STUDIES ON THE REPRODUCTIVE BIOLOGY OF THE GENUS CERITHIUM (GASTROPODA: PROSOBRANCHIA) IN THE WESTERN ATLANTIC
RICHARD S. (JOSEPH R.) HOUBRICKl Department of Biology, University of South Florida, Tampa, Florida 33620
ABSTRACT The reproductive biology of western Atlantic members of the genus Cerithium (C. muscarum, C. variabile, C. eburneum, C. floridanum, C. litteratum, and C. auricoma) is investigated. Pairing, spawning, descrip- tions of egg masses and early development are considered. Spermatophores and their method of transfer are described for C. muscarum. Eggs are laid by Cerithillm species in gelatinous strings or coils attached to a substratum as a tangled mass. There are two types of development in the genus in Florida: The first and most common is indirect development involving many eggs, rapid cleavage, a short encapsulated period, and emergence of free-swimming veligers. The second pattern, seen in C. mllscarum and C. variabile, in- volves direct development, fewer and larger eggs, and a longer period of encapsulation, with the young hatching only when metamorphosed as small crawling snails. Spawning and incubation periods, early developmental rates, and mea- surements of ova and larvae are established, and comparisons made with species from other parts of the world.
INTRODUCTION Knowledge of reproduction, development, and larval ecology of marine subtropical prosobranchs is sparse compared with that of north temperate species. In recent years our understanding of tropical species has increased considerably, but few members of the family Cerithiidae have been inves- tigated in any detail. Although many species of the genus Cerithium inhabit Florida and the Caribbean region, there are few published records of their reproductive anatomy, breeding habits, or early life histories. Reproductive anatomy of the genus Cerithium has been discussed by Sunderbrink (1929), Risbec (1943, 1955), Johansson (1947, 1953, 1956), Marcus & Marcus (1964 ), and Houbrick (1971). A summary of spawning and develop- mental information on the genus, from a worldwide point of view, is pre- sented in Table 1. Lebour (1945) described the eggs and larvae of C. ferrugineum from Bermuda, but it is unclear with which species she dealt, because C. ferrugineum is a synonym of C. variabile, and the egg masses and larvae depicted by her are definitely not those of C. variabile. Marcus
1 Present address: Supervisor for Invertebrates, Smithsonian Oceanographic Sorting Center, Smith- sonian Institution, Washington, D. C. 20560. 876 Bulletin of Marine Science [23(4) TABLE 1 SPAWNING AND DEVELOPMENTAL STUDIES ON THE GENUS Cerithium (x = published material)
Locale of study Authority C. auricoma Schwengel, 1940 x x x Florida D'Asaro (1970) C. lit/eratum (Born, 1778) x x x Florida D' Asaro (1970) C. {toridanum Morch, 1876 x x x Florida Torrance (1969) C. algicola C. B. Adams, 1848 x x x Jamaica Davis (1967) C. variabile C. B. Adams, 1845 x x x Florida Raeihle (1968) x x x Florida Houbrick (1970) C. atratum Born, 1778 x x x Brazil Marcus & Marcus (1964) C. ferrugineum Say, 1792 x x Bermuda Lebour (1945) C. stercusmuscarum Valenciennes, 1833 x x Baja California Wolfson (1969) C.morus Lamarck, 1822 x x x India Natarajan (1958) C. vulgatum Bruguiere, 1789 x Italy LoBianco (1888) C. ponticum Milaschewitsch, 1909 x Black Sea Chukhchin (1960) C. nodulosum Bruguiere, 1792 x x x Eniwetok Houbrick (1971)
& Marcus (1964) described the eggs and veliger larva of C. atrattlm, but the taxonomic position of this species is unclear. Breeding habits and larval development of closely related genera in the family Cerithiidae have likewise received little attention. Records include those of the genus Bittium (Thorson, 1946; Fretter & Graham, 1962; Mur- ray, 1969), and related genera in the Cerithiaceae: Cerithidea (Habe, 1955; Natarajan, 1958; Panikkar & Aiyar, 1939; Vohra 1970), and Ceri- thiopsis (Lebour, 1933, 1945). 1973] Houbrick: Reproductive Biology of Cerithium 877 The spawn masses for members of the genus Cerithium are described in the literature and in this study as tangled masses or flat coils deposited in gelatinous strings attached to the substratum. The ova of species discussed herein are typically telolecithal and exhibit holoblastic cleavage. In contrast with archaeogastropods and neogastropods, most larvae of mesogastropods tend to have indirect development and a long pelagic life. This is true of most of the species of Cerithium hitherto investigated. Their mode of reproduction and development is indicative of a typical pattern which in- volves many eggs, rapid cleavage and attainment of the veliger stage, and emergence as planktotrophic larvae. Since free-swimming larvae are hard to rear under laboratory conditions, most species of Cerithium are difficult subjects for complete life-history studies. Two of the species in this study, C. muscarum Say, 1832, and C. variabile C. B. Adams, 1845, were found to have direct development. The account which follows will first concern itself with these two species. Subsequently, the species with indirect development (C. eburneum Bruguiere, 1792, C. floridanum Morch, 1876, C. litteratum [Born, 1778], C. auricoma Schwen- gel, 1940) will be treated.
MATERIALS AND METHODS This study is based upon material collected in Florida. Observations were made in the field and laboratory from September 1968 through May 1971. Monthly samples and observations were taken at four field sta- tions, but other areas in the state were visited less regularly. The four main stations in Florida are located at Port Everglades (lat. 26° 6' N, long. 80° 4' W), Bear Cut (lat. 25° 44' N, long. 80° 8' W), Dunedin (lat. 28° l' N, long. 82° 47' W), and Mullet Key (lat. 27" 35' N, long. 82° 44' W). The first two stations are located on the lower east coast of Florida, where the environment and fauna are largely tropical and Caribbean in nature, while the latter two are located along the central Gulf coast of the state, where the marine fauna and environment are subtropical and largely Carolinian in composition. For life-history studies, various species of Cerithium were collected alive and maintained at a temperature of 25° C in aquaria of sea water with a salinity of 34i!c. Snails were fed on local algae from the Tampa Bay region and the detritus collected from grass beds. When snails spawned in the laboratory, eggs and larvae were reared at room temperature in finger bowls. Artificial sea water was used and was changed on a daily basis. No aeration was provided. Free-swimming veliger larvae were fed with dense cultures of Phaeodactylum tricornutum and CycloteUa nana, but despite such at- tempts no suitable food was found for the larvae. Living gametes and larvae were studied under oil or lower powers with a phase-contrast compound microscope, and drawings were made with the aid of a camera lucida. Eggs 878 Bulletin of Marine Science [23(4) and veligers were fixed in 60· C Bouin's solution for 3 to 4 minutes and transferred to 90 per cent ethanol before storage in 70 per cent ethanol, according to the method of Fretter (pers. commun.). Lynch's precipitation method of Grenacher's alcholic borax-carmine technique (Davenport, 1960) was used for whole mounts of larvae and eggs. Smears of spermatozoa were made using both the dry-smear technique and staining under the coverslip with Ehrlich's hematoxylin as suggested by Franzen (1956). Some sperm were fixed using Carnoy's fixative, but with poor results. Living spermato- zoa were stained with Janus green B in sea-water solution and observed under the compound microscope. Eggs and larvae were measured with an ocular micrometer and photomicrographs were taken of various develop- mental stages. Microscopic examinations of gonadal smears were made to determine sex ratios during the breeding season.
EXPLANATION OF LETTERING aI, albumen Ih, larval heart bm, basal membrane m, mouth ct, ctcnidium me, mantle edge dg, digestive gland mp, midpiece e, eye 0, operculum em, embryo s, stomach elm, external limiting membrane sh, shell f, foot st, statocyst hc, hyaline capsule t, tentacle j, jelly v, velum jc, jelly capsule z, zygote
REPRODUCTION, EGGS, AND LARVAE OF SPECIES OF Cerithium WITH DIRECT DEVELOPMENT 1. Cerithium muscarum Say, 1832 A population of C. muscarum from Mullet Key, Florida, was sampled monthly from April 1969 to February 1971. This population occurs just at, and below, the low-tide mark; extremely low tides will expose the entire population. C. muscarum is dioecious, with no apparent sexual dimorphism. A sex ratio of 1: 1.23 (39 per cent females; 48 per cent males) occurs during the middle of the breeding season. There is no evidence of sex reversal or hermaphroditism. Neuter specimens, due to parasitic castration by trema- todes, made up 13 per cent of the population. The breeding Season takes place from January through July, with more egg-laying activity occurring in the latter months. Gametogenesis.-Early in the reproductive season, females have cream- colored ovaries filled with oocytes and ova. The circular to oval ova average 1973] Houbrick: Reproductive Biology of Cerithium 879 800/.1.in diameter. Oocytes are smaller (700/.1.), and are distinguished from the ova by the presence of a germinal vesicle. During the early part of the reproductive period, winter maturation of eggs results in limited spawning, since many ova disintegrate within the ovary and are absorbed. During April, ova were observed moving down the ovarian duct into the open pallial gonadal duct, and sperm masses containing both eupyrene and apyrene sperm were seen in the female's sperm-collecting gutter. Only eupyrene sperm were found in the receptaculum seminis where they were oriented with their heads embedded in the receptaculum wall. In ripe males, the testes are bright orange and the seminal vesicles are packed with both eupyrene and apyrene sperm. The former were 40 /.I. in length and the latter 35/.1.. Eupyrene sperm are typical in form, having small heads, very long middle pieces and short flagella. Apyrene sperm have six flagella and heads 2 times the size of those of eupyrene sperm. Males produce small fusiform spermatophores, about 5 mm long and 2 mm wide, having a tapering mucus-like coiled strand at each end (Fig. 3, C). An outer membranous structure surrounds the central mass of sperm. More apyrene sperm occur in the central region of the spermatophore, while eupyrene sperm predominate near the edges of the mass. Pairing.-Pairing lasts from 1-3 hours. The male releases a spermatophore on the right pallial side, near the exhalant siphon. The spermatophore rests on the left anterior region of the female close to the inhalant siphon. The female occasionally touches the spermatophore with her snout and may rasp it with her radula. The male separates after transfer of the spermato- phore. The spermatophore then rests near the entrance of the female's mantle cavity for as long as 20 minutes. The spermatophore membrane disintegrates as it moves into the female's mantle cavity. Spermatophores often remain just beneath the margin of the mantle skirt and may take as long as 2 hours for total disintegration. Once this has occurred, the sperm pass to the right side of the mantle cavity by ciliary action of the mantle cavity's lining and are drawn into the open gonadal duct. Ciliary action then moves the sperm via the sperm-collecting gutter into the sperm-collecting pouch at the proximal end of the gonadal duct. From here they eventually pass to the receptaculum seminis. The method of transfer was not observed. Intact spermatophores seen on the bottom of aquaria where pairing took place indicate that not all attempts at transfer of spermatophores are successful. During pairing, both individuals are relatively inactive. The male is usually attached to the left anterior side of the female's shell so that his propodium makes contact near the edge of the female's foot or mantle skirt. Pairing was observed throughout the breeding period in both the field and laboratory. Spawning and Formation of Egg Masses.-Oviposition occurred during the months of January through June, suggesting a broad seasonal period of 880 Bulletin of Marine Science [23(4)
c
elm he
0.25mm he
he ~"~",,, .•,.,•.~.".""~ ~!"'~. ',.,~'.'~ '
em 0.5 mm elm FIGURE 1. A, Portion of egg mass of Cerithium muscarum; B, filament of egg mass of C. muscarum, showing egg capsules and embryos; C, 9-day embryo of C. muscarum, veliger stage, front view; D, II-day embryo of C. muscarum veliger stage, left side. reproduction. Although OvipOSitiOnoccurs as early as January, size-fre- quency data show that a peak of young individuals is reached in August, indicating that either great numbers of egg masses are deposited in June and July or environmental conditions are more favorable for the survival and development of the larval stages during this period. Egg masses are deposited on the angiosperms Thalassia, Ruppia, and Halodule, various types of algae, such as Viva, Hypnea, and Gracilaria, dead shells, stones, and other debris. In the laboratory, eggs are deposited on the walls of glass aquaria (Fig. 4, A). Oviposition takes place during both day and night. The behavior of a female (21 mm long, 9 mm wide) during the deposition of an egg mass was observed in detail. Short, jerky movements and turns of the foot occurred frequently as the eggs, embedded in a filament, emerged. The filament moved slowly from the right side of the mantle cavity near the exhalent siphon and proceeded down the right side of the foot in a furrow which was not evident at other times. Occasion- 1973] Houbrick: Reproductive Biology of Cerithium 881 ally, the filament emerged in "spurts" accompanied by jerky movements of the foot. During deposition, the tip of the shell periodically moved pen- dulously as the animal turned. The female's radula continuously rasped the side of the aquarium, perhaps preparing the surface for attachment. Ovi- position continued for 3~ hours, at which time the eggs in the initial portion of the mass were already undergoing cleavage and had reached the two- and four-cell stages. By 9 hours, late cleavage stages were evident. The egg masses of C. muscarum are deposited in long, tightly coiled filaments, which are compactly folded constituting spherical masses 15 to 30 mm in diameter (Fig. I,A). The filaments may be deposited loosely upon each other. They are composed of an external limiting membrane (elm, Fig. 1, A, B) and an internal jelly (j, Fig. 1, A, B) which is hard but resilient. Filaments are about 1 mm thick and are often externally coated with detritus and sand grains. The egg masses are also infested with nema- todes and ciliates, but few eggs are ever penetrated. Individual egg capsules, embedded within the gelatinous matrix of the filament, are arranged in pairs, each surrounded by a tough hyaline capsule (hc, Fig. 1,B). Within this hyaline capsule, the egg is surrounded and bathed in what is probably albumen (aI, Fig. 1,B) (Fretter & Graham, 1962). There are two layers of albumen, a viscous layer adhering to the inner surface of the hyaline capsule and a more fluid layer surrounding the egg. Within the egg capsule, zygotes average 250 p.. in diameter. There is an average of 70 eggs per cm of filament. A typical egg mass, uncoiled on a glass plate, is 700 cm in length and contains an estimated 52,000 eggs. Larval Development.-Cleavage is rather rapid, the 8-cell stage being at- tained within 4 hours of oviposition. Cleavage is spiral and unequal. Within 9 hours the 32-cell stage has been attained, with dark macromeres and lighter-colored micromeres. A stereoblastula appears in 2-3 days. Gastru- lation follows, brought about by epibolic growth of the micro meres over the macromeres. In the stereogastrula, a blastopore is not evident. Further development is rapid and by the fourth day a recognizable early larval stage has been attained. A prototroch is present and formation of the shell gland starts, indicating the beginning of the veliger stage. By the end of the fourth day, embryos show completed protoconchs. During this period an ill-defined stomodaeum is evident just above the pedal anlage. The apical plate region is ciliated. The cells here are generally smaller, in contrast to those in the large yolky region of the digestive anlage. Rotation of the embryo is first noticed during this stage. Rotation is within the albumen envelope and takes place in all directions. By five days, embryos have more prominent velar lobes, a better-defined foot, and the protoconch develops a cuplike shape completely covering the digestive gland. The mouth is well developed, lying between the velum and foot. No sign of an operculum is present. At 6-7 days of development the velum becomes 882 Bulletin of Marine Science [23(4) bilobed and weak eyespots appear. By 9 days an operculum appears (0, Fig. 1, C), along with further enlargement of the foot (f, Fig. 1, C) and the first evidence of coiling in the shell. The veliger has well-developed eyes (e, Fig. 1, C), a velum (v, Fig. 1, C), tentacle buds, and a rhythmically pulsating larval heart (lh, Fig. 1, C) just beneath the edge of the shell on the right side of the mantle cavity. In 10-11 days, a noticeably dextral protoconch with one coil appears, and the animal is able to retract com- pletely, closing the aperture with its operculum (0, Fig. 1,D). The tentacle buds (t, Fig. 1,D), eyes, and apical region are prominent, and the foot (f, Fig. 1,D) becomes very active. The ciliated ctenidium (ct, Fig. 1, D) and osphradium are prominent on the left side of the mantle cavity. The diges- tive gland is clearly visible through the shell. Many yolk granules are scattered throughout the digestive gland. The larvae, 250 JJ. long at this point, continue to spin within the egg capsules. After 11-12 days, the velum begins to shrink and the embryo, almost filling the egg capsule, creeps about it. It occasionally rasps and touches the capsule wall with its snout. No larval retractor muscles were observed and no sudden changes in symmetry were evident; accordingly the process of torsion remains unclear. Hatching.-Hatching from the egg capsule occurs when the larvae are about 2 weeks old. The velum disappears, and the apical region develops into the head region (snout) of the young snail. Upon emerging, young snails actively crawl about and feed on algae and detritus. It is not known whether the egg capsule breaks down because of the rasping of the radula or enzy- matic action. Newly hatched snails, now almost completely metamorphosed, average 0.5 mm in length from the snout to the apex of the shell. Rearing the young to adulthood was not successful.
2. Cerithium variabile C. B. Adams, 1845 A large population of C. variabile from Port Everglades was observed monthly from March 1969 to November 1970. This stable population was distributed intertidally, being exposed during each low-tide period. The reproductive season of this population is not as sharply defined as that of C. muscarum. Oviposition occurs throughout the year, but is most common and reaches its peak during late winter and spring. The greatest number of young appear during the late summer months, so that, although the reproductive period is prolonged, there is one broad peak. During this peak period of breeding, the population consists of twice as many females as males (59 per cent females; 25 per cent males), or a ratio of 2.4: 1. Sixteen per cent are neuter due to parasitic castration by trematodes. Length-width measurements of the shells of males and females show no significant sexual differences. There is no evidence of sex reversal or hermaphroditism. 1973] Houbrick: Reproductive Biology ot Cerithium 883 Gametogenesis.-Females dissected in January, the beginning of the breed- ing season, are found with oriented eupyrene sperm in their seminal recep- tacles, indicating that pairing is already underway. The cream-colored ovaries are tightly packed with ova and oocytes. The ova are spherical and are 200 Jk in diameter. In males, the orange-brown testes are filled with both eupyrene and apyrene sperm, identical in morphology at the light-microscope level to those already described for C. muscarum. Pairing.-Although pairing was frequently observed in the laboratory, the actual mechanism of sperm transfer was not discovered. C. variabile lacks spermatophore-forming glands in its gonadal ducts and does not produce spermatophores as does C. muscarum. Pairing resembles that already de- scribed for C. muscarum, and lasts from 20 to 90 minutes. Spawning and Oviposition.-C. variabile has no preference for any specific substratum for oviposition; egg masses are found on stones, leaves, and sticks, and on various marine plants and algae such as Rhizophora, Ruppia, Halophila, Graci/aria, and Acanthophora. Egg masses from several individ- ual snails often appear together. This is probably due to the high population density and is not indicative of communal egg-laying behavior. In an aquarium, egg masses are often deposited close to the surface of the water. They appear to be resistant to desiccation. In the field, eggs are frequently exposed to sun and air during low tide. Oviposition usually takes from 1 to 5 hours and the process is similar to that already described for C. l1luscarWll. As an example, a female began laying eggs at 11:45 A.M. and finished at 3: 10 P.M. A small semicircular mass about 1 cm in length and 0.5 em in width was deposited, containing approximately 250 eggs. The egg mass, unwound on a glass plate, was 37 mm long and the portion first laid contained embryos already in early cleavage stages. Egg masses are deposited in thin transparent filaments folded back and forth on themselves, forming flat, ribbonlike stacks (Fig. 2, A; 4, B). The end result is an arch- like or circular mass measuring from 1 to 2 cm. In the field, the egg masses may take on the configuration of the particular substrate to which they are attached by a basal membrane (bm, Fig. 2, A). Individual cylindrical fila- ments are 5 mm in width and consist of an external limiting membrane (elm, Fig. 2, A) enclosing a jelly matrix. The limiting membrane forms constrictions around each egg. Although the eggs are arranged in a single row within the filament, they appear to be arranged in "threes" due to the folded nature of the filaments. Zygotes (z, Fig. 2,A) are about 200 Jk in diameter and are enclosed within pock-marked double-walled hyaline cap- sules (hc, Fig. 2, A) averaging 400 Jk in diameter. The capsules contain a granular fluid albumen similar to that described for C. muscarum. Each hyaline capsule is surrounded by a larger jelly capsule (jc, Fig. 2, A) about 884 Bulletin of Marine Science [23(4)
z elm
he
he v v
st at
f
sh O.2mm sh
FIGURE 2. A, Portion of egg mass of Cerithium variabile; B, 3-day embryo of C. variabile, early veliger stage, right side; C, 3-day embryo of C. variabile, early veliger stage, front view.
550 Jk in diameter, continuous with or part of the limiting membrane of the filament. These capsules clearly separate consecutive eggs, but are not as well defined as the inner, hyaline capsules. Jelly capsules break easily, in contrast to the hyaline capsules, which are quite resistant and tough. Many eggs within some masses have two to three zygotes within one capsule. Eggs such as these undergo development normally. There was no evidence of adelphophagy or nurse-egg phenomenon. In the field, egg masses are not easily observed because the external 1973] Houbrick: Reproductive Biology of Cerithium 885 limiting membrane is usually covered with sand particles and other debris. As noted in C. muscarum, these masses are heavily infected with ciliates, nematodes, and polychaetes that do not seem to cause any appreciable damage. Larval Development.-The cleavage pattern of C. variabile closely follows that of C. nluscarum. By the end of 24 hours, most zygotes reach the 8-cell or more advanced stages. Gastrulation takes place by epiboly within I1h days, resulting in a stereogastrula. In contrast to C. muscarum, there is a well-defined blastopore. The gastrula is about 200 po and is more oval than that of C. muscarum. At the end of 2 days, an early larval stage is attained in which a shell gland, foot anlage, velar anlage, and stomodaeum are seen. Cilia are evident in the apical region and on the foot anlage, and the embryos begin rotating within their hyaline capsules. There is also some weak ciliation in the vicinity of the velar anlage, but this is not clearly defined. Within 3 days, a cuplike protoconch (sh, Fig. 2, B, C) completely covers the digestive gland. The velum (v, Fig. 2,B,C), foot (f, Fig. 2,B,C), and stomodaeum (st, Fig. 2, B, C) are more pronounced, and the veligers now rotate ran- domly by their preoral girdle of cilia within the capsules at a speed of 1 rotation per second at room temperature (240 C). The granular albumen is agitated by ciliary action as the embryos rotate. By 4 days, the first indication of an operculum appears. Development of the shell is rapid and by 5 days a single dextral coil is present. The larval shell differs from that of C. muscarum in that it is larger, more coiled, and has a lightly pitted surface. During this stage (5 days) the velum becomes bilobed and a prom- inent ciliated apical region appears. The larval heart is visible pulsating on the right side. A bilobed digestive gland along with much yolky material may be seen in the apex of the shell. Veligers at this stage average 200 po in length. Within six days, tentacle buds and eye spots are visible. By 8 days, the eyes become very dark and prominent, and the ctenidium and osphra- dium may be noticed by their heavy ciliary action on the left side. The bilobed digestive gland, intestine, and larval heart are also visible through the shell on the right side of the mantle cavity. No larval kidney was seen. At 10-12 days, the veligers are at an advanced stage in their development. The foot is very active and the velar lobes appear to be somewhat reduced. The shell has two dextral coils and is characteristically a tan color with red pigmentation visible in the sutures and on the outer lip of the aperture. The embryos are 325 po in length and almost fill the hyaline capsules. They are able to retract completely within their shells. As hatching approaches, the material of the outer surrounding jelly mass begins to break down. Torsion was not observed. Hatching.-Hatching usually occurs at an age of 2 weeks, but varies con- siderably, depending upon temperature. Embryos maintained at a constant 886 Bulletin of Marine Science [23(4) temperature of 20· C took as long as a month to hatch, while those kept at 24° C hatched in 12-18 days. At hatching the shells are 400 /L in length and have 2~ to 3 whorls. The young actively crawl about the substratum. No attempts were made to raise newly hatched snails to adulthood, but size-frequency data (to be presented in a later paper on growth) indicate that it takes about 1 year to attain maturity.
REPRODUCTION, EGGS, AND LARVAE OF SPECIES OF Cerithiwn WITH INDIRECT DEVELOPMENT 1. C. eburneum Bruguiere, 1792 A population of C. eburneum from Bear Cut, Miami, Florida, was sam- pled from May 1969 through February 1971. The population occurs subtidally in beds of Thalassia and in sandy areas. Although normally submerged, it is occasionally exposed during minus tides. The reproductive season of this species occurs from January through March. During this period the population had a sex ratio of 2: 1 (64 per cent females and 32 per cent males). The sex of 4 per cent of the population was impossible to determine because of parasitic castration by trematodes. Mean length of females was 2 mm greater than that of males, but no statistical differences in shell length or width were present. During the breeding season, oviposition occurs both in the field and laboratory, even though water temperature in the laboratory may be cooler (24° C-33° C). Although no egg masses were observed in the field or in the laboratory after March, oviposition may extend into the spring, because many young snails were seen in June, and females still had ripe gonads. Gametogenesis.-In May, females had yellow ovaries containing large spherical ova 200 fL in diameter. No oocytes were seen, but this may be because the germinal vesicles were difficult to detect. Just prior to the reproductive period, males had seminal vesicles packed with sperm, especially in the upper coils of the gonad. The sperm occurred in numerous disk-shaped masses in which the sperm heads converged toward the center while the flagella pointed radially in all directions. Such structures have been termed cytophores by Franzen (1956). The cyto- phores are 65 fL in diameter. Upon contact of cytophores with sea water, the sperm are slowly liberated. Both eupyrene and apyrene sperm are found in cytophores. An apyrene sperm bears six flagella and an enlarged head (Fig. 3,D), while a eupyrene sperm has a long middle piece and single short flagellum (Fig. 3,E). The apyrene sperm are 35 fL long, and the eupyrene are 40 fL long. Pairing.-Although C. eburneum was observed in what appeared to be a pairing position many times, the mechanism of sperm transfer was never 1973] Houbrick: Reproductive Biology of Cerithium 887
v
e v
s
0.14 mm
o E c
2.5 mm
FIGURE 3. A, Veliger of Cerithium floridanum, right side; B, veliger of C. floridanum, front view; C, spermatophore of C. muscarum; D, apyrene spermato- zoan of C. eburneum; E, eupyrene spermatozoan of C. eburneum. observed. It seems likely that sperm are discharged in compact clusters mixed with prostatic fluid in the immediate vicinity of the female's inhalant siphon. Fretter (1951) has suggested such a mechanism for Cerithiopsis. Spawning and Oviposition.-Egg masses found from January through March consisted of transparent cylindrical jelly strings, of a firm resilient consistency, covered with an external limiting membrane usually coated with sand and detritus. Early strings are filled with many ovate white zygotes and embryos. The filament is twisted and coiled upon itself to form an amorphous, tangled mass. An individual filament is about 990 fJ- in diam- eter and is packed with egg capsules. Four to five completely separate capsules occupy the diameter of a filament. There are about 455 capsules per centimeter of filament, and, although it is difficult accurately to untangle an egg mass and measure its total length, a conservative estimate of 85,000 888 Bulletin of Marine Science [23(4) eggs per mass can be made. The egg mass of C. eburneum has been de- scribed and illustrated as C. algicola by Davis (1967). Larval Development.-Individual egg capsules were observed in the labora- tory, where C. eburneum deposited its spawn on the glass walls of aquaria as well as on stones and algae on the bottom. Egg capsules are 130 p- in diameter. Zygotes in those portions of the spawn initially deposited have undergone cleavage by the time the last of the eggs have been deposited. Formation of an egg mass takes from 1-6 hours. Development occurs rapidly, so that a solid gastrula is formed within 24 hours. By 48 hours, trochophores are detected. About one in 10 eggs remains undeveloped, but undeveloped eggs do not function as nurse eggs. Early larvae have prototrochs and apical tufts with compound cilia of considerable length. Within 3 days, early veliger stages with extensive ciliation are observed. A ciliated foot, statocysts, a shell covering the digestive gland, intestine, stomach, and heart are visible, as well as a bilobed velum bearing long compound cilia that beat slowly within the albumen and rotate the embryo. By the third day, the operculum is visible as well as a brown, bilobed digestive gland. The statocysts are prominent between the foot and the stomodaeum. Veligers average 95 fL in length and the egg capsules average 144 p- in diameter. The veligers with their long velar cilia appear nearly to fill the capsules at this point and continue to rotate slowly in all directions. Hatching.-During the third and fourth days, hatching occurs. At the time of hatching, the jelly filaments, if touched, rupture easily and disintegrate. Hatching takes only a few minutes and appears to occur by the weakening of the capsule due to the ciliary action of the embryo. This was also the observation of Davis (1967) on eggs of C. algicola, from Jamaica. Freed veligers are tan, but somewhat transparent. The velar cilia no longer appear to be of a compound nature, but are single. Black eye spots, tentacles, and an apical region with long cilia are prominent. The foot is well developed and is also ciliated. The shell is a coiled, caplike structure consisting of one bulbous whorl with a rather large aperture and a moderate beaked edge. It is transparent and the internal organs and a heart beat are visible. Veli- gers were maintained for 3 days after hatching in 1000-ml beakers of sea water, where they were observed to swim consistently to the top of the container, retract into their shells, and sink to the bottom. They were fed with Phaeodactylum tricornutum and Cyclotella nana, but at the end of 3 days most had died.
2. C. {loridanum March, 1876 A large population of C. {loridanwn was studied at Dunedin, Florida, from June 1969 to February 1971. This population occurs just below the 1973] Houbrick: Reproductive Biology of Cerithium 889 low-tide mark, burrowing in pockets of sand among the rubble. The reproductive season is from March through July. A sex ratio of 1: 1 (45 per cent females and 47 per cent males) existed in April, with 8 per cent of the population exhibiting parasitic castration. Oviposition occurred in the field and laboratory, but few immature snails were ever found in the population, with the exception of a few in January and November. Gametogenesis.-In April, the gonads of males are bright orange and eupyrene sperm are in the sperm duct of the upper coils. Sperm masses from the sperm-collecting gutter of the pallial oviducts in females contain both apyrene and eupyrene spermatozoa closely resembling those described for C. eburneum. Ovaries are a yellow-cream color during the breeding season, and contain eggs as well as oocytes with prominent germinal vesicles. In the aquarium, snails are often found in a pairing position, but the mechanism of sperm transfer remains unknown. Spawning and Oviposition.-During oviposition, a bulge on the right side of the foot molds the egg mass and attaches it to the substratum. This has been described in C. atratum by Marcus & Marcus (1964). In the field, egg masses are attached to rocks and are covered with sand grains, render- ing detection difficult. In the aquarium, where they are cleaner, they consist of stringy masses of filaments. A filament is 450 jl< in diameter and is covered with an external limiting membrane (Fig. 5). Filaments are attached to the substratum by a basal membrane. Four to five zygotes are found within the diameter of a filament, and there are about 400 eggs per centimeter of filament. Completely unwound egg masses average 80 cm in length, and one mass was estimated to contain about 32,000 eggs. An egg mass from Boca Raton, Florida, contained 26,000 eggs. The spawn of C. fioridanum closely resembles that of C. eburneum, except that the filaments are looped back upon themselves, forming knotlike clusters. The spawn of C. fio- ridanum has been illustrated by Torrance (1969).
Larval Development.-Egg capsules (130 jl<) are found with zygotes (100 jl<) in different stages of development, according to their position in the egg mass. Cleavage is rapid and within 4-12 hours a blastula is formed, fol- lowed by a gastrula stage at 12-24 hours. Trochophores are seen in Ph days and veligers in 2-3 days. The veligers of C. fioridanum (Fig. 3, A, B) look much like those of C. eburneum. Encapsulated veligers have compound cilia. Statocysts (st, Fig. 3,A,B), digestive gland (dg, Fig. 3,A,B), stomach (s, Fig. 3,A), and heart may be seen through the transparent shell. At the end of 3 days, hatching occurs. Hatching.-At the time of hatching, the jelly filament begins to break down and the ve1igers emerge from their hyaline capsules with the aid of ciliary 890 Bulletin of Marine Science [23(4)
FIGURE 4. A, Cerithium muscarum, depositing egg mass; B, portion of egg mass of C. variabile. 1973J Houbrick: Reproductive Biology of Cerithium 891 action of the velum. Free veligers are rapid swimmers and are 180 J1. long (Fig.3,A,B). They have long cilia on a prominent velum (v, Fig. 3,A,B), a well-defined mouth (m, Fig. 3,B), and prominent eye spots (e, Fig. 3,B). The statocysts (st, Fig. 3, A, B), are clearly visible at the base of the foot (f, Fig. 3, A, B). The shell is tan and coiled, and the stomach (st, Fig. 3, B) and bilobed digestive gland (dg, Fig. 3, A, B) are prominent. Veligers were maintained alive for 3 days after hatching and fed on Phaeodactylum tricornutum and Cyclotella nana. They could not be kept alive any longer, and the length of their planktonic life is unknown.
3. C. litteratum (Born, 1778) An abundant population of this species was examined subtidally at depths of 1-3 m off Boca Raton, Florida. Sporadic observations were made there, as well as on populations from the Florida Keys. C. litteratum is dioecious. Although only a few samples were taken of this population, oviposition was observed to occur during June and July. Snails from the population also spawned in the laboratory during that period. D'Asaro (1970) kept this species in spawning condition in the laboratory from January through October, and suggested that C. litteratum probably spawns throughout the year. Gametogenesis.-In July, females had white ovaries, in which many small spherical to oval ova averaging 65 J1. in diameter were seen. Sex ratios were not determined, no males were dissected, and pairing was not observed. Spawning and Formation of Egg Mass.-Oviposition, illustration of the egg mass, and type of development have been described by D' Asaro (1970). The eggs laid by the Boca Raton population were deposited in tangled pinkish jelly masses closely resembling those of C. eburneum. Individual cylindrical filaments 540 J1. in diameter are surrounded by a limiting mem- brane. A thicker, stringy gelatinous portion functions as a basement mem- brane attaching the filament to the substratum. There are about 550 cap- sules per cm of filament. A small egg mass 16 cm in length contained about 8800 eggs. Some egg-mass filaments contained what appeared to be larger jelly capsules averaging 300 J1. in diameter, within which 7-20 egg capsules were found. Larval Development.-Development appears to be almost identical to that which I have described for C. eburneum. Blastulation and gastrulation occur in 10 hours. In 24 hours, early larval stages are present and revolution of the embryos within the capsules commences. By the second day, veliger stages with well-developed compound cilia, prominent velar lobes, a foot with oper- culum, shell, and statocysts appear. Veligers average 100 J1. in length and closely resemble those described for C. eburneum. 892 Bulletin of Marine Science [23(4)
FIGURE5. Filament from egg mass of Cerithium fioridanum.
Hatching.-By the end of the third day, egg masses disintegrate and cap- sules rupture. Hatching follows with the liberation of free-swimming veli- gers much as described for C. eburneum. The free larvae could not be maintained in aquaria. The length of the planktonic life remains unknown; however in August, one month after the first egg masses were observed, many tiny snails were seen in the population. It does not follow that these were from the generation that hatched out in July; they may have come from earlier spawns, since this species appears to spawn throughout the year. 1973] Houbrick: Reproductive Biology of Cerithium 893 4. C. auricoma Schwengel, 1940 This is an uncommon species in Florida, and it was difficult to locate a suitable population for study. In July 1970, one observation was made on a population at Sand Key, about 10 miles off Key West, Florida. The snails oCCur subtidally at a depth of about 3 m, living among sand and rubble on the bottom. No egg masses were observed from this population, although there were several young snails present and 29 per cent of the population showed new growth. D'Asaro (1970) has described and illus- trated the spawn of this species from Margot Fish Shoal, Florida. The egg mass is similar to the spawn of C. eburneum, C. floridanum, and C. lit- teratum. D'Asaro (1970) estimated that there were 600 egg capsules per em of filament and about 90,000 embryos per spawn. Development is indirect, with a free-swimming stage. Length of planktonic life is unknown.
DISCUSSION In the preceding life-history studies, the gametes, egg capsules, and larval development have been described for most of the western Atlantic species of Cerithium. Additional information has been compiled from a literature survey. Results of this study and those of other authors are summarized on a worldwide basis in Tables 2, 3, and 4. Most marine invertebrates are seasonal in their reproduction (Giese, 1959), and even tropical marine invertebrates tend to breed during certain periods (Gunter, 1957; Vohra, 1970). Many of the species of Cerithium studied during the course of this investigation show definite breeding periods. The environmental parameters and internal mechanisms which initiate gametogenesis in Cerithium and promote spawning are not known. Control of gametogenesis in mollusks may be either exogenous or endog- enous (Loosanoff & Davis, 1952). These authors demonstrated that some exogenous factor, such as temperature control, stimulated gametogenesis in Venus. Temperature has also been shown to stimulate gonadal develop- ment in Aplysia (Smith & Carefoot, 1967). Webber & Giese (1969), in a discussion of this subject, point out that another exogenous factor, nutrition, does not appear to control gametogenesis. They suggested photoperiod as another possible mechanism. The environmental parameters related to egg laying have been recently discussed by Allen (1963) and Vohra (1970). Although some studies of endocrine control have been described in detail for cephalopods (Wells & Wells, 1959), little is known about endocrine control or any other endogenous factors in mollusks. Tombes (1970) suggested that sexual maturation of prosobranchs may be related to certain groups of neurosecretory cells. Temperature and photoperiod may be the remote causes of the initiation of gametogenesis in Cerithium. Once the process is initiated, further changes in temperature and photoperiod do not affect the animals, because spawning and pairing occur in different environ- 894 Bulletin of Marine Science [23(4 ) ,-.. '
E: E: :::: E: E: <::l ::: E: E: 1::: ::: :::: ::: ~ III •... E: E <:l'" :::: •... 1::: <:l :::: '" <::l ~ ~ •... ~ <..> ~ ::: .~ <..> <::l .;::: III .;:: ";:l •... :::: •... t3•... <:l ~ '":::: .;:: <:l ooC:l ::: <:l <:l <::l q::, III ~ <::l t; l: E :::.. E ;>. 0 0 0 0 0 \.5 0 0 0 0 1973] Houbrick: Reproductive Biology of Cerithium 895 TABLE 3 EARLY DEVELOPMENTALRATES IN Cerithium
Early larval Veliger Blastula Gastrula stage stage Authority C. eburneum 2-12 hrs 24 hrs Ph days 2'1:1. days This study C. fioridanum 4-12 hrs ] 2-24 hrs )112days 2-3 days This study C. litteratum 12 hrs 12-24 hrs I-IV2 days 2 days This study; D'Asaro (1970) C. auricoma C. atratum 3 days Marcus & Marcus (1964) C. nodulosum 5 hrs 12 hrs 1 day 2 days Houbrick (1971) C. mOrtIs 3 days Natarajan (1958) C. variabile 1-1112 days 11/2-2 days 2-3 days 3-4 days This study C. muscarllln 1-3 days 3-31/2 days 4 days 4-5 days This study mcnts, the field and laboratory, and such differences (light and temperature) do not appear to make any difference. It is interesting to note that C. muscarum and C. varia bile begin spawning during the winter months, while most species spawn latcr in the spring. Winter environmental factors may severely limit the survival of the zygotes. Although most of the young are seen in the summer, there is no noticeable difference in the amount of spawn produced in the winter from that produced in late spring. All species of Cerithium observed produced eupyrene and apyrene sper- matozoa. Spermic dimorphism is well known in gastropods, but the exact function of the apyrene sperm is unknown and has been the subject of several studies. Among the more noteworthy is that of Reinke (1914), who
TABLE 4 AVERAGEMEASUREMENTSOF EGGS ANDLARVAEOF Cerithium
Ovum Egg capsule Veliger Authority
C. eburneum 90 J.t 130 J.t 95 J.t This study C. litteratum 100 J.t 133 J.t 100 J.t This study C. fioridanum 100 J.t 130 J.t 180 J.t This study C. auricoma 90 J.t 112 J.t D'Asaro (1970) C. nodulosum 200 J.t 280 J.t 300 J.t Houbrick (1971) C.morus 120 J.t 160 J.t 200 J.t Natarajan (1958) C. ponticum 74 J.t 130 J.t 175 J.t Chukhchin (1960) C. variabile 200 J.t 400 J.t 200 J.t This study C. muscarum 250 J.t 500 J.t 250 J.t This study 896 Bulletin of Marine Science [23(4) studied the development of apyrene sperm in Strombus raninus. He sug- gested that the apyrene sperm may serve as nurse cells to the eupyrene sperm after copulation and before the latter reach the receptaculum seminis. He further suggested that since they undergo catabolic changes in the uterus of the female, resulting in the total exhaustion of albuminous bodies, they may, by the liberation of some substance, stimulate the eupyrene sperm, the eggs, or both, during fertilization; they might also act in the final disposi- tion of eupyrene spermatozoa by liberating some substance to which eupy- rene sperm are negatively chemotactic. Woodard (1934, 1940) has exam- ined spermic dimorphism in Goniobasis, a freshwater pleurocerid related to Cerithium. He studied the gametogenesis of both types of sperm and found that the spermatozoa of Goniobasis form clumps whenever released from the concentrated state in which they normally exist. This is the result of entanglement of the flagella of the apyrene spermatozoa, with the eupyrene spermatozoa being inactive and passively included. Since the eupyrene spermatozoa do not clump in the absence of the apyrene ones, the phe- nomenon of clumping may be a mechanism which serves to insure the segregation and final disposition of the eupyrene spermatozoa in the female tract. It also prevents the premature dispersal of the eupyrene spermatozoa. Clusters of spermatozoa, in which the sperm are arranged around a cen- tral cytophore, have been described in this paper for Cerithium eburneum, and are not uncommon in the Mollusca. Such structures have been dis- cussed by Franzen (1956). Spermatophores, as found in C. muscarum, have never been recorded in a marine member of the family Cerithiidae. They have been found in Littorina (Lenderking, 1954) and in the vermetids (Hadfield, 1969). The spermatophores of C. muscarum are almost identical with those described and illustrated for Goniobasis by Jewell (1931), Woodard (1934; 1940), and Dazo (1965). Both eupyrene and apyrene sperm were found in the spermatophores of C. muscarum, in contrast to those of Goniobasis, which contained only eupyrene sperm (Woodard, 1934). The morphology of both eupyrene and apyrene spermatozoa observed during this study of Cerithium agree closely with those illustrated by Tuzet (1930) for the Mediterranean species, C. vulgatum. The eupyrene sperm also bear a close resemblance to those of the closely related genus Bittium and of Scala (Franzen, 1956). With the exception of C. muscarum, where spermatophores are used, the mechanism of sperm transfer was not observed in any other species. Pre- sumably, it is much like that described by Fretter (1951) for Cerithiopsis, a member of the Cerithiaceae. In this species, sperm mixed with prostatic secretion leave the mantle cavity of the male in the exhalant stream and are sucked through the inhalant siphons of adjacent females before becom- ing dispersed in the surrounding water. 1973] Houbrick: Reproductive Biology of Cerithium 897 The spawn of the local species of Cerithium, with the exception of the two species with direct development, is similar to spawn described for the genus in other parts of the world. Numbers of eggs per spawn vary with the size of the animal and time of the year. The egg masses of the related genus Cerithidea are somewhat similar (Habe, 1955) as are those of Bittium (Murray, 1969). The large, distinctive egg mass of the Indo-Pacific C. nodulosllm has been described by Houbrick (1971). In general, the egg masses of most of the species with a pelagic larval phase are difficult to distinguish. In some reports, confusion is compounded due to the uncertain taxonomic status of the species in question. The spawn of C. algicola has been described by Davis (1967) and closely resembles the spawn of C. eburnellm from the Biscayne Bay population. Abbott (1958) has suggested that C. algicola C. B. Adams, 1848 is merely a form of C. eburneum. Lebour (1945) described the egg mass of C. ferrugineum Say, 1792, a synonym of C. variabile. However, her figures bear no resemblance to the spawn of C. varia bile from Florida populations. I believe she may have described the spawn of the potamidid, Batillaria minima, a species frequently confused with C. variabile, and one which occupies the habitat she depicted. An cerithiids invest their egg capsules within jelly filaments. According to Fretter & Graham (1962), the jelly in some mesogastropod egg masses prevents the spawn from drying and protects the embryos from infection. It is significant that more jelly is found in the species with direct develop- ment. The albumen, divided into viscous and fluid layers surrounding the eggs of C. muscarum and C. varia bile, is similar to that in the egg capsule of Littorina littoralis (Fretter & Graham, 1962). Franc (1941) suggested that in Ocenebra the movement of the embryo in the albumen mixes en- zymes produced by the embryo in the surrounding albumen so that it becomes less viscous and is conveyed by the cilia to the mouth. Blastulation and gastrulation in Cerithium are similar to those described for Crepidula and other mesogastropods (Conklin, 1897). The direct development and larvae of C. muscarum and C. varia bile bear striking resemblance to the development and larvae of Littorina obtusata, L. lit- toralis, L. saxatalis, and Lacuna pallidula (Pelseneer, 1911; Fretter & Graham, 1962). It is surprising that no larval kidneys were observed in C. variabile or C. muscarum, since they are prominent in other mesogas- tropod larvae with direct development, such as Littorina and Lacuna (Pel- seneer, 1911; Fretter & Graham, 1962). The exact process and time of torsion in the species of Cerithium studied in this project were not detected, because detailed morphological studies on the internal anatomy of the larvae of each species would be necessary to document this. However, my observations on the species with indirect development suggest that torsion may occur shortly before hatching, because at this time the ctenidia of the larvae are located on the left side of the 898 Bulletin of Marine Science [23(4) mantIe cavity and both the encapsulated larvae and the hatched free-swim- ming veligers are able to retract completely into their shells. A type of torsion involving differential growth which does not cease until after hatching, has been described for some monotocardian gastropods with direct development: Littorina obtusata (Delsman, 1914), Lacuna pallidula (Pelseneer, 1911), Crepidula adunca (Moritz, 1939), and Littorina lit- taraTis (Fretter & Graham, 1962). Fretter & Graham (1962) have dis- cussed this lesser-known type of torsion and pointed out that in some specialized monotocardian mollusks, no larval muscles are developed before torsion is accomplished. Consequently, the process relies more upon differ- ential growth of the whole embryo and is not brought about in the classical manner by asymmetrical growth of the larval retractor muscles. In this study, the larvae of the two species with direct development, C. variabile and C. muscarum, closely resemble the larvae illustrated by Pelseneer (1911) for Littorina obtusata and Lacuna pallidula and may undergo similar development. Although the larvae of these two species of Cerithium are opaque, rendering observation of internal organs or muscles difficult, it is suggested that torsion may likewise occur in them by slow differential growth. The velum in Cerithiwn muscarum and C. variabile appeared to shrink somewhat prior to their hatching, but was not observed being discarded or ingested as recorded by Fretter (1972) for Lacuna, Crucibulum, Crepipa- tella and other monotocardians. In the preceding study, gametes, egg masses, and larval development have been described for most of the western Atlantic species of Cerithium. This study indicates that the mode of reproduction and development of the genus Cerithium in Florida is not indicative of a typical pattern but, rather, that there appear to be two patterns. The first and most common is the pattern seen frequently by past workers and in this study for the species with indirect development. This pattern involves many eggs, rapid cleavage and attainment of the veliger stage, a short encapsulated period, rapid torsion, and emergence of free-swimming planktotrophic veligers. This is followed by a pelagic phase of varying length before settling occurs. It is the type of pattern described for other genera of the Cerithiaceae, Bittium (Fretter & Graham, 1962), Cerithiopsis and Triphora (Lebour, 1933; Fretter, 1951). The second pattern was seen in the two Florida species with direct development and involves more jelly in the egg mass and tougher hyaline capsules, generally fewer and larger eggs, a slower encapsulated develop- ment, torsion possibly brought about by differential larval growth, and hatching when the young are completely metamorphosed. This mode of reproduction and development has not been previously described in any marine members of the family Cerithiidae except for the brief notes of 1973] Houbrick: Reproductive Biology of Cerithium 899 Raeihle (1968) and Houbrick (1970). This second pattern may possibly be correlated with the fact that such species are frequently exposed at low tides and may undergo periods of desiccation. However, this explanation is not entirely satisfactory, because some prosobranchs living high in the splash zone, such as the littorinids Tectarius, Nodilittorina, and Littorina, have an indirect development and pelagic larvae (Borkowski, 1970). An- other possible correlation may be the fact that C. muscarum and C. variabile appear to be more euryhaline than other species of Cerithium. Both species are found in brackish as well as oceanic environments, but it is unclear just what adaptive benefits direct development would confer in such a situation. All other species of Cerithium in Florida are distinct subtidal dwellers and appear to be more stenohaline, rarely being found in brackish environments. Thorson (1940) has pointed out that the percentage of prosobranchs in the Iranian Gulf without pelagic development is considerably larger among the tidal-zone dwellers than among the more submerged forms. The differences in species of the same genus with direct and indirect development are undoubtedly adaptive ones correlated with their ability to survive in their respective environments. The success of a species is largely dependent upon its ability to produce and maintain its larval stages. Fioroni (1967) has dealt comprehensively with this subject and has clas- sified the various types of development in a comparative study of proso- branch embryogenesis. Different types of larval development in populations of the same species inhabiting different, sometimes very closely situated regions have been recorded in polychaetes, wood-boring lamellibranchs, and some proso- branch gastropods. For example, Littorina angulifera has pelagic larvae at the beginning of its annual reproductive period, but later, the mode of reproduction changes to incomplete viviparity (Lenderking, 1954). Thor- son (1940) has recorded different modes of development in geographically separated populations of Planaxis sulcatus; namely, viviparity followed by a pelagic phase, indirect development with nurse eggs, and parthenogenesis. The prosobranch, Polinices triseriata undergoes direct development during years with wet, cool summers, and semiplanktonic development during years with dry, hot summers (Giglioli, 1955). Phenomena such as these have recently been reviewed by Mileikovsky (1971) and do not appear to be that unusual. Thus, C. muscarum and C. variabile may undergo indirect development in other parts of their range or under different environmental conditions, and further study is needed.
ACKNOWLEDGMENTS This paper forms part of a series dealing with the biology of the genus Cerithium. The work was done as part of a Ph.D. program at the University of South Florida at Tampa, under the direction of Dr. Joseph L. Simon. 900 Bulletin of Marine Science [23(4) I am indebted to him for his help, guidance, and criticism during the project. My thanks are also due to the members of my committee and the faculty of the Department of Biology. Appreciation is also extended to Dr. Vera Fretter of the University of Reading, England, for her helpful advice and encouragement. SUMMARY All species of Cerithium examined produce eupyrene and apyrene sper- matozoa. Only eupyrene spermatozoa are found in the receptaculum seminis. Cerithium muscarum produces spermatophores containing both eupyrene and apyrene spermatozoa. Spermatophore transfer to the female occurs by water currents generated by ciliary action of the siphons and mantle cavity. Spawning occurs from winter through spring in most species. Egg masses are deposited as tangled masses of gelatinous strings attached to a sub- stratum. Members of the genus Cerithium in Florida exhibit two modes of develop- ment, direct and indirect. C. muscarum and C. variabile have larger and fewer eggs than other species of Cerithium and undergo direct development. Cerithium eburneum, C. {Ioridanum, C. litteratum and C. auricoma produce many eggs and undergo indirect development with free-swimming veliger stages.
SUMARIO
ESTUDIOS SOBRE LA BIOLOGIA DE LA REPRODUCCI6N DEL GENERO Cerithium (GASTROPODA: PROSOBRANCHIA) EN EL ATLANTICO OCCIDENTAL Se investiga la biologia de la reproducci6n de los miembros del genero Cerithium en el Atlantico occidental (C. muscarum, C. variabile, C. ebur- neum, C. {Ioridanum, C. litteratum y C. auricoma). Se consideran el apa- reamiento, el desove, descripciones de las masas de huevos y las primeras etapas del desarrollo. En C. muscarum se describen los espermat6foros y el metodo de ser transferidos. Las especies de Cerithium depositan los huevos en cord ones 0 espirales gelatinosos adheridos al substrato en forma de masa enredada. En la Florida se presentan dos tipos de desarrollo del genero: el primero y mas comun es desarrollo indirecto que comprende muchos huevos, seg- mentaci6n rapida, un periodo corto de encapsulaci6n y la emergencia de larvas vellgeras nadando libremente. El segundo, observado en C. muscarum y C. variabile, comprende desarrollo directo, huevos menos numerosos y mayores y un periodo mas grande de encapsulaci6n, con los j6venes na- ciendo s610 cuando ya se han transform ado en pequeii.os caracolitos que se arrastran. Se establecen los periodos de desove e incubaci6n, proporci6n de las 1973] Houbrick: Reproductive Biology ot Cerithium 901 primeras etapas del desarrollo y medidas de los huevos y larvas, y se hacen comparaciones con especies de otras partes del mundo.
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NOTE ADDED IN GALLEYS During the time between submission and publication of this paper, the author completed a taxonomic revision of the genus Cerithium, which is presently in press with Johnsonia. Three of the names used in the present paper are now considered to be synonyms: Cerithium variabile = C. lutosum Menke, 1828; Cerithium fioridanum = C. atratum (Born, 1778); and Cerithium allricoma = C. guinaicum Philippi, 1849.