Onchidella binneyi Stearns, 1894

Dayrat, Benoît, Zimmermann, Sara & Raposa, Melissa, 2011, Taxonomic revision of the Onchidiidae (Mollusca: Gastropoda: Pulmonata) from the Tropical Eastern Pacific, Journal of Natural History 45 (15 - 16), pp. 939-1003 : 943-962

Onchidella binneyi Stearns, 1894

( Figures 2–10 )

Onchidella binneyi Stearns 1894: 342–343 , plate L, figs 1–2. — Watson 1925: 301. — Marcus and Marcus 1967: 227–230, fig. 83.

Onchidella carpenteri . – Stearns 1879: 399–401, pl. VII, figs 7–8. — Semper 1885: 281–282, plate XXI, figs 14, 25–26. — Binney 1890: 224, pl. VI, figs D–E, [not carpenteri Binney, 1861 ].

Onchidium carpenteri . – Semper 1885: 281–282, plate XXI, figs 14, 25–26, [not carpenteri Binney, 1861 ].

Onchidella hildae Hoffmann 1928: 35–38 , 69, 94, pl. 2, figs 1–2 [as Oncidiella ]. — Labbé 1934: 240. — Marcus and Marcus 1967: 230–231, figs 84–86. — Marcus and Marcus 1970: 214. syn. nov.

Type material Onchidella binneyi Stearns, 1894

Two syntypes ( NMNH 58824 ): two specimens 17/12 and 14/ 9 mm preserved, leg. Fisher, [no collecting date]. Type locality: not indicated on the current label, but indicated in the original description as “ San Francisquita Bay, Los Animas Bay, and Angeles Bay in the Gulf of California ”. Type material condition: Stearns mentions “several specimens” but only two are currently held at the NMNH. Both syntypes are still entire but they were probably dried for a while because the mantle is very hard and dark brown. Both syntypes are very poorly preserved, at least externally, and were not dissected for the present study .

Type material ( Onchidella hildae Hoffmann, 1928 )

The type material includes a total of 41 syntypes. Twenty-nine syntypes ( SMNH type-957): 29 specimens 12/12 to 6/ 6 mm preserved, leg. Eugenie Expedition station 656-9, 1851–1853. Eleven syntypes ( SMNH type-7521): 11 specimens 15/11 to 9/ 9 mm preserved, leg. Eugenie Expedition station 766(a), 1851–1853. One syntype ( SMNH type-7522): 1 specimen 7/ 4 mm preserved, leg. Eugenie Expedition station, 20 March 1852. Type locality: Insel Puna, Ecuador ( SMNH 957 ) and Panama [ Pacific Ocean ] ( SMNH 7521 and 7522). Type material condition: specimens are well-preserved ( SMNH 957 , 7521 and 7522). Four specimens were dissected prior to the present study, likely by Hoffmann: two from Ecuador ( SMNH 957 ) , and two from Panama ( SMNH 7521 and 7522). Six syntypes were dissected here, four from Ecuador and two from Panama: 12/12 (#1), 11/9 (#3), 10/12 (#4) and 6/6 (#2) from Ecuador ( SMNH 957 ) ; 14/11 (#1) and 12/11(#2) from Panama ( SMNH 7521 ) .

Remarks on the original description ( Onchidella binneyi )

Stearns’s original description contains observations on the external morphology as well as the natural history. However, the internal anatomy is not described.

Remarks on the original description ( Onchidella hildae )

Hoffmann’s original description of O. hildae is quite detailed, illustrated with several figures. Hoffmann (1928) even included a schematic diagram of the posterior reproductive organs which is quite accurate (e.g. he did not miss the distal, vaginal, accessory gland, or oviduktdrüse). Although Hoffmann had access to 40 syntypes from two localities, he only dissected four of them (two from Ecuador and two from Panama), which did not allow him to address individual variation of some key features, such as the shape of the penial caecum, which Hoffmann called the blindsack and which he thought was the main difference between O. binneyi and O. hildae .

Distribution

From the Gulf of California to Ecuador: Gulf of California (type locality of O. binneyi ; Stearns 1879, 1894; Semper 1885; Binney 1890; Marcus and Marcus 1967, 1970; present study), Nicaragua (present study), Costa Rica (present study), Panama (type locality of O. hildae ; present study), Colombia (present study), Ecuador (type locality of O. hildae ; present study).

Habitat

Intertidal, on rocks.

Additional material examined and dissected

A total of 319 non-type specimens were examined, 68 of which were dissected to study their internal anatomy. Those specimens were collected from 33 localities from 2.3 ◦ S on the Pacific coast of Ecuador to the northern end of the Gulf of California. ECUADOR, South Pacific Ocean , Punta Carnero , 4 March 1967, seven specimens 8/7 to 2/ 1 mm preserved [leg. D. Kirtley], identified as Onchidium sp. [unknown identifier], ( NMNH 706696 ) [two specimens dissected: 8/7 (#1) and 2.5/2.5 (#2)]; COLOMBIA, [Pacific Ocean], El Morro, Tumaco , 29 August 1948, 25 specimens 16/20 to 9/ 11 mm preserved [leg. E.M. Poulsen], identified as Onchidiidae [unknown identifier], ( ZMUC) [five specimens dissected: 16/20 (#1), 16/20 (#2), 13/15 (#3), 10/12 (#5) and 9/11 (#4)]; PANAMA, North Pacific coast, Gulf of Panama, Perlas Archipelago , Pajaro Island , NE cove, 8 ◦ 34.36’ N, 79 ◦ 01.18’ W, 1 May 1971, one specimen 7/ 7 mm preserved [leg. STRI Survey], identified as Onchidium sp. [unknown identifier], ( NMNH 733425 ) [not dissected]; North Pacific coast, Gulf of Panama, Panama, Perlas Archipelago , Chapera Island , small cove N of E point, 8 ◦ 35.36’ N, 79 ◦ 01.24’ W, 1 May 1971, five specimens 7/7 to 1.5/1.5 mm preserved [leg. STRI Survey], identified as Onchidium sp. [unknown identifier], ( NMNH 733414 ) [two specimens dissected: 7/7 (#1) and 3/3 (#2)]; North Pacific coast, Gulf of Panama, Panama, Canal Zone , Panama Bay , Culebra Island , Fort Amador , Causeway, E side of Naos Island , 8 ◦ 55.09’ N, 79 ◦ 32.06’ W, 28 April 1971, one specimen 10/ 10 mm preserved [leg. STRI Survey], identified as Onchidium sp. [unknown identifier], ( NMNH 733262 ) [not dissected]; North Pacific coast, Gulf of Panama, Panama, Canal Zone , Fort Amador , NW end of Culebra Island , 28 April 1971, nine specimens 13/16 to 3/ 4 mm preserved [leg. STRI Survey], identified as Onchidium sp. [unknown identifier], ( NMNH 733240 ) [two specimens dissected: 13/16 (#1) and 5/6 (#2)]; North Pacific coast, Gulf of Panama, Panama, Panama Bay, Taboguilla Island , N shore, 8 ◦ 48.52’ N, 79 ◦ 31.07’ W, 7 November 1971, one specimen 8/ 9 mm preserved [leg. STRI Survey], identified as Onchidium sp. [unknown identifier], ( NMNH 733282 ) [not dissected]; North Pacific coast, Gulf of Panama, Panama, Perlas Archipelago , Pajaro Island , NE cove, 8 ◦ 34.36’ N, 79 ◦ 01.18’ W, 7 November 1971, four specimens 8/10 (#1) to 6/7 (#2) mm preserved [leg. STRI Survey], identified as Onchidium sp. [unknown identifier], ( NMNH 733459 ) ; North Pacific coast, Gulf of Panama, Panama, Canal Zone , Perico Island , SE side of island, 12 April 1972, 11 specimens 12/10 (#1) to 5/5 (#2) mm preserved [leg. STRI Survey], identified as Onchidium sp. [unknown identifier], ( NMNH 734256 ) ; Panama, Pacific coast, Bahia de Panama, Taboga Island , 2 km SE of “Hotel Taboga”, 20 February 1975, three specimens 13/11 (#1) to 6/6 (#2) mm preserved [leg. A.J. Ferreira], identified as Onchidella binneyi by A.J. Ferreira, ( CASIZ 001430 ) ; Panama, Pacific coast, Gulf of Panama, Archipelago de las Perlas , Contadora Island , N side, 08 ◦ 38’ N, 79 ◦ 02’ W, 17–19 February 1975, one specimen 7/ 8 mm preserved [leg. A.J. Ferreira], identified as Onchidiidae by T. M. Gosliner, ( CASIZ 071739 ) [not dissected]; COSTA RICA, SW corner of Bahia del Coco , 10 ◦ 33.10’ N, 85 ◦ 43.15’ W, 23 April 1982, nine specimens 11/12 (#1) to 7/7 (#2) mm preserved [leg. V. Maes and C. Skoglund], identified as Onchidella sp. [unknown identifier], ( ANSP A9852 ) ; NICARAGUA, Pacific coast, Dept of Leon, immediately south of Puerto Somozo , El Velero , 12 ◦ 10’ N, 86 ◦ 45’ W, 22 January 1974, one specimen 10/ 7 mm preserved [leg. A.J. Ferreira], identified as Onchidella hildae by A.J. Ferreira, ( CASIZ 001445 ) [dissected]; MEXICO, Baja California Norte [north], Gulf of California, Bahia de Los Angeles , 7 June 1974, four specimens 20/17 (#1) to 15/ 13 mm preserved, leg. A.J. Ferreira, identified as Onchidella binneyi by A.J. Ferreira, ( CASIZ 078717 ) ; North Pacific Ocean, Gulf of California, Mexico, Sonora, San Augustin , 12 November 1966, five specimens 9/10 (#1) to 8/ 7 mm preserved, leg. P. Pickens, identified as Onchidella hildae , [identifier unknown], ( NMNH 753652 ) [those specimens are likely vouchers of Marcus and Marcus (1970)]; Mexico, Gulf of California, Sonora, Bahia San Carlos , 30–31 March 1940, 43 specimens 8/7 (#1) to 5/4 (#2) mm preserved [leg. unknown], identified as Onchidella binneyi by A.G. Smith, ( CASIZ 078725 ) [very poorly preserved internally]; Mexico, Gulf of California, Sonora, Puerto Penasco , in front of desalting plant, 5 August 1964, 11 specimens 8/5 (#1) to 5/4 (#2) mm preserved [leg. R. Ohmart and R. Crossin], identified as Onchidella hildae by A.G. Smith, ( CASIZ 078739 ) [very poorly preserved internally]; Mexico, Baja California Norte [north], Gulf of California, Isla San Lorenzo del Norte Isla Partida de Lorenzo , 29 April 1966, six specimens 13/13 (#1) to 6/6 (#2) mm preserved [leg. D. Chivers], identified as Onchidella binneyi by A.G. Smith, ( CASIZ 078724 ) ; Mexico, Baja California, [no collecting date], 23 specimens 16/12 (#1), 10/7 (#4), 7/6 (#3), to 5/4 (#4) mm preserved [leg. H. Hemphill], identified as Onchidella carpenteri by A.G. Smith, ( CASIZ 021518 ) ; Mexico, Gulf of California, Sonora, Puerto Penasco, Norse Beach , 6–9 June 1963, 16 specimens 16/13 to 6/ 6 mm preserved [leg. E. Coan], identified as Onchidella binneyi , [identifier unknown], ( CASIZ 078721 ) [two specimens dissected: 9/6 (#1) and 11/7 (#2) mm]; Mexico, Baja California Norte [north], Gulf of California, Sonora, Puerto Refugio, NW end of Isla Angel de la Guarda , 29 ◦ 20’ N, 113 ◦ 25’ W, 23 April 1953, 22 specimens 24/17 to 16/ 14 mm preserved [leg. J.W. Sefton Jr], identified as Onchidiidae by T. M. Gosliner, ( CASIZ 082076 ) [10 specimens dissected: 24/17 (#4), 23/19 (#10), 22/17 (#3), 21/20 (#6), 21/15 (#1), 21/17 (#7), 21/19 (#8), 19/15 (#5), 16/14 (#2), and 16/14 (#9) mm]; North Pacific Ocean, Gulf of California, Mexico, Sonora, Puerto Penasco , 31 ◦ 20’ N, 113 ◦ 35’ W, 7 May 1966, 12 specimens 23/15 to 15/ 10 mm preserved [leg. P. Pickens], identified as Onchidella binneyi [unknown identifier], ( NMNH 753656 ) [two specimens dissected: 23/15 (#1) and 18/15 (#2)]; North Pacific Ocean, Gulf of California, Mexico, Sonora, San Francisquito Bay , 9 April 1911, 23 specimens 16/12 (#1) to 7/5 (#2) mm preserved [leg. unknown], identified as Onchidiidae [unknown identifier], ( NMNH 805160 ) ; North Pacific Ocean, Gulf of California, Mexico, Sonora, Tiburon Island , Red Bluff Bay , 28 ◦ 45’ N, 112 ◦ 22’ W, 6 April 1934, four specimens 14/8 (#1) to 5/5 (#2) mm preserved [leg. F. Lewis], identified as Onchidium carpenteri [unknown identifier], ( NMNH 805170 ) ; North Pacific Ocean, Gulf of California, Mexico, Sonora, Puerto Penasco , 31 ◦ 20’ N, 113 ◦ 35’ W, 2 April 1966, one specimen ∼15/ 10 mm preserved [leg. P. Pickens], identified as Onchidella hildae [unknown identifier], ( NMNH 753654 ) [specimen in pieces, dissected prior to the present study, most internal organs missing; specimen is very likely a voucher of Marcus and Marcus (1967)]; Mexico, Baja California Norte [north], Gulf of California, Bahia San Francisquito , in inner bay, about halfway down its eastern side, 8 June 1973, 22 specimens 17/15 to 8/ 7 mm preserved [leg. A.J. Ferreira], identified as Onchidella hildae by A.J. Ferreira, ( CASIZ 010107 ) [four specimens dissected: 17/15 (#1), 12/11 (#4), 11/10 (#2), and 8/7 (#3) mm]; Mexico, Baja California Norte [north], Gulf of California, Puertecitos , 1957, eight specimens 15/10 to 8/ 5 mm preserved [leg. E.P. Chase], identified as Onchidella binneyi by A.G. Smith, ( CASIZ 078719 ) [two specimens dissected: 11/9 (#2) and 10/8 (#1) mm]; Mexico, Baja California Norte [north], Bahia de Las Animas , 23 December 1977, 32 specimens 11/9 to 9/ 7 mm preserved [leg. Baumback], identified as Onchidella by E. Naranjo-Garcia, ( CASIZ 080045 ) [three specimens dissected: 11/9 (#1), 11/9 (#3) and 10/8 (#2) mm]; Mexico, Baja California Norte [north], Gulf of California, Bahia de Los Angeles , 1 April 1940, four specimens 16/14 (#1) to 15/10 (#2) mm preserved [leg. E.F. Ricketts], identified as Hoffmannola lesliei by A.G. Smith, ( CASIZ 021492 ) ; North Pacific Ocean, Gulf of California, Mexico, Baja California, Cape Pulmo , 26 December 1966, one specimen ∼8/ 6 mm preserved [leg. P. Vreeland], identified as Onchidella hildae [unknown identifier], ( NMNH 753655 ) [specimen in pieces, dissected prior to the present study, most internal organs missing; this specimen is likely a voucher of Marcus and Marcus (1970)]; Mexico, Sinaloa [Pacific Coast], Mazatlan , 14 October 1975, four specimens 9/9 (#1) to 8/ 8 mm preserved [leg. D. Summers], identified as Onchidium sp. [unknown identifier], ( FMNH 195976 ) ; Mexico, Nayarit [Pacific Coast], Manzanilla, 10 miles north of Puerto Vallarta , March 1971, four specimens 11/4 (#1), 8/7 (#2), 8/8 (#3) and 6/ 6 mm preserved, leg. A.J. Ferreira, identified as Onchidella by A.J. Ferreira, ( CASIZ 006137 ) ; Mexico, Baja California Sur [south], Gulf of California , about four miles NE of La Paz, January 1959, 22 specimens 20/16 to 8/ 9 mm preserved [leg. A.G. Smith], identified as Onchidella binneyi [unknown identifier], ( CASIZ 078722 ) [four specimens dissected: 20/16 (#1), 12/11 (#2), 10/8 (#3), and 8/9 (#4) mm]; Mexico, Baja California Sur [south], Gulf of California, Isla Coronados , 5 November 1973, six specimens 7/5 (#1) to 4/4 (#2) mm preserved, leg. A.J. Ferreira, identified as Onchidella by A.G. Smith, ( CASIZ 078710 ) .

Description of new specimens

The description below is based on the non-type specimens examined and dissected as well as the type material, especially the six syntypes of O. hildae dissected for the present study.

External Morphology ( Figures 2 and 3 ). Background colour of dorsal notum of live animals brown to black-brown; papillae covering notum slightly lighter. In preserved animals, dorsal colour from homogeneously white to dark brownish grey. Hyponotum and pedal sole whitish tan both in live and preserved animals. Dorsal colour of preserved animals from tan to reddish brown or dark brownish grey. In most individuals, centre of notum lighter than its side.

Maximum size observed in preserved specimens 24 mm in length by 17 mm in width ( CASIZ 082076). All specimens outside Gulf of California less than 13 mm long, with the exception of a few specimens 16 mm long ( Colombia, ZMUC, no catalogue number). Smallest specimens 2 mm long. Body high, not flattened. Hyponotum horizontal. Dorsal notum oval, i.e. longer than wide. In most individuals, notum granular, covered by papillae of various sizes (usually all <1 mm high), more abundant on the side of the notum than in its centre (although papillae evenly distributed in some individuals). Generally, larger papillae surrounded by smaller ones. Size, number and distribution of the papillae on the notum likely affected by preservation. Margin of the notum not smooth, but characterized by warts of various sizes (<1.5 mm long). In some individuals, larger warts (locations with repugnatory glands) regularly separated by shorter ones (from three to nine). Distinguishing marginal warts based on their size not possible because most warts look similar in many individuals. Dorsal papillae with dorsal eyes absent. Dorsal gills absent.

In most individuals, left side of hyponotum, right side of hyponotum and pedal sole approximately same width: total width of the hyponotum (left and right sides) greater than pedal sole. Occasionally, total width of hyponotum same as that of pedal sole (e.g. 3/6/ 3 mm, NMNH 805160; 2/4/ 2 mm, CASIZ 021492; 2/4/ 2 mm, SMNH-type-957; 3/5/ 2 mm, NMNH 734256). On hyponotum, hyponotal line surrounds pedal sole and separates hyponotum into an inner area (close to the foot) and an outer area. Distance between hyponotal line and pedal sole from one fifth to one third of width of hyponotum (hyponotal line closer to pedal sole than to hyponotum margin) in specimens from Gulf of California. Outside Gulf of California, hyponotal line even closer to pedal sole (distance between hyponotal line and pedal sole from one sixth to one quarter of width of hyponotum). All openings within smooth area delimited by hyponotal line (pneumostome, male opening, eye tentacles).

Pedal sole surrounded by two grooves on left and right sides. However, left groove shallow. Peripodial groove present on right side, from posterior genital openings (female opening and anus) to opening of pedal gland in buccal area. Anus posterior, median, very close to pedal sole. Occasionally, however, slightly on right of median line (e.g. SMNH 7522, CASIZ 021492, CASIZ 021518). Posterior female genital opening very close to the anus. Position of pneumostome on hyponotum relative to notum margin and pedal sole varies among and within lots. In most individuals from Gulf of California, pneumostome at equal distance from pedal sole and notum margin; occasionally, pneumostome closer to pedal sole (e.g. CASIZ 75362, CASIZ 021492), although pneumostome sometimes closer to notum margin (e.g. CASIZ 0805170, CASIZ 021519). In specimens outside Gulf of California, position of pneumostome varies from close to pedal sole to about halfway between pedal sole and notum margin. Generally, pneumostome located slightly on right of median line, but, occasionally, median (e.g. NMNH 753656, CASIZ 021518, SMNH 957). In anterior region, head covered dorsally by notum. Head bears pair of retractile, ocular tentacles, with eyes at tip. In all preserved specimens, however, tentacles deeply retracted. Left and right oral lobes distinct, i.e. not fused medially, superior to mouth, but inferior to ocular tentacles. Opening of pedal gland median, inferior to mouth. Male genital opening on right lateral side of right oral lobe.

Marginal glands ( Figure 4 ). Marginal glands in body wall, around visceral cavity, and open in margin of notum. In most individuals, between seven and ten glands on each side. Glands about 1 mm in diameter. Adjacent glands separated by small gap (from 0.5 to 1.25 mm). Glands all on same frontal plane and single longitudinal row, although posterior glands slightly more ventral.

Digestive system ( Figures 4–6 ). Jaw-like structure present on the surface of oral tube. Thin, inconspicuous (between 300 and 500 µm long and less than 50 µm wide), whitish, and easily missed. Left and right salivary glands, heavily branched, join buccal mass dorsally, on either side of oesophagus. Radula in between two large posterolateral muscular masses. Radular maximum size 8/ 3 mm, when flattened. Each radular row with a rachidian tooth and two half rows of lateral teeth of similar size and shape (exception of first few innermost lateral teeth, smaller). Radular formulae vary a great deal among individuals ( Table 1). In specimens from Gulf of California, from 63 to 108 rows, and from 38 to 200 teeth per half row. In specimens from outside Gulf of California, from 42 to 80 rows, and from 29 to 112 teeth per half row. Larger specimens generally with radulae with more rows and more teeth per half row, but no strict correlation between size of specimens and radular formula. Rachidian tooth tricuspid: median cusp always present; two lateral cusps on two lateral branches of base of rachidian tooth, may be absent (especially in small rachidian teeth). Rachidian teeth tend to be smaller than lateral teeth: total length of base of rachidian tooth usually <50 µm, and median cusp usually <20 µm in length. Posterior-lateral aspect of base of rachidian teeth concave. Half rows of lateral teeth at an angle of approximately 45 ◦ to rachidian axis. Lateral teeth characterized by base, attached to radular membrane, with a dorsal, strong, flattened hook forming a 45 ◦ angle with radular membrane; triangular structure in between base and hook supports hook but does not reach its tip. In dorsal view, unless teeth misplaced, one can only see dorsal hooks: length of hook <80 µm but on average about 50 µm. Smaller (<20 µm) pointed cusp on outer, lateral expansion of base. In most cases, lateral cusp not observed on SEM picture because hidden below hook of adjacent, outer tooth; however, lateral cusps conspicuous when teeth are not too close (such as in innermost and outermost regions). With exception of, sometimes, first two to five innermost lateral teeth, size of lateral teeth even across half row, and among half rows. Shape of tip of hook from clearly truncate

of California; (C) buccal mass, nervous system, and male copulatory organ, ZMUC, no catalogue number #1, Colombia; (D) visceral cavity, dorsalview, syntype SMNH 957 #1, Ecuador; (E) stomach, dorsal view, CASIZ 021518 #4, Gulf of California. Scale bar: A, 250 µm; B, 3 mm; C, 1.3 mm; D, 2 mm; E, 1.3 mm. Abbreviations: au, auricle; bm, buccal mass; cr, crop; dd, deferent duct; dg, digestive gland; e, oesophagus; i, intestine; mgg, marginal gland; ps, penial sheath; rm, retractor muscle; rps, reproductive system; st, stomach; st1, stomach chamber #1; st2, stomach chamber #2; st3, stomach chamber #3; st4, stomach chamber #4; v, ventricle .

to clearly rounded; shape of tip of hook varies among individuals and between rows of same radula (e.g. hooks in oldest rows eroded, which give teeth an artificially different shape). Hooks not straight (slightly curved inward). Finally, although half rows at 45 ◦ angle with rachidian axis, hooks almost parallel to the rachidian axis.

Oesophagus narrow and straight at its proximal end but enlarged into wide crop before stomach. Oesophagus enters stomach anteriorly, close to connection of stomach with dorsal and lateral lobes of digestive gland. Only small portion of posterior aspect of stomach seen in dorsal view, because largely covered by three lobes of digestive gland: dorsal lobe mainly located on right aspect of visceral mass; left, lateral lobe mainly ventral; posterior lobe covers posterior aspect of visceral mass. Stomach U-shaped sac divided into three chambers: first chamber (receives oesophagus) delimited by thin layer of tissue, and receives ducts of dorsal and left lateral lobes of digestive gland; second chamber, posterior, delimited by thick muscular tissue and receives duct of posterior lobe of digestive gland; third chamber delimited by thin layer of tissue; in most individuals, third chamber funnel-shaped. Short pouch in proximal region of intestine, just distal to third chamber, regarded by some authors as fourth stomach chamber. No strong ridges found on internal surface of stomach. Intestine long, narrow, of type IV ( Labbé, 1934). No rectal gland.

Nervous system ( Figure 7 ). Central nervous system densely compact, often embedded and protected within layer of connective tissue. Circum-oesophageal nerve ring post-pharyngeal. Two cerebral ganglia not fused, separated by short commissure. Pleural and pedal ganglia distinct. Visceral ganglion not median, located slightly on left side of visceral loop. Cerebro-pleural and pleuro-pedal connectives very short: pleural, cerebral, and pedal ganglia touch each other. Nerves from cerebral ganglia innervate buccal area and ocular tentacles, and male anterior genital organs (penial complex) on right side. Nerves from pedal ganglia innervate foot. Nerves from pleural ganglia innervate lateral and dorsal regions of mantle. Nerves from visceral ganglia innervate visceral organs.

Pallial complex ( Figure 4 ). Heart enclosed in pericardium, in posterior half of right side of visceral cavity. Large, anterior ventricle becomes large aorta branching into smaller vessels delivering blood to visceral organs. Posterior auricle significantly smaller than the ventricle. Pericardium communicates through small hole with right portion of renal-pulmonary complex. Kidney intricately attached to pulmonary cavity and forms two symmetrical, left and right parts. Pulmonary cavity characterized by complex folds of internal lining (likely to increase tissue surface participating in gas exchange).

Reproductive system: posterior parts ( Figure 8 ). Hermaphroditic gland forms single mass subdivided into acini. Hermaphroditic duct, highly coiled, conveys gametes (eggs and autosperm) up to spermoviduct. Small branch of hermaphroditic duct goes directly to female gland mass. Another branch of hermaphroditic duct leads to small, coiled, finger-shaped pouch, the receptaculum seminis (= vesicula seminalis). From receptaculum seminis, duct goes back toward female gland mass. Latter includes mucous and albumen glands with ducts that open near where hermaphroditic duct becomes spermoviduct. Proximally, spermoviduct embedded within the female gland mass and not divided externally. Prostate not distinct externally, may be located within walls of the spermoviduct or vas deferens. Distally, male and female ducts separate: vas deferens conveys autosperm up to cephalic region; free oviduct conveys eggs up to female opening and exosperm from female opening up to fertilization chamber, near proximal end of spermoviduct. Distally, oviduct becomes vagina. Spherical spermatheca (which stores exosperm) connects to distal region of oviduct through short duct. Accessory vaginal gland (long and highly coiled to short and straight) opens into distal portion of the oviduct.

Reproductive system: male, anterior parts ( Figures 9 and 10 ). Male anterior organs only include penial complex (penial sheath, deferent duct, retractor muscle) because accessory penial gland absent. No distinct penis inside penial sheath. No conspicuous, solid papilla at distal end of deferens duct. Penial sheath not covered internally by folds. In most individuals, diameter of penial sheath about 500 µm. Exceptionally, in large specimens (> 20 mm long) from Gulf of California, diameter of penial sheath up to 2 mm. Length of penial sheath depends on sexual maturity and size of individual. In most specimens, penial sheath less than 2 mm long. In immature specimens or even specimens not fully mature, penial sheath usually not longer than buccal mass, although, in some cases, almost as long as visceral cavity: penial sheath 1.5 mm in length in 2.5 mm-long specimen from Ecuador ( NMNH 706696, #2). However, in largest specimens from Gulf of California (e.g. NMNH 753656 #1) or Colombia (e.g. ZMUC, #1) penial sheath up to twice as long as buccal mass and up to 8 mm long.

(Continued)

Caecum , digitiform pouch, joins penial sheath laterally. Caecum straight or curved (varies within lots). Filled by fewer than 10 small concretions that could be seen due to transparency of caecum. Function of concretions unknown. Caecum usually present and occasionally absent (but often absent in specimens from Panama). Presence /absence of caecum varied within and among lots, and not strictly correlated with sexual maturity: for instance, caecum found in male organs of two immature (no posterior female organs) specimens from Gulf of California ( CASIZ 021518 #2 and #3), but caecum absent from fully mature specimen (#4) from same lot. In Panama, most specimens dissected lacked caecum, although it was occasionally present ( NMNH 733882 ). In specimens from Panama lacking caecum, concretions could be seen within lumen of penial sheath, by transparency .

Deferent duct straight to loosely convoluted (up to five loops) from where it enters visceral cavity to where it joins penial sheath. Number of loops varied among individuals, even within same lot. Deferent duct with fewer loops in small but mature specimens (with all female organs developed). Immature specimens (with no or poorly-developed female organs) have short, straight deferent duct. Exceptionally, deferent duct found extremely convoluted, but only in two specimens from two different lots while regular deferent duct found in all other specimens from same lots ( NMNH 734256 #2, Panama; NMNH 706696 #1, Ecuador). Variation regarding deferent duct observed consistently within each geographical area represented in samples. However, deferent duct, straight, nearly straight, or with just one or two loose loops in specimens from Panama. Diameter of deferent duct more or less constant along its whole length, about 200 µm maximum .

Retractor muscle anchors on penial sheath near where deferent duct enters penial sheath and inserts at end of second posterior third of floor of visceral cavity. In small, immature specimens with small penial sheath, retractor muscle can be quite weak, even occasionally absent (e.g. NMNH 733425, Panama).

Discussion

A synonymy between O. binneyi (type locality: Gulf of Mexico) and O. hildae (type localities: Ecuador and Panama) has never been proposed, mainly because few specimens from few localities have been studied and compared so far. All descriptions of O. binneyi (as O. carpenteri or O. binneyi ) by Stearns (1879, 1894), Semper (1885) and Binney (1890) were based on the material collected by W.J. Fisher in the Gulf of California: Stearns (1894) mentioned he examined “several examples” (only two syntypes are now held at the NMNH) from three localities from the Gulf of California; Semper (1885) mentioned 17 individuals from one locality (Las Animas Bay); and Binney (1890) did not give any specific information on the material he studied, but he did receive it from W.J. Fisher (see Stearns 1894). As for O. hildae, Hoffmann had access to the 40 type specimens, but he only dissected four of them: two from Ecuador and two from Panama. Watson (1925) and Labbé (1934) did not study any new material. Finally, Eveline and Ernst Marcus redescribed O. hildae and O. binneyi based on 15 specimens from three localities: they identified seven specimens as O. binneyi and one specimen as O. hildae from Puerto Penasco, Gulf of California ( Marcus and Marcus 1967); they also identified seven other specimens as O. hildae from two other localities from the Gulf of California ( Marcus and Marcus 1970). Vouchers are available for some of the material studied by Marcus and Marcus, but those were entirely dissected and are now largely destroyed ( NMNH 753652, 753654, and 753655). It is important to emphasize that Marcus and Marcus only examined material from the Gulf of California, i.e. they did not examine material of O. hildae from Panama or Ecuador. Before Marcus and Marcus (1967, 1970), it was thought that O. hildae was restricted to Panama and Ecuador, and O. binneyi was restricted to the Gulf of California. Marcus and Marcus (1967, 1970) thought that both species were found in the Gulf of California.

The abundant material studied here offers for the first time the opportunity to address individual variation of important taxonomic characters, including in relation to geography. Indeed, a total of 319 non-type specimens were examined (68 of which were dissected), collected from 33 localities from six different countries ( Ecuador, Colombia, Panama, Costa Rica, Nicaragua, Mexico), from 2.3 ◦ S’ on the Pacific coast of Ecuador to the northern end of the Gulf of California. All type material available was also examined: two syntypes of O. binneyi from the Gulf of California (not dissected here); 41 syntypes of O. hildae from Ecuador and Panama (four specimens from Ecuador and two from Panama dissected here) .

According to Hoffmann (1928), the main difference between O. binneyi and O. hildae was the shape of the penial caecum: curved and straight, respectively. After Hoffmann, the differences between O. binneyi and O. hildae were only discussed by Marcus and Marcus (1967, 1970) who added the following differences: course of the deferent duct in the body cavity (runs straight from the body wall to the penial sheath in O. binneyi ; forms a free spiral in O. hildae ); size of the vaginal gland (very long and coiled in O. binneyi ; short and blunt in O. hildae ); width of the pedal sole relative to the hyponotum (narrow in O. hildae ); maximum size of the smallest papillae (60 µm in O. binneyi ; 200 µm in O. hildae ); position of the hyponotal line (very close to the foot in O. hildae ).

However, observations made by Marcus and Marcus were also based on few specimens dissected from few localities. Our present data show that the individual variation is much higher than expected and that it is not possible to find discrete differences between two groups of populations or individuals. The penial caecum is not either curved or straight, but its shape (which is likely affected by preservation) varies from curved to straight. The number of loops, the arrangement and the length of the deferent duct vary from straight and short with no loop, to highly convoluted and long. The size of the vaginal gland varies from short and slightly curved to long and highly convoluted. The width of the pedal sole may be greater than, equal to, or less than the width of the hyponotum. The size of the dorsal papillae varies a great deal (from ∼ 40 µm up to 1 mm) within the same individual. Finally, the position of the hyponotal line varies from one sixth to one third closer to the foot than the notal margin. More importantly, beyond their variation, those features are not combined in two distinct sets: a specimen can have a short and blunt vaginal gland (supposedly diagnostic of O. hildae ) and a curved penial caecum (supposedly diagnostic of O. binneyi ). Finally, all the specimens of O. binneyi and O. hildae seem to share a diagnostic feature that is not found in other species from the north-eastern Pacific: the presence of a penial caecum hosting some concretions; in most specimens in which the caecum is lacking, the concretions are found in the penial sheath itself.

As a result, O. binneyi and O. hildae are regarded as two synonyms. Although only one species of Onchidella is thought to inhabit the eastern Pacific coasts from Ecuador to the Gulf of California (excluding the Galapagos), there are some variation patterns which suggest that there might be more than one species. For instance, large specimens (> 20 mm) are common in the Gulf of California, whereas the vast majority of the specimens outside the Gulf of California measure less than 13 mm long. Also, a penial caecum is only exceptionally found in specimens from Panama, whereas it is exceptionally missing in specimens from the Gulf of California. Thus, it is possible that cryptic species might be found in the future. At this stage however, given the data available, all the specimens studied here are regarded as part of one variable species.

The fact that binneyi belongs to Onchidella has never been challenged. Semper classified binneyi in Onchidium , but he did not consider the genus Onchidella to be a valid genus and classified all Onchidella in Onchidium .

Pepe and Pepe (1985) showed that the activities of O. binneyi are synchronous with the tides. Also, O. binneyi has been studied for its pharmacology ( Abramson et al. 1989).

Figures

Figure 2. External morphology of Onchidella binneyi: (A) ventral surface, syntype SMNH 957 #1, Ecuador; (B) ventral surface, CASIZ 082076 #3, Gulf of California; (C) ventral surface, NMNH 753656 #1, Gulf of California; (D) dorsal and marginal papillae, CASIZ 082076 #3, Gulf of California; (E) dorsal and marginal papillae, syntype SMNH 7521 #1, Panama. Scale bar: A, 4.6 mm; B, 6 mm; C, 6 mm; D, 3 mm; E, 5 mm. Abbreviations: a, anus; fo, female opening; hl, hyponotal line; mo, male opening; ol, oral lobe; pn, pneumostome; ppg, peripodial groove.

Figure 3. External morphology of Onchidella binneyi: (A) posterior hyponotum and pedal sole, CASIZ 082076 #3, Gulf of California; (B–C) papillae on dorsal notum, ZMUC, no catalogue number #1, Colombia. Scale bars: A, 1 mm; B, 0.5 mm; C, 0.2 mm. Abbreviations: a, anus; fo, female opening; hl, hyponotal line; ppg, peripodal groove.

Figure 4. Visceral cavity and digestive system of Onchidella binneyi: (A) jaw-like structure, NMNH 753656 #2, Gulf of California; (B) visceral mass, dorsal view, NMNH 805160 #1, Gulf

Figure 5. Radular teeth of Onchidella binneyi, Gulf of California: (A) entire radula, CASIZ 010107 #1; (B) left half rows, CASIZ 010107 #1; (C) rachidian and innermost lateral teeth, CASIZ 010107 #1; (D) lateral teeth, CASIZ 010107 #1; (E) rachidian and right innermost lateral teeth, CASIZ 078722 #4; (F) rachidian and innermost lateral teeth, CASIZ 078719 #1. Scale bars: A, 1 mm; B, 250 µm; C, 25 µm; D, 25 µm; E, 20 µm; F, 25 µm.

Figure 6. Radular teeth of Onchidella binneyi: (A) left half rows, CASIZ 006137 #2, Pacific Coast of Mexico; (B) rachidian and right innermost lateral teeth, CASIZ 006137 #2, Pacific Coast of Mexico; (C) rachidian and innermost lateral teeth, syntype SMNH 7521 #2, Panama; (D) rachidian and innermost lateral teeth, syntype SMNH 7521 #1, Panama, arrows indicate small pointed cusp on outer, lateral expansion of base of rachidian and lateral teeth (most cusps cannot be seen because covered by hooks). Scale bars: A, 50 µm; B, 25 µm; C, 50 µm; D, 25 µm.

Figure 7. Nervous system of Onchidella binneyi: (A) dorsal, posterior view, syntype SMNH 957 #1, Ecuador; (B) dorsal view, NMNH 733240 #1, Panama. Scale bar: A, 1 mm; B, 0.7 mm. Abbreviations: lc, left cerebral ganglion; lpd, left pedal ganglion; lpl, left pleural ganglion; vs, visceral ganglion.

Figure 8. Posterior genital (female) organs of Onchidella binneyi: (A) NMNH 753652 #1, Gulf of California; (B) ZMUC, no catalogue number #1, Colombia; (C) CASIZ 021518 #1, Gulf of California. Scale bar: A, 1 mm; B, 1.6 mm; C, 1.6 mm. Abbreviations: dd, deferent duct; fgm, female gland mass; hd, hermaphroditic duct; hg, hermaphroditic gland; ov, oviduct; rs, receptaculum seminis; sp, spermatheca; spv, spermoviduct; vg, vaginal gland.

Figure 9. Anterior genital (male) organs of Onchidella binneyi, Gulf of California: (A) CASIZ 082076 #1, mature; (B) FMNH 195976 #1, mature; (C) NMNH 805160 #2, immature; (D) CASIZ 021518 #4, mature; (E) CASIZ 078724 #1, mature; (F) CASIZ 078710 #1, mature; (G) CASIZ 078721 #1, mature; (H) CASIZ 021518 #2, immature; (I) CASIZ 006137 #3, not fully mature; (J) CASIZ 082076 #3, mature. Scale bar: A, 2 mm; B, 1 mm; C, 1 mm; D, 1 mm; E, 2 mm; F, 0.8 mm; G, 3 mm; H, 0.4 mm; I, 0.7 mm; J, 4 mm. Abbreviations: c, caecum; dd, deferent duct; ps, penial sheath; rm, retractor muscle.

Figure 10. Anterior genital (male) organs of Onchidella binneyi: (A) NMNH 734256 #2, Panama, mature; (B) ANSP A9852 #1, Costa Rica, mature; (C) CASIZ 001445, Nicaragua, mature; (D) NMNH 733425, Panama, mature; (E) NMNH 706696 #2, Ecuador, immature; (F) NMNH 733882 #1, Panama, mature; (G) syntype, SMNH 957 #2, Ecuador, not fully mature; (H) syntype, SMNH 7521 #1, Panama, mature. Scale bar: A, 0.5 mm; B, 0.5 mm; C, 0.4 mm; D, 0.5 mm; E, 0.5 mm; F, 0.5 mm; G, 1 mm; H, 2.2 mm. Abbreviations: c, caecum; co, concretions; dd, deferent duct; ps, penial sheath; rm, retractor muscle.