Usefulness of the opercular nucleus for inferring early development in neritimorph gastropods

Abstract

The early ontogeny of gastropods (i.e., planktotrophic vs. nonplanktotrophic) may be inferable from the morphology of the protoconch in adult shells. The protoconch consists of both embryonic and larval shells in species with planktotrophic development; the embryonic shell forms in the intracapsular period and the succeeding larval shell gradually develops during the larval period. In nonplanktotrophic species, on the other hand, there is no additional growth of the larval shell and the protoconch consists exclusively of a relatively large embryonic shell formed prior to hatching. This "shell apex theory" has been applied to many species of shell-bearing gastropods, but biotic and abiotic erosion of the apex often prevents detailed examination of the protoconch and subsequent inferences about ontogeny. I examined the gastropod operculum to test its utility for predicting developmental mode, drawing on the Neritimorpha as model taxa. Most aquatic members of Neritimorpha were found to bear an operculum with a clearly demarcated nucleus; SEM observations reveal four types of nuclei, which correspond to different types of protoconch morphologies and observed ontogenies for the study species. The nucleus is secreted before metamorphosis, fits into the shell aperture of the larva, and reflects early ontogeny as morphology, as does the protoconch. Moreover, the apparently organic (rather than calcareous) composition of the nucleus makes it nearly invulnerable to erosion and very advantageous, compared to the protoconch, in this ecologically diverse group, whose habitats range from freshwater streams and mangrove swamps to rocky shores and deep-sea hydrothermal vents. The measurements of the nucleus are also valuable for taxonomic purposes, especially in the species identification of veliger larvae and juvenile snails. On the other hand, the opercular nuclei of the Caenogastropoda and Heterobranchia are often eroded away in adult individuals; even if present, the morphology of the nuclei does not seem to clearly reflect early ontogeny in those groups.

High gene flow due to pelagic larval dispersal among South Pacific archipelagos in two amphidromous gastropods (Neritomorpha: Neritidae)

“…Other amphidromous species found on oceanic islands have a similarly lengthy PLD (Radtke et al, 2001;Kano, 2006;Hoareau et al, 2007b), an absence of genetic structure across long pelagic distances ( (Myers et al, 2000;Kano and Kase, 2004;Cook et al, 2008). The pelagic larva has only been lost from the life history a few times among the extant freshwater Neritids, and only once in an island species (Holthuis, 1995), even though pelagic larvae have been lost multiple times in other families of marine invertebrates (Duda and Palumbi, 1999;Hart, 2000).…”

“…However, although a community ecologist would view them as freshwater animals (for example, Bandel and Riedel, 1998;Smith et al, 2003), their population ecology may be more similar to that of a marine species, because of their pelagically dispersing larvae. Relatively long pelagic larval durations (PLDs) have been estimated from laboratory cultures of amphidromous gastropod veligers (40-98 days, Holthuis, 1995;Kano, 2006) and the otoliths of amphidromous Galaxiid fishes and gobies (63-266 days, Radtke et al, 1988Radtke et al, , 2001Mcdowall et al, 1994;Hoareau et al, 2007b). These PLDs fall at or above the high end of the range found in the planktotrophic larvae of marine invertebrates (7-293 days, Shanks et al, 2003) and fish (B20-90 days, Brothers et al, 1983).…”

“…Neritina canalis (Sowerby, 1825) and Neripteron dilatatus (Lesson, 1830) have planktotrophic larvae, as indicated by the 'D'-shaped initial region of their opercula (Kano, 2006) and probably share an amphidromous common ancestor (Holthuis, 1995). Neritina canalis is found under stones in riffles within 1-2 km of the sea, and has a range that extends from the Philippines to the Marquesas (Haynes, 2001).…”

Platyceratid gastropods - stem group of patellogastropods, neritimorphs or something else?

“…However, there is very rich fossil material of isolated cyrtoneritimorph protoconchs from different stratigraphical levels of Ordovician to Lower Devonian strata showing that the cyrtoneritimorphs were common in the Early Paleozoic gastropod faunas. Open-coiled protoconchs were found in several clades of Paleozoic gastropods such as the Euomphalomorpha, Peruneloidea, Macluritoidea, and Cyrtoneritimorpha (Frýda 1999;Bandel & Frýda 1998Nützel 2002;Frýda & Rohr 2004, 2006Frýda et al 2008a). A documented general trend towards decreasing proportions of open-coiled protoconchs through the Paleozoic may also explain the decrease in frequency of cyrtoneritimorph protoconchs (Nützel & Frýda 2003;Frýda et al 2008a).…”

“…In addition, the shell ontogenetic pattern is very stable for long temporal ranges which make the recognition of major phylogenetic lineages of living gastropods in the past possible. Analysis of these characters in fossil gastropods has shown that all four living orthogastropod clades (Caenogastropoda, Heterobranchia, Neritimorpha, and Archaeogastropoda) may be traced back to the Paleozoic (Bandel 1997;Frýda 1998aFrýda -c, 1999Nützel 1998;Nützel et al 2000;Bandel 2002a, b;Frýda & Rohr 2004, 2006Frýda et al 2008a, and references therein). Moreover, studies of the shell ontogeny in fossil gastropods have revealed the presence of several Paleozoic gastropod clades which existed for a long time and which were characterized by unique ontogenetic patterns unknown in post-Paleozoic gastropods (Frýda 1999a, Frýda & Rohr 2004, Frýda et al 2008a and references therein).…”