Ennucula puelcha ( d’Orbigny, 1842 )

Simone, Luiz Ricardo L., 2009, Comparative morphology among representatives of main taxa of Scaphopoda and basal protobranch Bivalvia (Mollusca), Papéis Avulsos de Zoologia 49 (32), pp. 405-457 : 418-423

Ennucula puelcha ( d’Orbigny, 1842)

( Figs. 30-38 , 95-105 )

Nucula puelcha d’Orbigny, 1842: 162 ; 1846: 624 (pl. 84, figs. 24-26); Schenck,1939: 30; Carcelles,1944: 268; Ihering, 1907: 371; Castellanos, 1967: 189 (pl. 14, fig. 5); Figueiras, 1976: 73; Roux et al., 1995: 295, 301-303; Bremec & Roux, 1997: 157; Paiva, 2001: 428; Soares-Gomes & Pires-Vanin, 2003: 721; Acha et al., 2004: 93; Absalão et al., 2006: 67; Giberto et al., 2006: 5; Vinuesa & Varisco, 2007: 29.

Nucula puelchana d’Orbigny, 1842 (pl. 84, fig. 24-26); Borchert, 1901: 32 (pl. 3) [error].

Nucula uruguayensis E.A. Smith, 1880: 320-321 [loc: 36°47’S, 55°17’W, 51.2 m depth, off Rio de la Plata mouth].

Nucula savatieri Mabille & Rochebrune in Rochebrune & Mabille, 1889: 112 (pl. 8, fig. 2) [loc: Canal du Beagle; Baie Orange, Tierra del Fuego].

Ennucula puelcha : Dell, 1964: 141; Camacho, 1966: 53 (pl. 8, fig. 6); Scarabino, 2003: 229; Rosenberg, 2005; Clavijo et al., 2005: 391.

Nucula (Ennucula) puelcha : Rios, 1970: 146 (pl. 50); 1975: 188 (pl. 60, fig. 918); Figueiras & Broggi, 1973: 203.

Nucula (Leionucula) puelcha : Abbott, 1974: 411; Del Rio, 1991: 27 (pl. 27, fig. 1); Rios, 1985: 203 (pl. 74, fig. 1040); 1994: 225 (pl. 78, fig. 1111).

Nucula (Nucula) semiornata : Del Rio, 1992: 12 (pl. 1, fig. 11).

Leionucula puelcha : Del Rio, 1998: 14, 48 (pl. 4, figs. 10, 11; pl. 16, fig. 5; pl. 24, fig. 10).

Types: lectotype BMNH 1854.12.4.774/1 (single valve; designation Aguirre, 1994). Paralectotypes BMNH 1854.12.4.774/2-3 (possibly of another species, see below) .

Type locality: Riacho del Ingles , au fond de la Bahia de San-Blas, Patagonia (fossil) .

Redescription

Shell ( Figs. 30-38 ): Size about 15 mm, color pale to dark brown. Height about 80% of length; width about 60% of length. Periostracum glossy, smooth, relatively thick. Sculpture lacking except for growth lines ( Figs. 32, 38 ). Umbos tall, rounded, located close to each other ( Fig. 31 ) approximate angle 110°, located about 20% of total length from posterior margin, extending about 10% of total height dorsal from hinge ( Figs. 30, 31 ). Resilium internal, conic (wider region posterior), located approximately between posterior and middle thirds of hinge ( Figs. 33, 34 ). Ligament length about 10% of shell length and height about 5% of shell height. Inner surface glossy, silvernacred, including hinge. Hinge with approximately 18 teeth anterior and 8 posterior to ligament; teeth increasing height from umbonal region towards both (anterior and posterior) ends ( Figs. 35, 36 ); anterior set of teeth becoming dorso-ventrally wider towards anterior ( Figs. 30, 31, 33-35 ); posterior set of teeth of similar width. Scar of anterior adductor muscle elliptical, about twice tall than long, located in middle level of anterior edge, about 15% of shell length away from anterior margin; occupying about 4% of inner surface of valve ( Figs. 30, 31. 36 ). Scar of posterior adductor muscle with similar characters than anterior adductor scar, located in opposed side and with about 75% anterior scar size. Pallial line simple, located edging ventral edge a distance equivalent to 17% of shell height.

Main muscle system ( Figs. 37 , 95, 99 ): Anterior adductor muscle elliptical in section; about twice high than wide; occupying approximately 4% of valve; located between middle and ventral thirds of animal’s height, and about 15% of shell length posterior to anterior edge; anterior region about half of posterior region ( Fig. 35 ). Posterior adductor muscle approximately 75% anterior adductor muscle size, and positioned slightly in opposite region; remaining characters, including horizontal level, similar; clearly divided into two equally sized portions (quick and slow components) along dorso-ventral axis ( Figs. 95, 98-100 : pa). Pair of auxiliary protractor muscle of foot ( Fig. 99 : ap) very narrow and long; each one originating in dorso-posterior region of anterior adductor muscle in area approximately 1/150 of that of this adductor; running posteriorly and ventrally between integument and anterior foot musculature, splaying superficially along anterior foot base. Pair of foot protractor muscle ( Fig. 99 : fp), relatively thick and long; each one originating dorsally to anterior adductor muscle in area equivalent to 1/30 of this adductor; running towards posterior and slightly ventral a distance equivalent to half shell length, gradually broadening; inserting along lateral walls of visceral sac and middle pedal base. Pair of anterior pedal retractor muscle, very broad and thick ( Fig. 99 : fa); each one originating just dorsal and slightly posterior to origin of anterior protractor muscle in area equivalent to half of anterior adductor muscle; running towards ventral and slightly posterior, close to median plane, broadening weakly along their length; inserting along anterior foot base, fulfilling almost entire anterior volume of visceral sac. Pair of middle pedal retractor muscle, broad and thick ( Figs. 95, 98, 99 : rm); each one originating in umbonal cavity, between posterior and middle thirds of distance between umbo and anterior shell margin, close to dorsal medial line, in area equivalent to 1/5 that of anterior adductor muscle; running towards ventral and slightly posterior, weakly curved (concavity anterior), widening gradually, positioning closer to medial plane; insertion in middle-posterior region of foot base, fulfilling most of middle-ventral volume of visceral sac. Pair of auxiliary middle pedal retractor muscle, narrow and long ( Fig. 99 : fr); each one originating just ventral to origin of middle pedal retractor muscle; running almost vertically towards ventral (slightly posteriorly), somewhat away from middle retractor muscle; inserting in middle region of foot base, flanked externally by middle pedal retractor muscles. Pair of posterior pedal retractor muscles, very broad and thick ( Figs. 95, 98, 99 : fm); each one originating at some distance dorsal and slightly anterior to posterior adductor muscle, in area slightly larger than half that of anterior adductor muscle, antero-posteriorly long (about three times longer than wide); running close to median plane towards ventral, almost vertically (slightly anterior); inserting along posterior pedal base.

Foot ( Figs. 45 , 95 , 101 ): Laterally flattened, about 1/3 of shell volume. Distal region with expanded edges, umbrella-like, extending about twice foot width beyond lateral edges. Posterior vertical posterior flap ( Fig. 101 : ff) rounded, extending about 1/6 of entire foot length towards posterior, occupying ventral half of posterior foot surface, along medial plane.

Mantle ( Figs. 35 , 95 ): Mantle lobes symmetrical, thin, translucent, colorless. Mantle border trifolded ( Fig. 96 ); outer fold tall and thin (about 1/3 of shell thickness), about 15 times taller than thick; middle fold with about same thickness of outer fold and about half its height; inner fold about double thick than remaining folds, only 1/5 of middle fold height. Periostracum positioned between outer and middle folds. Mantle border slightly thicker in base of folds. Inner fold differentiated in about 12 small pairs of papillae in ventro-posterior region ( Fig. 95 : ma); each papilla about as tall and as wide as middle fold, tip rounded, separated between neighboring papillae by space equivalent to width of each papilla. Mantle lobes totally separated from each other along entire ventral edges; connection between both lobes only in hinge region. Hinge dorsal fold of mantle ( Fig. 35 : hf), relatively tall, closely related to every shell tooth.

Pallial cavity ( Figs. 37 , 95 , 101 ): Occupying about half of inner shell volume. Palps with about 1/3 of valves size; main (broader) region oval, slightly longer than half shell length and height ( Figs. 101 : pp); inner surface entirely covered by narrow transverse folds; each fold very narrow and close to each other, ventral end rounded, dorsal end connected with its pair of other hemipalp; inner palp folds diminishing in both ends, posterior folds situated slightly more separated from each other and in oblique, curved way ( Figs. 101 ). Palp inner folds end before palp ventral edges, producing smooth, uniform margin. Proboscis of palps about as long as main portion of palps, and about 1/6 its width; located as posterior continuation of furrow between both hemipalps; inner surface as wide groove, smooth; proboscis tapering gradually, tip slightly rounded; edges undulating. Two pairs of small projections located only in inner hemipalps, by side and internally from proboscis; similar in characters to proboscis but about 1/10 its length and half its width; more ventral projection weakly smaller than dorsal projection ( Fig. 101 : pj). Palps inner folds reaching region close to mouth. Pair of small palp muscles located in postero-dorsal corner between both hemipalps ( Figs. 95, 99 : mu), running immersed in adjacent integument up to posterior region carving base of both posterior pedal retractor muscles. Gills bipectinate and proportionally small (about 1/15 of shell volume), about 6 times longer than tall; located obliquely from pericardial area to region ventral to posterior adductor muscle; anterior end rounded, gradually narrowing up to pointed posterior end. Gills posterior end supported by pair of suspensory stalks ( Figs. 98, 100 : gs), as thick membranes connected to ventral surface of posterior adductor muscle, close to median line. Suspensory membrane becoming shorter and wider towards anterior, supporting entire gills ( Figs. 97, 98 ); in anterior region bearing some muscular fibers, and thin hypobranchial gland in both sides ( Fig. 97 : hg). Gills periphery connected to mantle and to visceral sac by cilia. Gill filaments symmetrical in both sides ( Fig. 97 ), edges somewhat thicker, rounded ventrally and bluntly angled dorsally; afferent and efferent gill vessels ( Fig. 97 : af, cv) narrow, located in opposed sides of central rod, efferent vessel slightly broader than afferent vessel. Supra-branchial chamber about 1/6 of infra-branchial chamber.

Visceral mass ( Figs. 35, 37 , 98, 99 , 102 ): With about half shell volume, placed as dorsal continuation of foot; strongly compressed by pedal musculature ( Fig. 99 ). Stomach as central structure, positioned vertically from umbonal cavity up to region close to ventral foot surface. Digestive diverticula pale green, located surrounding dorsal half of stomach, occupying about 1/4 of inner visceral volume. Gonad fulfilling remaining regions, mainly umbonal cavities, color cream to white. Digestive tubes mainly positioned at right from stomach, looping through digestive diverticula and gonad. Pericardium occupying about 1/5 of visceral volume, located posteriorly to umbos, flanking posterior pedal retractor muscles ( Fig. 98 ); about twice wider than long. Transverse muscles well developed in region surrounding stomach ( Fig. 102 : tm), crossing through gonad, connecting both sides of pedal base integument; generally four anterior and five posterior to stomach.

Circulatory and excretory systems ( Fig. 98 ): Located compressed between pair of posterior pedal retractor muscles and middle pedal retractor muscles. Pair of auricles elongated, connected to efferent gill vessel in ventral region of gills anterior end; crossing perpendicularly towards medial a distance equivalent to 1/4 shell width. Ventricle relatively small, located in middle region of pericardium, on median line, surrounding intestinal portion crossing pericardium. Kidneys solid, small (about 1/8 of pericardial volume), pale brown; located in both sides of pericardium, covering anterior region of gill.

Digestive system ( Figs. 99 , 102 ): Palps and digestive diverticula described above. Mouth small, located terminally between both palps ( Fig. 101 : mo). Esophagus located relatively far from anterior adductor muscle, passing between both anterior pedal retractor muscles, running a distance equivalent to 1/4 shell length on dorsal region of visceral sac; width about 1/6 that of anterior adductor muscle. Esophagus inner surface smooth ( Fig. 103 ). Stomach large (about 1/4 visceral volume), broader and irregular dorsally, tapering ventrally ( Fig. 102 : st). Pair of ducts to digestive diverticula located ventral to esophageal insertion ( Figs. 102, 103 : dd). Inner surface of stomach ( Fig. 103 ), mostly smooth; distinct thickness located on dorsal-right region, occupying about 1/3 of gastric inner area, supposedly gastric shield (gh); middle transverse gastric fold dividing horizontally entire circumference (middle gf) into two similar-sized halves. Pair of longitudinal folds located on left side of intestinal origin, separating style sac (ss) from intestinal portion of that region of stomach (inferior gf). This region corresponding to style sac equivalent to 1/8 of entire gastric volume. Intestine region after style sac forming strongly angled loop ventral to stomach ( Figs. 99 , 102 ); after this, running ventro-dorsally between posterior series of transverse muscles and middle pedal retractor muscles ( Figs. 99 , 102 ); after this, performing complex series of loops ( Fig. 99 ) at right from stomach; finally crossing from anterior to posterior in dorsal region of visceral mass along medial line, crossing through origins of middle and posterior retractor pedal muscles ( Fig. 99 ) and pericardium. Entire intestine narrow (about 3/4 esophageal width), uniform width along its length. Rectum crossing along median line attached to dorsal and posterior surface of posterior adductor muscle. Anus simple, sessile ( Figs. 98, 100 ).

Genital system: Gonad above described. No gonoducts detected.

Central nervous system ( Fig. 99 ): Pair of cerebral ganglia located close to origins of foot protractor muscle ( Fig. 99 ; ce); each one rounded, size equivalent to half esophageal transverse section. Cerebral commissure with about half shell maximum width. Pair of pedal ganglia ( Figs. 99 , 102 : pg) 6-7 times larger than cerebral ganglia, about three times longer than wide; located close to median plane, flanking posterior surface of base of anterior pedal retractor muscle; each pedal ganglion with single main connective in both ends. Pair of visceral ganglia of similar size than cerebral ganglia ( Figs. 98, 99 : vg), located in space between pair of posterior pedal retractor muscle and ventro-posterior region of posterior adductor muscle. Cerebro-visceral connectives crossing gonad close to lateral regions of integument of visceral sac.

Measurements (respectively length, height and maximum inflation in mm): MZUSP 19101 #1: 13.0 by 10.0 by 7.6.

Distribution: From south Bahia, Brazil, to north Argentina (Pacific records contested, see below).

Habitat: Muddy bottoms, from infratidal to ~ 100 m depth.

Material examined: BRAZIL. Bahia. Alcobaça; Parcel de Paredes , 2-3 m depth , MZUSP 46333 , 7 valves (Souza & Gonçalves col., 2005). Espírito Santo. Guarapari ; MZUSP 77268 , 6 specimens (Coltro col., 2006). Rio de Janeiro. off Campos, 22°34’S 40°29’W, 213 m depth , MZUSP 18793 , 1 specimen (R.V.W. Besnard sta. 9, 11/ii/1969, laminarias); Angra dos Reis ; MZUSP 56232 , 1 shell (IOUSP sta. 327, iii/1969) ; Ilha Grande Bay (R.V. Emilia) ; MZUSP 18287 , 1 specimen (sta. 5B, 1968) MZUSP 18284 , 45 shells (sta. 132, 12/v/1966) , 25.5 m depth, MZUSP 18289 , 2 shells (sta. 7B, v/1965) , 17.5 m depth, MZUSP 18276 , 1 shell (sta. 31, 13/xii/1965) , MZUSP 18281 , 1 shell (sta. 65, 18/v/1966) , MZUSP 18277 , 4 specimens, (sta. 40, 12/xii/1965) , MZUSP 18288 , 1 specimen (sta. 6B) , MZUSP 18278 , 1 specimen (sta. 43, 11/xii/1965) , MZUSP 18283 , 1 specimen (sta. 118, 2/vii/1966) , MZUSP 18286 , 1 specimen (sta. 137, 4/vii/1966) , MZUSP 18282 , 1 specimen (sta. 104, 1/vii/1966) , MZUSP 18280 , 2 specimens (sta. 99, 1/vii/1966) , MZUSP 18285 , 6 specimens (sta. 134, 12/v/1966) , 50-60 m depth, MZUSP 38458 , 1 specimen (o.t., Magenta leg. vii/2003), (R.V.W. Besnard ) 22 m depth, MZUSP 23658 , 1 specimen (sta. 331, 21/iii/1969) , MZUSP 23660 , 1 specimen (sta. 341, 14/iii/1969) , 30 m depth, MZUSP 23659 m, 2 specimens (sta. 339, 19/iii/1969) . São Paulo. Ubatuba ( Projeto Integrado ; R.V. Veliger II); 23°37’24”S 45°03’48”W, 35 m depth , MZUSP 86366 , 25 valves (sta. 2, 26/x/1985) , 23°50’S 45°10’W, MZUSP 83141 , 1 shell (sta. 22, 16/iv/1986) ; off Queimada Grande Island , 40-50 m depth (o.t., Coltro leg.) , MZUSP 65891 , 2 specimens (vii/2002) , MZUSP 65892 , 2 specimens (vii/2000) , 50-60 m depth (Magenta leg., viii/2002), MZUSP 35717 , 20 specimens , MZUSP 35753 , 12 specimens. Paraná. off Paranaguá , MZUSP 35371 , 8 specimens (o.t., Magenta leg, xi/1999) Santa Catarina. Bombinhas; Zimbros Bay , 5-8 m depth , MZUSP 32079 , 1 specimen , MZUSP 32080 , 1 specimen (in starfish stomach, o.t., Tarasconi leg. vii/1993) ; off Gaivotas , 29°33’S 48°57’W, 91 m depth , MZUSP 18787 , 13 specimens (R.V.W. Besnard sta. 1706, 6/iv/1972) . Rio Grande do Sul (R.V.W. Besnard). Off Tramandai, 30°12’S 50°11’W, 90 m depth , MZUSP 18788 , 37 specimens (sta. 1723, 10/iv/1972) ; off Mostardas , 30°50’S 50°06’W, 79 m depth , MZUSP 18790 , 10 specimens (sta. 1860, 6/viii/1972) ; Off Rio Grande , 32°48’S 50°27’W, 197 m depth , MZUSP 18789 , 2 specimens (sta. 1758, 22/iv/1972) . URUGUAY. Off Maldonado, 35°00’S 54°50’W, 23 m depth , MZUSP 19101 , 62 specimens (GEDIP-RS sta. 1866; R.V.W. Besnard col., 11/viii/1972) . Rocha (R.V.W. Besnard). Off Punta del Diablo , 34°05’S 53°30’W, 20 m depth , MZUSP 18792 , 2 specimens (sta. 1877, 14/ viii/1972) ; off La Paloma , 35°51’S 53°06’W, 206 m depth , MZUSP 18791 , 1 specimen (sta. 1870, 12/viii/1972) .

Discussion

Some reports of Ennucula puelcha have referred the species to the Pacific coast of South America [ Bernard, 1983: 10; Villarroel & Stuardo, 1998: 134-136 (figs. 29-32, 72, 110-112); Osorio & Reid, 2004: 78-79 (fig. 2J)]. However, the shells of the Pacific samples have more pointed umbones. This shell difference, allied to a relatively wide geographic distance and the glacial separation between that region and the south Atlantic coast of South America, are indicative of the reports from Chile and Peru that the species actually belongs to another, possible new species. This shell difference has also been pointed out in the literature ( Osorio & Reid, 2004: 79). However, remarkably, the papers on the Pacific samples are those that changed the species from Nucula (Lamarck, 1799) to the genus Ennucula .

The type specimens of Ennucula puelcha were examined at BMNH ( Figs. 104-110 ). The lectotype ( Figs. 104, 105 ) matches with the specimens examined herein. On the other hand, the paralectotypes ( Figs. 106-110 ) do not; in the meantime, they are somewhat similar to Nucula semiornata d’Orbigny, 1846 , of which they can possibly be the types. The paralectotypes ( Figs. 106-110 ) have taller umbones, the apical angle is narrower, the outer concentric sculpture is more evident ( Figs. 106, 107, 110 ), the resilium is more projected and the hinge is narrower and possesses slightly more teeth ( Figs. 108, 109 ). These characters fit the description of N. semiornata and differentiates it from that of E. puelcha . With the above mentioned possibility that the Pacific and Atlantic specimens belong to separate species, some species supposedly synonymous to E. puelcha were not included in the present synonymic list. These species are: Nucula agujana Dall, 1908 (described from Aguja, Peru; 1895 m depth). N. pigafettae Dall, 1908 (described from Magellan Strait; 494 m depth); and possibly N. felipponei Marshall, 1928 ( Bernard, 1983); as well as some Pacific citations of E. puelcha , such as Villarroel & Stuardo (1998) and Osorio & Reid (2004). Accounts on the anatomy of Pacific samples identified as E. puelcha are provided by Villarroel & Stuardo (1998, figs. 29-31, 72, 110-112). The stomach of the Atlantic specimens has a shorter style sac, about 20% in contrast to 60% of the Pacific species, and less developed dorsal sorting area and dorsal hood. Additionally, the gills are proportionally smaller, and the papillae in mantle edge are restricted to the posterior region in Atlantic species, while papillae occur in most mantle edges in Pacific samples.

Another Ennucula has accounts written on its anatomy, E. tenuis (Montagu, 1818) ( Kuznetsov et al. 1983) . in such E. puelcha differs in having proportionally larger palps and respective proboscises, as well as larger adductor muscles.

Family Solemyidae

Genus Solemya Lamarck, 1818 (Type: Solemya mediterranea Lamarck, 1818 , SD Children, 1823)

Figures

FIGURES 30‑38: Shell and anatomical aspects of Ennucula puelcha (MZUSP 19101; length = 13.0 mm): 30) Right valve, inner view; 31) Same, left valve; 32) Dorsal-slightly right view; 33) Left valve, detail of hinge, inner view; 34) Same, right valve; 35) Dorsal region with left valve somewhat still in situ, dorsal-slightly right partial view; 36) Whole shell, ventral view, valves somewhat deflected; 37) Whole left view, left mantle lobe partially removed; 38) Anterior-slightly ventral view.

FIGURES 95‑100: Ennucula puelcha anatomy: 95) Whole right view, right valve and part of mantle right lobe removed; 96) Mantle edge, transverse section in middle portion of its ventral region; 97) Gill, transverse section in its middle region along 5 filaments; 98) Posterior half of visceral mass, dorsal-slightly right view, right mantle lobe and dorsal portion of pericardium removed; 99) Digestive tubes, main musculature and central nervous system in situ, right view, semi-diagrammatic representation artificially transparent; 100) Region of posterior adductor muscle, right-slightly posterior view, pallial lobes fully removed. Scales = 1 mm.

FIGURES 101‑103: Ennucula puelcha anatomy: 101) Whole ventral-slightly right view, right hemipalps deflected, pallial lobes removed; 102) Midgut and adjacent structures in situ, right view; 103) Stomach and adjacent digestive tubes,right view, mostly opened longitudinally. Scales = 1 mm.

FIGURES 104‑110: Ennucula puelcha BMNH type lot (1854-12-4-774): 104-105) Lectotype single (left) valve, outer and inner views, length = 13.0 mm; 106-107) Paralectotype #2, outer views of both valves, length = 6.8 mm; 108-110) Paralectotype #3, inner view of both valves and outer view of left valve, length = 7.8 mm; Paralectotypes 2-3 appear to be Nucula semiornata d’Orbigny, 1846.

FIGURES 39‑46: Shell aspects of Solemya notialis n. sp: 39) Holotype, left view, length = 10.6 mm; 40) Same, right view; 41) Same, dorsal view; 42) Same, ventral view; 43) Same, detail of peri-umbonal region, left-slightly dorsal view, scale = 1 mm; 44) Same, right valve, inner view, detail of hinge and anterior region, scale = 1 mm; 45-46) Paratype MZUSP 20397, right valve with extended periostracum, outer and inner views respectively, length = 12.9 mm.