Studies on the Structure and Function of the Larval Kidney Complex of Prosobranch Gastropods

Abstract

The larval kidneys of prosobranch gastropods have long been assumed to be involved in handling wastes, but with little supporting evidence. In this study, the larval kidneys of Searlesia dira and Nucella canaliculata were studied with light, electron, and fluorescence microscopy. They consist of three cell types: (1) a large external absorptive cell swollen with heterophagosomes and possessing an endocytotically active external surface; (2) an internal crystal cell with numerous vacuole-bound crystals of a calcium salt and with morphologically complex canaliculi; (3) an internal pore cell characterized by slit-pores that lead to subsurface cisternae, a tubular network, and one or two ciliated ducts that open into the hemocoel. Empirical evidence indicates that the absorptive cell rapidly takes up and stores albumen proteins from the capsular fluid. Absorptive cells were found in 17 of 19 species tested, representing three prosobranch orders, but were not found in 2 opisthobranch or 1 pulmonate species. We hypothesize that the absorptive cells have become specialized for the uptake of capsular albumen prior to the functional differentiation of the gut. However, the nutritional importance of the absorbed albumen proteins and the functions of the crystal and pore cells are presently unknown. No evidence for an excretory function was found for the larval kidney complex; it may be a vestigial protonephridium, the components of which have become disorganized and functionally altered.

Effect of oxygen conditions on intracapsular development in two calyptraeid species with different modes of larval development

“…Given that the embryos of this species do not have yolk or other nutrition sources supplied by the parents, it is possible that the increase in the total embryo dry weight was due to consumption of intracapsular material. Previous studies have shown that this behavior is common among encapsulated embryos of gastropod species (De Mahieu et al 1974, Rivest 1992, Rivest & Strathmann 1995, Moran 1999, Ojeda & Chaparro 2004). For example, encapsulated embryos of the indirect developer C. fecunda, and of indirect and direct developer species of the genus Littorina have provided evidence of consumption of capsular material by embryos (Moran 1999, Ojeda & Chaparro 2004).…”

Limiting factors to encapsulation: the combined effects of dissolved protein and oxygen availability on embryonic growth and survival of species with contrasting feeding strategies

“…Therefore, the experimental treatments (incubation times and albumen concentrations) were only used to gain resolution in microscopical observations (see also Moran, 1999). A solution of bovine serum albumen labelled with commercial fluoroscein isothiocyanate (FITC-BSA, Sigma A9771, Sigma Chemical Co., St Louis, MO, USA) was offered to the embryos (Rivest, 1992;Rivest and Strathmann, 1995). Fluorescence in embryonic organs was taken as evidence of protein intake by embryos and this assumption was based on previous studies showing endocytosis in invertebrate embryos using a scanning electron microscope (Rivest, 1992;Rivest and Strathmann, 1995;Moran, 1999).…”

“…A solution of bovine serum albumen labelled with commercial fluoroscein isothiocyanate (FITC-BSA, Sigma A9771, Sigma Chemical Co., St Louis, MO, USA) was offered to the embryos (Rivest, 1992;Rivest and Strathmann, 1995). Fluorescence in embryonic organs was taken as evidence of protein intake by embryos and this assumption was based on previous studies showing endocytosis in invertebrate embryos using a scanning electron microscope (Rivest, 1992;Rivest and Strathmann, 1995;Moran, 1999). Additionally, we observed embryos fed with unlabelled albumen (control) in order to discard the hypothesis of natural fluorescence of embryos when analysing our experimental data using labelled albumen.…”

“…The main sources of energy may be incorporated into the eggs as yolk (lecitotrophy) or laid in the capsules in the form of nurse eggs (ovophagy) or nurse embryos (cannibalism or adelphophagy) that are ingested during development by the embryos (see Chaparro et al, 1999;Poulin et al, 2001;Collin, 2003). Additional energy sources have been reported, such as the albumen (protein) commonly found in the intracapsular fluid of gastropods (De Mahieu et al, 1974;Rivest, 1992;Penchaszadeh and Rincón, 1996). This protein can be provided dissolved in the intracapsular fluid at the time of egg laying (Rivest and Strathman, 1995) or can be the result of mechanical or chemical degradation of the internal layer of the capsule wall (Ojeda and Chaparro, 2004).…”

“…This protein can be provided dissolved in the intracapsular fluid at the time of egg laying (Rivest and Strathman, 1995) or can be the result of mechanical or chemical degradation of the internal layer of the capsule wall (Ojeda and Chaparro, 2004). This dissolved protein can be incorporated by active feeding through the oral aperture using the ciliary activity of the velum or by endocytocis, which is observed in cells of the velum, pedal complex or in the larval kidney (De Maheiu et al, 1974;Rivest, 1992;Rivest and Strathmann, 1995;Moran, 1999). Although it is clear that embryos of marine gastropods can incorporate dissolved intracapsular protein, the consequences on important life history traits, such as developmental time, hatching size or embryo survival, are still poorly understood.…”