Comparative Morphology of Dorsanum miran and Bullia granulosa from Morocco (Mollusca: Caenogastropoda: Nassariidae) (original) (raw)

INTRODUCTION

This paper is part of a project reviewing the South American species usually included in the region's nassariid genus Buccinanops d'Orbigny, 1841. Since the original description, the species of Buccinanops have been included in several different genera (Pastorino 1993). Two of the most used, Dorsanum Gray, 1847 and Bulli a Gray, 1834 (in Griffith & Pidgeon 1834), both originally described from Africa, have some taxonomic problems associated with them and they are poorly defined at the anatomical level. The most recent and comprehensive revisions of these genera were published more than two decades ago. Adam and Knudsen (1984) regarded Dorsanum as a junior synonym of Bullia. Allmon (1990) considered Dorsanum to be valid, but restricted to the type species only, i.e., D. miran (Bruguière, 1789). In that paper, he introduced the subfamily Bulliinae to include Bullia, with Buccinanops as a subgenus, and Dorsanum. Pastorino (1993) re-established the full generic status of Buccinanops for all South American species, but a more complete discussion on the genera Bullia and Dorsanum is still wanting. Only a few papers (e.g. Simone 1996, 2011) describe the anatomy of soft parts of these taxa and all of those descriptions have been restricted so far to South American species.

These three genera were included by Brown (1982) in what he called the “Bullia group”. Later, Allmon (1990) extended this informal group, as Bulliinae, to fossil species, mostly from North America. He defined three subfamilies in Nassariidae: Nassariinae, Dorsaninae and Bulliinae. He included in Bulliinae a set of nassariids of relatively large size, having thin-walled shells, and confined to temperate and subtropical waters in the mid and south Atlantic and Indian Oceans. Dorsaninae is restricted to Dorsanum, while the genera Bullia (from Africa) and Buccinanops (from South America) comprise the Bulliinae. Despite these definitions, the differences amongst the subfamilies remain somewhat unclear. It is quite possible that additional information on their representatives, in terms of anatomy, could bring new insights, as the shell characters so far invoked have been insufficient to define the subfamilies and are not applicable to all included species.

As regards this scenario, the present paper deals with two species from the western coast of Africa: Dorsanum miran, type species of Dorsanum, and Bullia granulosa (Lamarck, 1822). Both are formally redescribed, including consideration of previously neglected anatomical aspects. Provision of the new information explored here has the target of laying a better foundation for future discussions and analysis concerning monophyly, and the phylogenetic and taxonomic allocation of the “Bullia group” (Brown 1982) and the Bulliinae/Dorsaninae (Allmon 1990), as well as the included genera Bullia, Dorsanum and Buccinanops. However, the present paper is almost purely descriptive, with discussion limited to data published so far.

MATERIAL AND METHODS

Most of the material is from the Muséum national d'Histoire naturelle, Paris (MNHN); and some other comparative specimens are housed at the Muséum d'histoire naturelle de la Ville de Genève (MHNG), Academy of Natural Sciences of Drexel University, Philadelphia (ANSP) and the United States National Museum of Natural History, Smithsonian Institution, Washington, DC (USNM). The specimens had been fixed in 70% ethanol. One female of D. miran was examined after the shell had been broken in order to complete the extraction of soft parts. In the remaining specimens, extraction was carried out by pulling tissue with forceps to obtain only the soft parts from the last whorl. Study of the visceral mass was precluded. The specimens were dissected by standard techniques under a stereo-microscope while immersed in ethanol. All drawings were made with the aid of a camera lucida. Scanning electron microscopy under a Phillips XL 30 was used to study the radulae, with the usual coating, at the Laboratorio de Microscopia Eletrônica, Museu de Zoologia da USP, and Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” (MACN). For the main terminology, including that relating to odontophore muscles, see Simone (2011).

In the figures, the following abbreviations are used: aa, anterior aorta; ad, adrectal sinus; af, afferent gill vessel; ag, albumen gland; an, anus; ao, posterior aorta; au, auricle; bc, bursa copulatrix; bg, buccal ganglion; br, subradular membrane; bs, buccal sphincter; ce, cerebral-pleural ganglia; eg, capsule gland; cm, columellar muscle; cv, ctenidial vein; dd, duct to digestive gland; df, dorsal fold of buccal mass; dg, digestive gland; di, diaphragmatic membrane separating haemocoel from visceral cavity; ea, anterior oesophagus; ef, oesophageal folds; em, middle oesophagus; ep, posterior oesophagus; es, oesophagus; et, metapodial tentacles; ey, eye; fp, female pore; fs, foot sole; ft, foot; ga, aperture of gland of Leiblein; gc, cement gland; gi, gill or gill filament; gl, gland of Leiblein; ha, haemocoel; he, head; hg, hypobranchial gland; in, intestine; ki, kidney; kl, dorsal lobe of kidney; m1–m14, extrinsic and intrinsic odontophore muscles; ma, longitudinal muscle of odontophore; mb, mantle border; mc, circular muscles of odontophore; mf, muscle fibres; mo, mouth; ne, nephrostome; ng, nephridial gland; nr, nerve ring; nv, nerve; oa, opercular pad; oc, odontophore cartilage; od, odontophore; oo, odontophore tube connecting to oral tube; op, operculum; os, osphradium; ot, oral tube; oy, ovary; pb, proboscis; pc, pericardium; pd, penis duct; pe, penis; pg, anterior furrow of pedal glands; ph, penis terminal or preputial chamber; pp, penis papilla; pt, prostate; pu, pedal ganglion; py, palliai cavity; ra, radula; rh, rhynchostome; rm, retractor muscle of proboscis; rn, radular nucleus; rs, radular sac; rt, rectum; sa, salivary gland aperture at oral tube; sc, subradular cartilage; sd, salivary duct; sf, siphonal basal flap; sg, salivary gland; si, siphon; st, stomach; su, suboesophageal ganglion; sy, statocyst; te cephalic tentacle; tg, integument; tm, transverse muscles between oesophagus and odontophore; vc, cilia of valve of Leiblein; vd, vas deferens; ve, ventricle ; vl, valve of Leiblein; vo, visceral oviduct.

TAXONOMY

Genus Dorsanum Gray, 1847

Type species Buccinum politum Lamarck, 1822 (non Röding, 1798) = Buccinum miran Bruguière, 1789, by original designation.

Dorsanum miran (Bruguière, 1789)

Figs 1–8, 16, 17, 21–42

Figs 1–20.

SEM of shells, opercula and radulae: (1–8) Dorsanum miran; (1) shell, apertural view (length 22.9 mm); (2) right view; (3) dorsal view; (4) apical, slightly apertural view, broken shell showing columellar fold; (5) apertural view, detail of last whorl; (6) outer SEM view of operculum (4.0 × 3.0 mm); (7) operculum of shell in Fig. 1, inner (upper) and outer views (3.8 × 3.5 mm); (8) detail of extracted protoconch, profile; (9–15_) Bullia granulosa_; (9) shell, apertural view (length 29.4 mm); (10) right view; (11) dorsal view; (12) apertural view, detail of last whorl; (13) detail of shell apex in profile; (14) operculum, outer view (4.7 × 3.4 mm); (15) same, inner view; (16–17) D. miran radula, scale bar =100 µm; (18–20)5. granulosa radula; (18) wide view, scale bar = 100 µm; (19) detail of lateral teeth, scale bar = 50 µm; (20) detail of rachidian teeth, scale bar = 50 µm.

f01_125.jpg

Figs 21–26.

Dorsanum miran anatomy: (21) head-foot, female, anterior view, specimen with extended proboscis; (22) same, foot sole, ventral view; (23) same, longitudinal section through median line; (24) same, dorsal whole view; (25) head, ventral view, foot extracted; (26) palliai cavity roof, transverse section at mid-level of osphradium. Scale bars = 2 mm.

f21_125.jpg

Figs 27–31.

Dorsanum miran anatomy: (27) detail of anterior end of palliai oviduct, ventral view, partially sectioned longitudinally; (28) palliai cavity roof and adjacent region of visceral mass, inner ventral view, ventral wall of pericardium removed, transverse section of palliai oviduct also shown; (29) foregut, right view, topology of nerve ring also shown; (30) head and haemocoel, ventral view, foot removed, proboscis opened longitudinally; (31) buccal mass, detail of its anterior end opened longitudinally, odontophore partially deflected. Scale bars = 2 mm.

f27_125.jpg

Figs 32–34.

Dorsanum miran odontophore: (32) whole dorsal view, superficial membranes removed; (33) same, ventral view; (34) dorsal muscles mc and ma sectioned longitudinally and deflected, some narrow muscles also deflected and some sectioned transversely. Scale bars = 1 mm.

f32_125.jpg

Figs 35–39.

Dorsanum miran anatomy: (35) odontophore cartilages and adjacent part of intrinsic muscles, showing their origins, dorsal view; (36) right side of palliai cavity, male, ventral view; (37) penis in situ, deflected upwards, dorsal view, inner structures revealed by artificial translucence; (38) head and uncoiled penis, dorsal view, adjacent region of penis base also shown; (39) penis, dorsal view, detail of its apical region, inner structures revealed by artificial translucence. Scale bars = 1 mm.

f35_125.jpg

Figs 40–42.

Dorsanum miran anatomy: (40) last whorl of visceral mass, ventral view, stomach seen in situ, renal region also shown; (41) nerve ring, dorsal view, oesophageal passage indicated by arrows; (42) same, ventral view. Scale bars = 1 mm.

f40_125.jpg

Genus Bullia Gray in Griffith & Pidgeon, 1834

Type species Bullia semiplicata Gray, 1834 = B. callosa (Wood, 1828), by original designation.

Bullia granulosa (Lamarck, 1822)

Figs 9–15, 18–20, 43–55

Figs 43–48.

Bullia granulosa anatomy: (43) head-foot, female, right view; (44) head and haemocoel, ventral view, foot and columellar muscles removed; (45) palliai cavity roof, transverse section in mid-level of osphradium; (46) same, whole ventral view, transverse section in palliai oviduct artificially done, adjacent portion of visceral structures also shown; (47) foregut, ventral view, topology of some adjacent structures shown; (48) same, right view, proboscis and odontophore extracted. Scale bars = 2 mm.

f43_125.jpg

Figs 49–53.

Bullia granulosa foregut anatomy: (49) buccal mass, right view, odontophore partially removed and deflected to the right, buccal cavity and oesophagus partially sectioned longitudinally, topology of transverse muscles also shown; (50) odontophore, ventral view, superficial layer of membrane and muscles removed and shown partially deflected to the right, radula still in situ, (51) region of mid-oesophagus sectioned longitudinally to show inner surface; (52) odontophore, dorsal view, outer layer of membrane and muscles removed, cartilages also deflected, some muscles on right side with portions artificially sectioned; (53) odontophore cartilages and some adjacent portions of intrinsic muscles, dorsal view. Scale bars = 1 mm.

f49_125.jpg

Figs 54–55.

Bullia granulosa anatomy of nerve ring, topology of oesophagus indicated by arrows: (54) dorsal view; (55) ventral view. Scale bar = 1 mm.

f54_125.jpg

DISCUSSION

Although there is no doubt about the validity of both species, the shells of Dorsanum miran and Bullia granulosa are so similar that they are commonly found together in the same lot in collections, as if the shells are those of a single species. Only after more detailed study of both shells and anatomy did the specific and even generic distinctions become apparent. The main shell differences include the apex, which is more sharply pointed in D. miran than in B. granulosa (compare Figs 1–3 with 9–11). The sculpture is also different in that D. miran has some broad nodulation in the first teleoconch whorl (Figs 1–3), whereas B. granulosa has a delicate pair of sub sutural nodes extending all along the whorls (Figs 9–11). The sculpture of the region to the left of the aperture is also dissimilar, as D. miran has only a single pair of broad folds (Fig. 5), and B. granulosa has 7–8 delicate ones (Fig. 12). The protuberance in the canal's left base, almost a tooth, is well-developed in D. miran (Fig. 5) but weaker in B. granulosa (Fig. 12); it is at the end of the columellar fold (Fig. 4) in the former, a feature that was not confirmed for the latter because the shell could not be broken.

The main anatomical differences and similarities were incorporated into the distinctive description of B. granulosa. The absence of eyes in B. granulosa (Figs 43, 44) clearly separates this species from D. miran, where the eyes are very characteristic (Figs 24, 25). The fold of the siphonal base separating the anterior end of the osphradium from the gill in B. granulosa (Fig. 46: sf) is taller than in D. miran (Fig. 28). The gill and osphradium filaments are much larger in D. miran (Fig. 26) than in B. granulosa (Fig. 45). The transverse musculature of the haemocoel is much more developed in B. granulosa than in D. miran in the ventral rhynchodeal wall (Fig. 47: mf) and between the oesophagus and odontophore (Fig. 49: tm). As regards odontophore muscles, the multiplicity of m2b that creates the pair m2d (Fig. 52) in B. granulosa is the main distinctive feature, this muscle being much simpler in D. miran. That aside, the pair m9a of B. granulosa are enlarged (Fig. 52). All these features indicate that B. granulosa has stronger odontophore musculature than D. miran. The extent of fusion between both odontophore cartilages is greater in B. granulosa (Fig. 53) than in D. miran (Fig. 35). Moreover, the anterior oesophagus and valve of Leiblein of B. granulosa are proportionally broader in B. granulosa (Fig. 48) than in D. miran (Fig. 29). Both species have in common a somewhat reduced gland of Leiblein. However, that of B. granulosa is elongated and filiform (Fig. 48: gl) as compared with the “usual” form exhibited by D. miran (Fig. 29). Related to the nerve ring, B. granulosa has the cerebral and buccal commissures longer than those of D. miran (Figs 42, 55), but both are very concentrated as in all buccinoid nerve rings (Bailey 1966).

The marked conchological similarity between D. miran and B. granulosa has been pointed out in the literature. Allmon (1990: 28, 29) invoked anatomical studies to resolve the taxonomy. In fact, several characters allow the specific and even generic distinctions to be made, as reflected above. However, knowledge based on additional species is necessary for a more complete taxonomical evaluation. Despite B. granulosa having been used here as representative of the genus Bullia, it is important to emphasize that the type species, B. callosa, still needs to be studied. Generic inferences can then be made in the light of such an assessment.

Allmon (1990) erected the subfamily Bulliinae in his revision of the so called “Bullia group”, for which he studied mostly fossil representatives from North America. He mentioned the uncertain generic position of B. granulosa and several other genera. In his diagnosis of the subfamily, he included mainly shell characters, comparing Bulliinae with Dorsaninae and Nassariinae. Whereas those characters are clear when representatives of the Nassariinae are compared, they are not easy to see in Dorsaninae. He mentioned as main shell differences in Bulliinae the lack of a recurved siphonal channel with a carina on the dorsal side of the fasciole, and the reduced ornamentation.

The diagnostic features are the large size for a nassariid, considering that some species attain a shell length of 100 mm, such as Buccinanops cochlidium (Dillwyn, 1817), while the typical nassariid is approximately 10 mm. The absence of a well-developed callus is another exclusivity, this structure being particularly robust in most nassariids. The callus and a more developed sculpture of the typical nassariids generate a thicker shell wall. The lack of or reduction in these features produces the thinner shell typical of the Bullia group. In general, the shells of the species so far included in the Bullia group resemble those of the Buccinidae more closely than shells of nassariids.

In regard to anatomy, the tendency for the gland of Leiblein to be reduced and the simplification of the female palliai oviduct are noteworthy attributes in comparison with the situation in other buccinoideans (Fretter 1942; Haasl 2000; Kantor & Harasewych 2008; Kosyan et al. 2009). The nassariid nature of the Bullia group species comes from the socket-like head and the metapodial tentacles, which are paired in both examined species, but single in Buccinanops (Simone 1996). The term “socket-like” for the head was coined by Marcus and Marcus (1962), and means a head that protrudes in a form that resembles an electric socket, in which the tentacles are the pins.

The nerve rings of both species are closely similar (Figs 41, 42, 54, 55), highly concentrated in such a way that the pleural and cerebral ganglia cannot be distinguished from each other. This is an accepted feature for a neogastropod (Fretter 1942). However, the cerebral commissure is somewhat long in both species studied. The concentration of ganglia and the closure of the buccal ganglia has been referred to for another allied species, Bullia digitalis (Dillwyn, 1817) (Brown 1982, figs 16A, B), as well as the protuberances on opposite sides of the buccal ganglia (Figs 42, 54), which have been termed the sub and supra-intestinal ganglion, respectively (Brown 1982). They are not so distinct in the presently studied species, however. Conversely, the elongated suboesophageal ganglion close to the nerve ring, present in both species (Figs 41, 54: su), is not shown by Brown (1982) for B. digitalis.

An interesting feature is the absence of eyes, which is typical for Buccinanops. This trait is shared with B. granulosa, but not with D. miran, which has well-developed eyes (Fig. 25). On the other hand, the reduced gland of Leiblein of the anatomically known Buccinanops resembles more closely that of D. miran.

The elongated odontophore of both examined species is typical for buccinoideans (Wilsmann 1942; Simone 1996, 2011), including the main features of the muscles and cartilages. The degree of cartilage fusion and the length of the horizontal muscles (m6) are, by contrast, smaller in both examined species (Figs 35, 53). The pair or pairs of protractor muscles of the radula, here called m9, is so far another exclusivity, but a more detailed assessment of these and other odontophore characters will be needed in the future, in comparison with Buccinanops.

B. granulosa has previously been assigned to the genus Dorsanum, more precisely the sub genus Fluviodorsum Boettger, 1885 (Cernohorsky 1984). However, since no character fully agrees with that classification, we have kept the species in the genus Bullia, following most previous authors.

Although the original intention was to improve upon the definition of nassariid subfamilies, as set out by Allmon (1990), by providing anatomical details, is it still unclear whether the differences outlined above have validity as distinguishing characters at the specific, generic or subfamilial level. Discussion in this regard is accordingly postponed to a time when the anatomy of more species has become better known. A phylogenetic analysis will then be feasible; and this will be the next step in this ongoing investigation.