies.
In summary, we conclude that Elma probably belongs neither to the Enneinae nor to the Ptychotrematinae, but should instead be included in either the Streptaxinae or the Gibbinae.Elma is the first high-spired Southeast-Asian streptaxid to be classified in one of these two groups.It is also unrelated to either the Asian Diapheridae or to the Comoros Pseudelma, although a link to the other Indian Ocean genera in the Gibbinae is not ruled out.
Finally, one other high-spired Southeast-Asian streptaxid deserves a mention.Ennea aliena Bavay et Dautzenberg, 1912 (Fig. 11) from Tonkin, Vietnam is striking in its (relatively) large shell size, shape and dentition.It was tentatively classified in Indoennea by scHileyKo (2011: 26, with a question mark)."Ennea" aliena certainly does not belong to Ennea, and differs from Indoennea species in the straight aperture and the absence of a columellar lamella.As we suggest above, Indoennea may actually belong in the Diapheridae based on such features.Therefore on a conchological basis, "Ennea" aliena seems to be more closely related to Elma than to Indoennea, and may even deserve its own genus.Since Elma is shown to belong to the Streptaxinae or the Gibbinae, we hypothesise that "Ennea" aliena might belong to the same subfamily.This could be tested by obtaining data on its anatomy.

ACKNOWLEDGEMENTS
Comments by luis r. l. simone and two anonymous referees helped improve the manuscript.We are grateful to Kanji oKuBo for loaning us Taiwanese Elma shells.We are indebted to The Biodiversity Heritage Library for the multitude of rare literature made available to us (http://www.biodiversitylibrary. org/).1912, NMW.1955.158.25364 .158.25364 on molecular and anatomical evidence, sutcHarit et al. (2010) introduced the family Diapheridae Panha et Naggs, 2010 to accommodate Diaphera Albers, 1850 and Sinoennea Kobelt, 1904.With this, Diapheridae and Streptaxidae formed the superfamily Streptaxoidea Gray, 1860.All genera not classified in the Diapheridae, including those with unknown anatomy, remained in the family Streptaxidae.rowson et al. ( (see: siriBoon et al. 2014) and Huttonella (see: simone 2013), about 1.5 whorls long, sigmure-throus, with kidney sub-rectangular.Salivary gland single, soft, with two ducts leaving separately (rather than together as in Huttonella; simone 2013), each duct of even thickness throughout its length.Radula (Figs 8-9): Teeth arranged in anteriorly V-shaped rows, each row containing at least 20 teeth.Central tooth sharp, triangular with pointed cusp, approximately half the size of the first laterals.
Streptaxoidea, with a particular emphasis on its subfamily position.Elma was placed in the Enneinae by both ZilcH (1960) and scHileyKo (2000), initially based on the high-spired shell, although scHileyKo (2000) also used the genital anatomy (from other genera) in his classification.Due to the absence of anatomical data in ZilcH (1960), and the evident oversimplification of his classification, we do not further discuss the Enneinae and Streptaxinae sensu ZilcH (1960), but only in the senses of later authors.Firstly, Elma has penial hooks, confirming its placement in the Streptaxidae rather than the Diapheridae (sutcHarit et al. 2010) where most high-spired Asian Streptaxoidea (i.e.Diaphera and Sinoennea) belong.Incidentally, we hypothesise that

Fig. 2 .
Fig. 2. Genital anatomy of Elma cf.swinhoei (H.Adams, 1866): A -atrium, AG -albumen gland, BC -bursa copulatrix, P1 -part of penis covered by penial sheath, P2 -part of penis not covered by sheath, RMP -retractor muscle of penis, RMS -retractor muscle of penial sheath, SO -spermoviduct, T -talon, V -vagina, VD -vas deferens.Scale bar 1 mm Carinartemis Siriboon et Panha, 2014, one species has a loop-forming vas deferens, but the other does not (siriBoon et al. 2014).It is also possible that the presence of a loop (although not the presence of a sheath) might vary with the maturity of the animal.The presence of penial sheath makes Elma highly dissimilar to the African Ennea H. Adams et A. Adams, 1855 (as illustrated by deGner (1934) and scHileyKo (2000)).In Enneinae sensu Schileyko the only taxa with a penial sheath are the African Raffraya Bourguignat, 1883 and the Madagascan Makrokonche Emberton, 1994, both ranked by scHileyKo (2000) as subgenera of the African Streptostele Dohrn, 1866.Like Elma, these genera have high-spired, tapering, edentate shells.Ennea has a pupiform, dentate shell, and since PilsBry (1919) it has often been considered a subgenus of the African Ptychotrema L. Pfeiffer, 1853 (to which it may well be related; rowson et al. 2010).However, scHileyKo's (2000) Enneinae are evidently polyphyletic, e.g.including both streptaxid and diapherid taxa (rowson et al. 2010, sutcHarit et al. 2010).To be useful it should arguably be restricted to close relatives of Ennea.The molecular evidence suggests that there are other species and subgenera of Ptychotrema, none of which have a penial sheath.Raffraya does not appear to be related, while Makrokonche has yet to be sequenced (rowson et al. 2010).As a result, we do not think that Elma should be classified in either the Enneinae or the Ptychotrematinae.Incidentally, a close relationship between Ennea and Ptychotrema would call into question the usefulness of the subfamily name Ptychotrematinae, used by scHileyKo (2000) to place the two genera in different subfamilies.Likewise, the same features show that Elma is dissimilar to the genus Huttonella L. Pfeiffer, 1856.Despite being introduced nearly circumtropically, Huttonella is probably originally Asian (e.g.simone 2013).The molecular data of rowson et al. (2010) show Huttonella to be closely related to the African genus Gulella L. Pfeiffer, 1856 and to the Mauritian Maurennea Schileyko, 2000.All three genera lack penial sheath and are classified by scHileyKo (2000)

Figs 5- 9 .
Figs 5-9.Elma cf.swinhoei (H.Adams, 1866): 5 -inner wall of vagina, 6-7 -inner wall of penis, 8-9 -radula.Scale bars for Figs 5-7 500 μm demic to Mayotte Island (Comoros Islands; between Madagascar and Africa), the name reflecting a strong conchological similarity to Elma.Pseudelma was classified in the Enneinae by ZilcH (1960) along with Elma, whereas scHileyKo (2000) placed Pseudelma in the Gibbinae.Neither author had anatomical information on Pseudelma.aBdou et al. (2008) revised Pseudelma and described the anatomy of several species.Based on the absence of penial sheath, the presence of a short penial caecum, the large talon and the uniform, undifferentiated, small hooks in the penis, they transferred Pseudelma into the Enneinae sensu scHileyKo