^/
MALACOLOGIA, 1980, 20(1): 117-142
OBSERVATIONS ON THE ANATOMY AND LIFE HISTORY OF MODULUS MODULUS (PROSOBRANCHIA: MODULIDAE)
Richard S, Houbrick
Department of Invertebrate Zoology (Mollusks), National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560, U.S.A.
ABSTRACT
Modulus modulus (Linnaeus), family Modulidae, is a style-bearing marine prosobranch in the superfamily Cerithiacea. It diflers from other cerithiaceans by its turbinate shell and certain anatomical features. The basic anatomy of fJlodulus is that of a typical mesogastropod but the open palliai gonoducts are similar to those of other cerithiaceans. Characteristic anatomical featur( s are the large hypobranchial gland, aphallic males, open palliai oviduct with complex inner ciucts, and the forward position of the salivan/ glands relative to the nerve ring. Modulus modulus lives on marine angiosperm grasses and feeds primarily on diatoms. Ferti''zation is internal and is effected by spermatophores that contain eupyrene and apyrene sperms. Tfie life cycle of a population from Fort Pierce, Florida lasts about one year. Mating occurs in early winter and spawning in spring. Females have complex palliai oviducts and ovipositors. Spawn masses are cylindrical, comprised of gelatinous tubes and deposited on marine grasses. Development is direct. Young snails emerge after tfiree weeks of incubation. Within the Cerithiacea, the Modulidae are phylefically close to the Cerithiidae and Potamididae.
INTRODUCTION phology, developmental biology and aspects of the life history of Modulus modulus The family Modulidae Fischer consists of a (Linnaeus, 1758), the type-species of the single genus. Modulus Gray, 1842, and about genus. On the basis of these data, the rela- six species that are largely confined to the tionship of the Modulidae to other families of shallow waters of tropical and subtropical re- the Cerithiacea will be considered. gions. These prosobranchs are epifaunal, style-bearing, microphagous herbivores and are moderately small animals, having shells HISTORICAL REVIEW 10-25 mm in length. Modulus species occur in the fossil record back to the Cretaceous The family Modulidae has been reviewed (Daii, 1892). Historically, the family Modulidae by A. Adams (1851), Sowerby (1855), Reeve has been assigned to the large mesogastro- (1865), Tryon (1887) and more recently by podan superfamily Cerithiacea Fleming, Abbott (1944), who limited his work to the which is comprised of numerous families of western Atlantic. The older monographs were herbivorous snails, having open palliai gono- confined to strict conchological taxonomy and ducts, aphallic males, and shells that are usu- did not address relationships above the alpha ally high-spired and elongate. Members of the level. Modulidae, however, differ strikingly from all The anatomy of Modulus was first de- other cerithiaceans by their top-shaped, scribed by Risbec (1927), who dealt with trochiform shells. Although the family Modu- Modulus candidus Petit, 1853 [= M. tectum lidae has been included in most of the classic (Gmelin, 1791 )]. He placed the Modulidae be- iconographies and the western Atlantic spe- tween the Strombidae and Cerithiidae. Al- cies have recently been monographed by though Risbec (1927) noted the aphallic con- Abbott (1944), there have been no serious dition of males, he did not adequately study anatomical or life history studies of the group. the reproductive tract and neglected to de- Its standing as a valid family and relationship scribe the complex palliai gonoducts. His to other higher taxa in the superfamily has other anatomical observations are sketchy been conjectural. and sometimes erroneous. Abbott (1944) fig- This paper addresses the functional mor- ured and described the external soft parts of
(117) m HOUBRICK Í
the head and foot of Modulus modulus and MgCl2, and dissected in an anesthetized presented a few brief notes on its ecology. state. Carmine particles were used to deter- To my knowledge, only two papers have mine ciliary tracts and a one percent Méthyl- considered the developmental biology of ène Blue aqueous solution was used as a vital Modulus: Lebour (1945: 470-471) has de- stain. Stomach contents and fecal pellets scribed the spawn and laivae of Modulus were studied under a compound microscope modulus, and more recently Bändel (1976: to determine the algae that were ingested. 258-259) described and figured the spawn Animals were fixed in Bouin's fluid, embedded and larvae of Modulus modulus and Modulus in paraffin, sectioned at 9.0/^.m, and stained carchedonlus (Lamarck, 1822). Both of these with Basic Fuchsin Picric Indigo Carmine for descriptions are brief and the taxonomic iden- histological studies. Photomicrographs of tity of the species is questionable. This will be sections were taken with a Zeiss photomicro- discussed in more detail later in this paper. scope-3. Spermatozoa were fixed in a 2.5 Mook (1977) is the only author to have writ- percent gluteraldehyde solution in 0.2 molar ten anything about the ecology of Modulus. Mellonig's phosphate buffer and were brought His study was concerned with the role of up to 50 percent EtOH and air dried on cover Modulus modulus as a control of fouling or- slips prior to SEM studies. Spermatophores, ganisms on marine angiosperm grasses and eggs and embryos were prepared for critical did not consider the ecology of Modulus. point drying by fixation in 2.5 percent gluteral- To my knowledge, nothing more has been dehyde in 0.2 molar Mellonig's phosphate published about the biology of Modulus spe- buffer at pH 7.4. Material was rinsed in dis- cies, despite the fact that some species, such tilled water, dehydrated and the critical point as Modulus modulus, commonly occur in drying was done with liquid COj. Spermato- great numbers and are easily collected and zoa, spermatophores, eggs, embryos, observed. radulae and embryonic shells were studied with a Nova-Scan SEM. Observations on pair- ing, spawning and feeding were made in the MATERIALS AND METHODS field and in the lab. Eggs and embryos were maintained in culture dishes with daily sea Modulus modulus specimens were ob- water changes until hatching. Measurements tained from a large population in a seagrass of eggs and embryos were made with an ocu- bed north of Link Port on the west bank of the lar micrometer. Indian River lagoon near Fort Pierce, Florida In addition to the above work, the anatomy (27°32.1'N, 80°20.9'W). For a more detailed of Modulus tectum (Gmelin, 1791) was stud- description of this site, see Young et al. ied at Suva, Fiji for comparison with that of (1976). The subtidal site consisted of dense Modulus modulus, but this work was only at a stands of Halodule wrightii Ascherson and superficial level. occasional beds of Thalassia tesludinum All measurements are relative to average König & Sims interspersed with sandy sized snails (see Table 1). patches. Snails from this population were studied during January, February, May and September of 1978 and in January of 1979. ANATOMY Living animals were studied in the field and in sea water aquaria or petri dishes placed Shell (Fig. la-c).•The shell is top-shaped, under a Wild M-5 stereo dissecting micro- umbilicate, wider than high, and consists of scope. Animals were extracted from their 5-6 strongly convex, angulate whorls of which shells and relaxed in a 7.5 percent solution of the body whorl is disproportionately large.
FIG. 1. Shells, spawn mass and embryos of Modulus modulus; a-c, Apical, apertural and basal views of adult shell with typical sculpture; d-f, Apical, aperlural and side view of young shell. Note sharp transition between sculpture of embryonic shell and that of teleoconcfi (1.5 mm wide); g. Newly Inatched snail showing distinctive sculpture (0.5 mm long); h. Five day old snail showing sharp transition in sculpture between embryonic shell and new growth area of outer lip (0.8 mm long); i. Portion of spawn mass critical point dried and fractured to show hyaline capsule surrounding each embryo. Embryonic shell sculpture is visible beneath surface of each capsule; j. Typical spawn mass attactned to grass blade (9 mm long); k. Portion of spawn mass with surface debris removed to display encapsulated embryos. BIOLOGY OF MODULUS 119 120 HOUBRICK
The spire is low and turbinate. The suture is slightly irregular and moderately impressed. The periphery of each whorl has a prominent spiral cord that forms a keel. Three to four weaker spiral cords are above the peripheral cord. Adapical to the peripheral cord each whorl is sculptured with 12-13 axial ribs that form low, blunt nodules where they cross the pp.f spiral cords. The body whorl descends just before the aperture in adults and has 4-5 spi- ral cords on its base sculptured with numer- ous tiny nodules that are aligned to form weak axial riblets. In juvenile shells the body whorl is extremely angulate and keeled (Fig. ld-f). The aperture is ovate and the columella deep- ly concave and terminated with a deep notch or chink that forms a tooth-like lamella. This notch accommodates the palliai tentacles of the inhalant siphon. The outer lip is moderate- ly thin and strongly crenulate, each scallop fitting a palliai tentacle. The inner surface of the outer lip is reinforced with 5-6 spiral ridges. The umbilicus is small but deep and in adults is slightly covered by the columellar fold. The protoconch consists of two whorls that are convex but not angulate, and sculp- tured with 5-6 thin, spiral lirae except for the smooth nuclear tip. Basic shell color is a dirty white but is normally hidden by the periostra- cum and algal epiphytes. Brownish purple splotches occur on the spiral chords and ad- jacent to the suture of the body whorl. The columella is tinged with purple and the colu- mellar notch has a purple spot. Average shell dimensions of the Link Port population were FIG. 2. A, Modulus modulus, male removed from 8.31 mm in length and 9.24 mm in width (see shell and viewed from leftside. S, Female removed Table 1). The operculum is thin, corneous, from shell and seen from right side, ag, albumen circular and multispiral with a central nucleus. gland; cl, ciliated furrow; eg, capsule gland; cm, It fits snugly into the aperture of the shell columellar muscle; ct, ctenidium; dg, digestive gland; f. foot; hg, hypobranchial gland; In, inhalant when the animal is retracted. The penostra- siphon; int, intestine; k, kidney; mi, mantle tentacle; cum is thin, and tan. op, operculum; ov, ovary; ovp, ovipositor; pp, Animal: external features (Fig. 2).•The propodium; ppi, propodial furrow; pt. palliai tenta- base color of the head, neck and foot regions cle; sn, snout; si, stomach; i, tentacle; ie, testis.
TABLE 1. Analysis of shell dimensions (measurements in mm).
Length Width Statistic No. % x Sd Range X Sd Range
All shells 61 100 1.31 0.63 6.3-10.1 9.24 0.66 7.7-10.6 Males 27 44.26 ;,24 0.78 6.3-10.1 9.09 0.67 7.7-10.6 Females 32 52.46 1.40 0.47 7.5- 9.5 9.94 0.64 9.2-10.5 Parasitized 2 3.27 No., number of snails Sd. standard deviation X. mean BIOLOGY OF MODULUS 121
is pinkish-cream witti dusl
covering the ctenidium and osphradium is tracts filled with rediae, cercariae and sporo- orange. The mantle cavity is 5-6 mm deep cysts and have pinkish-colored gonads. and is broadest at its distal end where the Mantle cavity and associated organs (Fig, edge flairs up and backwards. The exhalant 3).•At the lower left side of the mantle cavity siphon is marked on the mantle surface by a is the brown-pigmented osphradium (Fig. 3A, prominent, rounded ridge that is thick, muscu- OS), a thin, ridge-like structure that is triangu- lar and curved in a semicircle down towards lar in cross section and about 5 mm long and the medial right part of the mantle edge. 0.35 mm wide. The osphradium begins at the The columellar muscle (Fig. 2S, cm) is proximal end of the mantle cavity and extends broad and quite large (2.5 mm long; 3 mm forward, adjacent to the ctenidium for about wide) in relation to the animal. It is tightly at- two-thirds of its length. As the osphradium tached for one complete whorl to the inner nears the inhalant siphon it sharply turns to columella of the shell about one-half whorl's form an "S" shape and tapers to an end about distance from the aperture. The columellar 0.25 mm from the mantle edge. It is separated muscle is located at the ventral surface of the from the ctenidium by an orange-russet pig- snail just behind and on the ventral mantle mented strip about 0.20 mm wide. Sections of edge where it extends diagonally backwards the osphradium show a highly ciliated surface in relation to the anterio-posterior orientation and numerous, darkly staining cells. At its of the mantle cavity. This muscle is powerful base is a thick osphradial nerve that has con- in Modulus and is used by the animal to re- nections with the left mantle nerve. tract into the shell and to produce quick jerky The ctenidium (Fig. 3A, cf) is relatively movements and violent twisting behavior that large, about 6 mm in length and 1.5 mm in will be described in more detail later in this width. It extends the length of the mantle cavi- paper. ty and comprises about 125 long finger- The whorls of the animal comprising the shaped, flattened filaments. Each filament is stomach, gonads and digestive gland taper 1.5 mm long and 0.45 mm wide at its attached off sharply and curl beneath the columellar base and tapers toward the tip. Individual fila- muscle. The stomach (Figs. 2A,B, st) occu- ments are strengthened on the right side pies about 1.5 whorls and is colored white, (edge) by an internal rod (Fig. 3S, r). A ciliated brown and green. The remaining two and a longitudinal band (Fig. 3S, cb) is on each side half to three whorls comprise the digestive of the flattened surface of a filament, adjacent gland and gonad. The digestive gland (Fig. 2A, to the rod. The narrow edges of each filament dg) is chocolate brown and is almost entirely are lined with cilia and exceptionally lengthy overlain by the gonad in ripe animals. The cilia are on the filament tip (Fig. 3S, cl). Thin ovary (Fig. 26, ov) is white and extends over transverse bands of muscles (Fig. 36, mb) the digestive gland in a branching network. allow each filament to respond to the stimulus The testis (Fig. 2A, te) is yellow-orange and of a probe by quickly retracting and bending. covers most of the digesive gland. Since The hypobranchial gland (Fig, 3A, tib) lies males are aphallic, the pigmentation of the to the right and next to the ctenidium. It is testis is an easy way to sex ripe individuals. about 4,0 mm long and 1,0 mm wide and Animals parasitized by trematodes frequently highly conspicuous because of its swollen, have their gonadial and lower alimentary glandular state and bright russet-green color.
FIG, 3, Anatomical features o1 Modulus modulus. A, Animal removed from shell and mantle cavity opened mid-dorsally. The kidney has been pulled back to expose the kidney opening and heart, S, Individual ctenidial filament, C, Cross section through mantle edge showing trilobed condition and ciliated groove containing debris. D, Dorsal view of mantle edge displaying ciliated groove and inner lobe, E, Stomach opened by dorsal longitudinal cut. Crystalline style has been removed, a, anus; ag, albumen gland; cb, ciliated band; eg, capsule gland; cgr, ciliated groove; cl, long cilia; ct, ctenidium; dd, digestive gland duct; dg, digestive gland; ebv, efferent branchial vessel; es, esophagus; ex, exhalant siphon; fee, fold emerging from spiral caecum; gs, gastric shield; gspr, groove leading to spermatophore receptacle; gsr, groove leading to seminal receptacle; hb, hypobranchial gland; //, outer lobe of mantle edge; in, inhalant siphon; int, intestine; k, kidney; ko, kidney opening; lib, baffle of lateral lamina; m, mouth; mb, muscle band; me, mantle edge; od, palliai oviduct groove; oes, opening from esophagus to stomach; os, osphradium; ov, ovary; pc, pericardial sac; pod, proximal portion of palliai oviduct; pt, palliai tentacle; r, internal strengthening rod; s, shell; sa, sorting area; sc, reduced spiral caecum; ss, style sac; si, stomach; i^, typhlosole 1; Í2, typhlosole 2; ve, ventricle. 124 HOUBRICK
Tapering at both ends, it begins at the proxi- a typical slit-like opening on its ventral surface mal end of the mantle cavity and rapidly (Fig. 3A, ko). widens, extending longitudinally and ending Alimentary system (Figs. 3A 4, 5).•This behind the anus. The hypobranchial gland system is typically mesogastropodan and is lies close to and slightly overlaps the intes- somewhat like that described by Fretter & tine. It is covered externally with numerous Graham (1962: 25-32) for LIttorina. The tiny papillae and has a transversely ridged mouth lies at the tip of the snout but is usually surface that is russet colored. Oval and gob- recessed between the two lobes that comprise let-shaped areas appear within the gland the snout apex. At the anterior end of the buc- when viewed from the surface. If a snail is cal cavity and inserted in its lateral walls are a violently disturbed or if the hypobranchial pair of chitinous jaws (Fig. 4, j) composed of gland is stimulated with a probe, it exudes tiny rhomboidal plates. Dissection of the buc- copious strands of tiny, globular, mucus-like cal apparatus reveals two large radular retrac- bodies. These are shot out in salvos from tor muscles that anse from the walls of the small openings in the surface of the gland un- anterior body cavity and insert on the post- til the mantle cavity is nearly filled with them. median surface of the buccal mass (Fig. 4, The exúdate is rapidly moved by cilia and ex- Irm, rrm). pelled by the exhalant siphon. The animal will The buccal mass (Fig. 4, bm) is about continue to exude globular particles whenever 1.65 mm long and 1.24 mm wide. The radular stimulated until the gland is spent. The exú- ribbon is 2.25 mm long and 0.35 mm wide, date is probably used defensively by the snail comprises about 68 rows of teeth, and is one- when under attack. The composition and fourth the length of the shell (see Table 2). It is nature of the exúdate is unknown. I have not typically taenioglossate (2-1-1-i-l-i-l+2) and seen this phenomenon in other cerithiacean has a rounded, quadrate-shaped rachidian snails. Sections of the hypobranchial gland tooth (Fig, 5). The basal plate of the rachidian show numerous columnar, vesicular and is smooth and has a long central projection darkly stained glandular cells at its surface. and convex lateral sides. It is similar to that of Beneath these are vesicle-like chambers that Cerithium species and lacks the basal cusps appear to store the hypobranchial exúdate. that are seen on potamidid species such as No ducts leading from these chambers to the Batillaria. The top of the rachidian tooth is surface of the gland were seen. markedly convex and has a cutting edge The intestine (Fig. 3/A, int) is 0.25 mm wide comprised of a large, pointed central denticle and usually dark colored due to many small, that is flanked on each side with 2-3 smaller transversely oriented, ovoid fecal pellets that pointed denticles that diminish in size lateral- fill it. The palliai epithelium overlying the in- ly. The lateral tooth of the radula is trapezoidal testine is covered with tiny papillae that ex- in shape, and has a long lateral extension that tend over it from the adjacent hypobranchial curves down at its insertion point in the radu- gland. The anus, borne on a large papilla, is lar membrane. On the basal plate of the later- about 2.5 mm from the mantle edge (Fig. 3A, al tooth there is a long, blunt longitudinal ex- a). tension. The top of the lateral tooth is straight The palliai gonoducts are open in both males and serrated with a small inner cusp, a sec- and females and males are aphallic. The ond larger cusp and 3-4 smaller ones. The open condition of the gonoducts is best visu- inner and outer marginal teeth are long, alized as a slit tube that runs the length of the spatulate and serrated at their tips with 5-6 mantle cavity, consisting of inner and outer closely set, blunt denticles. The two marginal laminae. The male pallia! gonoduct (Fig. 8A, teeth are virtually identical, and thus differfrom C) is a thin-walled, glandular, open tube while those of Cerithium species, which have the palliai oviduct of females (Fig. 8S) is a distinguishable outer and inner marginal larger, white glandular organ comprising teeth. The radular sac begins ventral to the laminae with complex inner chambers and esophagus and coils in a spiral to the nght. tiny ducts. The functional aspects of both There are no esophageal pouches. A large male and female palliai gonoducts are dis- spade-shaped esophageal valve is present. cussed in detail later in this paper, in the sec- The paired salivary glands (Fig. 4, Isg, rsg) tion on the reproductive system. are loosely compacted lobes, lying behind the At the proximal end of the mantle cavity lies buccal mass above and beside the anterior the anterior wall of the pericardial sac (Fig. esophagus. The left is four-lobed, and twice 3/A, pc) and to its right is the kidney which has as large as the hght, and extends through the BIOLOGY OF MODULUS 125
1mm
FIG. 4. Dissection of the hiead of Modulus modulus opened by a dorsal longitudinal cut exposing anterior alimentary tract, ae, anterior esophagus; bm, buccal mass; bn, buccal nerve; cpc, cerebal-pedal connective; epic, cerebral-pleural connective; dfe, dorsal fold of esophagus; dsg, duct of right salivary gland;/, jaw; leg, left cerebral ganglion; Imn, left mantle nerve; Ipg, left pleural ganglion; Irm, left radular retractor muscle; Isg, left salivary gland; me, mid-esophagus; opn, optic nerve; osn, osphradial nerve; pg, right pedal ganglion; ppc, pleural-pedal connective; r, radula; rcg, right cerebral ganglion; rmn, right mantle nerve; rpg, right pleural ganglion; rrm, right radular retractor muscle; rsg, right salivary gland; sec, supraesophageal connec- tive; seg, supraesophageal ganglion; srm, subradular membrane; svc, subvisceral connective; tn, tentacle nerve. 126 HOUBRICK
FIG. 5. Radula of Modulus modulus. Left, general view of radular ribbon; right, half row showing cusp arrangent on rachidian, lateral and marginal teeth. Rachidian tooth length = 0.06 mm.
TABLE 2. Statistical summary of radular and shell The stomach (Fig. 3E) is about 4 mm long, measurements. occupies about two-thirds of a whorl, and is typically cehthioid in layout. Topographically, Statistic No. Sd Range it is not unlike that depicted for Turritella by Graham (1938), It has a short, wide style sac Shell length 8 8,75 0.37 8.1- 9.2 Shell width 8 9,75 0.49 9.1-10.2 and a well-formed crystalline style. If the Radula length 8 2.21 0.17 2.0- 2.5 stomach is opened by a dorsal longitudinal Rows of teeth 8 68,8 2.60 66 -73 cut, the esophagus is seen to enter at its hght anterior end. An opening to the digestive No., number of sna s Sd, slandard devial on gland (Fig. 3E, dd) and what appears to be a X, mean much reduced spiral caecum (Fig. 3£, sc) are both near the esophageal opening. A broad nerve ring a shiort way down the mid-esopha- sorting area (Fig. 3f, sa) is in the ventral por- gus. The right gland is three lobed, and lies tion of the stomach. A thick cuticular gastric wholly in front of the nerve ring. The ducts shield (Fig. 3E, gs) lies to the left, directly arise in front of the cerebral ganglia, and enter across from the anterior opening of the intes- the buccal cavity at each side (Fig. 4, dsg). tine and style sac. The crystalline style is The anterior esophagus has a pronounced present in all freshly collected specimens and dorsal food groove, and twists, due to torsion, is a short, transparent dumb-bell shaped rod at the cerebral ganglia; but the dorsal folds do about 2.8 mm in length. The style sac (Fig. 3E, not extend back ventrally as in Uttorina. The ss) from which it emerges, although joined to darl<-pigmented mid-esophagus can be seen the intestine, is a separate structure with a through the dorsal body wall. It is enlarged blind end. The major typhlosole (Fig. 3£, f,) into a well developed esophageal gland com- emerges from the intestinal groove and prising numerous deep folds and diverticula, cun/es around to the spiral caecum. A small giving it a loosely compacted flocculent struc- minor typhlosole (Fig. 3E, ij) runs from the ture that easily falls apart under dissection, sorting area into the intestine. Begining behind the nerve ring, it tapers The intestine leaves the stomach at the left rapidly, like the mid-esophagus itself towards anterior end of the style sac region and coils the rear of the mantle region. The posterior back over the style sac before turning anteri- esophagus is also dark-pigmented, and has orly where it enters the mantle cavity. The 4-6 longitudinal ridges, it opens into the portion of the intestine that exits from the stomach shortly behind the mantle cavity. stomach has a large dorsal typhlosole that is BIOLOGY OF MODULUS 127 gradually lost as the intestine nears tlie man- male gonoduct nor the method of transfer to tle cavity where it has a smooth interior. It the female, but it probably occurs via siphonal becomes ridged and more glandular in the currents as I have described in Cerithium mantle skirt. muscarum (Houbrick, 1973). in the aquarium Reproductive system (Fig. 8).•Open palli- I saw some spermatophores pass out the ex- ai gonoducts in both sexes, the lack of a penis halant siphon of a male and fall to the bottom. in males and the formation of spermatophores The bright orange testis lies on the outer by males are fundamental features of the re- dorsal surface of the digestive gland. The productive system in Modulus modulus. The seminiferous tubules empty into a branching basic groundplan of the palliai gonoducts in network of microscopic ducts that lead to Modulus is the same as in other cerithiaceans about 10 vasa efferentia. These empty into such as Cerittiium, Bittium, Rhinoclavis and the vas deferens that lies on the inside of the Batillaha but differs in the placement and ar- visceral coil and appears as a white duct that rangement of internal ducts and seminal re- in ripe males is packed with eupyrene and ceptacles in the laminae of the gonoduct. The apyrene sperm. palliai gonoduct is best visualized as a tube- SEM preparations of spermatozoa reveal like duct, extending from the proximal end of that a eupyrene spermatozoon (Fig. 6, f) is the mantle cavity to the mantle edge, and slit about 36 yu,m in length, has a pointed acro- open along its longitudinal axis. In both sexes some, a short, cylindrical, thick head and con- the paillai gonoduct comprises lateral (right) stricted neck region, and a long midpiece and medial (left) laminae that are fused dor- about one-fifth the length of the spermato- sally to each other and to the lateral mantle zoon. A long narrow flagellum follows the wall. The ventral margins of the laminae are midpiece. Eupyrene spermatozoa taken from free and open to the mantle cavity. In the vas deferens are attached by their acro- Modulus both laminae have internal ducts somes in small clusters. and pouches used for the reception, trans- Apyrene spermatozoa (Fig. 6a, g) are larg- mission and storage of spermatophores and er, about 48 ¡xm in length, bear six flagella, spermatozoa. have a spiral configuration, and very long Male reproductive tract (Fig. 8).•In males pointed heads almost one-half the length of a the laminae of the gonoducts are white, thin- sperm. It is not clear if there is a midpiece; walled structures (Fig. 8). The medial (left) consequently, this long head region may con- lamina is membranous and semi-opaque and sist of head and midpiece. Although no counts its inner surface has numerous, transversely were made, there appears to be an equal oriented ridges. Near the axis of attachment number of both kinds of sperms, tangled to- there are wider, denser and less numerous gether by the numerous flagella into dense ridges. The lateral (hght) lamina (Fig. 8A ") is masses. Thus the apyrene spermatozoa may fused along its axis to the mantle and partially serve to bind the mass together with their on its left side to the epidermis of the visceral flagella. Apyrene sperm move in a slow sinu- hump. It is opaque and thick and its inner sur- ous manner while eupyrene sperm are fast face has thick convoluted ridges. The male moving. palliai gonoduct is slightly closed at its proxi- The spermatophores of Modulus are im- mal end due to the medial lamina folding over mobile, thinly walled, acellular structures of the posterior portion of the lateral lamina (Fig. 1-3 mm length. Fresh spermatophores are SA, pmg). This creates a closed pouch filled white, shiny, crescent-shaped and swollen with numerous glandular axial ridges. This with spermatozoa. One end is round and area of the gonoduct is probably the prostate pointed and the other more flattened and bi- gland (Fig. 8C, pg). Distal to the closed por- furcate (Figs. 6, 7a-b). A prominent keel ex- tion of the gonoduct is a thicker longitudinal tends axially along one side of the spermato- glandular ridge and several wide axial glandu- phore (Fig. 6a). The pointed end (Fig. 7c), lar folds that stain darkly with Méthylène Blue. when lodged in the female gonoduct, lies Adajcent to these folds are numerous smaller closest to its proximal end. If pressure is ap- axial folds. This glandular area of the inner plied to a fresh spermatophore, sperm surface of the lateral lamina extends to the emerge from the lower branch of the bifurcat- distal end of the gonoduct and is probably the ed end, where there appears to be a tube-like spermatophore organ. Its exact mode of func- exit (Fig. 7b). Equal numbers of eupyrene and tioning is unknown. I have not seen a devel- apyrene spermatozoa are contained in the oping or a completed spermatophore in the spermatophore. 128 HOUBRICK
FIG. 6, Spermatophore and sperm of Modulus modulus. SEM micrographs; a, Spermatophore, critical poirnt dried and partially collapsed. Note distinctive axial l FIG, 7. Spermatophore of Módulos modulus showing details of keel (a), bifurcate end (b), round pointed end (c), and acellular fibrous matrix comprising surface structure (d-e); f, Eupyrene and apyrene sperm extract- ed from seminal receptacle of female. SEM preparations of critical point dried ends of individual fibers are free, creating a spermatophores reveal a complex surface shaggy appearance (Fig. 7b), The edge of the structure (Fig, 7a-e). Spermatophores are keel is serrated due to free fiber ends that composed of long, axially oriented string-like point away from the pointed tip, SEM pictures fibers embedded in a matrix (Fig, 7d-e). At of a fractured spermatophore wall show that it the pointed end the fibrous matrix is closely is about 5 /^m thick and composed of three bound together and the external surface is layers: an outer fibrous layer, a thick middle relatively smooth. In the bifurcate part, the layer filled with spongy-looking globules of 130 HOUBRICK ^ £ .ro O) ro 6 > 5"S "'Si ro E t3 E^^ É 01 =1 ^ •> -t oj ^ "O o m o Q 0) 8 O "ií " " O »z 0) ï: 6 « a> ro ^ ra Q E Ç5 f^ S 5 E H_ . -n 1 •="•« o m o o c tz c c tF a>O o ro (O m E E > E £ ^ •^ .- CL ^-o ÍT!(D o • ro ^ O) -o c Q - o ro •> ^ t O) 0) o c ro croo)ro • o. ro o E S ?i "9 S "O o g> ro o t; 0) o>"oro «í =! •- Q ^ "O 0) £ o o .£ > c ro ro o. o 0) _ ' CD ro ro • E ro Ë 0) ^ro Ä^ ¿ " ti E ^ ro Q.-o" c/) ^ .2 E B ° CD *- ro «T 'S f; o ro o E ro o S-ro l^oro^ ^ - CD .2 S CD ro .Ist 8l ' x:a> j¿(j -a¡- cji• •ro'» _ o ra ^51-ai CL-ß E ^Ü enQ. (D> '^o ro o n u o = 1*E o>- Q_ 2 i2 le • ro _ CX5Q.ro oil- o.Ç ÏL3,E. Si- BIOLOGY OF MODULUS 131 unknown composition, and atliin inner fibrous The lateral lamina (Fig. 83) has the same layer. layout as the medial lamina: i.e., a thick Female reproductive tract (Figs. 3, 8).• glandular, attached axial base separated from The palliai oviduct is an opaque, cream- the upper membranous, free part of the lami- colored organ about 5.5 mm long and differs na by an axial constriction. The upper mem- from thie male gonoduct by its larger size and branous part of the lateral lamina also has the longer, swollen laminae. The bases of the same groundplan as the membranous part of laminae stain darkly in sections and are highly the medial lamina, but is mostly fused to the glandular. The medial (left) lamina (Fig. 8S, columellar muscle. Not tar from the distal end ml) has a thick lower portion composed of of the lateral lamina, an open slit develops transversely ohented glandular folds adjacent into a long ciliated gutter (Fig. SB, gsr), that to the line of axial fusion to the mantle. There proximally becomes a closed pouch. This is a construction in the medial lamina, about pouch is the seminal receptacle (Fig. 86, sr) half-way to its outer edge, separating the low- and is distended with sperm during the repro- er swollen, glandular part from the upper, ductive season, when its inner walls are more membranous part. An open slit in the glandular and villous. upper portion of the lamina begins at the distal The morphology of the gutter and seminal end and becomes a ciliated gutter (Fig. 8S, receptacle of the upper lateral lamina is com- gspr). The highly ciliated gutter gets deeper plicated by an involution and doubling back of and becomes a large, closed, internally ciliat- the upper lateral, membranous wall of the ed tube-like pouch occupying the proximal ciliated gutter. This involution in the wall of the third of the medial lamina. Both the ciliated gutter assumes the form of a large flap of tis- gutter and pouch comprise the spermatophore sue (Fig. 8S), covering the top of the open slit receptacle (Fig. 8S, spr) which is probably and gutter at the upper part of the distal third homologous to the "bursa copulatrix" or of the gonoduct. The flap probably serves as sperm-collecting pouch in Cerithium and a baffle which may prevent spermatophores Rhinoclavis (Houbrick, 1974a; 1978). Sec- from entering the seminal receptacle instead tions show that the inner walls of the recepta- of the spermatophore receptacle. It may also cle consist of columnar epithelial cells with guide released sperm into the seminal recep- darker staining glandular cells. tacle. Spermatophores are drawn by ciliary cur- The thick, lower, inner portions of both rents into the mantle and enter the spermato- laminae form the albumen gland and the phore receptacle pointed end first. An individ- capsule gland. The albumen gland (Fig. 8S, ual spermatophore fills the entire length of the ag) is located in the proximal part of the axial spermatophore receptacle, its bifurcated end base of the oviduct. The capsule gland (Fig. sticking out at the distal end. Both the ser- &B, eg) is a loosely compacted darkly staining rated edge of the spermatophore keel and the area located in the middle portion of the later- minute free fibrous ends of its surface help to al lamina. anchor it in the receptacle. An individual The pale green ovary consists of numer- spermatophore receptacle normally holds one ous, tiny, compact lobes. A thin-walled ovan- spermatophore but occasionally two may be an duct, about 0.4 mm wide, extends from the found. ovary and runs fonward along the ventral side Sperm emerge from the lower, bifurcate of the viscera where it passes under part of end of the spermatophore and move into an- the kidney and lies adjacent to the intestine other ciliated groove formed by a told ansing and pehcardial cavity before entering the from a baffle on the middle part of the free mantle cavity. Oocytes from the ovanan duct edge of the medial lamina. This forms a long, are about 0.15 mm in diameter. deep, highly ciliated slit with an open edge Nervous system (Fig. 4).•The nen/ous facing and slightly overhanging the tree edge system is similar to that of Cerithium and of the lateral lamina. Sperm leaving the Hhinoclavis and is typically cerithioid. It is not spermatophore are probably transferred by as highly condensed as in other mesogastro- this ciliated groove to the ciliated gutter (Fig. pods such as the rissoaceans. If one uses the SB, gsr) of the lateral lamina leading to the "RPG" ratio of Davis et al. (1976: 263) (length seminal receptacle in the upper portion of the of the pleurosupraesophageal connective di- lateral lamina (Fig. QB, sr). Spermatophores vided by the sum of the lengths of the right slowly dissolve within the spermatophore re- pleural ganglion) to determine the state of ceptacle and may be recovered in vanous condensation, a mean value of 0.59 is ob- stages of disintegration. tained which is a little above an intermediate 132 HOUBRiCK TABLE 3. The RPG ratio for Modulus modulus. is frequent. The male's foot is attached to the This ratio is the length of the pleuro-esophageal female's shell so that the two edges of their connective divided by the sum of the lengths of the mantle cavities are adjacent, Spermato- supra-esophageal ganglion, pleuro-supraesopha- phores leave the mantle cavity of males by geal connective and right pleural ganglion. the exhalant siphon and presumably enter the No, Sd Range female's mantle cavity via her inhalant siphon because males lack a penis or other organ of 7 0.59 5.21 0,54-0,70 intromission. Not all spermatophores are suc- No,, number of snails cessfully introduced: some drop to the bottom Sd, standard deviation of the aquarium. The same phenomenon was X, mean seen in Cerithium muscarum (Houbrick, 1973) and may be due to artificial lab condi- tions. Spermatophores in the female's mantle value (Table 3). As Davis pointed out, the cavity are moved by ciliary currents over the higher the value the "looser" and more primi- head-foot into the open ciliated gutter and tive is the nervous system. Distinctive char- spermatophore receptacle in the medial lami- acters are the lightly pigmented cerebral, na of the palliai oviduct. The flap on the distal pleural and pedal ganglia which are covered part of the lateral lamina and the second cili- with tiny dots of tan color. The origin of the ated gutter of the medial lamina overhanging tentacular nerve is also lightly pigmented and the lateral lamina probably prevent premature is slightly swollen. The cerebral ganglia are entry of the spermatophore into the seminal moderately fused to the pleural ganglia and receptacle. have virtually no connectives (Fig. 4, rcg, rpg, Spawn.•Deposition of spawn was first leg, Ipg). The cerebral-pedal connective is seen in May, although spawning may have also short, about 0.25 mm long. The pedal occurred in March and AphI when I was away ganglia are large, about 0.50 mm in length from the study site. Spawn is deposited on and deeply embedded in the muscle of the grassy blades of manne angiosperms, such foot. The cerebral ganglia are of equal size as Halodule, in worm-like gelatinous tubes (0.50 mm) and joined by a very short com- about 14.10 mm in length, and 2.13 mm in missure. The pleural ganglia are slightly smal- width (Fig. Ij-k). Each spawn mass contains ler, each about 0.40 mm long. A schematic an average of 121 eggs. Within the gelatinous representation of the ganglia and their rela- tubes fertilized eggs are enclosed in hyaline- tionship to other organs of the head are capsules of 0.50 mm diameter, each capsule shown in Fig. 4. containing a single egg, 0.15 mm in diameter Circulatory and excretory systems.•There (Fig. 1i, k). Although a few eggs contain tera- is nothing particularly distinctive about either tological embryos, there are no nurse eggs. of these systems in Modulus. Both kidney and Table 4 presents more statistics about egg heart are typically monotocardian and not un- masses. lil detritus of the outer wall of the spawn mass shell has reached its maximum size. Adults and gradually move off onto grass blades. In appear to die after spawning, when many May, thousands of juvenile snails, from 0.5- empty adult shells may be found, 1.8 mm in diameter were observed in the A summary of thoso data and other ob- grass beds (Fig. Ig-h). Although obviously of servations indicate that the Link Port popula- different size classes due to different hatching tion of Modulus modulus has a life cycle of times and the long spawning period, these one year. Although the spawning period is young snails may be considered to form one long and results in various cohorts of young, large group of young. Newly hatched snails these overlap to form one large group that quickly twist and lurn as they explore the en- develops during spring and grows quickly vironment. Young snails each have large throughout the year, reaching maturity in late black eyes, a typical radula and a long tactile winter-eeiiy spring, when spawning occurs. propodium that bears a heavily ciliated groove Developmental stages occur throughout the along its anterior margin. spring with the subsequent emergence of the Growth.•New growth of the protoconch new progeny and death of adults. occurs rapidly. Within a few days, a change in These conclusions are supported by ex- sculpture separates the embryonic shell from amination of large monthly samples of benthic the new shell growth (Fig. 1h). This is marked animals taken from other sites in the Indian by axial shell sculpture that lacks the spiral River during the Indian River Study conducted elements of the protoconch. The aperture be- by the Harbor Branch Consortium in 1973- comes angulate and flaring due to the ap- 1974 (see Young et al., 1974). Growth stages pearance of the median keel that is so indica- of Modulus from these samples fit the general tive of adult shells. pattern given above. It thus appears that By mid June young snails have added a populations of Modulus from other areas of much larger whorl sculptured with spiral cords thi' Indian River estuary have a similar life and a prominent median keel and have shells cycle that lasts about one year. that rtinge from 1.3-2 mm in diameter. The outer lip is sharply angulate and the distinctive columellar notch of adults is present (Fiq. 1d- ECOLOGY Observations were not made during the Modulus modulus is one of the more com- mid-summer months, but in September young mon prosobranchs associated with manne Modulus were abundant in the grass beds. grassbeds in Flonda and the Caribbean. As No living adults v«/ere found but numerous an abundant primary consumer it is an impor- adult shells occupied by hermit crabs were tant factor in the trophic structure of this eco- seen. Adolescent Modulus, 2-5 mm in size, tope. It is thus surprising that so little was were covered with thick filamentous green known about its anatomy and ecology. algae and were difficult to detect in the grass General observations.•A thorough study beds. Shells were thick and had typical adult of the autecology of Modulus was not at- sculpture except for their outer lips which tempted; nevertheless, some ecological ob- were thin due to recent growth. Animals had servations made during this study will provide adult pigmentation and the internal anatomy information for future workers. appeared normal except for the incipient The study site consisted of dense stands of palliai gonoducts. The ctenidium was slightly Halodule wrightil Ascherson, and two other smaller and comprised only 80 filaments. The less common angiosperm grasses, Syrlngod- pleuro-esophageal connective was slightly lum fillformis Knetz and Thalassia testudlnum longer than in adults; consequently, the RPG König & Sims, all covered with dense epi- ratio of adolescent snails is higher, about phytic growth which traps detritus. The entire 0.70. This indicates a looser concentration of site is rich with detritus, and the water is fre- the nen^e ring. The ganglia probably become quently turbid with suspended paniculate more condensed as they grow larger. matter. The salinity in this habitat, normally By December, snails have nearly reached 337oo, undergoes considerable variation -adult size and males are ripe. Females be- sometimes within a short period of time due to come ripe in January. The palliai oviducts are heavy rainfall. developed but ovaries are just beginning to Modulus occurs on the grass blades and ripen. By spring (late February-early March) occasionally on the substratum. The popula- Modulus is reproductively mature and the tion studied lives at a depth of about one BIOLOGY OF MODULUS 135 TABLE 5. Epiphytic algae growing on shells of complete diatoms, and diatom fragments Modulus modulus {' = dominant). pass through the gut. The most common un- broken diatoms in fecal pellets were Nitzschia Phaeophyta and Navícula species. The evidence of stom- *Sphacelaria furcigera Kützing ach, gut and fecal pellet contents leaves no Cyanophyta doubt that Modulus ingests primarily diatoms. Microcoleus lyngbyaceus (Kützing) Crouan Analysis of the dominant diatoms suggests Callothrix Crustacea Thurel that larger diatoms are preferred to smaller Rhodophyta Gonlothchum alsidii (Zanardini) Howe ones. Although ingested food is not neces- Chlorophyta sarily what is digested by the snail, it is prob- Enteromorpha linguleta J. Agardh able that diatoms are the chief source of en- Cladophora sp. ergy. Gut contents of very young Modulus had no appreciable diatom content. This in- dicates that the young are feeding on different meter and is never exposed, even at extreme plant food. low tides. Associations and predators.•The most Shells of living Modulus are normally common prosobranchs co-existing with densely covered with algal epiphytes. A list of Modulus modulus on seagrasses are Cerith- these is given in Table 5. The dominant epi- ium muscarum Say and Bittium varium phyte is Sphacelaria furcigera Kützing. It is (Pfeiffer), both cerithiaceans and also style- noteworthy that this alga does not grow on the bearing, algal-detritus feeders. Several other sea grasses whereas all of the other epi- common snails found on the seagrass are the phytes on Modulus occur also on the grasses. carnivores Mitrella lunata (Say) and Haml- Living Modulus snails frequently have an noea elegans (Gray). unidentified colonial hydroid growing on the The blue crab, Callinectes sapidus Rath- bases and peripheries of their shells. The bun was the only predator obsen/ed feeding slipper shell, Crepidula fornicata (Linnaeus) on Modulus and many shells with chipped may also occur on the base of the shell and apertures point to heavy crab prédation. Very barnacles occasionally are found on the shell few drilled shells of Modulus were found, sug- top. gesting that prédation by naticid snails is in- Empty shells are common and are fre- significant. This is not surprising because quently utilized by the hermit crab Pagurus Modulus is generally found on the grass bonairensis Schmitt and the sipunculid blades and not as frequently on the substrate. Phascolion cryptus Hendrix. Large rays were frequently seen in the grass Food and feeding.•Modulus modulus is beds and these along with other fish such as an active browser that engulfs microphytic the sheepshead, Archosargus probato- algae and detrital particles. Like other micro- cepfialus Walbaum, are suspected as chief phagous, style-bearing mesogastropods it predators. The numerous young snails ob- feeds more or less constantly. Mook (1977: served in the spring are thin-shelled and small 136) presented evidence that the grazing ac- and are probably eaten by a variety of pre- tion of Modulus may retard the accumulation dators. of fouling organisms by dislodging their newly Befiavlor•Modulus is a slow-crawling settled larvae. Modulus thus aids in keeping grazer and does not demonstrate a wide vari- the surfaces of seagrass blades clear and ety of behavior. It moves with retrograde, available as a substratum for microphytic monotaxic muscular waves and sudden jerky algae. motions. Although its normal habitat is on the Stomach contents of freshly-collected spec- blades of seagrass it will move down onto the imens contained sand grains, occasional substratum when weather conditions cause foraminifer tests, numerous diatoms, algae, estuary waters to be rough. detrital particles, and fragments of larger When irritated or attacked. Modulus strong- filamentous macro-algae. The bulk of the ly twists itself, turning its shell back and forth algal contents comprises diatoms and of with the columellar muscle, as if to dislodge a these, the dominant species is Melosira predator. If the irritation continues, the hypo- moniliformis, a relatively large diatom. An branchial gland exudes a mass of sticky parti- analysis and identification of stomach con- cles that probably discourages predators. The tents is presented in Table 6. Fecal pellet animal will then withdraw completely into its analysis shows that detrital particles, sand. shell, about 5 mm beyond the edge of the 136 HOUBRICK TABLE 6. Analysis of algal stomach contents of Modulus modulus. Mean size (M) Taxon Diameter Height Form Jan, Feb. fvlay Class BACILLARIOPHYCEAE Order Centrales Suborder COSCINODISCINEAE Family IVlELOSIñACEAE Melosira monilitormis O. F. Müller 24.4 26.9 chains Melosira sulcata Ehrenberg 19.5 17.1 chains Order PENNALES Suborder ARAPHIDINEAE Family FRAGIU\RIACEA Synedra sp. (fragments only) 16.1 chains Striatella unipunctata Agardh (fragments only) 56.1 68,3 chains Rhabdonema sp. 9.8 44.0 chains Suborder BIRAPHIDINEAE Family NITZSCHIACEAE Nitzschia sp. 5.2 61 solitary Family NAVICULACEA Mastogloia crucicula (Grunow) Cleve 14,22 10 solitary Mastogloia sp, 11.5 solitary Navícula sp. 25.3 solitary Family SURIRELLANCEAE Camplyodiscus sp. 95 solitary "Dominant species + Present -Absent outer lip, until the operculum snugly fills the frequently incomplete and/or contradictory. aperture. Thus my conclusions, while based on ana- Modulus reacts violently with the same tomical evidence, are tentative and partially twisting movements when it is exposed to speculative. secretions given off by other wounded Modu- On the basis of anatomy, I believe thaï the lus snails, and will move rapidly away. This Modulidae should be regarded as a distinct behavior has been documented in other family within the Centhiacea. On balance. marine and freshwater snails by Snyder Modulus species share more anatomical (1967; 1971), characters in common with members of this superfamily than with any other group. They appear to be closest to the Cerithiidae and DISCUSSION Potamididae, My reasons for these conclu- sions are developed in the following discus- A consideration of the interrelationships of sion. higher taxa is contingent upon the amount Phylogenetic relationships.•Modulus spe- and quality of comparative data available. cies differ conchologically from other ceri- Many familial definitions are based only on thiaceans by their turbinate shape and um- shell characters and there are few compre- bilical notch. The family is a small one (one hensive anatomical studies upon which to genus and about 6 species) in comparison rely, I have used the anatomical data I found with other cerithiacean families such as the available for cerithiaceans, although this was Cehthiidae, Potamididae, Dialidae, Turntel- BIOLOGY OF MODULUS 137 laidae and Vermetidae, all comprising numer- present in cerithiid genera such as Cerithium, ous genera and species. Rhinoclavis, Pseudovertagus, Clypeomorus Risbec (1927: 17) believed that the family and Bittium, but in relation to the animals' Modulidae was intermediate between the body they are never of the same size as are Cerithiidae and Strombidae and cited a num- those of Modulus. Another distinctive feature ber of characters that he said were shared of the external anatomy is the forward position with each group. His remark that both cerithiid of the eyes on the tentacles. In the Cerithi- and Modulus species have short anterior idae, Potamididae, Turritellidae and Vermet- siphons is incorrect: two genera of cerithiids, idae, the eyes are located at the bases of the e.g. Rhinoclavis and Pseudovertagus, are cephalic tentacles. Although the Strombidae characterized by long siphonal canals are similar to the Modulidae in regard to eye (Houbrick, 1978), Risbec (1927) also errone- placement, this does not necessarily indicate ously reported that Modulus and the ceri- close relationship, as noted before. thiids lacked salivary glands. As I have dem- An unusual feature of the mantle cavity in onstrated in this paper and others (Houbrick, Modulus modulus is the large and highly 1974a, 1978) both Modulus and all cerithiids glandular hypobranchial gland. The ability of heretofore studied have salivary glands. this gland to exude salvos of sticky mucoid Bright (1958: 135) has reported salivary particles and discharge them via the exhalant glands in a potamidid, Cerithidea, and I have siphon is, to my knowledge, unrecorded for obsen/ed them mBatillaria. I donot agree with other cerithiaceans, I assume that this behav- Risbec's (1927) opinion that Modulus has ior, coupled with quick twisting movements of close affinities with the Strombidae, While his the body, is a deterrent to predators. Although observation that the anterior position of the the hypobranchial gland of M. tectum is not eyes on the tentacles of Modulus is shared exactly the same, the identical twisting behav- with the strombs is correct, his citation of a ior was noted. Another noteworthy feature of crystalline style as a unique shared character the mantle cavity of Modulus is the sinuously is incorrect because a style is characteristic of twisted distal portion of the osphradium that most algal-dethtal feeders in the Mesogastro- ends near the entrance of the inhalant siphon. poda. He was apparently unaware that many The osphradium is a ridge-shaped structure cerithiaceans have styles. Risbec's (1927) much like the osphradium seen in the mem- citation of an osphradium with indistinct lamel- bers of the Potamididae, while in species of lae as a shared character between the Modu- the Cerithiidae, it is bipectinate. lidae and Strombidae is accurate, but among The placement of the salivary glands and the Cerithiinae, the Potamididae also have a their ducts anterior to the cerebral commis- similar osphradium (personal observation). sure is a noteworthy feature of Modulus. The The similahty of the radula between Modulus salivary ducts do not appear to pass through and Strombus species is superficial: any simi- the nerve ring, but sections show that they lanty is probably due to convergence of gen- begin very close to it. Although this arrange- eralized taenioglossate raduiae adapted for ment is unlike that of many monotocardians, it feeding on epiphytic algae and detntus. The is shared by the cerithiid genera Cehttiium, reproductive tract of Modulus is very different Rhinoclavis, Pseudovertagus and Clypeo- from that of Strombus. The open condition of morus (personal observation) and has been the palliai gonoducts in both sexes and a lack described by Davis et al. (1976: 276) in mem- of a penis in males are conservative cerithi- bers of the rissoacean families Assimineidae, acean characters not seen in the Strombidae. Truncatellidae, Bithyniidae and Hydrobiidae. Although comparison may be made be- In Modulus, the passage of a portion of the tween the sudden jerk-like motions of a crawl- left salivary gland through the nerve ring and ing Modulus and those of Strombus. the partially behind the cerebral commissure, movement o1 the former is more like that of shows that the Modulidae stand in an inter- other cerithiids, only more pronounced, and is mediate position among the Mesogastropoda in no way similar to the jumping motions of in regard to this trait. Some Cerithium species Strombus. also have a similar arrangement of the left Aside from the turbinate shape of the shell. salivary gland. Bright (1958: 134) found that Modulus also has some distinctive anatomi- the salivary glands and ducts of the potami- cal features. Among these are short, stout did, Cerithidea californica (Haldeman, 1840) palliai tentacles that reach extreme develop- were located behind the nerve ring next to the ment in M. tectum. Palliai tentacles are also "crop" (esophageal gland). He noted that the 138 HOUBRICK left gland was the largest and that the salivary itive the nervous system. In Table 7, I com- ducts were highly convoluted and partially pare the ratios of selected cerithiacean taxa. embedded in the connective tissue of the The mean value for Modulus is the same as In "preesophagus" (anterior esophagus). It is Cerithium, 0.59, but both of these taxa have not clear from his statement that the ducts lower values than the potamidid, Batiliaria pass through the nerve ring but his figure indi- minima, which has a value of 0.77, closer to cates this is the case. Thus, while most meso- the littorinid value. gastropods have their salivary glands located Modulus has one of the more complex pal- behind the cerebral commissure they lie an- liai oviduct systems found in the Cerithiacea. teriorly in some rissoaceans and have an in- The open palliai gonoducts of some Cerithi- termediate position in the Modulidae and in acea have been surveyed by Johansson many Cerithiidae. This supports Davis' (1976: (1953; 1956), Pretter (1951), Fretter & 276) position that location of salivary glands Graham (1962: 625) and Houbrick (1971; and their ducts is a poor character to differen- 1974a, 1977, 1978). Although all of the spe- tiate mesogastropods from stenoglossan cies studied have a basic groundplan of open neogastropods. palliai gonoducts, those of Bittium and The combination of a well-developed Cerlthlopsis are very complex in organization. esophageal gland and a crystalline siyle in However, the allocation of Cerlthlopsis within Modulus, although thought to be unusual in the Cerithiacea is uncertain. The layout of the mesogastropods (Fretter & Graham, 1962: paillai gonoducts of Modulus are even more 220), is a common condition shared with complex and unusual. While one can interpret cerithiids I have examined in the genera the palliai gonoducts of the Cerithiacea from a Cerithium, Rhinoclavis, Pseudovertagus and functional viewpoint, it is difficult to relate Clypeomorus. Sections of this large gland in these open systems to each other in a com- Modulus clearly show numerous and deep parative systematic manner. As Johansson glandular lateral outpouchings arising from (1953: 8) pointed out, palliai gonoducts some- the mid-esophagus, leaving no doubt about times differ considerably, even in closely re- its function. lated species. This has been seen in several The nervous system of Modulus differs rissoaceans (Johansson, 1953) and I have from that of Cerithium or Rhinociavis in lack- found many differences in the arrangement of ing a large siphonal ganglion, but this may be the sperm gutter, bursa copulatrix and semin- due to the short siphon of Modulus. It is inter- al receptacle in different species of Cerithium, esting to compare the RPG ratio of Modulus Clypeomorus and Rhinoclavis. Too little is with that of other marine mesogastropods. known of the arrangement of the gonoducts in Davis et al. (1976: 267) presented a table of other members of the Cerithiacea to discuss RPG ratios which compared selected hydro- their comparative anatomy satisfactorily; blid, rissold and littorinid taxa. As mentioned moreover, the epithelial origin of palliai gono- previously, the higher the value of the RPG ducts renders any homologies suspect. Thus, ratio the less concentrated are the ganglia of any attempt to decide what is a primitive or the nerve ring and presumably the more prim- derived state would be premature and purely speculative. Nevertheless the unique ground- TA8LE 7, The RPG ratio for selected cerithiid, plan of the paillai gonoducts of Modulus clear- modulid and potamidid taxa, (Thiis ratio is the length ly separates the Modulidae from other ceri- of the pleuro-esophageal connective divided by the thiacean families and is a reliable discriminat- sum of the lengths of the supraesophageal gangli- ing character. on, pleuro-supraesophageal connective and right I have observed spermatophores in other pleural ganglion). cerithiid members of the genera Cerithium, Rhinociavis, and Gourmya and suspect that Taxon RPG this method of sperm transfer is characteristic of the group. Spermatophores have also been Cerithiacea Cerithiidae described by Dazo (1965) in the freshwater Cerithium tutosum Menke 0,59 cerithiacean Goniobasis. The spermatophore Cerithium atratum (Born) 0,59 of Modulus has a more complex surface Modulidae structure and shape than those I have seen in Modulus modulus (Linnaeus) 0.59 the cerithiid species. The general physiog- Potamididae nomy of the sperm of Modulus and In particu- Batiliaria minima (Gmelin) 0.77 lar the elongate midpiece of the eupyrene BIOLOGY OF MODULUS 139 spermatozoon, are comparable to those de- to that I have descnbed in M. modulus. Within scribed for other cerithiids, e.g. Cerithium the buccal cavity of M. tectum, lying anterior (Tuzet, 1930; Houbrick, 1973), Bittium and to the nerve ring, are paired salivary glands Cerithiopsis (Fretter & Graham, 1962). with ducts that empty into the anterior esoph- Interspecific comparisons.•Aside from agus. The radula is very much like that of M. the observations presented in this paper and modulus. Behind the nerve ring the esoph- those recorded on the anatomy of ¡Modulus agus rapidly widens and a large, wide, choco- tectum by Risbec (1927) (cited as Modulus late-colored esophageal gland is present. Candidas Petit), nothing is known of the ana- The large black kidney is covered with a tomy or ecology of other Modulus species. I network of fine white branch-like blood ves- was able to study Modulus tectum in Fiji and sels. The testis is light green and a large vas offer the following observations for compari- efferens runs from the testis to the palliai son with M. modulus. Modulus tectum differs gonoduct along the inside of the whorls. In from M. modulus by living on hard substrates females the ovary is dark green and filled with in coral reef habitats. It is a much larger snail large green ova that suggest direct develop- and not abundant. Modulus tectum clamps ment may take place. Green ova were also tightly on dead coral rubble when disturbed seen in M. modulus. and is dislodged with difficulty. It has a trans- Reproductive biology.•Spawn masses of parent operculum through which may be seen Modulus modulus are deposited at Link Port the foot, brightly colored with large orange at the same time as those of Cerithium spots and irregular white blotches on a black muscarum. Both species are abundant on pigmented background. These bright colors seagrasses, undergo direct development, and and the eye-like spots may startle predators their spawn is somewhat similar. Thus, spawn who are able to remove snails from the rocks. masses of both species may be confused and Males are smaller than females and both future workers should be alerted to this fact. sexes have highly colored soft parts. The They can be easily separated with careful ex- snout is dark brown and spotted with white amination. The spawn of Modulus is deposit- while the tentacles are reddish and papillate. ed along the axis of a seagrass blade as a The eyes are located near the distal ends of cylindrical tube with smooth outer walls and each tentacle, as in M. modulus. The foot is resembles a caterpillar, whereas that of reddish brown and covered with whitish Cerithium muscarum is a more irregular, disk- blotches and small brown dots. A large pro- like mass witli a lumpy outer surface. I have podial furrow is present. The foot is much figured the spawn of Cerithium muscarum broader than in M. modulus and serves to elsewhere (Houbrick, 1973: 880; 1974a: 78). keep the animal tightly clamped to the sub- The embryos and young snails of the two strate. The mantle edge has long pinnate or species are also different. Cerithium embryos multi-branched papillae in contrast to the do not have the pale green color of Modulus simpler mantle papillae of M. modulus. The embryos during their earlier stages of devel- hypobranchiai gland is smaller than that of M. opment. The embryonic shells and proto- modulus. When irritated, M. tectum does not conchs of newly hatched Cerithium muscar- emit salvos of sticky mucoid particles as does um are characterized by the purple color of M. modulus. Modulus tectum, however, the outer lip and umbilical region. The aper- makes the same violent twists as M. modulus ture is oval while in Modulus it is more angu- when irritated, but the former also clamps late. Finally, the embryonic shell and proto- down on the substratum to discourage preda- conch of Cerithium muscarum lack the spiral tors. striae so characteristic of Modulus. The thick, open palliai oviduct of Modulus The reproductive mode of the Link Port tectum is highly glandular and the outer lami- population of Modulus modulus is direct. It is na is internally more convoluted with glandu- interesting to note that Lebour (1945: 470- lar folds than that of M. modulus. The male 471), in Bermuda, and Bändel (1976: 258) in palliai gonoduct has a large yellow glandular Santa IVlarta, Colombia, each observed indi- area located on the inner lamina adjacent to rect development in Modulus modulus. These the columellar muscle. This may be homolo- observations are contrary to what I have seen gous to the structure seen in M. modulus and and present a discrepancy for which there are is probably a spermatophore-forming organ. several possible explanations: 1) Both Lebour Females of M. tectum have a large ovipositor (1945) and Bändel (1976) were mistaken on the mid right side of the foot that is identical about the identity of their specimens: 2) What 140 HOUBRICK has been called Modulus modulus in the short incubation period of 5-7 days prior to stenohallne environments of Bermuda and hatching, typical of indirect development. In the Caribbean is a separate species; 3) these populations the egg capsules dissolved Modulus modulus has two developmental and the veligers swam into the hollow center modes. of the spawn mass and then to the outside. The first explanation is unlil 142 HOUBRICK - - >^ GORE, R., JONES, R,,KERR,G., SEIBERT, H.. YOUNG, D., BUZAS, M., & YOUNG, M• 1976, VAN ZWECK, O., & WILCOX, J,, 1974, Indian Species densities of macrobenthos associated River study. First annual report. Harbor Branch with seagrass: A field experimental study of pre- consortium. Unpublished manuscript, 2 vols., dation. Journal of Marine Research, 34: 577- 385 p. 592.