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The Effect of Age at Metamorphosis on the Transition from Larval to Adult Suspension-Feeding of the Slipper Limpet Crepidula Fornicata

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The Effect of Age at Metamorphosis on the Transition from Larval to Adult Suspension-Feeding of the Slipper Limpet Crepidula Fornicata Invertebrate Biology x(x): 1–12. © 2017, The American Microscopical Society, Inc. DOI: 10.1111/ivb.12165 The effect of age at metamorphosis on the transition from larval to adult suspension-feeding of the slipper limpet Crepidula fornicata Jan A. Pechenik1 and Richard R. Strathmann2,a 1Biology Department, Tufts University Medford, Medford, Massachusetts 02155, USA 2Friday Harbor Laboratories and Department of Biology, University of Washington, Friday Harbor, Washington 98250, USA Abstract. Slipper limpets use different ciliary feeding mechanisms as larvae and adults. Veli- ger larvae of Crepidula fornicata developed part of the adult feeding apparatus, including ctenidial filaments, neck lobe, and radula, before metamorphosis, but ctenidial feeding did not begin until well after loss of the larval feeding apparatus (velum) at metamorphosis. Earlier initiation of ctenidial feeding by individuals that were older larvae when metamor- phosis occurred suggests continued development toward ctenidial feeding during delay of metamorphosis. Early juveniles produced a ciliary current through the mantle cavity and moved the radula in a grasping action before they began to capture algal cells on mucous strands or form a food cord. Either early juveniles could not yet form mucous strands or they delayed their production until development of other necessary structures. The neck canal for transporting food from ctenidium to mouth cannot develop before velar loss. In their first feeding, juveniles fed much like the adults except that the neck canal was less developed and the path of the food cord toward the mouth sometimes varied. As suspen- sion feeders, calyptraeids lack the elaborations of foregut that complicate transition to juve- nile feeding for many caenogastropods, but a path for the food cord must develop after velar loss. Why individuals can initiate ctenidial feeding sooner when they are older at metamorphosis is not yet known. The juveniles became sedentary soon after metamorphosis and were not observed to feed by scraping the substratum with the radula, in contrast to the first feeding by juveniles of another calyptraeid species, observed by Montiel et al. (2005). Additional key words: Calyptraeidae, ctenidium, mucus, suspension-feeding Both larvae and adults of Crepidula fornicata (LIN- between the opposed bands. By contrast, adults of C. NAEUS 1758) are ciliary suspension feeders, but the fornicata, as in other calyptraeids, employ the ctenid- feeding mechanisms at these two stages are entirely dif- ium for suspension-feeding (Werner 1953). Ctenidial ferent. Like many marine gastropods, C. fornicata feeding by calyptraeids was most recently described hatches as a veliger and then swims and feeds for sev- by Shumway et al. (2014) for C. fornicata and by eral weeks in the plankton before metamorphosing. Chaparro et al. (2002b) for Crepipatella peruviana A veliger uses the cilia on its velum for both feeding (LAMARCK 1822) (formerly identified as Crepidula on phytoplankton and swimming (Werner 1955; fecunda). Cilia on the ctenidial filaments create a cur- Strathmann & Leise 1979; Klinzing & Pechenik 2000; rent through the mantle cavity. Particles are caught on Chaparro et al. 2002a; Romero et al. 2010). Veligers mucous strands that are transported across the cteni- capture algal cells and other food particles between dial filaments. The mucous strands and adhering food two bands of cilia at the edge of each velar lobe that particles are then added to a food cord that rotates beat toward each other; the band with longer cilia also between the tips of the ctenidial filaments and the propels the veliger. Captured particles are transported snail’s neck. At intervals a food cord is moved along a toward the mouth along a ciliated food groove situated semi-enclosed groove (the neck canal) to the mouth, grasped by the radula, and swallowed. Attachment to aAuthor for correspondence. a solid substrate plays an important role in suspen- E-mail: [email protected] sion-feeding in these species (Pechenik et al. 2015). 2 Pechenik & Strathmann Our study concerns the transition from velar to evolution of diverse feeding mechanisms in ctenidial feeding. At metamorphosis, C. fornicata caenogastropods, including feeding that is dependent loses the velum as a structure for ciliary suspension- on a proboscis and secretions for overcoming prey. feeding. We take loss of the velum to mark meta- In contrast to these other kinds of feeding, the oral morphosis. The newly metamorphosed juvenile apparatus for ctenidial feeding is relatively simple. attaches to a hard benthic surface, such as rock, Ctenidial feeding does not require a proboscis, pene- shell, or (in the lab) glass. Postmetamorphic juve- tration of prey by the radula, or secretions to sub- niles of a related species (C. peruviana) rasp food due prey. Ctenidial feeding does, however, require from the substrate within 24 h of metamorphosis elaborate structures distinct from the oral appara- but do not initiate suspension-feeding with the cteni- tus. dium for 9 d, although the juveniles have some Because ctenidial feeding requires distinctive fea- ctenidial filaments at metamorphosis (Montiel et al. tures, because some of the adult feeding apparatus 2005). By contrast, the transition from velar to develops before metamorphosis, because juveniles of ctenidial feeding after metamorphosis, though unde- C. fornicata feed on planktonic algae soon after scribed, is more rapid in C. fornicata. Rates of feed- metamorphosis, and because slipper limpets appear ing on the planktonic alga Isochrysis galbana to differ in timing of initiation of ctenidial feeding, suggest that suspension-feeding begins as early as we asked three questions. (1) What capabilities for one day after metamorphosis (Eyster & Pechenik suspension-feeding develop before and after meta- 1988). Ctenidial filaments develop in the larval man- morphosis? (2) Do larvae continue to develop tle cavity prior to metamorphosis (Werner 1955; toward ctenidial feeding as they age prior to meta- Pechenik & Lima 1984). Werner (1955) described morphosis? That is, do they initiate ctenidial feeding five to eight ctenidial filaments, added from poste- sooner if metamorphosis has been delayed in the rior to anterior, whose cilia produce currents absence of a stimulus? (3) Do juveniles of C. forni- through the veliger’s mantle cavity. He also cata initiate ctenidial feeding directly after metamor- observed in the veliger the rudiment of the mucus- phosis rather than after an extended period of producing endostyle between the darkly pigmented radular scraping? rudiment of the osphradium and the base of the ctenididial filaments. He mentioned continued devel- Methods opment of papillae of the osphradium after meta- morphosis. Adults of Crepidula fornicata were mostly Development of the structures for ctenidial sus- obtained from Totten Inlet in Puget Sound, Wash- pension-feeding begins before competence for meta- ington, and maintained at the Friday Harbor Labo- morphosis. These preparations in the larva for ratories (University of Washington), at the Salish ctenidial feeding after metamorphosis are expected Sea, in aerated glass jars filled with filtered seawater to continue after veligers become competent to at 20–23°C and salinities of 29–30 ppt; as noted metamorphose. Near the time that veligers become below, individuals from one brood were obtained competent, the growing edge of the shell takes the from adults collected at Nahant, Massachusetts, and form of the shell of juvenile and adult, becoming reared and observed at Tufts University (salinity hat-shaped with the edge of the growing shell 30 ppt, ~23°C). extending linearly as a brim (Pechenik 1980). Other Veligers were released naturally from egg capsules caenogastropod veligers exhibit ctenidial filaments brooded by adults, reared to metamorphic compe- and rudiments of osphradium, radula, and other tence, and maintained beyond competence until structures that function in the juvenile after meta- stimulated to metamorphose. Competence was morphosis (Thiriot-Quievreux 1974). Ctenidial fila- assessed, and metamorphosis was induced, by trans- ments and the radula continue to grow and ferring larvae to seawater (~29–30 ppt) whose KCl differentiate when metamorphosis is delayed in some concentration had been elevated by 20 mM (Peche- caenogastropods (Lesoway & Page 2008). nik & Gee 1993). Juveniles and unmetamorphosed In diverse caenogastropods the oral apparatus of larvae were maintained in 100 mL of seawater in the juvenile develops to varying extents as a rudi- glass bowls. For larvae, water was changed by ment that does not interfere with larval feeding reverse filtration or by pipetting individuals. Each (Fretter 1969; Thiriot-Quievreux 1974; Page 2000, juvenile was placed on the underside of a cover glass 2011; Parries & Page 2003). These features speed the that was supported on its corners by modeling clay. transition to a different method of feeding after For observations on flat slides, this support for metamorphosis and appear to have facilitated the cover glasses allowed introduction or renewal of Invertebrate Biology vol. x, no. x, xxx 2017 Larval age, advanced juvenile function 3 algal suspensions. For continued maintenance, juve- We measured larval age as days from hatching, niles on cover glasses were moved to clean bowls of considered loss of the velum to constitute metamor- filtered seawater and fresh algal suspension. Larvae phosis, and took the formation and ingestion of a and juveniles were fed the
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