Brooding in cocculiniform limpets (Gastropoda) and familial distinctiveness of the Nucellicolidae (Copepoda): misconceptions reviewed from a chitonophilid perspective

Abstract

Nauplii, copepodids and adults of a new mesoparasitic genus and species of Chitonophilidae, Lepetellicola brescianii, are described from the pallial cavity of a deepwater cocculiniform limpet, Lepetella sierrai, collected in the Bay of Biscay and Gulf of Cádiz. Re‐examination of the type material of the recently established Nucellicolidae revealed several important observational errors in the original description, such as the oversight of the rootlet system in the adult female and misinterpretations of the tagmosis and antennulary segmentation in the late copepodid. Lamb et al.’s (1996) criteria used to justify the familial distinctiveness of the Nucellicolidae are all invalid. The family is relegated to a junior synonym of the Chitonophilidae on the basis of overwhelming support provided by copepodid and adult morphology. The impact of heterochrony on the body plan of adults and developmental stages is discussed. Phylogenetic analysis supports a basal dichotomy dividing the Chitonophilidae into a mesoparasitic clade, utilizing exclusively polyplacophoran hosts, and a sisterclade grouping genera associated with chitons, prosobranch gastropods and cocculiniform limpets. The presence of maxillipeds and postmaxillipedal apodemes in the adult males of the latter clade is considered as apomorphic rather than plesiomorphic, being the result of incomplete moulting and correlated with the ventral position of the genital apertures. Nucellicola is identified as the sistergroup of the only other endoparasitic genus, Tesonesma, found in the body cavity of chitons. The inferred relationships indicate that host switching has occurred twice in the evolution of the Chitonophilidae. Examination of the antennulary segmentation and setation patterns of copepodids in Lepetellicola and Nucellicola unequivocally refutes both the current placement of the Chitonophilidae in the Poecilostomatoida and its alternative assignment to the Siphonostomatoida. Exclusion from the Poecilostomatoida is reinforced by the absence of a coxo‐basis in the antenna. The family is placed with the cyclopoids, providing further evidence for the crown‐group status of the Poecilostomatoida within the currently paraphyletic Cyclopoida. A critical review of the published reports of brooding in cocculiniform limpets demonstrated that there is, as yet, no tangible evidence for this phenomenon in either the Lepetelloidea or Cocculinoidea. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 75, 187–217.

The anatomy of Lepetella sierrai (Vetigastropoda, Lepetelloidea): implications for reproduction, feeding, and symbiosis in lepetellid limpets

“…However, it is possible that the observed instance of parasitism is an early stage of the parasitic chitonophilid copepods observed by other researchers in this species (Dantart & Luque ; Huys et al. ), similar to the “vermiform endosome” stage seen in lepetodrilid limpets by Tunnicliffe et al. ().…”

“…Although the sections are not clear, there does appear to be a “rootlet system” ( sensu Huys et al. ) and what may be a small female body on the outside of the body wall.…”

“…The first recognized parasites in Lepetella were chitonophilid copepods whose eggs were originally identified as brooded limpet eggs by Dantart & Luque () and subsequently investigated in detail and identified as copepods by Huys et al. (). Distinct, round, white eggs can be seen in the mantle cavity when this parasite is present.…”

“…laterocompressa ; however, the “brood” later turned out to be parasitic copepods (Huys et al. ). Moskalev () studied a large number of specimens (>180 of L. tubicola and 14 of T. lypidellaeformis ) and even performed some histological sectioning, but did not report on lepetellid anatomy in detail.…”

An extraordinary shift in life habit within a genus of cyclopid copepods in Lake Tanganyika

“…Thus, the present description represents a rare account of a freshwater copepod parasitic on an invertebrate host, the first record from a host in the freshwater Cerithioidea, as well as the first report from a nonampullariid host. It also represents a unique foray into an obligate parasitic life mode in the otherwise free living Cyclopidae; although the order Cyclopoida ( sensu Huys & Boxshall, 1991) is almost certainly paraphyletic, in addition to the Chitinophilidae, Mantridae and Ozmanidae, the Cyclopidae can be added to the list of cyclopoid families that utilize molluscs as hosts (see in Huys et al ., 2002). As such, this discovery highlights yet another intriguing facet of the endemic fauna of Lake Tanganyika.…”