Helicina variabilis Wagner, 1827

Simone, Luiz Ricardo L., 2018, Phenotypic features of Helicina variabilis (Gastropoda: Neritimorpha) from Minas Gerais, Brazil, Papéis Avulsos de Zoologia (Pap. Avulsos Zool., S. Paulo) 58, pp. 1-9 : 2-4

Helicina variabilis Wagner, 1827

( Figs. 1‑35 )

Helicina variabilis Wagner, 1827: 25 (pl. 16, figs. 3-5) [see authority designation in Cowie et al., 2004]; Wagner, 1906: 226 (pl. 13, figs. 2a-c.); Salgado & Coelho, 2003: 152 (pl. 1, fig. 1); Simone, 2006: 41 (fig. 32); Simone & Salvador, 2016: 10, 11, 29 (figs. 84-89).

Type locality: Pará state, Brazil.

Material analyzed: BRAZIL. Minas Gerais: Nanuque : MZSP 106171 (1 specimen), 106172 (4 specimens), 106173 (1 shell). Bahia: NE Ilhéus ; MZSP 128202 (~2000 shells) (Femorale team col. xii/1994) .

Description

Shell ( Figs. 1‑10 ): diameter ~ 12 mm, lenticular; diameter ~5/4 shell length. Base color white, with broad spiral band running along median upper portion of whorls; varying in thickness, sometimes covering all of upper portion of whorls, and changing from orange to light brown or reddish purple; second, narrow colored band (of same color as other band and also varying in thickness, although less so) sometimes present on lower surface of whorls, closer to median portion. Both bands stopping few millimeters before reaching peristome. Peristome white. Spire angle ~90°. Protoconch of 1.5 whorls, acuminate, first 0.75 whorl smooth, rest sculptured by axial parallel sinuous striae; transition to teleoconch distinct. Teleoconch sculptured with weak axial parallel sinuous striae and with stronger spiral parallel striae.Whorl profiles slightly convex. Suture well marked. Very weak carina on body whorl.Aperture medium-sized, prosocline, triangular, about as broad as high; ~2/3 shell length, ~3/5 shell width. Peristome reflected, with shallow furrow on median upper portion (following colored band) and slight angle at junction of basal and columellar regions. Body whorl ~3/4 shell length. Umbilicus imperforate. Internal visceral cavity ample, separated from head-foot cavity by thin septum ( Figs. 9-10 ); occupying ~2/3 of shell volume; intra-sutural fold (vestigial internal coiling) low, but visible ( Fig. 10 ).

Head‑foot ( Figs. 8 , 30‑22 ): Color of exposed regions brown; snout pale beige ( Fig. 8 ). Length ~3/4 whorl when retracted. Head protruded, occupying ~1/ 2 foot width. Tentacles stubby, simple, ca. four times longer than wide; tip blunt ( Figs. 20, 26 : te). Ommatophore (om) ~1/3 tentacle length, tip rounded; located close to outer side of tentacle base. Eye (ey) located on ommatophore tip. Foot simple, thick, subtriangular ( Figs. 20-22 : ft); anterior edge bilabiate, aperture of pedal glands median, relatively deep ( Fig. 20 : pg). Distance between anterior edge of foot and snout base ~1/10 whorl. Both columellar muscles diverging towards posterior portion of body, very thick, gradually tapering posteriorly; originating from both sides of pseudo-columellar region; left columellar muscle ( Figs. 20-21 : cr) ~3/4 shorter and more inclined than right columellar muscle (cl). Opercular pad simple ( Fig. 22 : oa), slightly elliptical. Haemocoel ca. three times longer than wide, slightly narrowing posteriorly; occupying ~1/3 of headfoot volume ( Fig. 24 ).

Operculum ( Figs. 11‑13 ): Hard, translucent, occupying entire aperture. Extending ~20% beyond lateral sides of foot ( Fig. 21 : op). Color pale brown, scantly calcified; relatively thin ( Fig. 13 ). Nucleus barely visible, located in middle of inferior half ( Fig. 11 ). Outer surface smooth, weakly undulating concentrically. Edges somewhat flexiclaudent. Inner surface smooth, glossy; scar elliptical, close to inner margin, occupying ~40% of inner surface ( Fig. 12 ).

Pallial cavity ( Figs. 23‑25 ): Length ~1/2 whorl ( Fig. 14 ), relatively narrow. Mantle border thin, bifolded ( Fig. 23 : mb). Lung venation relatively weak and barely visible ( Fig. 23 : pu), except for collar vessel running parallel to mantle border, and large pulmonary vein (cv) running along left edge of cavity to pericardium. No vestige of gill or osphradium. Rectum and gonoducts occupying ~1/3 of right pallial volume, along its entire length ( Fig. 23 : rt, ov). Anus located close to right side of mantle border (an). Adrectal sinus ( Figs. 23, 25 : ar) narrow, running parallel to left side of rectum, inserting in anterior corner of kidney.

Visceral mass ( Figs. 14 , 25 ): Single compact discoid mass as inner mold of visceral cavity of shell (vm) ( Figs. 9-10 ). Gonad (go) occupying ~70% of inner visceral volume, granular, cream-colored. Stomach and digestive gland occupying remaining ~30% of visceral volume, located anteriorly and ventrally. Diaphragm muscle narrow ( Figs. 14 , 25, 26 : dm), originating from small area close to origin of left columellar muscle; running ventrally and posteriorly flanking ventral surface of visceral mass; tapering to its insertion in posterior region of pallial cavity floor.

Reno‑pericardial system ( Fig. 25 ): Located as anterior structures of visceral mass ( Fig. 23 : pc), both combined occupying ~15% of visceral volume. Kidney narrow, oblique, mostly hollow (ki); occupying ~1/3 of reno-pericardial volume. Renal lobe on anterior surface (kl), small, as pair of parallel glandular folds bearing successive transverse folds. Nephrostome (ne) as simple, transverse slit located in posterior right corner of pallial cavity. Pericardium simple (pc), located on posterior region of pallial roof. Auricle (au) wide, thin-walled, situated anterior-right; with connections with pulmonary vein (cv) anterior-left, with kidney middle-right, and also posteriorly. Ventricle (ve) smaller and thicker-walled, turned to left and slightly posterior. Posterior aorta very small, splaying in visceral mass. Anterior aorta four to five times wider than posterior aorta, running anteriorly along haemocoel to buccal mass ( Figs. 27-28 : aa).

Digestive system ( Figs. 24‑31 ): Mouth subtriangular, located at median level of posterior region of snout central surface ( Fig. 24 : mo). Oral tube short, thin-walled ( Fig. 27 : mo); no jaw plates detectable, muscular wall relatively thin ( Fig. 28 : mj). Buccal mass occupying ~1/3 of haemocoel volume ( Fig. 24 ); odontophore (od) ventral, almost entirely surrounded by esophageal crop ( Figs. 24 , 27, 28 : ec), except for its posterior surface. Esophageal crop (ec) simple, inner surface smooth, velvet-like. Pair of esophageal pouches ( Figs. 24 , 27, 28 : ep) as elongated diverticula, almost as long as buccal mass; right pouch ca. three times longer than wide; left pouch ca. four times longer than wide ( Fig. 28 : ep); posterior end rounded; running parallel to esophagus; inner surface simple, similar to esophageal crop. Anterior aorta inserting in region between odontophore and esophageal origin ( Fig. 28 : aa). Odontophore ca. twice longer than wide, occupying ~1/2 of buccal mass volume.

Odontophore muscles ( Figs. 29‑31 ): m1, several small pairs of jugal muscles connecting structures of haemocoel with adjacent inner surface of haemocoel, more concentrated close to oral tube; m2, pair of retractor muscles of buccal mass, originating from inner lateral surface of haemocoel, just posterior to snout, running short distance towards anterior and medial, inserting in latero-ventral edge of anterior cartilages, between their middle and anterior thirds ( Fig. 30 : m2); m3, two pairs of dorsal protractor muscles of odontophore, originating from antero-ventral surface of esophageal crop, running posterior-ventrally, inserting in anterior-ventral edge of posterior cartilages ( Fig. 31 : m3); m4, pair of thick dorsal tensor muscles of radula; originating from surrounding posterior and lateral edges of posterior cartilages (po) and postero-ventral edge of anterior cartilages (oc) ( Fig. 30 : m4), running short distance, narrowing, inserting along radular sac on posterior half of odontophore ( Fig. 30 : ir); m5, auxiliary dorsal tensor muscle of radula absent or indistinct, as part of m4; m6, horizontal muscle connecting both anterior odontophore cartilages (oc) with each other, along ~2/3 of their ventro-medial edge ( Figs. 30-31 : m6), initiating ~1/10 of anterior cartilage length posterior to their anterior end; m8, pair of approximator muscles of cartilages, connecting anterior surface of posterior cartilages (po) with ventro-posterior surfaces of anterior cartilages (oc) ( Fig. 31 : m8), relatively thick, covering ~1/2 of anterior cartilages outer surface; m10, pair of wide ventral protractor muscles of odontophore, originating from ventral region of snout close to buccal tube origin, running along almost entire odontophore length, covering its ventro-lateral surface ( Fig. 29 : m10), inserting in latero-ventral edge of posterior cartilages ( Figs. 29, 31 : m10), close to m3 insertions; m11, pair of narrow ventral tensor muscles of radula,originating from median edge of posterior cartilages, running anteriorly close to median line, flanking ventral edge of anterior cartilages ( Fig. 31 : m11), inserting in terminal edge of radular ribbon. Non-muscular odontophore structures: oc, pair of anterior odontophore cartilages, each one ca. four times longer than wide, slightly flattened, anterior tip bluntly pointed, weakly curved inwards, posterior edge almost straight, articulating with posterior cartilages ( Fig. 30 : oc); po, pair of posterior odontophore cartilages, subspherical, slightly flattened, located just posterior to anterior cartilages,~1/5 their length; sc, subradular cartilage, thin, transparent, running along entire ventral surface of radular ribbon (connecting radular teeth), expanding ca. twice radular ribbon width in oral cavity ( Fig. 28 : sc), protecting subradular membrane.

Radular teeth ( Figs. 15‑19 ): rachidian tooth slightly longer than wide, occupying ~1/10 of radula width, cutting edge strongly curved inwards, slightly wider than base, composed of transverse secondary folds, no cusps; four pairs of lateral teeth ( Figs. 16, 18 ), pair of inner lateral teeth sigmoid, ca. three times narrower than rachidian, pair of small terminal cusps on tip, sometimes 1-2 more cusps along internal edge, turned outwards; pair of second lateral teeth similar to inner lateral, but ca. twice wider,with 5-7 small cusps on cutting edge, medial cusps slightly smaller than lateral cusps; pair of third lateral teeth similar to inner lateral, but positioned turned inwards; pair of outer lateral teeth large, each occupying ~20% of radular width, tooth base wide, triangular, ca. twice rachidian length and width, outer edge reinforced, thicker at base, terminal rod also triangular and turned inwards, but narrower than base, 10-12 cusps on outer edge, turned inwards, middle cusps slightly larg- er than terminal cusps; lateral teeth forming chevron, second and third teeth lying at midlevel of two successive rachidians; ca. 50 pairs of marginal teeth arranged obliquely as continuation of outer lateral tooth; all marginal teeth similarly shaped, but gradually decreasing in size laterally. More internal marginal teeth ~10 times longer than wide, base flattened, tip curved inwards, with 4 terminal cusps, middle cusps larger than distal and proximal cusps ( Figs. 17, 18 ); 3-4 pairs of more marginal teeth differently shaped than remaining more medial marginal teeth, claviform, flattened, tip rounded, simple, lacking cusps ( Figs. 18, 19 ).

Esophagus simple, relatively wide; inner surface smooth, lacking folds ( Figs. 27-28 : es); running along ~1/2 whorl to stomach insertion ( Fig. 26 : es). Stomach as wide blind sac, located in central region of visceral sac, occupying ~1/5 visceral sac volume ( Fig. 26 : st); inner surface simple, lacking special folds or sorting areas, pair of ducts to digestive gland ( Fig. 26 : dd) located close to each other, in anterior region of esophageal insertion in stomach. Border between stomach and intestine indistinct. Intestine formed by gradual narrowing of stomach, with two loops ( Fig. 26 : in), anterior loop into haemocoel, reaching left-posterior region of buccal mass ( Fig. 26 ); next,loop running along ventral visceral surface,crossing kidney, reaching pallial cavity as rectum ( Fig. 23 : in, rt). Rectum relatively wide (~1/5 of pallial-cavity width), running along right side of pallial cavity. Anus wide, located close to right side of mantle border ( Figs. 23 , 35 : an).

Genital system: Male: No males examined. Female ( Figs. 23, 24‑35 ): Ovary described above ( Fig. 14 : go).

Visceral oviduct (vo) very narrow,running along columellar surface of visceral mass to right side of posterior pallial cavity end ( Figs. 23, 25 : vo). Pallial oviduct (ov) wide, almost as long as pallial cavity; running along pallial cavity right side, covering rectum ventrally ( Fig. 23 : ov). Posterior region of pallial oviduct as abrupt expansion of visceral oviduct ( Figs. 23 , 34 ), performing short zigzag (~1/8 of entire pallial-oviduct length), albumen gland (ag) as initial paler region. Seminal receptacle absent. Bursa copulatrix ( Fig. 34 : bc) as three branched diverticula, located in postero-ventral region of albumen gland; its duct placed anteriorly, between albumen and capsule glands. Posterior oviduct diverticulum ( Fig. 34 : dv) simple, located in opposed side from bursa, filled by gland. Capsule gland (cg) occupying most of pallial oviduct, walls thick, glandular ( Figs. 34, 35 : cg), pale beige, somewhat convolute ( Fig. 23 : ov). Genital atrium short, located just anterior to capsule gland. Female aperture as elongated, simple papilla ( Fig. 35 : fp), preceded by thin walls; papilla located inside wide anal aperture ( Figs. 23 , 35 ).

Central nervous system ( Figs. 32, 33 ): Nerve ring located in ventral region of snout base, occupying ~1/20 of haemocoel volume ( Fig. 24 : nr), surrounding oral tube close to its posterior region ( Fig. 27 : nr). Pair of cerebral ganglia (ce), each ganglion occupying ~20% of nervering volume, relatively spherical; cerebral commissure slightly longer than each ganglion length. Pair of pedal ganglia(gp)about as large as cerebral ganglia,very closely connected with each other; each ganglion subspherical, tapering to large anterior pedal nerve. Statocyst (cy) ~1/5 pedal ganglion volume, bearing several statoconia; located on ventral side of middle region of each pedal ganglion. Pair of pleural ganglia (pl) located close to pedal ganglia, ~1/2 of their size; both widely connected on median side. Cerebro-pleural and cerebro-pedal connectives relatively symmetrical, about as long as cerebral commissure; right pair somewhat more widely separated from each other than left pair.

Mean measurements (in mm; n = 6): 4.5 to 5 whorls; H = 9.7 ± 0.7 (max 10.7; min 8.7); D = 12.4 ± 0.6 (max 13.2; min 11.6); S = 4.0 ± 0.6 (max 4.5; min 3.1); S’ = 2.3 ± 0.3 (max 2.9; min 2.0); h = 7.1 ± 0.4 (max 7.7; min 6.7); d = 7.3 ± 0.4 (max 7.9; min 6.7).

Figures

Figures 1-19. Helicina variabilis. (1-14) phenotypic features; (1) specimen #1 (MZSP 106171; D = 12.9 mm), frontal view. (2) same,lateral view. (3) same, apical view.(4)same,umbilicalview.(5)specimen#2(MZSP106172;D=12.5mm),frontalview.(6)same,apicalview.(7) same,umbilicalview.(8)livingspecimen(MZSP 106172) (D = 11.8 mm).(9) shell,dorsal view,withpart of shell wall removedin order to expose visceralcavity.(10) same,oblique umbilical view.(11) operculum, outer view(width = 5.8mm).(12) same,inner view.(13)same,lateral view.(14)specimen removed fromshell,mostly frontalview,pallial cavity partially removed and deflected downwards (scale = 2 mm). (15-19) radulae in SEM,arrow showing rachidian column;(15) wide view (scale = 100 µm).(16) detail of central region (scale= 50 µm).(17) detail of marginal region (scale = 50 µm). (18) central and marginal region (scale = 50µm). (19) detail of marginal region (scale = 50 µm).

Figures 20-26. Helicina variabilis.anatomy;(20) head-foot,anterior view.(21) same,posterior view.(22) detail of posterior region of foot,dorsal view.(23) pallial cavity roof and adjacent region of visceral mass and head-foot, ventral-inner view, artificially sectioned in middle of mantle border. (24) head and haemocoel, ventral view,foot and columellarmuscles removed.(25)posterior end of pallial cavity and adjacent region of visceral mass,ventral view,ventral wall of pericardium removed.(26)digestive tubes as in situ,left view,topology of some adjacent structures also shown.Scales = 2 mm.

Figures 27-33.Helicinavariabilis.anatomy;(27) foregut,left view,topology of nerve ring also shown.(28) same,ventral view,odontophore partially removed and deflected.(29) odontophore, left view. (30) same, dorsal view,superficial layer of membrane and muscles removed,both anterior cartilages deflected. (31) same, ventral view,part of right extrinsicmuscles removed.(32) nerve ring,ventral view.(33) same,dorsal view.Scales = 1 mm.

Figures 34-35.Helicinavariabilis,portionsof pallial oviduct,ventral view;(34)detail of posteriorregion.(35)detail of anteriorregion,anusedgeartificially opened longitudinally.Scales = 1 mm. Ampullariidae (basal Caenogastropoda) (Simone, 2004, and loss of the right kidney. All features were confirmed as gastric muscle), another air-breathing group. in the species studied here. With respect to the odontophore, H. variabilis, as well The monotocardian condition of the Helicinidae, as other helicinids (Bourne, 1911:figs. 5-7), has some sim- i.e., a single auricle in the heart, has been an interesting ilarity with that of the neritid N.zebra (Barroso et al., 2012: enigma (Little, 1972), as this character is shared with the figs. 25-29), with an inner arrangement in two pairs of higher gastropods. The basal neritimorphs, despite havcartilages, one anterior and one posterior. However, the ing lost the right pallial structures, still retain the left auhelicinids so far known have the horizontal muscle (m6) ricle (Estabrooks et al., 1999; Barroso et al., 2012). Taking single, not divided into two components (Figs. 30, 31). into consideration the information provided by Simone The pair of odontophore protractors (m10) is inserted (2011), the monotocardian condition of the helicinids far posteriorly (Fig. 29) in both species, separating them is a remarkable convergence with the apogastropods from related taxa (Simone,2011); however,that of H. vari‑ (sensu Simone, 2011), also known as Monotocardia. abilis is longer and slender. The pair of retractor odonto- However, a different situation was found by Uribe et al. phore muscles (Figs. 29, 30: m2) is simple in H. variabi‑ (2016), using a molecular approach, in that the marine lis, but is highly branched in N. zebra (“ml” Barroso et al., diotocardian neritids appeared as a more derivative 2012). Details of the pairs m3 are different from those of taxon inside Neritimorpha, preceded by the representa- N. zebra, but these m3 muscles, as well as the jugal mus- tives of the three terrestrial superfamilies Neritopsoidea, cles m1, normally are the most variable, even in closely Hydrocenoidea, and Helicinoidea in their phylogram related species. The stomach of H. variabilis has a pair (Uribe et al., 2016: fig. 2). From a morphological point of of ducts to the digestive gland, located close to each view, this arrangement is not the most parsimonious, as other (Fig. 26: dd); the other known helicinids usually the most derived taxon (Neritidae) supposedly would have these ducts on opposite sides of the stomach (e.g., have reverted to the marine environment and recov- Bourne, 1911: figs. 10-15), but the remaining digestive ered several morphological plesiomorphies, such as the features appear similar, including the well-developed bipectinate gill, the osphradium, and the right auricle. pair of esophageal pouches (Fig. 24: ep). Possibly to resolve this dilemma, Uribe et al. (2016) sug- In the phylogenetic scheme of Simone (2011), gested a non-parsimonious explanation, in which the H. variabilis would certainly be placed in the “node three most basal superfamilies evolved independently U – Neritimorpha” (fig. 20), in having the main neri- from different marine ancestors. timorph synapomorphies, such as the absorption of the inner shell whorls, the pair of columellar muscles inserting directly on the columellar side of the aper- ACKNOWLEDGMENTS ture, and the calcareous operculum. The presence of well-developed pallial gonoducts, indicating internal We are deeply grateful to José Coltro Jr. (Femorale) fertilization and production of egg capsules, as shown for providing the material studied here, and to Lara in Figs. 23, 34 and 35, are one of the synapomorphies of Guimarães (MZSP) for helping with the SEM examination. the Adenogonogastropoda Simone, 2011, a taxon unit- To Rodrigo B. Salvador for suggestions in an early phase ing Neritimorpha with the Apogastropoda. Other main of the paper. I also thank the editor and both anonymous characters are the eyes with a lens,loss of the right pallial referees for their suggestions and comments, and Janet structures (gill, osphradium, and hypobranchial gland), Reid for English polishing.