The effect of age at metamorphosis on the transition from larval to adult suspensionfeeding of the slipper limpet Crepidula fornicata

Slipper limpets use different ciliary feeding mechanisms as larvae and adults. Veliger 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 metamorphosis 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 suspension feeders, calyptraeids lack the elaborations of foregut that complicate transition to juvenile 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 (LINNAEUS 1758) are ciliary suspension feeders, but the feeding mechanisms at these two stages are entirely different. Like many marine gastropods, C. fornicata hatches as a veliger and then swims and feeds for several weeks in the plankton before metamorphosing. A veliger uses the cilia on its velum for both feeding on phytoplankton and swimming (Werner 1955; Strathmann & Leise 1979; Klinzing & Pechenik 2000; Chaparro et al. 2002a; Romero et al. 2010). Veligers capture algal cells and other food particles between two bands of cilia at the edge of each velar lobe that beat toward each other; the band with longer cilia also propels the veliger. Captured particles are transported toward the mouth along a ciliated food groove situated between the opposed bands. By contrast, adults of C. fornicata, as in other calyptraeids, employ the ctenidium for suspension-feeding (Werner 1953). Ctenidial feeding by calyptraeids was most recently described by Shumway et al. (2014) for C. fornicata and by Chaparro et al. (2002b) for Crepipatella peruviana (LAMARCK 1822) (formerly identified as Crepidula fecunda). Cilia on the ctenidial filaments create a current through the mantle cavity. Particles are caught on mucous strands that are transported across the ctenidial filaments. The mucous strands and adhering food particles are then added to a food cord that rotates between the tips of the ctenidial filaments and the snail’s neck. At intervals a food cord is moved along a semi-enclosed groove (the neck canal) to the mouth, grasped by the radula, and swallowed. Attachment to a solid substrate plays an important role in suspension-feeding in these species (Pechenik et al. 2015). Author for correspondence. E-mail: [email protected] Invertebrate Biology x(x): 1–12. © 2017, The American Microscopical Society, Inc. DOI: 10.1111/ivb.12165 Our study concerns the transition from velar to ctenidial feeding. At metamorphosis, C. fornicata loses the velum as a structure for ciliary suspensionfeeding. We take loss of the velum to mark metamorphosis. The newly metamorphosed juvenile attaches to a hard benthic surface, such as rock, shell, or (in the lab) glass. Postmetamorphic juveniles of a related species (C. peruviana) rasp food from the substrate within 24 h of metamorphosis but do not initiate suspension-feeding with the ctenidium for 9 d, although the juveniles have some ctenidial filaments at metamorphosis (Montiel et al. 2005). By contrast, the transition from velar to ctenidial feeding after metamorphosis, though undescribed, is more rapid in C. fornicata. Rates of feeding on the planktonic alga Isochrysis galbana suggest that suspension-feeding begins as early as one day after metamorphosis (Eyster & Pechenik 1988). Ctenidial filaments develop in the larval mantle cavity prior to metamorphosis (Werner 1955; Pechenik & Lima 1984). Werner (1955) described five to eight ctenidial filaments, added from posterior to anterior, whose cilia produce currents through the veliger’s mantle cavity. He also observed in the veliger the rudiment of the mucusproducing endostyle between the darkly pigmented rudiment of the osphradium and the base of the ctenididial filaments. He mentioned continued development of papillae of the osphradium after metamorphosis. Development of the structures for ctenidial suspension-feeding begins before competence for metamorphosis. These preparations in the larva for ctenidial feeding after metamorphosis are expected to continue after veligers become competent to metamorphose. Near the time that veligers become competent, the growing edge of the shell takes the form of the shell of juvenile and adult, becoming hat-shaped with the edge of the growing shell extending linearly as a brim (Pechenik 1980). Other caenogastropod veligers exhibit ctenidial filaments and rudiments of osphradium, radula, and other structures that function in the juvenile after metamorphosis (Thiriot-Qui evreux 1974). Ctenidial filaments and the radula continue to grow and differentiate when metamorphosis is delayed in some caenogastropods (Lesoway & Page 2008). In diverse caenogastropods the oral apparatus of the juvenile develops to varying extents as a rudiment that does not interfere with larval feeding (Fretter 1969; Thiriot-Qui evreux 1974; Page 2000, 2011; Parries & Page 2003). These features speed the transition to a different method of feeding after metamorphosis and appear to have facilitated the evolution of diverse feeding mechanisms in caenogastropods, including feeding that is dependent on a proboscis and secretions for overcoming prey. In contrast to these other kinds of feeding, the oral apparatus for ctenidial feeding is relatively simple. Ctenidial feeding does not require a proboscis, penetration of prey by the radula, or secretions to subdue prey. Ctenidial feeding does, however, require elaborate structures distinct from the oral apparatus. Because ctenidial feeding requires distinctive features, because some of the adult feeding apparatus develops before metamorphosis, because juveniles of C. fornicata feed on planktonic algae soon after metamorphosis, and because slipper limpets appear to differ in timing of initiation of ctenidial feeding, we asked three questions. (1) What capabilities for suspension-feeding develop before and after metamorphosis? (2) Do larvae continue to develop toward ctenidial feeding as they age prior to metamorphosis? That is, do they initiate ctenidial feeding sooner if metamorphosis has been delayed in the absence of a stimulus? (3) Do juveniles of C. fornicata initiate ctenidial feeding directly after metamorphosis rather than after an extended period of radular scraping?