Huttonella bicolor ( Hutton, 1834 )

Simone, Luiz Ricardo L., 2013, Anatomy Of Predator Snail Huttonella Bicolor, An Invasive Species In Amazon Rainforest, Brazil (Pulmonata, Streptaxidae), Papéis Avulsos de Zoologia 53 (3), pp. 47-58 : 47-58

Huttonella bicolor ( Hutton, 1834)

( Figs. 1-24 )

Pupa bicolor Hutton, 1834: 86 , 93 [Mirzapore and Agra, India]; Martens, 1867: 384-385 (with complementary ancient synonymy).

Ennea (Huttonella) bicolor : Pfeiffer, 1854 ( 1854 -1879): 115 (pl. 32, figs. 15-17), 1856: 120; Nevill, 1868: 6; Tryon, 1885: 104 (pl. 19, figs. 14, 17-18; pl. 20, fig. 24).

Ennea bicolor : Nevill, 1869: 64; Mörch, 1872: 315; Issel, 1874: 51; Fischer, 1891: 18; Fischer & Dautzenberg, 1904: 2; Blanford & Austin, 1908: 19-20 (fig. 12); Barnacle, 1962: 54; Lionnet, 1984: 240; Morgan, 1885: 372; Annandale & Prashad, 1920: 189-190; Laidlaw, 1933: 233; Gerlach, 1987: 10 (2 figs.).

Huttonella bicolor : Stoliczka, 1871: 169; 1873: 11; Jaeckel, 1950: 18; Jutting, 1961: 8; Dance, 1970: 153; Sanisic, 1981: 84-86; Turgeon et al., 1988: 277; 1998: 526; Chan, 1995: 4-5; Ho, 1995: 91, 100-101; Vermeulen & Whitten, 1998; Schileyko, 2000: 822 (fig. 1075A); Auffenberg & Stange, 2008: 3 (fig. 8); Santos et al., 2008: 145-148 (figs. 1-3); Pérez et al., 2008: 331; Robinson et al., 2009: 634, 646, (figs. 7C, 8D); Sutcharit et al., 2010: 3, 9, 13; Schileyko, 2011: 27.

Ennea bicolor barkudensis Annandale & Prashad, 1920: 191-194 (figs. 1-3) [Barkuda Is., Chilka Lake, Odisha, India].

Gulella (Huttonella) bicolor : Jutting, 1950: 504-505 (figs. 106-107); Ramakrishna & Mitra, 2010: 39.

Gulella bicolor : Berry, 1963a: 15 (fig. 73); Dundee & Baerewald, 1984: 63-67 (figs. 2-7); Naggs, 1989: 165-168; Cowie, 1997: 31; Gerlach & Bruggen, 1999: 20-21 (figs. 1b; 6a); Vermeulen, 2007: 174-175 (fig. 4); Chaijirawowg et al., 2008: 251-254 (figs. 2-3).

Complementary description

Shell ( Figs. 1-6 , 11 ): about 6 mm long, turriform, elongated; width ~30% of length. Walls thin, fragile, translucent ( Figs. 5-6 ) to opaque ( Figs. 1-4 ). Color mostly white, with some reddish or yellowish tones close to apex. Spire elongated, occupying ~70% of shell length. Whorls convex, weakly rounded, suture relatively deep. Protoconch with little more than 1 whorl, smooth, dome-shaped, with ~10% of shell length and ~62% of maximum diameter ( Figs. 1-6 ). Transition protoconch-teleoconch unclear, orthocline ( Fig. 4 ). Teleoconch of three whorls; penultimate whorl about 30% wider than preceding and last whorls ( Figs. 2, 5 ). Sculpture mostly smooth, with irregular axial, subsutural ribs, ~ 20 in penultimate whorl, restricted to superior 10% of each whorl ( Figs. 1-6 ); axial sculpture stronger in last half whorl, becoming complete axial ribs ( Figs. 3, 1, 6 ). Umbilicus practically absent ( Fig. 2 ). Aperture with strongly deflected, thick lips, orthocline ( Figs. 2, 4 ); occupying ~30% of shell length and ~85% of shell width. Outline of aperture somewhat rectangular, weakly longer than wide, ( Figs. 1, 5 ). Outer lip rounded, straight in middle; inner lip thick by flattened callus. Apertural teeth ( Figs. 1, 5 , 11 ): tall, triangular, wide teeth located in middle of outer lip; palatal teeth located in middle of superior region of callus, with concavity right, forming a canal with tooth of outer lip; parietal tooth elongated, located in middle to inner lip, obliquely placed; inferior toot small, located in middle level of inferior apertural edge.

Head-foot ( Figs. 12, 16 ): of normal shape. Color uniform pale yellow to cream. Pair of ommatophores well-developed, with strong retractor muscles (tm), normally orange pigmented. Eyes dark. No tentacles found. Columellar muscle thick, 1whorl in length.

Mantle organs ( Fig. 15 ): mantle border thick, lacking pigments. Pneumostome protected by ventral, right flap (pv), with ~1/4 of aperture length. Pneumostome about 1/8 of aperture length, having on dorsal edge anus right and nephrostome left ( Fig. 15 : an, ua). Lung almost 2 whorls in length, narrow and elongated. Pulmonary vessels inconspicuous, concentrated in anterior third, surrounded by mucosa strongly pigmented orange ( Fig. 6 ). Pulmonary vein (cv) running longitudinally and weakly oblique, anteriorly between middle and right thirds of pallial cavity, approaching to median line gradually. Middle and posterior thirds of cavity lacking visible vessels except for pulmonary vein. Kidney yellow, located posteriorly, occupying ~20% of cavity length and ~50% of its width (details below). Rectum (rt) and ureter (ur) narrow, running along right edge.

Visceral mass ( Figs. 5 , 13, 14 ): about 4 whorls in length. Both digestive gland lobes pale yellow in color. Anterior lobe ( Figs. 13, 16 : da) flattened, occupying ~1/6 of visceral volume, located just posterior to pallial cavity continuous to kidney. Posterior lobe (dg) with 3 spiral, similar sized whorls, with ~75% of visceral volume. Stomach with about 1/10 of visceral volume, located between both digestive gland lobes, about half whorl posterior to pallial cavity ( Fig. 13 ). Digestive tubes (described below) surrounding anterior lobe of digestive gland. Gonad clearly multi-lobed, cream color, somewhat spherical, encased in middleright region of posterior lobe of digestive gland, occupying ~1/15 of visceral volume.

Circulatory and excretory systems ( Fig. 15 ): Pericardium about twice as long as wide, located longitudinally between middle and left thirds of posterior end of pallial hoof; occupying ~5% of lung area. Auricle located anteriorly, as continuation from pulmonary vein, with about same ventricle size. Kidney size reported above, simple, entirely solid ( Fig. 15 : ki), dorso-ventrally flattened. Nephropore small, in anterior-left corner, as tip of small projection of renal tissue, turned right ( Fig. 15 : ka). Primary and secondary ureter complete and closed (tubular); primary ureter lying on anterior edge of kidney, somewhat perpendicular to pallial cavity longitudinal axis, after running ~half pallial cavity width abruptly turning anteriorly, running as secondary ureter (ur) along right half of posterior end of lung, and along left edge of rectum. Urinary aperture ( Fig. 15 : ua) simple, turned anteriorly, located on edge of pneumostome.

Digestive system ( Figs. 12, 16-22 ): Oral tube relatively long in retracted condition ( Fig. 12 : ot), passing through nerve ring (nr). Buccal mass elongated, ~4 times longer than wide, with ~1/4 volume of head-foot and ~1/3 whorl in length. Dorsal region of buccal mass totally fulfilled by odontophore; ventral region mostly hollow, forming oral cavity ( Fig. 17 : oy; showed opened in Fig. 18 ). Jaws wanting. Pair of radular muscles, or retractors of buccal mass ( Figs. 16-21 : rm), very thick, fused with each other, originating in columella, in right side of columellar muscle, running towards ventral side about 1.5 times buccal mass length. Radular muscles inserted in postero-ventral end of odontophore posterior surface. Pair of buccal muscles ( Fig. 18 : mj) weakly thick, inserted in both sides of odontophore cartilages, extending along entire buccal cavity towards posterior as thin layer of circular fibers ( Fig. 18 : se). Pair of differentiated jugal muscles ( Figs. 17-18 : m1v), working as narrow ventral protractors of buccal mass; originating in ventral-anterior region of radular muscles, running towards anterior close to buccal mass ventral surface; inserting in ventral side of mouth. Odontophore with about 90% of buccal mass volume, as long as it, placed ventrally to esophagus but dorsal in a diverticulum forming buccal mass ( Fig. 16 : od). Odontophore muscles ( Figs. 18-21 ): m2, pair of narrow odontophore retractor muscles originating with radular retractors (rm); running close to median line as part of radular muscles ( Figs. 20, 21 ); inserting in posterior end of odontophore cartilages; mc, thin muscular layer connecting both outer edge of odontophore cartilages, covering entire odontophore ventral surface along ~85% of odontophore cartilages length ( Figs. 20, 21 ), from posterior end to certain distance from anterior end; m4, main pair of dorsal tensor muscles of radula, very thick, originating in central region of radular muscles, apparently lacking connections with odontophore cartilages ( Figs. 20, 21 ), surrounding entire radular sac; inserting in radular sac along its region immediately posterior to buccal cavity ( Fig. 21 ); m5, pair of thin auxiliary dorsal tensor muscles; originating in outer edges of odontophore cartilages ( Figs. 20, 21 ), along ~1/5 of their length, ~2/5 of cartilages length posterior to their anterior end; running short distance towards median line; inserting in radular sac just dorsal to m4 insertion; m6, horizontal muscle absent (cartilages totally fused with each other); m8, pair of narrow muscles running along both sides of subradular cartilage (sc) in its region in buccal cavity, continuing longitudinally through entire odontophore on dorsal side of m4, close to medina line, inserting in radular muscles ( Figs. 20, 21 ); m11, pair of narrow ventral tensor muscles of radula ( Fig. 19 ), originating in ventro-lateral surface of mc, running close to mc towards anterior and ventral, inserting in ventral end of subradular cartilage. Odontophore non-muscular structures ( Figs. 19-21 ): oc, odontophore cartilages, flattened, entirely fused with each other forming a wide groove ( Fig. 21 ), anterior end roughly rounded, remaining with uniform width along length, ~5 times longer than wide, posterior end concave, with pair of posterior, thick, short projections, middle (fusional) region thinner than lateral edges; sc, subradular cartilage, with expanding region in buccal cavity protecting subradular membrane ( Fig. 21 ).

Radula about as long as odontophore length. Radula ( Figs. 7-10 ) with rachidian teeth, 9 pairs of lateral teeth; no clear distinction of marginal teeth. Rachidian tooth ( Figs. 8, 10 ) small, ~5% of radular width and ~5 times longer than wide; base wider and triangular, remaining as rod tapering up to sharp pointed terminal cusp. Lateral teeth similar to rachidian ( Figs. 9, 10 ), except in being slightly asymmetrical, weakly arched, and ~3 times larger; lateral teeth similarly sized, except for marginal teeth, being ~1/2 of remaining teeth. Each radular row disposed as chevrons of ~75°.

Salivary glands covering anterior half of esophagus ( Fig. 16 : sg), and forming a single, white, thin mass. Single salivary duct differentiable along entire ventral side of glands, with about 1/12 esophageal width. Salivary duct bifurcating only in region anterior to glands ( Fig. 16 : sd), becoming pair of ducts, running to both sides of esophageal origin. Salivary ducts opening in anterior end of lateral sides of odontophore cavity.

Esophagus as long as about ¾ whorl, with thin, flaccid walls lacking clear subdivisions ( Figs. 12, 16 : es); inner surface of anterior half possessing 4-5 folds. Posterior esophageal half slightly wider, with a smooth inner surface. Stomach position and size described above (visceral mass) ( Fig. 13 ), relatively narrow, curved, somewhat fusiform; gastric walls thin, flaccid; inner surface smooth. Esophageal insertion right, intestinal origin on left side, both close to columella. Duct to anterior lobe of digestive gland encased between esophagus and intestine ( Fig. 16 : dd). Duct to posterior lobe of digestive gland located a short distance from intestinal origin and posterior do previously described duct ( Fig. 16 ). Intestine initially as wide as esophageal insertion, shortly tapering, flanking left side of anterior lobe of digestive gland, then in region of kidney gradually turning right and anterior, running almost straight forward in pallial cavity ( Fig. 16 ). Rectum and anus described above (pallial cavity) ( Figs. 15 ).

Genital system ( Fig. 22 ): gonad described above (visceral mass). Hermaphroditic duct (hd) narrow and weakly coiled; running for ~1/2 whorl close to columella. Seminal receptacle (sr) elongated, sac-like, with ~5 times hermaphroditic duct width, and ~1/3 its length. Fertilization complex (fc) as a zigzag, thick muscular, iridescent walled, located as continuation of hermaphroditic duct and duct of seminal receptacle, about as wide as receptacle; length, if straightened, ~twice receptacle length. Fertilization complex gradually becoming immersed in albumen gland, inserting in posterior end of spermoviduct, just in region of albumen gland duct (ad); all of them with similar width. Albumen gland (ag) solid, white, elliptical, ~3 times larger than gonad (about 1/4 whorl). Albumen gland duct subterminal, connected to distal end of spermoviduct (ad). Spermoviduct as single curve, of about 1 whorl in length and about as wide as albumen gland. Prostate gland occupying ~1/8 of spermoviduct volume (pt). Uterus occupying about 80% of spermoviduct space, external walls thick-glandular (ut), inner surface smooth, fulfilled by large quantity of iridescent granules. Vas deferens initiating preceding anterior 1/6 of spermoviduct (vd), ~1/5 of anterior spermoviduct width, weakly coiled. Vagina with about 1/6 spermoviduct length, inner surface simple, with 4-5 longitudinal, low folds (vg). Bursa copulatrix wanting. Penis of ~1/5 spermoviduct length, and about 2/3 its anterior width (pe), with penis muscle inserting subterminally. Penial (epiphalic) gland distal, spherical, of about 1/5 penis width and 1/1o penis length (ep); internally solid, no duct detectable ( Fig. 23 ). Internal penial surface simple, smooth ( Fig. 23 ), insertion of vas deferens prceded by region running immersed in penis wall along /1/5 of penis length. Genital pore rounded, simple.

Central nervous system ( Fig. 24 ): located at base of buccal mass ( Figs. 12, 16 ). Paired cerebral ganglia (ce) elliptical, about twice as long as wide; cerebral commissure short, with about half width and length of each ganglion. Each cerebral ganglion of about 1/4 width of local oral tube. Pair of optical ganglia slightly smaller than cerebral ganglia, located close to these, connected to antero-median side. Tentacular nerves connected more internally than connection of optical ganglia. Pair of pedal-pleural ganglia (pp) forming single mass located opposite cerebral ganglia, and of about the same size as cerebral ganglia. No differentiable ganglion detectable. Several pairs of nerves originate from these ganglia towards anterior. Pair of cerebro-pedal and cerebro-pleural connectives (cn) similar-sized, about as long as cerebral ganglia. Pair of possible odontophore ganglia (of) fused with each other, located a distance equivalent to nerve ring length away from pedal ganglia, connected with them by pair of connectives, inserted in median-ventral side of each ganglion. Pair of buccal ganglia located in antero-dorsal region of buccal mass, close to esophageal origin and salivary insertion ( Figs. 12, 17 : bg); each ganglion spherical, of about 1/3 cerebral ganglion size. Pair of statocysts located in ventral region of pedal ganglia, close to median line (sy), containing statoconia. Visceral ganglion located in posterior level of columellar muscle, with ~1/2 size of cerebral ganglion; connective with nerve ring running towards anterior ~1/3 whorl, passing just between penis and vagina.

Measurements (in mm): MZSP 98761(1): 6.1 by 1.9; MZSP 99734(1): 6.0 by 1.8.

Distribution: Described from India, but possibly originated from Africa or SW Asia. Presently introduced in Tropical and Temperate regions all over the world (see Introduction). In Brazil so far known from Acre and Rio de Janeiro.

Habitat: Normally in cultivated plains on the ground among fallen leaves, decaying wood, preferably in damp places ( Jutting, 1961, Vermeulen, 2007).

Material examined: BRAZIL. Acre (Edson Guilherme col, 2011); Zoobotanic Park of Universidade Federal do Acre, 09°57’20.5”S, 67°52’30.2”W, MZSP 98763 , 3 specimens (sta. IA448); Stare Park Chandless, 09°31’31.2”S, 69°55’34.6”W, MZSP 98760 , 4 specimens (sta. IA468) .

Figures

FIGURES 1‑6: Huttonella bicolor shell: 1) MZSP 98761 (Acre, Brazil), apertural view (H 6.1 mm); 2) same, left view; 3) same, dorsal view; 4) same, right view; 5) MZSP 99734 (Acre, Brazil), specimens with thinner shell, apertural view (H 6.0 mm); 6) same, dorsal view.

FIGURES 7‑11: Huttonella bicolor hard parts in SEM: 7) radula, whole view, scale: 20 µm; 8) same, detail of central region, scale: 20 µm; 9) same, detail of lateral region, scale: 10 µm; 10) same, detail of central region, rachidian close to right side, scale: 10 µm; 11) detail of aperture, MZSP 98761, apertural-slightly right view, scale: 300 µm.

FIGURES 12‑17: Huttonella bicolor anatomy: 12) foregut and peribuccal region, dorsal-slightly right view; 13) whole specimen just extracted from shell, right view; 14) same, ventral view; 15) pulmonary-pallial cavity, ventral-inner view; 16) digestive tubes as in situ and some adjacent structures, dorsal-slightly right view; 17) buccal mass isolated, right view. Scales = 0.5 mm.

FIGURES 18‑24: Huttonella bicolor anatomy: 18) buccal mass, opened longitudinally on median line in its dorsal wall, dorsal view; 19) same, right view, outer muscular layer removed; 20) same, inner-dorsal layer of muscles sectioned longitudinally and deflected, dorsal view, left m5 only partially shown; 21) same, radular sac and adjacent structures partially removed and deflected to right; 22) genital system, ventral view, base of fertilization complex seen if albumen gland was translucent; 23) detail of penis, sectioned longitudinally, dorsal view; 24) nerve ring, ventral view. Scales = 0.5 mm.