Locomotion, pedal retraction and extension, and the hydraulic systems of Bullia (Gastropoda: Nassaridae)

Abstract

Surface locomotion and burrowing by Bullia digitalis have been analysed by use of ciné film and electronic recording. Both movements are shown to be carried out by a series of steps in which the propodium is first extended whilst the snail is anchored by the posterior of the foot (penetration anchor) and, when buried, also by the shell; secondly the shell is drawn forwards and downwards towards the anchored propodium (terminal anchor). The extremely flattened foot of this snail contains a greatly enlarged pedal sinus containing blood and functions as a hydraulic organ. This contrasts with the foot of most gastropods, e.g. Patella, which crawl over hard surfaces and have no large fluid filled pedal cavity. During each step, or digging cycle, there are two pressure pulses, one effecting propodial extension, the second occurring as the shell is drawn forwards. The pedal haemocoel is isolated from the remainder of the circulation for at least part of the locomotory cycle so enabling the foot to function as a fluid‐muscle system at constant volume. Bullia exhibits convergence with burrowing bivalve molluscs having a similar pattern of alternating anchorages in sand and in both water is ejected from the mantle cavity to liquefy the sand in front of the shell. The energy cost of burrowing by B. digitalis is estimated to be 6.6 times 10‐6 J/mg dry tissue weight, a figure comparable to that of the clam Donax provided that burial occurs at a similar rate. By contrast the energy requirement for Bullia to move over the surface of sand is about one tenth of that for burial. Pedal extension involves both blood flow, so that the foot may function as a hydraulic system, and direct muscular antagonism between the fibres of a three dimensional muscle network in the opercular muscle. When the snail is extended the shell contains some sea‐water which plays a dynamic role in pedal expansion and retraction independently of the pedal blood sinus. The possible role of this cavity in other prosobranchs is discussed.

Shell features associated with the sand-burying habit in gastropods

“…Unlike most of the other sand-burying gastropods considered here, nassariids have a large, powerful foot, enabling them to bury rapidly (Trueman & Brown, 1976, 1992aVermeij & Zipser, 1986;Savazzi, 1989Savazzi, , 1994Trueman & Hodgson, 1990). In keeping with the trade-off between foot size and streamlining, most nassariids are less streamlined than most sand-buriers in the other clades examined (Fig.…”

PALAEOBIOLOGY OF THE CLIMACTICHNITES TRACEMAKER

“…16). Bullia digitalis, Bullia rhodostoma , Hydrobia ulvae , Littorina littorea , Lunatia heros and Polinices duplicatus produce trails with lateral ridges and transverse bars (Raymond 1922; Abel 1935; Häntzschel 1938; Gräff 1956; Brown 1971; Schäfer 1972; Trueman and Brown 1976; Knox and Miller 1985).…”

The mechanism of shell elevation in Haliotis (Mollusca: Gastropoda) and a consideration of the evolution of the hydrostatic skeleton in Mollusca

“…The absence of any fluid-filled cavities in these sections suggests that antagonism occurs directly between sets of muscle fibres, as in other muscular antagonistic systems, e.g. the columellar muscle of Bullia (Trueman & Brown, 1976) and of other gastropods (Brown & Trueman, 1982).…”

“…Examination of sections of the columellar muscle of the latter species showed that the muscle consisted of a three dimensional network of closely associated fibres, in which the principal or retractor fibres had their long axes parallel to the length of the muscle, while the others were arranged transversely to this ( Fig. 5(c)) (Trueman & Brown, 1976). Contraction of these latter fibres compresses the longitudinal fibres and so brings about their extension.…”

“…Huliotis midae L. was particularly suitable for this investigation since a shadow or change in light intensity elicits the 'shadow withdrawal reflex' (Crofts, 1929), and the conveniently wide conical shell, together with the availability of specimens of 10-15 cm shell length near to Cape Town, facilitated experimental work. Few studies have been made of the pressures generated within gastropods, except for those directly concerned with the circulation of the blood (Bourne & Redmond, 1977a, b;Jones, 1983), the respiratory movements and extrusion of Helix from its shell (Dale, 1973(Dale, , 1974, the fluid skeleton in terrestrial and aquatic pulmonates (Jones, 1978) and locomotion and pedal extension in the nassarid Bullia digitalis (Trueman & Brown, 1976;Brown, 1982). Examination of sections of the columellar muscle of the latter species showed that the muscle consisted of a three dimensional network of closely associated fibres, in which the principal or retractor fibres had their long axes parallel to the length of the muscle, while the others were arranged transversely to this ( Fig.…”