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Reproductive period. Note the presence of several calcic particles ( arrowheads ) in the acinar lumen secretion ( ac albumen secretory cells, lc labyrinthic cell). Bar 1 μ m
Source publication
Seasonal variations in the morphology of the parenchymal mass and function of the albumen gland/capsule gland complex have been studied in Pomacea canaliculata, together with the cellular types involved in the synthesis and secretion of perivitellin fluid components. The two major parenchymal cell types, albumen secretory cells (AS) and labyrinthic...
Context in source publication
Context 1
... our latitude, P. canaliculata has a seasonal reproduction with three different periods that we have termed pre- reproductive, reproductive and post-reproductive. All show specific functional characteristics related to structural variations of the cells of the albumen gland/capsule gland complex. The most voluminous and conspicuous component of this glandular complex is the parenchymal mass, which is composed of tubular-acinous adenomeres formed by two cell types: albumen secretory cells interdispersed between labyrinthic cells ( Fig. 1). During the reproductive period that occurs in spring and summer (September to March), the parenchymal cells reach their maximal development and structural complexity. The albumen secretory cells, which are voluminous and pyramidal in shape, have short microvilli on their apical surfaces (Fig. 2). Laterally, adherens and septate junctions allow the attachment of cells to each other and to the labyrinthic cells, contributing to the structural unity of the adenomere (Figs. 3, 11). They show the typical ultrastructural organization of cells that synthe- size and secrete large amounts of complex macromole- cules of a glycoprotein nature. The nuclei, which are basally and eccentrically located, are electron-lucid and exhibit an irregular profile and a prominent nucleolus (Fig. 2). The rough endoplasmic reticulum is well- developed. Its dilated cisternae, with numerous ribo- somes attached to their membranes, are arranged linearly or concentrically and possess fine granular material of moderate to low electron density (Fig. 4). The Golgi complex is formed by numerous dictyosomes in whose cisternae small electron-dense particles of about 20 nm in diameter can be observed (Fig. 5). The product of the biosynthetic activity of the rough endoplasmic reticulum and the Golgi complex is packed into large spherical or ovoid secretory granules. During the period of maximal cellular activity, these granules acquire a polyhedral shape attributable to the presence of neighbouring granules. They have a homogeneous matrix of moderate electron density on which electron-dense particles, simi- lar in size and shape to those observed in the Golgi cisternae, can be seen. These particles progressively accumulate and finally fill the granular matrix (Fig. 6). Some granules also have a spherical electron-dense core that is eccentrically located. The secretory granules associated with microtubules in the cytoplasm reach the cell apical region and release their contents into the acinar lumen (Fig. 3). Small spheroidal mitochondria are scattered throughout the cytoplasm. Another remarkable characteristic of the albumen secretory cells at this reproductive period is the presence of electron-dense calcium deposits that infiltrate the cytoplasmic matrix, organelles and secretory granules to various degrees (Fig. 4). The calcic nature of these deposits has been previously demonstrated by histochemistry by the Von Kossa technique (Catalán et al. 2004). To characterize these deposits further, we have performed an electron microscope analysis of the electron-dense material with an energy dispersive X-ray spectrometer. Fig. 7 shows the major elemental composition of the samples was demonstrated to be Ca, P and C. Calcium salts within the albumen secretory cell are usually found as fibrous aggregates or as large compact spherical or ovoid structures called calcipherites (Fig. 8). During the reproductive period, the labyrinthic cells, which are columnar or pyramidal in shape, exhibit long cilia intermingled with a few short microvilli at their luminal surfaces. Basally, the plasma membrane shows deep irregular folds that extend through the cellular cytoplasm up to the subapical region, forming a conspicuous and complex basal labyrinth. This labyrinth determines the formation of multiple cytoplasmic compartments that house numerous elongated mitochondria. The ovoidal electron-lucid nuclei are located in the basolateral region of the cell (Fig. 9). Basal bodies, ciliar rootlets, mitochondria and multivesicular bodies can be seen in the apical cytoplasm. Electron-dense calcium deposits can be observed not only infiltrating the cellular cytoplasm and nucleus (Fig. 9), but also in the extracellular space of the basal labyrinth (Fig. 10) or as tiny particles (Fig. 11). According to our observations, these calcium deposits in parenchymal cells are part of a normal physiological process in P. canaliculata , characteristic of the reproductive period. When the calcic electron-dense material saturates the extracellular space, the basal labyrinth folds are clearly outlined. Fibres and nerve terminals with electron-lucid and dense-core vesicles can be clearly seen in close proximity to the folds of the labyrinthic cells (Fig. 11). Finally, the granular contents of the albumen secretory cells and the calcic material pass from the adenomere lumen (Fig. 12) and ultimately reach the main albumen gland duct. In the autumn, during the short post-reproductive period (April-May), the albumen secretory cells markedly change their aspect, as most secretory granules have been released into the acinar lumen. Nuclei show a greater electron density. Organelles involved in biosynthesis processes are poorly developed. Lysosomes, glycogen granules and lipids are typical structures in the cytoplasm (Fig. 13). During this period, the labyrinthic cells are the main acinous components. Like the albumen secretory cells, the labyrinthic cells have also markedly decreased in volume. They exhibit an apical cytoplasmic band that maintains adenomere integrity via junction complexes. Cilia are reduced in number. The basal labyrinth cytoplasmic folds are much thinner, outlining a dilated extracellular space with no electron-dense calcic particles (Fig. 14). Multivesicular bodies, lysosomes and mitochondria can be observed in the cytoplasm. During the pre-reproductive period, when the lowest water temperatures are recorded (May-August), a reorganization of the biosynthetic organelles in the albumen secretory cells begins. A progressive development of the rough endoplasmic reticulum, Golgi cisternae and nuclei with a prominent nucleolus is observed (Fig. 15). Secretory granules increase in number and size and, consequently, so does the cellular volume. Labyrinthic cells also show a process of cellular recovery together with a reorganization of their structural components, although no circulating calcic particles can as yet be seen in the extracellular space of the basal labyrinth (data not ...
Citations
... In particular, the AG synthesizes and secretes perivitelline fluid (PVF), which provides the embryos the nutrients and defenses for development (Heras et al., 1998;Dreon et al., 2013Dreon et al., , 2014, while the CG stores large amounts of calcium that later form the eggshell (Runham, 1988). Histological studies of the AG-CG have shown that its parenchymal cells undergo large seasonal variation related to egg production (Catalán et al., 2006). ...
... As a whole, these results highlight the high biosynthetic activity of the organ. This agrees with previous studies on AG perivitellin synthesis (Dreon et al., 2002(Dreon et al., , 2003 and its storage in granules of secretory cells during the reproductive period (Catalán et al., 2006). A similar restoration period after the release of PVF during oviposition was observed for the AG of the pulmonate snail Lymnaea stagnalis (Wijsman and Wijck-Batenburg, 1987). ...
... A similar restoration period after the release of PVF during oviposition was observed for the AG of the pulmonate snail Lymnaea stagnalis (Wijsman and Wijck-Batenburg, 1987). In P. canaliculata and other freshwater snail species, this synthesis and release during multiple oviposition events seem to be under neuroendocrine control (Mukai et al., 2004;Catalán et al., 2006). It is worth recalling that multiple spawnings are characteristic of an opportunistic reproductive strategy, commonly found in species that inhabit adverse or unpredictable environments (Chiarello-Sosa et al., 2016). ...
High fecundity often contributes to successful invasives. In molluscs, this may be facilitated by the albumen gland-capsule gland complex, which in gastropods secretes the egg perivitelline fluid that nourishes and protects embryos. The biochemistry of the albumen gland-capsule gland complex and its relationship with fecundity remain largely unknown. We addressed these issues in Pomacea canaliculata (Lamarck, 1822), a highly invasive gastropod whose fecundity and reproductive effort exceed those of ecologically similar gastropods. We evaluated the dynamics of its major secretion compounds (calcium, polysaccharides, and total proteins) as well as the gene expression and stored levels of perivitellins during key moments of the reproductive cycle, that is, before and after first copulation and at low, medium, and high reproductive output. Copulation and first oviposition do not trigger the onset of albumen gland-capsule gland complex biosynthesis. On the contrary, soon after an intermediate reproductive effort, genes encoding perivitellins overexpressed. A high reproductive effort caused a decrease in all albumen gland-capsule gland complex secretion components. Right after a high reproductive output, the albumen gland-capsule gland complex restored the main secretion components, and calcium recovered baseline reserves, but proteins and polysaccharides did not. These metabolic changes in the albumen gland-capsule gland complex after multiple ovipositions were reflected in a reduction in egg mass but did not compromise egg quality. At the end of the cycle, egg dry weight almost doubled the initial albumen glandcapsule gland complex weight. Results indicate that albumen gland-capsule gland complex biosynthesis limits a constantly high reproductive output. Therefore, lowering fecundity by targeting biosynthesis could effectively reduce the rate of this species’ spread.
... Some field reports state that Snail Kites also discard a bulky accessory reproductive organ called the albumen-capsule gland complex or pallial oviduct, commonly referred to as the albumen gland (AG), when feeding on female snails (Snyder and Kale 1983). The AG synthesises the egg perivitelline fluid providing nutrients, protective compounds, and the calcareous eggshell (Catalán et al. 2006;Hayes et al. 2015). However, its biochemical composition is unknown for Pomacea species. ...
Snail Kites (Rostrhamus sociabilis) feed almost exclusively on Apple Snails (Pomacea spp.). While field observations indicate they discard the noxious albumen gland (AG) when feeding on female snails, there is no information on the energy lost by this behavior, the gland composition, or if there are snail sex preferences associated. We addressed for the first time these aspects for Snail Kites foraging on Pomacea canaliculata in southern South America. Whole snail’s biochemical composition exhibited significant differences between sexes. Proteins and carbohydrates were the major energy-providing components. Soft parts provide ~2.91±0.16 and 2.50±0.14 Kcal g-1 dw for male and female without AG, respectively while AG accounts for 15 % of available energy. Size and sex of prey consumed, determined at foraging perches sampled monthly, showed that Kites preferentially feed on the largest snails available throughout the sampling period. Even though the remains of female body without the AG have less energy than males, sex preferential predation toward females was observed. Our study demonstrates for the first time the optimal foraging trade-off between prey size/sex and nutrition/energy in Snail Kites. After discarding the albumen gland, male and female snails of equivalent size provide different nutrients and energy, though Snail Kite foraging is generally biased toward females mostly due to their bigger size suggesting Snail Kites are unable to distinguish between sex.
... Notably, these large egg clutches have no reported predators in their native range and only one predator (the fire ant, Solenopsis geminata (Fabricius, 1804)) in their invasive range, which is probably related to their bright coloration (aposematic) advertising the presence of noxious components (Snyder and Snyder 1971;Yusa et al. 2000;Stevens 2015). Furthermore, common predators of adult apple snails, such as rats, avoid eating Pomacea eggs and the albumen gland, a female gland of the reproductive tract that synthesizes and stores the egg perivitellinic proteins and large amounts of calcium for the calcareous egg shell (Yusa et al. 2000;Dreon et al. 2002;Catalán et al. 2006). ...
The freshwater snails Pomacea Perry, 1810 lay conspicuous aerial egg clutches that are ignored by most predators. Egg biochemical defenses in the apple snail Pomacea canaliculata (Lamarck, 1822) are provided by multifunctional proteins. We analyzed the eggs of a sympatric species, Pomacea maculata Perry, 1810, studying the gross composition, toxicity, hemagglutinating activity, and its antinutritive and antidigestive properties. Eggs are mostly composed of polysaccharides (mainly galactogen) and proteins, followed by lipids and nonsoluble calcium. Two perivitellins account for ∼85% dry mass of the egg protein. The major lipids are phospholipids and sterols. A suite of potential defenses was determined, including strong lethal neurotoxicity on mice and moderate antidigestive and lectin activities. Remarkably, their polysaccharides were refractive to in vitro digestion by digestive glycosidases. This study characterized ∼99% of egg composition and identified multiple potential defenses, provided not only by proteins but also by polysaccharides. This is the first evidence to our knowledge that reserve sugars may be involved in defenses, giving further insight into the unusual reproductive strategy of these well-defended snail eggs.
... The metabolites were inoculated with G. citri-aurantii (10 6 cells/mL) and incubated for 24 h at 28°C to determine their antifungal activity. After centrifugation (6708g), the supernatant was recovered and pellets were processed (Catalan et al. 2006) for ultrastructural analysis by transmission electron microscopy (TEM) technique. Untreated G. citri-aurantii cells have a cytoplasm, delineated with a thin, smooth plasmatic membrane, containing organelles such as mitochondria, vacuoles, and nuclei (Figs. ...
Geotrichum citri-aurantii is a postharvest phytopathogenic fungus of lemons. We studied the mode of action of antifungal metabolites from Bacillus sp. strain IBA 33 on arthroconidia of G. citri-aurantii. These metabolites are lipopeptides belonging to the iturin family. Membrane permeabilization of G. citri-aurantii was analyzed and mitochondrial respiratory rate was evaluated. Disturbance of the plasma membrane promotes the leakage of many cellular components into the surrounding media, and mitochondrial membrane disorganization promotes the inhibition of the respiratory rate. Our findings provide insights into the ability of lipopeptides to suppress plant fungal pathogens and their possible agronomical applications.
... Though filled with a perivitellin fluid (PVF) containing large amounts of carbohydrates and storage proteins (called perivitellins), these toxic eggs have no predators reported in their original South American range and only one in the newly colonized habitats in SE Asia: the fire ant Solenopsis geminata (Fabricius, 1804). The presence of these egg defenses [6;8;9] would explain the behavior of the snail kite Rostrhamus sociabilis (Vieillot, 1817) and Norway rat Rattus norvegicus (Berkenhout, 1769) that invariably discard the gland that synthesizes the egg defenses when predating on adult female P. canaliculata [10][11][12][13][14]. ...
Background
The spread of the invasive snail Pomacea canaliculata is expanding the rat lungworm disease beyond its native range. Their toxic eggs have virtually no predators and unusual defenses including a neurotoxic lectin and a proteinase inhibitor, presumably advertised by a warning coloration. We explored the effect of egg perivitellin fluid (PVF) ingestion on the rat small intestine morphology and physiology.
Methodology/Principal Findings
Through a combination of biochemical, histochemical, histopathological, scanning electron microscopy, cell culture and feeding experiments, we analyzed intestinal morphology, growth rate, hemaglutinating activity, cytotoxicity and cell proliferation after oral administration of PVF to rats. PVF adversely affects small intestine metabolism and morphology and consequently the standard growth rate, presumably by lectin-like proteins, as suggested by PVF hemaglutinating activity and its cytotoxic effect on Caco-2 cell culture. Short-term effects of ingested PVF were studied in growing rats. PVF-supplemented diet induced the appearance of shorter and wider villi as well as fused villi. This was associated with changes in glycoconjugate expression, increased cell proliferation at crypt base, and hypertrophic mucosal growth. This resulted in a decreased absorptive surface after 3 days of treatment and a diminished rat growth rate that reverted to normal after the fourth day of treatment. Longer exposure to PVF induced a time-dependent lengthening of the small intestine while switching to a control diet restored intestine length and morphology after 4 days.
Conclusions/Significance
Ingestion of PVF rapidly limits the ability of potential predators to absorb nutrients by inducing large, reversible changes in intestinal morphology and growth rate. The occurrence of toxins that affect intestinal morphology and absorption is a strategy against predation not recognized among animals before. Remarkably, this defense is rather similar to the toxic effect of plant antipredator strategies. This defense mechanism may explain the near absence of predators of apple snail eggs.
... The archenteron of P. canaliculata does not show any infoldings as those reported for Pila globosa (Ranjah, 1942) and this may be possibly related to the apparent role of giant cells in the midgut of P. canaliculata, since they would have assumed the role of endocytosing and concentrating the albumen contained in the midgut (Fig. 9B and C). Both the albumen in the central lake and within the vesicles of giant cells contain 20 nm granules of moderate electron density, which are interpreted as being identical to the galactogen-containing granules found in the albumen secretory cells of the maternal albumen gland (Catalán et al., 2006). The adult midgut gland in P. canaliculata is an organ in which any lobe can hardly be recognized. ...
... A feasible mechanism that might explain the effect of FA in females relates to the growth of the albumen gland-capsule gland (AG-CG) complex, the most bulky component of the female reproductive system (Catalán et al. 2006). This massive complex bulges into the mantle cavity (Andrews 1965) and modifies the water flow and compresses the pallial organs, which probably results in a modification in the shape of the aperture and consequently of the shell it generates. ...
Pomacea canaliculata, an invasive apple snail native to South America, is a serious pest of aquatic crops in several parts of the world. The origin of inter-population variation in shell shape is thought to be both genetic and environmental but the reaction norms to specific environmental factors are still poorly understood. Our aims were to analyze the existence of direct and indirect (allometric) effects of food availability (FA) on the shape of young adults of P. canaliculata. Full sibling hatchlings were reared under different levels of FA. Nine landmarks and 10 semi-landmarks were determined on photographs of mature shells and analyzed using geometric morphometrics. In both sexes significant allometry was found: a decrease in the spire height in both sexes, and an increase of the aperture size in males and of the last whorl in females. When this allometric component was removed a relationship between size-corrected shape and FA was found only in females, which were more globose and had a larger aperture when grown under high FA. This effect may be explained by the faster growth of the reproductive organs and the thinner shells of the best fed females.
... The archenteron of P. canaliculata does not show any infoldings as those reported for Pila globosa (Ranjah, 1942) and this may be possibly related to the apparent role of giant cells in the midgut of P. canaliculata, since they would have assumed the role of endocytosing and concentrating the albumen contained in the midgut (Fig. 9B and C). Both the albumen in the central lake and within the vesicles of giant cells contain 20 nm granules of moderate electron density, which are interpreted as being identical to the galactogen-containing granules found in the albumen secretory cells of the maternal albumen gland (Catalán et al., 2006). The adult midgut gland in P. canaliculata is an organ in which any lobe can hardly be recognized. ...
... Scale bars: 250 mm (A-C); 100 mm (a, b); 1 mm (D). Lach et al., 2001;Winik, Catalán, Schlick, 2001;Yusa, 2001Yusa, , 2004Yusa, , 2006Yusa, , 2007aCatalán, Fernández, & Winik, 2002;Ito, 2002;Yusa & Suzuki, 2003;Dreon et al., 2004;Gamarra-Luques et al., 2004, 2006Martín, Estebenet, & Burela, 2005;Vega et al. 2005Vega et al. , 2006Vega et al. , 2007Wu et al., 2005;Catalán et al., 2006;Damborenea, Brusa, & Paola, 2006;Koch et al., 2006;Levin et al., 2006;Liu et al., 2006;Yusa, Wada, & Takahashi, 2006;Burela & Martín, 2007Cowie et al., 2007;Matsukura & Wada, 2007;Takeichi, Hirai, & Yusa, 2007;Giraud-Billoud et al., 2008;Heiler et al., 2008;Heras et al., 2008;Jørgensen, Kristensen, & Madsen, 2008;Kwong et al., 2008Kwong et al., , 2009Matsukura et al., 2008a, b;Tran et al. 2008;Aizaki & Yusa, 2009;Koch, Winik, & Castro-Vazquez, 2009;Tamburi, & Martín, 2009;Winik et al., 2009;Wong, Kwong, & Qiu, 2009;Dreon, Ituarte, & Heras, 2010; et Kwong et al., 2010;Seuffert, Burela, & Martín, 2010;Wu et al., 2010Wu et al., , 2011Dong et al., 2011;Qiu et al., 2011, Tamburi, & Martín, 2011Wada & Matsukura, 2011;Thiengo et al., 2011. Pomacea cuprina -Mochida, 1991. ...
Ampullariidae comprises two lineages of freshwater gastropods: one Old World and one New World. Recent molecular work confirmed the monophyly of the family and began to clarify generic relationships, but current systematics remains unsatisfactory. With more than 300 available species group names for New World taxa alone, taxonomic confusion is rampant, as illustrated by two species that have been introduced widely and are difficult to differentiate conchologically, Pomacea maculata Perry, 1810 and Pomacea canaliculata (Lamarck, 1822). Misidentification hampers efforts to manage their spread and impacts as invasives, and prevents meaningful comparative analyses of their biology. Here we clarify the taxonomy, describe the morphological and genetic distinctiveness of the two species, and re-evaluate their biogeographic ranges. They differ most clearly genetically, with no shared haplotypes and a mean genetic distance of 0.135 at cytochrome c oxidase subunit I (COI). Differences in shell morphology are most obvious in recently hatched juveniles; the number of eggs per clutch is higher in P. maculata, and the individual eggs are smaller, so P. canaliculata hatchlings are nearly twice as large as those of P. maculata. Adult shells differ primarily in the angulation of the whorl shoulder and pigmentation of the inner pallial lip, with the latter a distinctive feature of P. maculata. They also differ in reproductive anatomy, most notably in P. canaliculata having two distinctive glandular tissues in the apical penial sheath gland, and P. maculata lacking a medial sheath gland but possessing a basal sheath gland. Pomacea canaliculata is restricted to a narrower southern range, whereas P. maculata ranges extensively throughout much of South America. Ampullaria gigas Spix, 1827 and Ampullaria insularum d'Orbigny, 1835 are herein synonymized with P. maculata. Neotypes are designated for P. maculata and A. gigas, and a lectotype is designated for A. insularum. A neotype is designated for P. canaliculata.
© 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 166, 723–753.
... The shell, uterus, and eggs are characterized by a high Ca content in P. canaliculata, both as concretions in shells and egg capsules, and in solution and concretions ("calcipherites") in the egg perivitellin fluid and the uterine albumensecreting cells (Catalán et al. 2006). These tissues showed the lowest BCFs for the 10 elements (Table 1). ...
The differential ability of apple snail tissues, endosymbionts, and eggs to bioaccumulate several metals (Sb, As, Ba, Br, Zn, Cr, Fe, Hg, Se, and U) was investigated.
Metal concentrations were determined by neutron activation analysis in several tissues, endosymbionts, and eggs from mature apple snails cultured in either drinking water or reconstituted water (prepared with American Society for Testing and Materials type I water).
The highest bioconcentration factors (BCFs) in the midgut gland were found for Ba, Zn, Se, As, U, Br, and Hg (in decreasing order), while the highest in the kidney were for Ba, Br, and Hg. The foot showed the highest BCFs for Ba, Hg, Br, and Se (in decreasing order). Calcified tissues (uterus, shell) and eggs showed low BCFs, except for Ba. Both C corpuscles and gland tissue showed statistically higher BCFs than K corpuscles for Ba, Fe, U, Br, and Sb. The concentration of most of the studied elements was significantly lower in tissues and endosymbionts obtained from snails cultured in reconstituted water instead of drinking water. Snails cultured in reconstituted water and then exposed or not to Hg, As, and U (at the maximum contaminant level allowed by the US Environmental Protection Agency) also resulted in high levels accumulated in midgut gland, endosymbionts and kidney.
Our findings suggest that the midgut gland (and the symbionts contained therein), the kidney, and the foot of Pomacea canaliculata may be useful bioindicators of Hg, As and U pollution in freshwater bodies and that the unrestricted use of ampullariid snails as human and animal food must be considered with caution.
