Egg Capsules of Eleven Marine Prosobranchs from Northwest Florida

BULLETIN OF MARINE SCIENCE, 39(\): 76-91,1986

EGG CAPSULES OF ELEVEN MARINE PROSOBRANCHS FROM NORTHWEST FLORIDA

Charles N. D 'Asaro

ABSTRACT Egg capsules of eleven prosobranchs are described and illustrated, including Strombus ala/us, Murex fulvescens, Urosalpinx perrugata, Favartia cellulosa, Eupleura sulcidentata, Calo/rophon ostrearum, Cantharus cancellarius, C. multangulus, Fasciolaria /ilium hunteria, Conus j/oridanus j/oridensis, and C. jaspideus stearnsi. Enumerations of capsules and embryos, and capsular dimensions, developmental pattern, and observations on reproductive behavior are given.

Along the northwest coast of Florida, prosobranch egg masses are conspicuous, even to the casual observer, because they are concentrated on certain substrata. In a barrier island environment where shifting sand predominates, and where there is little exposed native rock, prosobranchs requiring unfouled, solid substrata for oviposition have limited choices. Thus they aggregate to spawn on available substrata, often in multispecific populations. Aggregation on available, unfouled substrata leads to use of novel substrata for spawning: exuviae of arthropods, especially Limulus polyphemus, and plastic and aluminum debris. Egg masses and capsules of some aggregating and non aggregating prosobranchs from Florida have been described by Perry and Schwengel (1955), D' Asaro (1970), Radwin and Chamberlin (1973), and others. Many commonly observed species remain undescribed. Also, some existing descriptions are incorrect, usually because field observations were not confirmed by laboratory observations. Descrip- tions that are hard to decipher and lack adequate illustrations drawn in perspective or to represent an average specimen from several egg masses make identification difficult and prevent comparison with related species. The purpose of this report is to provide descriptions and illustrations for identifying egg capsules of 11 species of prosobranchs encountered in northwest Florida.

METHODS

Specimens were collected in spring and summer between September 1981 and April 1984 at high salinity stations between Pensacola Bay and St. Joseph Bay in northwest Florida. At least 10 egg masses of most species were collected. Temperature and salinity were recorded in situ. Spawning was confirmed in the field by observing egg capsules in the pallial oviduct or pedal gland of spawning females and by holding spawning females and attending males in the laboratory in a 400-liter recirculating seawater system (22-24"C, 30-340/00).Spawners were isolated in nylon-mesh cages with abundant, living food-organisms and natural substrata for spawning, until another egg mass was produced. Egg masses were preserved in 10% seawater formalin. Illustrations were prepared from newly deposited, preserved egg capsules using Wild M-5 or M-20 microscopes equipped with drawing at- tachments. Several egg capsules taken from near the center ofthree or four egg masses were compared during the process. Correct aerial perspective in terms of lines and shading, as demonstrated by Knudsen (1966), was a primary concern. Measurements were taken from 10 centrally positioned capsules, ignoring spines, selected from three or four egg masses. The greatest dimension or that between the basal membrane and the apical plate with an escape aperture defined length ofa capsule. Width was the greatest dimension at right angles to length. Thickness was the greatest dimension at right angles to length and width. Morphological terminology is that used by D'Asaro (1970); identification and systematic terminology are based on Abbott (1974). Egg masses of each species and spawning females of the smaller species were deposited in the National Museum of Natural History, Washington, D.C. Catalog numbers identifying appropriate lots are included with each description. 76 D'ASARO: EGG CAPSULES OF PROSOBRANCHS 77

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RESULTS Strombus alatus Gmelin, 1791 (USNM 847142) Figure lA Spawning conchs were observed in S1. Joseph Bay on sandy substrata, 2 m deep. Such areas were adjacent to extensive Thalassia testudinum beds or lay 78 BULLETIN OF MARINE SCIENCE, VOL. 39, NO. I, 1986 between occasional sparse patches of the same seagrass. No spawn was found in the grass beds. The preferred spawning sites were crisscrossed by conch tracks. Deviations in the tracks often led to completed egg masses that appeared as slight, sandy mounds on the substratum. Males were following females, and copulating and attempting to copulate during oviposition. This pattern of behavior is similar to that reported for S. pugilis by Bradshaw-Hawkins and Sander (1981). Strombus alatus egg masses are roughly crescentic, nearly thick as wide, and are molded by the propodium and shell from sand-encrusted tubes containing egg capsules. Crescentic masses are formed gradually, from one end to the other, by dorsoventral looping movements of the propodium. In eight egg masses examined, the sand encrusted tubes were positioned parallel and perpendicular to the width of the crescentic masses. None were positioned parallel to the long axis. Egg masses were compact, with few large internal spaces. Two masses of average size, as produced by this spawning population, contained approximately 87,000 and 97,000 embryos (based on counted subsamples and total length of the outer tube; Table 1). Gross anatomy of egg capsule bearing tubes is similar to other strom bids from Florida (Robertson, 1959; D'Asaro, 1970). Each bilayered tube is composed of an outer layer with indistinct linear plications and occasional indistinct annula- tions at irregular intervals that were probably caused by pauses during oviposition (Fig. lA) and a transparent inner layer. Sand grains are very securely cemented to the outer surface of this tube. Spherical, transparent egg capsules, each containing a single embryo, are enclosed in a second, very transparent, mucous thread and coiled in a somewhat helical manner. In sections of the tube, coiling may give the impression that capsules are arranged in two roughly parallel rows separated by mucus. Average capsular diameter is 0.17 mm. Development is indirect with a planktotrophic veliger stage (Thiriot-Quievreux, 1983).

Murexfulvescens Sowerby, 1834 (USNM 847149) Figure IB-D Three prosobranchs produce the largest and most conspicuous communal egg masses in shallow coastal waters of northwest Florida: Thais haemastoma j/.ori- dana (Conrad, 1837), Murex pomum Gmelin, 1791, and Murexfulvescens. Spawn of M. fulvescens was observed only in habitats with considerable hard substrate (shell reefs, jetty rock, or rocky ledges several kilometers offshore in the Gulf of Mexico). Small egg masses «50 capsules) produced in the laboratory or observed in the field are not a good measure of fecundity. In the field with conspecifics present, an individuall O-cm long can produce hundreds of capsules. It was difficult to estimate production per female because of intermingling that occurs during communal spawning. Mature individuals gather under ledges or in other somewhat protected areas and begin to spawn almost simultaneously (judged by comparing development of embryos from adjacent masses near the center of the communal aggregation). Late arrivals add capsules on the periphery, on the shells of other spawners, or in a few cases, on previously deposited capsules. Individual spawners in an aggregation can have their shells enveloped with capsules. I witnessed several large aggregations on jetties at the mouth of St. Andrew Bay, Florida, containing between 16 and 55 spawning females, as well as several non-spawning females and males. Each communal mass contained several thousand capsules. One included certainly more than 10,000 capsules, and covered an irregular area ex- ceeding 1 m in diameter. Egg capsules are normally positioned in the muricine D'ASARO: EGG CAPSULES OF PROSOBRANCHS 79

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Urosalpinx perrugata (Conrad, 1846) (USNM 847139) Figure lE-G This drill selects any hard, stable object as a substratum for its egg capsules; however, purely organic substrata are selected least frequently. Urosalpinx perrugata often makes no attempt to hide or camouflage its egg mass. Females will spawn on exposed bivalve shells, such as on the lip of living Atrina. Individual egg capsules are normally inclined from the point of attachment toward the position occupied by the female during oviposition so that all capsules in a single spawning episode point in the same direction. Some egg masses have capsules aligned in several directions. Ifthese are equal in size and contain ontogenetically equivalent embryos, and the mass contains less than approximately 30 capsules, then it is presumably formed by one female. This species often deposits several capsules, moves a few centimeters, and resumes spawning. Extremely large egg masses, with capsules of different size and stage of development, are communal egg masses. I observed communal masses containing the contribution of as many as nine females. Large communal masses are formed only where sufficient hard substratum is available. Communal masses frequently contain egg capsules of Cantharus cancellarius and occasionally a few capsules of Calotrophon ostrearum. Egg masses produced by individuals in the field had 5 to 19 capsules (x = 11). In the laboratory, when provided with abundant food (Brachidontes exustus), U. perrugata spawned at 3-week intervals for at least 3 months, producing egg masses equal in size to those observed in the field. Capsules have a tubular apex with an apical plate completely covered by a thin escape membrane (Fig. IE). Below the tubular apex, lateral ridges arise suddenly to form shoulders, then taper gradually toward the basal plate (Fig. IF, G). Es- sentially the ridges divide the capsule into two regions, a slightly concave side toward which the ridges project and a convex side. The convex side may have a rounded or even a sharp keel extending from the tubular apical region to the peduncle. Close inspection shows that fibers in the outer layers are oriented at right angles to the keel. Individual capsules project from the substrate at a slight angle from the vertical. Average capsular dimensions are shown in Table 1.Newly deposited capsules have dense albumen. Development is direct; 5-8 juveniles (x = 6) hatch from each capsule. Because the number of embryos in a capsule declines with time, Radwin and Chamberlin (1973) suggested that this species has nurse eggs. D'ASARO: EGG CAPSULES OF PROSOBRANCHS 81

Favartia cellulosa (Conrad, 1846) (USNM 847146) Figure 2A-C Egg capsules of Favartia cellulosa are difficult to locate in the field, because spawning populations are scattered and eggcapsules are small and rarely deposited in large, obvious masses. Ten was the maximum number of capsules observed at one location. These may have been the product of several females because the capsules were positioned at radically different angles relative to each other. Most spawning sites observed in the field or laboratory contained only two to four capsules. Females do not hide during spawning, as many related species do. Rather, they select shallow recesses into which they can position egg capsules with the propodium. Females appear to select subtrata inclined toward the vertical on which to attach their capsules. Of seven spawning sites examined in the field, only one contained a single capsule that was attached to a nearly horizontal substratum. Small, dead mussels, with both valves intact, or egg masses of other prosobranchs were selected. One or two capsules of this species were found in Fasciolaria egg masses adjacent to capsules of Calotrophon ostrearum, which selects similar spawning sites. In the laboratory, females always selected substrata that were inclined toward the vertical even if the site was the side of a nylon- mesh holding cup. The preference for vertical sites is reflected in the shape of capsules which have a basal plate positioned to one side perpendicular to the apical plate (Fig. 2A, B). Although F. cellulosa egg capsules appear adapted for positioning on vertical substrata, other aspects of gross structure resemble muricine capsules. The apical plate has rounded edges and an ovate to somewhat rounded, semilunate outline (Fig. 2A). Distinct suture lines intersect the edges of the thin membranous escape aperture. Some specimens have an escape aperture one third larger than that shown in Figure 2A. Placement in shallow recesses on vertical substrata dictates that length be reduced. The side opposite the apical plate has a narrow concavity, not sharply defined, that extends toward the pedunclar area and gradually becomes obsolete (Fig. 2B, C). Average capsular dimensions are shown in Table 1. Capsules contained 7-13 embryos (x = 9). Development is direct, as reported by Raeihle (1966); no nurse eggs were observed.

Eup/eura su/cidentata Dall, 1890 (USNM 847145) Figure 2D, E Egg masses of E. su/cidentata are easily overlooked in the field because the capsules are less than 5 mm long and are hidden under hard, stable objects, frequently among polychaete tubes similar in appearance. Six eggmasses collected in the field and four deposited in the laboratory included 3 to 12 capsules (x = 9) with embryos suspended in albuminous fluid. The mean number of capsules deposited per spawning event is the same as that MacKenzie (1961) reported for a closely related species, E. caudata (Say, 1822). Eup/eura su/cidentata capsules are often placed in irregular rows with each capsule exhibiting the same orientation. When in close proximity, capsules deposited by one individual had overlapping basal membranes. There was no evidence of communal spawning. The eggcapsules are tubular structures, ovate in cross section; they taper basally to a thin stalk attached to a broad basal membrane (Fig. 2D, E). The basal membrane is quite easily detached from the substratum. Near the apex, the tube decreases in diameter by one-third to one-half and projects at an oblique angle to the midline. The apical area is capped by a transparent, oval and pustulate membrane crossed by a faint suture line. At the point where the capsule is bent 82 BULLETIN OF MARINE SCIENCE. VOL. 39. NO. I. 1986

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Figure 2. Egg capsules of prosobranchs. A, Favarita cellulosa, apical plate; B, F. cellulosa, lateral view; C, F. cellulosa, frontal view; D, Eupleura sulcidentata, view of side with longitudinal suture; E, E. sulcidentata, view of side opposite the suture; F, Calotrophon ostrearum, flat top; G, C. ostrearum, frontal view; H, C. ostrearum, bulbous base; I, C. cancellarius, concave side; J, C. cancellarius, apical plate; K, C. cancellarius, lateral view. D'ASARO: EGG CAPSULES OF PROSOBRANCHS 83 obliquely, there is a conical projection extending at right angles, The tubular capsule has distinct, closely spaced lirae that circumscribe the tube and meet at a transparent suture that transverses the length of the capsule (Fig. 20). Near the apex, the suture is indistinct but it is continuous with the faint suture that passes across the apical membrane. Average capsular dimensions are shown in Table 1. Four to nine juveniles leave the capsules via the escape aperture. Capsules of E. caudata. as described by MacKenzie (1961), very closely resemble those of E. su/cidentata except E. caudata capsules are twice as large and are triangular in cross section. Lirae or similar sculpture were not mentioned by MacKenzie (1961), but his figures suggest that E. caudata egg capsules also have them.

Calotrophon ostrearum (Conrad, 1846) (USNM 847147) Figure 2F-H Every viable egg capsule (> 500) of C. ostrearum observed was immediately adjacent or attached directly to newly deposited egg capsules of larger prosobranchs, especially fasciolariids, busyconids, and muricids. Oviposition by C. ostrearum often begins while the larger or host prosobranch is still depositing capsules. With few exceptions (3 in 100 spawning sites), C. ostrearum capsules were positioned on the sides of host capsules so that they were hidden within the host egg mass. The exceptions were observed on Fascio/aria tu!ipa (Linne, 1758) capsules, where C. ostrearum capsules were positioned on deeply recessive apical plates of individual host capsules. Only four capsules were positioned on immediately adjacent substrata that were not part of the host capsules. These were hidden, however, by overlapping host capsules. Radwin and Chamberlin (1973) observed C. ostrearum capsules attached to egg capsules of Ficus communis Ro- ding, 1798. When I transferred spawning females to a recirculating seawater system, none continued to spawn, even when presented with abundant food and fasciolariid egg capsules less than 24-h old. Radwin and Chamberlin (1973) were successful in that their specimens of C. ostrearum attached capsules to the walls of an aquarium. In the spring, mature female C. ostrearum gather on newly deposited egg capsules of host prosobranchs, probably in response to metabolites released during or just after spawning. If the host capsules are sufficiently large, a female pushes between the host capsules so that her propodium is directed toward the core of the host mass; there she attaches 1-7 egg capsules (x = 3) to the side of a host capsule. Usually 2-4 capsules are arranged in a single row. Each capsule is positioned at an oblique angle with reference to the surface of the host capsule; thus it can lie in the intercapsular space without greatly distorting alignment of the host capsules. The size of C. ostrearum relative to its capsules suggests that females are capable of spawning several times in different positions on a host egg mass. In habitats with large C. ostrearum populations, nearly every host egg mass will contain scores or even hundreds of C. ostrearum capsules. For example, a small Fascio/aria tu!ipa egg mass (43 capsules) from St. Joseph Bay, Florida, had 164 C. ostrearum capsules attached in the intercapsular space. Some had been deposited on nearly every host capsule, and a few were on the fused, basal membrane. Newly deposited egg capsules are transparent and contain 2-6 light pink embryos (x = 4) and some slightly opaque, albuminous fluid enveloped by a more opaque, pale bluish-white inner capsule. Each outer capsule has the shape of a covered, ovate bowl with a smooth, flat top, bulbous base, and three rounded sides marked by narrow plications and veination radiating toward the fourth side that is attached to the host capsule (Fig. 2F-H). During oviposition, the flat top 84 BULLETIN OF MARINE SCIENCE, VOL. 39, NO. I, 1986 is proximal to the female. The basal membrane extends directly from the flattened top of the capsule. Illustrations of C. ostrearum capsules by Radwin and Cham- berlin (1973) show more angular edges and possibly an escape aperture on one edge. No specimen I examined had an obvious escape aperture, but some did have circular plicae or veination on one edge. It is quite possible that newly hatched C. ostrearum prey on embryos in the host egg mass, but I have no evidence to confirm this suggestion. Average capsular dimensions are shown in Table 1.

Cantharus cancellarius (Conrad, 1846) (USNM 847140) Figure 21-K Egg capsules deposited by this species were common in shallow, high salinity habitats, but were less obvious than those produced by C. multangulus (refer to the following section of this report) because individual capsules and egg masses are smaller and because C. cancellarius attempts to hide its egg masses. Spawning individuals were found frequently under bivalve shells on patches of sand between Thalassia beds, sites concurrently used by Conus jloridanus jloridensis, C. jas- pedius stearnsi, and various marginellids. Field-collected egg masses had 27 to 104 capsules (x = 72). Positions of capsules in the three largest masses observed suggested that either the female interrupted spawning and reversed her position, or a second female added capsules to the mass. Communal spawning occurred frequently. Where availability of substrata is limited, and communal spawning is occurring, the habit of this species to hide an egg mass is abandoned. For example, a spawning event that started on an aluminum beer can resulted in a communal response that covered nearly the whole exterior of the can with over 5,000 capsules. In aquaria, C. cancellarius produced only four egg capsules. Within most egg masses, capsules were arranged almost in rows with the projecting lip (adjacent to the escape aperture) oriented in the same direction as other capsules produced during a single spawning event. As with C. multangulus, the length of spines and projecting ridges approximated the distance between capsules. Freshly deposited capsules are transparent but appear white due to the color of closely packed embryos. Color changes to gray-brown as embryos develop. Em- bryos are enveloped in opaque albumen. When viewed on the widest side with a distinct concavity, capsules appear vasiform (Fig. 21). When compared to C. multangulus, there is distinct similarity in capsular morphology. C. cancellarius capsules are smaller and proportionally longer than wide, although a few may have the same length to width ratio. The apical plate is distinctly concave or impressed with a slightly protruding lip capped by an oval escape aperture (Fig. 21). On each side, narrow, flattened spines project laterally in the same direction as the lip. One edge of each spine at the base merges into a ridge that forms the lateral edge of the capsule. The other edge merges into a suture that passes across the escape aperture. When viewed apically, the extended lateral ridges may appear to be spines (Fig. 21) and have been described as such by Radwin and Chamberlin (1973). Moore (1961) included a figure ofa C. cancellarius capsule (labeled C. reticulatus) that resembles Figure 21. He also mentioned four spine-like projections. Since they are not shown in Moore's figure, the reference must be to an apical view. On the side opposite the lip the concavity tapers gradually, almost to the base (Fig. 21, K). The edges of the concavity are bordered at the apical plate by sharp ridges that gradually become obsolete near the base. The points where the sharp ridges originate at the apical plate may project somewhat and appear to be another pair of spines when viewed apically. (This is the position at which the shorter pair of spines are located on C. multangu- D'ASARO: EGG CAPSULES OF PROSOBRANCHS 85

Ius capsules.) Just below these projections, the previously mentioned sharp ridge on each side divides into secondary ridges that project laterally to the edge of the capsule and extend one-half to three-quarters the distance to the base. Average capsular dimensions are shown in Table 1. The number of embryos per capsule ranged from 43 to 126 but was very constant within an egg mass. As development progressed, the number per capsule declined, indicating that some are nurse eggs. Hatching was not directly observed. However, one egg mass collected in the field was empty except for one juvenile. Size and development of this individual were consistent with a pattern of direct development. Radwin and Chamberlin (1973) reported that 10-20 larvae in each capsule develop directly to the crawling stage.

Cantharus multangulus (Philippi, 1848) (USNM 847143) Figure 3A-D In northwest Florida, this species begins to spawn when the water temperature exceeds 18°C, which may occur as early as late March. Spawning ceases after 2 months. Typically, spawning individuals are found in sparse Thalassia testudinum beds and are associated with populations of Atrina, Brachidontes, and Modiolus, Unlike Cantharus cancellarius, C. multangulus often does not hide their egg masses; thus any relatively unfouled, hard surface, especially Limulus exuviae, will be selected. Occasionally, egg masses were found on isolated shells on patches of sand or in association with, but not attached to, fasciolariid capsules. Radwin and Chamberlin (1973) found capsules attached to blades of Thalassia testudinum. Egg masses produced by individuals in the field had 3-23 capsules (x = 16). Spawning individuals transported to a recirculating seawater system spawned readily but produced only 3-4 capsules per incident. Cantharus multangulus tended to deposit several capsules in a mass, interrupt spawning, move, and then return later to the same mass and resume spawning in a new position. Communal eggmasses were common. Those observed in the field had as many as 73 capsules. Typically, egg masses of C. multangulus with capsules of greatly differing size oriented in multiple directions are communal. During oviposition, capsules are positioned so that each has its projecting lip (adjacent to the escape aperture) oriented in the same direction. The intercapsular distance at the apex is approximately equal to the length of the projecting spines or the previously mentioned lip. Newly deposited capsules, which are white and somewhat transparent, rapidly darken as various periphytic communities form on their surface. Embryos initially occupy only one-third of the capsular volume, the remainder containing dense, somewhat opaque albumen. When viewed on the side with the protruding apical lip, capsules appear vasiform and are twice as wide as thick (Fig. 3A, B). The apical plate is slightly impressed with an obvious protruding lip on which an oval or circular escape aperture is located (Fig. 3B). Two pairs of spines with inflated and rounded tips protrude laterally from the apical plate. The longer pair on the same side as the lip extend basally to the lateral edge of the capsule and toward a weak suture that passes through the membrane of the escape aperture, a character also seen in C. cancellarius. When viewed apically with low magnification, the lateral edges of the capsule may appear to be a third pair of spines. On the side opposite the lip, there is a concavity between the base of the spines that extends one-third to one-half the distance to the basal membrane (Fig. 3C). One side of the concavity may have a rib that extends to the basal membrane. Additional supportive ribs may appear on the peduncle (Fig. 3C, D). Most of these details 86 BULLETIN OF MARINE SCIENCE. VOL. 39. NO. I, 1986

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Figure 3. Egg capsules ofprosobranchs. A, Cantharus multangulus. convex side; B, C. multangulus. apical plate; C, C. multangulus. concave side; D, C. multangulus. lateral view; E, Fascl"olarialilium hunteria. apical plate; F, F. I. hunteria, view of side opposite the apical veil; G, F. I. hunteria. lateral view. are not shown in figures of this species by Perry and Schwengel (1955) and Radwin and Chamberlin (1973). Capsular dimensions are listed in Table 1. At oviposition, capsules contain 55-82 embryos (x = 67). Development is direct, supported by nurse eggs and albumen. Only 5-8 embryos (x = 7) hatch from each capsule.

Fascia/aria lilium hunteria (G. Perry, 1811) (USNM 847144) Figure 3E-G Fasciolariid spawn is especially common in coastal seagrass habitats of North- west Florida. Egg masses of Fascia/aria lilium hunteria first appear in late April, D'ASARO: EGG CAPSULES OF PROSOBRANCHS 87

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Figure 4. Egg capsules of prosobranchs. A, Conus jloridanus jloridensis, concave side; B, C. f jloridensis, convex side; C, C. f jloridensis, lateral view; D, C. jaspideus stearnsi, frontal view; E, C. j. stearnsi, apex; F, C. j. stearnsi, lateral view.

usually when the water temperature is above 18°C. Almost any firm substratum can be used for the initial spawning. For example, a small bivalve shell can be selected, and as spawning progresses, the confluent bases of newly deposited capsules form their own substratum. Fascialaria tulipa and Pleuraplaca gigantea (Kiener, 1840) have similar spawning habits (D'Asaro, 1970). Quite frequently Fascialaria tu!ipa capsules were observed adjacent to F. !ilium hunteria capsules. Egg masses deposited by individual females had 16-27 capsules (x = 20). F. l. hunteria produced communal egg masses that included the spawn of two or three females. Individual contributions could be separated using size and presence of a fused basal membrane as criteria. Also, capsules produced by an individual always face the same direction and are in close proximity, so that the expanded apical veils of one row of capsules overlaps the apical veils of capsules in an adjacent row. In typical fasciolariid fashion, dense albumen with a central mass of hundreds of small embryos fills the newly deposited smooth, vasiform egg capsules. Each apical plate is slightly pustulate with its outer edge or ridge extended as a thin veil of capsular material (Fig. 2E-G). One edge of the veil is reflexed over the apical plate almost to the center line and partially obscures the escape aperture. 88 BULLETIN OF MARINE SCIENCE, VOL. 39, NO. I, 1986

A suture extends to the lateral edges across the thin membrane of the escape aperture. When viewed laterally, the folded apical veil is prominent (Fig. 2G). An illustration of a F. hunteria capsule by Perry and Schwengel (1955) shows a much less prominent veil than observed in most specimens from northwest Flor- ida. Average capsular dimensions are given in Table 1. Each contains approximately 700 to 1,200 embryos, of which only 5-7 embryos survive and hatch as juveniles.

Conusfloridanusfloridensis Sowerby, 1870 (USNM 847141) Figure 4A-C Only three of six Florida cone egg masses studied were found in the field, including one with a female in oviposition. All were attached to the unexposed side of single Dinocardium or Noetia valves on patches of sand between Tha/assia beds. These masses contained 18, 26, and 39 capsules. Individual capsules were attached to the substratum at a slight angle from perpendicular and also inclined toward a central point common to most other capsules in the mass, suggesting that the female gradually rotated in an arc during oviposition. A few capsules in masses with apical plates facing radically different directions could have been deposited after the spawner repositioned herself or are the contribution of a second female. One spawning individual that had produced 18capsules in the field almost immediately produced 15additional capsules in the laboratory. Two other females also spawned in the laboratory immediately after capture. Capsules are opaque white with the malleated appearance typical of conid egg capsules. Enclosed embryos are only faintly visible. Viewed from the widest, slightly concave side, each capsule has nearly the outline of an acute triangle with the angles of the base rounded where they meet the peduncle and basal membrane (Fig. 4A). Contents of the capsules do not extend into the peduncle. Lateral edges have sinuations that may be rounded or quite sharp on some specimens. Fine, irregular ridges may traverse this side of the capsule. The opposite side is inflated, has irregular ridges only on the edges, and is continuous with the apical plate (Fig. 4B). Laterally, the apical plate is bordered on three sides by an elevated, irregular collar (Fig. 2B, C). The plate is depressed and, close to the apex, contains a prominent escape aperture covered by a very thin, transparent membrane. Average capsular dimensions are given in Table 1. The capsules contain transparent and very viscous albumen and 24-33 large embryos (x = 31). Size and number of embryos suggest direct development, but hatching was not observed. Perry and Schwengel (1955) illustrated eggcapsules attributed to C. spurius at/anticus Clench, 1942 that appear identical to those produced by C. fioridanus.

Conus jaspideus stearnsi Conrad, 1869 (USNM 847148) Figure 4D-F Although Conus jaspideus stearnsi will deposit egg capsules on many types of exposed, solid substrate in aquaria, spawning sites in the field were only found under bivalve shells on patches of sand between Tha/assia beds. This species seeks a dark, protected chamber for its egg capsules and may attach its capsules to eggcapsules of other prosobranchs (marginellids) that have previously spawned in such locations. Bandel (1976a) reported that Conus jaspideus pygmaeus Reeve, 1844, on the coast of Colombia, exhibits similar cryptic behavior. Egg masses observed had 2-12 capsules (x = 5). Isolated capsules were observed in the laboratory. It is difficult to estimate fecundity of this species because females typically deposit a few capsules more or less in a row, and then move, often several D'ASARO: EGG CAPSULES OF PROSOBRANCHS 89 centimeters, before producing more capsules with a completely different spatial orientation. Capsules found in a discrete mass frequently face the same direction, but may not be separated by equal distances. In masses produced by a single female, the intercapsular distance is usually equal to the thickness of adjacent capsules. Since three spawners were found under a single shell, the largest egg masses observed were probably communal, a behavior already described for C. j. pygmaeus by Bandel (1976a). Each smooth, narrow, and slightly inflated capsule has an oval or occasionally square outline with the raised apical plate positioned to one side (Fig. 4D). The peduncle is broad and may occupy the whole basal area in specimens that have a squarish outline. The apical plate, which is completely occupied by an oval escape aperture, has a flaring ridge on its upper border. This ridge is continuous with the median capsular suture and almost always has a small fold near the central edge of the escape aperture. The apical area is actually continuous with one side of the capsule (Fig. 4E, F). Average capsular dimensions are given in Table 1. Capsules contain 1-8 pink embryos (x = 5) that occupy halfthe volume. Development to hatching was not observed, but size and number of embryos indicate direct development. When comparing C. j. stearnsi with C. j. pygmaeus, as described by Bandel (1976a), there are some immediately recognizable differ- ences. The Colombian subspecies is more vasiform and inflated and has an apical escape aperture that covers the entire apex.

DISCUSSION Higher prosobranchs enclose fertilized ova in proteinaceous capsules that are molded into morphologically distinct structures of varying complexity attributable to specific genera or, less often, to specific families. In this report, families with distinctive capsular structure include Strombidae (Robertson, 1959), Fasciolari- idae (D'Asaro, 1970), and Conidae (Kohn, 1961a; 1961b). Strombus alatus egg masses and egg filaments or tubes containing capsules conform to the expected familial norm, crescentic masses composed of sand encrusted tubes with egg capsules in a coiled, mucous thread or tube enclosed in the first tube. Identification of sympatric strombid spawn can be difficult because the basic morphological pattern within the family is uniform; pedal molding of individual capsules is not employed. Most distinctive characters are enumerations of capsules within the helical inner thread and texture of the outer tube. Capsular diameter has no comparative value because species that mature at the same size, for example Strombus alatus and S. gallus Linne, 1758 (D'Asaro, 1970), produce capsules of equivalent size. Fasciolariids and conids have distinctive familial capsular morphology but exhibit sufficient specific variation to allow separation of sympatric spawn. Typical fasciolariid capsules are broadly vasiform with expanded apical collars and are attached to a common basal membrane. The capsules of Fasciolaria lilium hunteria are easily recognized as fasciolariid, but distinct from sympatric F. tulipa and Pleuroploca gigantea (D'Asaro, 1970). Typical conid capsules are opaque white and are flattened with wrinkled or malleated texture and transparent oval or elongated escape apertures occupying most of the apical plate. The collar of Conus jloridanus jloridensis is an example of distinctive anatomy that separates it from sympatric species. The degree of ecophenotypic variation between two subspecies, C. jaspideus stearnsi and C. j. pygmaeus from the Caribbean coast of Colombia (Bandel, 1976a), was surprising because it appeared greater than that between many conid species. 90 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.1, 1986

Egg capsules of the muricids and buccinids examined demonstrated similarity of structure within certain genera but also showed that in some, intrageneric capsular structure can include extreme divergence. Eupleura sulcidentata capsules are morphologically similar to capsules of allopatric E. caudata as described by MacKenzie (1961). Sympatric Cantharus cancellarius and C. multangulus from northwest Florida have obvious similarities in capsular shape and spination. The capsular structure of Urosalpinx perrugata differs from that of allopatric U. cinerea (Tamarin and Carriker, 1967) mainly in that capsules of the latter lack lateral ridges. The major difference between the capsules of sympatric Murex fulvescens and M. jIorifer dilectus A. Adams, 1885 (D'Asaro, 1970) is dimensional; yet both muricines are obviously distinct from another sympatric species, M. pomum Gmelin, 1791 (Moore and Sander, 1978) that does not have vasiform capsules with concave and convex sides. Higher prosobranchs that employ the pedal molding mechanism (Fretter and Graham, 1962) can be expected to produce capsules that are of value in recognizing taxonomic relationships. Bandel (1976b; 1976c) attempted to demonstrate such relationships by grouping related taxa with morphologically similar capsules. The degree of taxonomic value remains to be determined, especially after more and complete descriptions become available.

ACKNOWLEDGMENTS

I wish to thank the students who helped me collect specimens, in particular Messrs. L. Dilmore, H. Hayes, and W, Plaia, Dr. P. Hamilton's suggestions on the manuscript are gratefully acknowledged. This project was financed in part with funds from the U.S. Environmental Protection Agency (CR- 811649-01).

LITERATURE CITED

Abbott, R, T. 1974. American seashells, 2nd cd. Van Nostrand Reinhold Co., New York. 663 pp. Bandel, K. 1976a. Spawning, development and ecology of some higher Neogastropoda from the Caribbean Sea of Colombia (South America). Veliger 19: 176-193. --. 1976b. Morphologic der Gelege und okologische Beobachtungen an Muriciden (Gastropoda) aus der siidlichen Karibischen See. Verh. Naturforsch. Ges. Basel 85(1/2): 1-32. --. 1976c. Morphologic der Ge1ege und okologische Beobachtungen an Buccinaceen (Gastro- poda) aus der siidlichen Karibischen See. Bonn. Zool. Beitr. 27: 98-133. Bradshaw-Hawkins, V. T. and F. Sander. 1981. Notes on the reproductive biology and behavior of the West Indian fighting conch, Strombus pugilis Linnaeus in Barbados, with evidence of male guarding. Veliger 24: 159-164. D'Asaro, C. N. 1970. Egg capsules of prosobranch mollusks from south Florida and the Bahamas and notes on spawning in the laboratory. Bull. Mar. Sci. 20: 414-440. Fretter, V. and A. Graham. 1962. British prosobranch molluscs: their functional anatomy and ecology. Ray Society, London. 755 pp. Knudsen, J. W. 1966. Biological techniques. Harper and Row, New York. pp. 454-457. Kohn, A. J. 1961a. Studies on spawning behavior, egg masses, and larval development in the gastropod genus Conus. I. Observations on nine species in Hawaii. Pac. Sci. 15: 163-180. --. 1961b. Studies on spawning behavior, egg masses, and larval development in the gastropod genus Conus. II. Observations in the Indian Ocean during the Yale Seychelles Expedition. Bull. Bingham Oceanogr. Coli. 17(4): 4-51. MacKenzie, C. L., Jr. 1961. Growth and reproduction of the oyster drill Eupleura caudata in the York River,.Virginia. Ecology 42: 317-338. Moore, D. R. 1961. The marine and brackish water Mollusca of the state of Mississippi. Gulf Res. Rep. 1(1): I-58. Moore, E. A. and F. Sander. 1978. Spawning and early life history of Murexpomum Gme1in, 1791. Veliger 20: 251-259. Perry, L. M. and J. S. Schwengel. 1955. Marine shells of the western coast of Florida. Paleontological Research Institution. Ithaca, New York. 318 pp. Radwin, G. E. and J. L. Chamberlin. 1973. Patterns oflarval development in stenoglossan gastropods. Trans. San Diego Soc. Nat. Hist. 17(9): 107-118. D'ASARO: EGG CAPSULES OF PROSOBRANCHS 91

Raeihle, D. 1966. An observation of captive Murex cel/ulosus Conrad, Am. Malacol. Union, Annual Report. p. 28. Robertson, R. 1959. Observations on the spawn and veligers of conchs (Strombus) in the Bahamas. Proc. Malacol. Soc. London 33(4): 164-172. Tamarin, A. and M. R. Carriker. 1967. The egg capsule of the muricid gastropod Urosalpinx cinerea: an integrated study of the wall by ordinary light, polarized light and electron microscopy. J. Ultrastruct. Res. 21: 26-40. Thiriot-Quievreux, C. 1983. Summer mero-planktonic prosobranch larvae occurring off Beaufort, North Carolina USA. Estuaries 6(4): 387-398.

DATE ACCEPTED: April I, 1985.

ADDRESS: Department of Biology, University of West Florida, Pensacola, Florida 32514.