Pallial oviduct of Pomacea canaliculata (Gastropoda): ultrastructural studies of the parenchymal cellular types involved in the metabolism of perivitellins

Abstract

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 cells (LC), undergo seasonal variations throughout the annual reproductive cycle, which is divided into three periods. Both cellular types show maximal development and structural complexity during the reproductive period (spring and summer). AS cells have a well-developed Golgi complex and rough endoplasmic reticulum and their secretory granules show electron-dense particles of about 20 nm (probably galactogen). These cells are uniquely involved in ovorubin and PV2 perivitellin synthesis and their secretory granules are the single storage site for these two major perivitellins, as revealed by immunoelectron microscopy. AS also possess calcium deposits that infiltrate the cytoplasmic matrix. The luminal surfaces of LC exhibit long cilia intermingled with sparce short microvilli. Basally, the plasma membrane shows deep irregular folds that extend through the cytoplasm up to the subapical region. Calcium deposits infiltrate the cytoplasm and accumulate in the extracellular space of the basal labyrinth. Nerve terminals seem to be involved in the regulation of parenchymal cell secretion. At the post-reproductive period, AS markedly change their aspect following the release of most of the secretory granules into the acinar lumen. LC decrease in volume, the number of their cilia decreases, their cytoplasmic folds are much thinner and their extracellular spaces lack calcium particles. At the pre-reproductive period (winter), AS and LC recover and prepare for the subsequent period.

Comparing apples with apples: clarifying the identities of two highly invasive Neotropical Ampullariidae (Caenogastropoda)

“…Pomacea canaliculata – Cheesman, 1958; Andrews, 1964, 1965; Estebenet & Cazzaniga, 1992, 1993; Smith, 1992; Cowie, 1995; Heras, Garin, & Pollero, 1998; Lach & Cowie, 1999; Watanabe et al ., 2000; Lach et al ., 2001; Winik, Catalán, Schlick, 2001; Yusa, 2001, 2004, 2006, 2007a, b; Catalán, Fernández, & Winik, 2002; Ito, 2002; Yusa & Suzuki, 2003; Dreon et al ., 2004; Gamarra‐Luques et al ., 2004, 2006; Martín, Estebenet, & Burela, 2005; Vega et al . 2005, 2006, 2007; Wu 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, 2007, 2011; Cowie et al ., 2007; Hayes, Tran, & Cowie, 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 ., 2008, 2009; Matsukura et al ., 2008a, b; Tran et al . 2008; Aizaki & Yusa, 2009; Koch, Winik, & Castro‐Vazquez, 2009; Qiu & Kwong, 2009; Tamburi, & Martín, 2009; Winik et al ., 2009; Wong, Kwong, & Qiu, 2009; Dreon, Ituarte, & Heras, 2010; Fang et al ., 2010; Kwong et al ., 2010; Seuffert, Burela, & Martín, 2010; Seuffert & Martín, 2010; Wu et al ., 2010, 2011; Dong et al ., 2011; Qiu et al ., 2011, Tamburi, & Martín, 2011; Wada & Matsukura, 2011; Thiengo et al ., 2011.…”

“…The oviduct of what has been previously referred to as P. canaliculata is typically portrayed as possessing a small, sac‐like copulatory bursa (Simone, 2004), or vestigial pseudobursa (Berthold, 1991), at the junction of the seminal receptacle with the capsule gland. The two blind diverticulae of the albumen gland are represented as ‘ducts’ of the albumen gland, each draining towards the junction with the capsule gland and bursa (Andrews, 1964; Thiengo et al ., 1993; Catalán et al ., 2002; 2006). It seems this interpretation can be traced to Andrews (1964), who was the first to label the blind diverticulae ‘ducts of the albumen gland’ (although only one was shown for P. canaliculata ), and stated that there was no evidence the eggs entered the ‘duct’.…”

The eggs of the apple snailPomacea maculataare defended by indigestible polysaccharides and toxic proteins

“…Notably, these large eggs clutches have no reported predators in their native range and only one predator (the 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 amount of calcium for the calcareous egg shell (Yusa et al 2000;Dreon et al 2002;Catalán et al 2006).…”

Insights into Embryo Defenses of the Invasive Apple Snail Pomacea canaliculata: Egg Mass Ingestion Affects Rat Intestine Morphology and Growth

“…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]–[14].…”