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Home , Fiona (gastropod), Fiona pinnata, Janthina, Nudibranch, Velella

OBSER V ATIONS ON PELAGIC lVIOLLUSKS ASSOCIATED WITH THE SIPHONOPHORES AND PHYSALIA1

FREDERICK M. BAYER Institute of Marine Science, University of Miami

ABSTRACT Specimens of three of violet snail. Ianthina . I. pallida and I. prolongata, and of a , pinnata, all of which feed upon siphonophores, were collected during strandings of Velella and studied in the aquarium. Observations were made upon float-building and feeding behavior of Ianthina, and upon feeding, growth and reproduction of Fiona.

INTRODUCTION

During the winter months in southern Florida, strong easterly breezes often blow ashore various members of the pelagic community of the Florida Current. The most conspicuous of these are three siphonophores, Physalia physalis (Linnaeus), the Portuguese man-of-war; Velella velella (Lin- naeus), the By-the-wind sailor or Purple sail; and the less abundant Porpita umbella (Muller). Accompanying these in greater or lesser numbers are several moJlusks that prey upon them. The abundance of these varies from year to year, depending upon weather conditions. During the winter of 1961-62, Physalia was present, as it usually is, but there were no Velella or Porpita; in 1962-63, moderate numbers of Vdella and fewer Porpita accompanied heavy strandings of Physalia. Collections made along the beach of Biscayne Key, the shore of Virginia Key facing the open ocean through Bear Cut, the beach adjacent to the Marine Laboratory on Virginia Key, and the south side of Rickenbacker Causeway just west of Virginia Key provided specimens of three species of Ianthina and an eolid nudibranch, . Most of these were maintained alive in running-water aquaria for considerable periods of time, thus affording the biological observations reported herein. Subclass PROSOBRANCHIA Ianthina Roding The many nominal species of this genus have been reduced by Laursen (1953) to five, of which three were taken at Miami during February and March of 1963. In view of the fact that the names used in the popular conchologicalliterature are not entirely correct, the three species discussed here are briefly described and illustrated in order to facilitate their identi- IContribution No. 488 from The Marine Laboratory, Institute of Marine Science, University of Miami, Florida. 19631 Bayer: Pelagic Mollusks 455 fication by those who may have an opportunity to conduct further studies of their biology. During the time that specimens of Ianthina were maintained alive in the laboratory, observations were made upon float-building, feeding and reproduction. .-Three of the five known species were collected in the vicinity of Miami during February and March of 1963; the other two have been obtained in past years but appear to be less abundant and therefore not so commonly washed ashore. The nomenclature employed here follows that used by Laursen in his DANA Report.

FIGURE I. Ianthina janthina (Linnaeus). Virginia Key, opposite Bear Cut, Miami, Florida. X 1.5. Ianthina janthina (Linnaeus) This is the most abundant species around southern Florida. The trochoid shape of its shell is characteristic (Fig. 1). Because of its variable color and height of spire, it has received a number of names of which the most familiar are communis, fragilis, and violacea, but it is correctly identified under the name janthina in the most recent conchological works (Abbott, 1954; Keen, 1958; Kira, 1961, 1962; Morris, 1947; Warmke and Abbott, 1961). A few authors still employ incorrect nomenclature or recognize variant forms (Kira, 1961, 1962: balteata Reeve; Rippingale and McMi- chael, 1961: violacea Roding). Thompson This species was second in abundance during February and March of 1963. It is often misidentified as I. globosa because of its globose shell 456 Bulletin of Marine Science of the Gulf and Caribbean [13(3)

FIGURE2. Ianthina pallida Thompson. Key Biscayne, Florida. X 1.5. (Fig. 2). The shell characters used by Laursen (1953) to separate this species from I. umbilicata appear to be variable and must be corroborated by reference to the shape of the radular teeth. The color of the shell is pale violet; the outer lip merges with the columella in a smooth arc; the sinus is shallow and leaves behind inconspicuous traces of sculpture called a "keel" by Laursen.

FIGURE3. Ianthina prolongata Blainville. Key Biscayne, Florida. X 1.5. Ianthina prolongata Blainville This species was found only once in 1963, during strong easterly winds on February 12. It often is identified as 1. globosa and not infrequently is confounded with I. pallida. The color is usually much deeper purple than in I. paUMa; the outer lip forms a right angle with the columella and does not describe a regular arc (Fig. 3). The sinus is rather shallow and leaves behind an inconspicuous keel-like trace on the body whorl only (Laursen, 19631 Bayer: Pelagic Mollusks 457 1953:15,28, fig. 30). This species is called I. globosa Swainson 1823 (not globosa Blainville 1825 = umbilicata d'Orbigny 1840) in some recent works (Morris; Kira; Abbott; Warmke and Abbott). OBSERVATIONS Feeding.-As reviewed by Laursen (1953: 14), not much is known of the food and feeding of Ianthina. Although it sometimes is stated that the food of violet snails consists entirely of Velella, Laursen discovered from an examination of contents that they will eat anything available. Specimens kept in the laboratory tend to confirm that observation. When undisturbed, I. janthina hangs from its float with head and extended from the shell and the proboscis more or less everted. When an extended was very gently touched with the edge of a Velella, the snail extended its head to the maximum extent and fully everted the proboscis, exposing the radular teeth. When the tentacle was again touched with the Velella, the whole anterior part of the snail made a swift, darting movement toward the source of stimulus. This usually brought the tip of the extended proboscis in contact with the fleshy margin of the siphonophore, which was firmly grasped by the "lips" of the slit-like mouth. Radular action was evident immediately, and the snail chewed rapidly along the edge of the coelenterate, ingesting most of the fleshy part as it moved along. When a supply of Velella was not available, the lanthinas were offered Physalia as a substitute. Upon first contact with the Physalia, the snails performed feeding responses identical to those elicited by Velella. The proboscis was thrust deep into the fringe of zooids and showed no evidence of being affected by the powerful nematocysts. Two violet snails of moderate size virtually devoured a Physalia with a float about four inches long in less than one day, leaving only some remnants of the pneumato- phore and a small mass of zooids. On one occasion when Velella was not available, a specimen of I. janthina caught and ate a large I. pallida. Laursen observed the radular apparatus of I. janthina in the stomach of another of the same species, indicating that occurs. Laursen (p. 8) mentions the numerous published references to the fact that Janthina emits a purple fluid when irritated, but attributes no function to it other than defense. Hardy (1956: 113) recounts the observations of P. David aboard the RRS DISCOVERYII, who stated that Ianthina released the purple dye periodically while browsing on the zooids of Velella and concluded that it may have an anesthetic function to block the action of nematocysts. The specimens of I. janthina observed in aquaria usually emitted purple fluid when disturbed, especially in the first few hours after collection. They did not release the dye when feeding upon Velella, but did so when feeding 458 Bulletin of Marine Science of the Gulf and Caribbean l13(3) upon Physalia. It could not be determined whether this was due to the disturbance associated with placing the food organism near the snails, or to the nature of the coelenterate itself. Several examples of I. pallida were observed while attached to Velella and browsing upon its zooids, but they were not seen to release the colored fluid. Furthermore, they did not do so when disturbed, or when attached to their own floats and feeding upon Velella in the manner of I. janthina. A number of very small individuals of I. pallida were observed feeding upon Velella and it is evident that the coelenterate is large enough to maintain the young mollusks for a substantial period. The smallest Ianthina observed was situated in the fleshy edge of a large Velella, in which it had eaten a hole larger than itself. Slightly larger individuals were found crawling freely about on the siphonophores. It seems likely that I. pallida, and possibly the other ovigerous species, may have no need for a float when young and do not construct one until the original host has been eaten. Possibly the metamorphose upon contact with the host coelenterate and undergo a substantial part of post-larval development there. The observations of Ganapati and Rao (1960) concerning the feeding of Ianthina upon Porpita undoubtedly deal with one of the ovigerous species rather than with I. janthina as reported. The photograph illustrating their note shows a globose shell which could belong to either I. pallida or I. umbilicata, less probably to I. prolongata, but almost certainly not to I. janthina. Float-building.-Construction of the float has been described by several authors, summarized by Laursen (1953). Photographs of the steps in bubble formation by I. janthina are given herewith. From its usual position at the end of the float (Fig. 4, a), the propodium advances along the surface of the water in a broad, fan shape (Fig. 4, b). The edge of the propodium then curves downward hollowing the sole (Fig. 4, c), quickly followed by an in-rolling (Fig. 4, d) and constriction of the margin (Fig. 4, e) that encloses a bubble of air, which is surrounded by mucus. The bubble is then appressed to the end of the float (Fig. 4, f) and the procedure repeated. The operation requires 10-20 seconds. The earlier observations that an detached from its float is unable to form a new one can be confirmed and are attributed to circumstances only. The animal sinks to the bottom where it has no access to air; quite naturally, it is unable to form a float even though the capacity to do so remains, as Wilson and Wilson (1956) and others have noted. A specimen in the seawater aquarium became detached from its float and was found groping about helplessly on the bottom. The animal was picked up and carefully held just beneath the surface of the water at the angle at which it normally hangs from its float. As soon as it recovered from alarm, it extended the propodium along the surface film as just 19631 Bayer: Pelagic Mollusks 459

FIGURE 4. Ianthina janthina (Linnaeus). Bubble formation: a, propodium clinging to float; b, propodium extended along surface of water; c, sole of propodium hollowed to form air space; d, edge of propodium rolled inward to trap air bubble; e, formation of bubble completed; t, propodium presses bubble in place at end of float. described, and trapped a bubble of air which formed the first chamber of a new float. The process was repeated immediately and in five minutes the float was large enough to provide some buoyancy but not enough to hold the animal at the surface. The specimen was then propped on a rock near the surface of the water, but in this position the foot was unable to contact the surface film at the proper angle and could not form bubbles. Then the animal was placed in a finger bowl containing just enough water to hold it in its natural position when its shell touched the bottom of the dish. In this position, the foot was able to reach the surface of the water in a satisfactory manner and bubble formation resumed. In about one hour the 460 Bulletin of Marine Science of the Gulf and Caribbean [13(3) snail had formed a float adequate to hold it at the surface but not as large as fully formed floats usually seen in healthy specimens. While the animal that had lost its float was busy forming a new one, it did not respond to prey upon contact, but continued actively making bubbles. After its new float was large enough to suspend it normally, the snail resumed feeding. Individuals of Janthina pallida more commonly were found without a float, creeping on the lower surface of large Velellas, where they were browsing on the zooids. While maintained in the aquarium, the snail continues to crawl about by means of its foot on the coelentrate and feeding upon its tissues until it is consumed or begins to disintegrate. Then the snail proceeds to the edge of the Velella and begins construction of a float. When the float is large enough to support it, the Ianthina releases its hold of the host and floats about until a new one is contacted. Then it feeds as I. janthina does, hanging from its own float. In the aquarium it did not resume creeping on the new host. Miscellaneous.-Laursen has reviewed and described at some length the reproduction of ianthinids. Wilson and Wilson (1956:302) described the ejection of masses of larvae by I. janthina, which we also have observed. Living examples that had been in the laboratory for some days were seen to extrude irregular dark masses that resembled fecal material but which proved to be dense concentrations of active larvae in various stages of development from early veligers with a cap-shaped shell to fully developed ones with a coiled shell. One freshly caught specimen placed in a finger bowl for photographic purposes ejected from its -cavity via the left side (i.e., over the "anterior canal" of the shell) a regularly oval mass about 3 x 4 mm in size, which fell to the bottom of the dish. After remaining intact for about five minutes, the pellet spontaneously disintegrated, forming a small heap of larvae which rapidly dispersed. Within 15 minutes the veligers were evenly distributed and actively swimming across the bottom of the vessel. Although lacking eyes, I. janthina must be extremely sensitive to small variations in illumination. When resting quietly with head extended, they invariably withdrew into their shells upon the approach of any object from above, and it was not necessary for a shadow to fall across the animals. The reaction took place readily in low, indirect illumination but was more pronounced in brighter light. Subclass Suborder NUDIBRANCHIA Fiona pinnata (Eschscholtz) On March 1, 1963, several specimens of a blue aeolidian nudibranch, Fiona pinnata, were collected by Gary Hendrix and Jon Staiger on Velella lY631 Bayer: Pelagic Mollusks 461 drifting past the laboratory dock or washed ashore on the adjacent beach. Two of the nudibranchs were almost dead at the time of collection and were preserved at once. A third example, crawling on a healthy Velella, was in good condition and was placed with the siphonophore in a large finger bowl with running seawater. It was then discovered that there were four additional nudibranchs of minute size inhabiting the same Vdella. These five specimens were maintained alive and provided the following notes.

Behavior.-When placed in a shallow dish for photography, the large Fiona remained almost motionless and made no effort to crawl about as other nudibranchs usually do under these circumstances. When replaced in a larger container, it clung to the side of the dish, raising the anterior two-thirds of its body upward and feeling from side to side with tentacles widely extended. When a Velella was gently brushed near the head of the nudibranch, the latter made active searching motions in the general direction of the stimulus. The lower surface of the siphonophore was then placed within reach of the mollusk, which felt about, made contact with the zooids, and then performed avoiding reactions, withdrawing its tentacles and turning it head aside. The Fiona consistently refused to cling to the. lower surface of Velella. When the upper surface of the coelenterate was brought near the nudibranch, it made contact with a very quick movement and held fast with the anterior part of its foot. The posterior end of the foot was immediately released from the dish and the slug began crawling about on the siphonophore, actively feeding. In repeated trials, the nudibranch invariably clung tenaciously to the upper surface and sail of the Velella but would not venture on the lower surface. Feeding.-In feeding, Fiona browses freely over the upper surface of Velella, scraping the float and sail clean of tissue and devouring the fleshy edge of the disk, but ignoring the lower surface and its zooids. When all edible tissue has been consumed, the nudibranch clings to the edge of the Velella float by the posterior end of its foot and extends the anterior part of its body far outward, feeling about in all directions. When a fresh Velella is touched, the slug immediately grasps it firmly with the anterior part of its foot and promptly releases hold of the old Velella, making the transfer with astonishing alacrity. As the availability of Velella depended upon a favorable onshore wind and a supply of them could not be kept healthy for any great length of time even in running water, the Fionas were several times left with nothing to eat. After one such fast of about three days, during which time their color had faded from deep blue to a pale, milky blue, the four nudibranchs were placed on a freshly collected Velella, which they began at once to feed upon. In less than one hour they began producing fecal strings which contained convoluted strands of homogeneous, blue colored matter, irregu- 462 Bulletin of Marine Science of the Gulf and Caribbean l13(3) lar wisps and clumps of yellowish material containing abundant intact zooxanthellae, and many clumps of nematocysts, mostly undischarged. In about two hours the distinctly showed intensification of the blue color, and in 24 hours the animals had regained their usual bright blue color. Kropp (1931) reported that the blue coloration of his starved specimens returned in two hours after they resumed feeding on Velella. The same author observed that specimens of Fiona fed upon bits of fish became yellow. However, our specimens did not take other food readily, even after starvation for several days. Physalia was offered when other food was not available but, unlike Ianthina, the nudibranchs responded to it negatively, with conspicuous avoidance reactions, and could not be induced to feed upon or even cling to any part of the siphonophore. In view of the reports that Fiona inhabits as well as Velella, fresh pieces of gulf-weed overgrown with the usual epiphytes were placed in the container with the nudibranchs. They crawled about upon the alga with apparent reluctance, avoiding the small, brown sea anemones (A ne- monia sargassensis) and the numerous hydroids, and resorted to the sides of the dish at the first opportunity, where they crept sluggishly about, reaching out in an exploratory manner. As Pruvot-Fol (1947) reports the food of Fiona to include goose- , the nudibranchs were placed upon a large floating seed covered with small examples of those crustaceans, as well as many sea anemones. Although the slugs developed a brownish color, none of them was secn to feed and it could not be determined what had been consumed. A second seed, bearing several larger barnacles of two species ( anatifera and L. pectinata), was placed with the nudibranchs, which immediately showed interest in L. anatifera. They chewed into the stalk of the barnacles, thoroughly cleaning out the interior, leaving behind the tough, empty skin of the stalk and the empty shell. After feeding upon barnacles, the nudibranchs assumed a rich pink color similar to "pastel red" of the Reinhold Color Atlas (Kornerup and Wanscher, 1962: 204, pI. 10, A4). When all the specimens of L. anatifera were consumed, the nudibranchs did not commence feeding upon L. peetinata, even after several days without other food. Perhaps the stalk of this species is too tough and hard for the nudibranchs to eat. Growth and Reproduetion.- The most remarkable observation made upon these nudibranchs concerns their rapid growth. Although nudibranchs have been observed to mature rapidly, as reported for Ga/vina pieta in England and for gopa/ai in India, Fiona pinnata reaches full size and matur- ity in a shorter time than heretofore reported for other nudibranchs. Orton (1914) found adult individuals of Galvina pieta and G. exigua among hydroids growing on a raft that had been afloat for 6 weeks and 2 days, and assumed that they had grown from veligers to maturity in that period. 1963 I Bayer: Pelagic Mollusks 463 Rao (1937) reared StiUger gopalai from young individuals 1.25 mm in length to full maturity in 15-16 days. The present observations upon Fiona pin nata show that this species may reach maturity in an even shorter time.

FIGURE 5. Fiona pinnata (Eschscholtz). Adult and three juvenile specimens on Velella, photographed March 1, 1963.

The four small individuals found March 1 measured about 8 mm in length on March 2 when they were photographed with the adult specimen feeding on a Velella (Fig. 5). Four days later, on March 6, the young nudibranchs almost equalled the size of the adult (Fig. 6) and obviously were mature, as they began copulating freely. On March 8, one week after they were collected as minute juveniles, they began producing masses smaller than but identical in form with many masses found on Velella floats washed ashore on Virginia Key. Those produced subsequently were larger and could not be distinguished from masses collected in the field (Fig. 7). During the ensuing three weeks, the four individuals produced a total of 89 egg masses. deposited in late afternoon (estimated at 6 p.m.) on March 8 were gastrulae in 30 hours (at midnight May 9) and shelled veligers in about 46 hours. The cell-lineage of this nudibranch has been investigated 464 Bulletin of Marine Science of the Gulf and Caribbean [13(3) by Casteel (1904) from preserved material. Detailed studies of the larval development of our material will be reported as part of a survey of opisthobranch development now in progress by Robert A. Smith, to whom I am indebted for the information briefly mentioned here.

FIGURE 6. Fiona pinnata (Eschscholtz). The same young individuals shown in Fig. 5, photographed March 8, 1963.

FIGURE 7. Fiona pinnata (Eschscholtz). Egg masses on Velella float. 19631 Bayer: Pelagic Mollusks 465

SUMARIO OBSERVACIONES DE MOLUSCOS PELAGICOS ASOCIADOS CON LOS SIFON6FOROS Velella Y Physalia Tres especies de Ianthina: I. janthina, I. pal/ida e I. pr%ngata fueron coleccionadas vivas y estudiadas en un acuario. Es sabido que especies de Ianthina se alimentan de Velella, pero I. janthina tambien come los zooides y aun los pneumat6foros 0 f1otadores de Physalia, asr como otros especi- mens de Ianthina. I. janthina responde violentamente al contacto con organismos alimenti- cios y lanza su prob6scide extendida hacia el estimulo. Cuando la presa es atrapada, el molusco se pega fuertemente con su boca y nipidamente devora el tejido del celenterado. Aunque I. janthina come mientras esta suspendida del monton de burbujas, I. pallida frecuentemente es encon- trada sin su f1otador, pegada a Velella y comiendo de sus tentaculos. Cuando al alimento es consumido el molusco se arrastra hasta el borde de la Velella donde construye un f1otador, f1otando entonces hasta que una nueva presa es encontrada. Cuando es separada de su f1otador, Ianthina es incapaz de alcanzar la superficie del agua y muere. Un ejemplar de I. janthina que habra perdido su f1otador, fue sostenida cerca de la superficie del agua y entonces fue capaz de formar burbujas y producir un nuevo f1otador. Las burbujas son formadas nipidamente atrapando aire con el propodium, cada burbuja requiere solamente de 10-20 segundos. Mientras esta en el proceso de reconstruir su f1otador Ianthina no muestra reacciones alimenticias en presencia de una presa. Ianthina janthina fue vista expeliendo bolas de larvas activas en varios estados de desarrollo. Un nudibranquio azul, Fiona pinnata, f10ta alrededor de Velella, ali- mentandose de tejidos de su vela y de la superficie superior, pero no ingiere los tentaculos. Cuando es privada de alimento, no come otros sifon6foros como la Physalia, ni los hidroides ni las anemonas que crecen en el Sargazo, can el cual el nudibranquio ha sido reportado. Camera una lepa, L. anatifera, y cuando se alimenta de esos animales toma color rosado. Fiona joven se aliment6 de Velella, creci6 hasta la madurez en el laboratorio en una semana, y en tres semanas cuatro individuos produjeron un total de 89 masas de huevos. REFERENCES ABBOTT, R. T. 1954. American . D. Van Nostrand Co., New York, xiv+541 pp., 97 figs., 40 pis.

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