The ultrastructure of the integument and proventriculus in the raptorial rotifer Cupelopagis vorax (Monogononta: Collothecaceae: Atrochidae)

Abstract

Members of the sessile rotifer species Cupelopagis vorax are unusual ambush predators that live permanently attached to submerged freshwater plants. Previous light microscopical research has revealed several uncommon features in this species including a stellate‐patterned integument and an expansive foregut region called the proventriculus. In this study, we apply transmission electron microscopy to explore the ultrastructure of both the integument and foregut to determine how they differ from other rotifers. Our results reveal that the integument is covered by a thick glycocalyx and is patterned with tubercles that originate from the intracytoplasmic lamina (ICL) within the syncytial epidermis. The ICL forms an apical layer within the syncytium, is electron dense and mostly amorphous, and forms tubercles up to 2.3 μm; these tubercles probably account for the patterned appearance of the integument and are similar to what has been found in other gnesiotrochan rotifers. The basal cytoplasm is highly granular and contains two types of membrane‐bound vesicles: large ovoid vesicles (320–411 nm) with amorphous, opaque contents, and secretory bulbs (110–264 nm) with electron‐lucent cores and occasionally electron‐dense contents. Only the secretory bulbs were observed to form connections to the apical plasmalemma, and so are probably exocytotic. Internally, the proventriculus is a large distensible sack that connects the anterior pharyngeal tube to the posterior mastax. The proventricular epithelium is a thin syncytium mostly covered with a dense glycocalyx and a strong brush border of microvilli underlain by a thin terminal web. The cytoplasm contains few organelles and there is no evidence that it is either secretory or has features (e.g., ICL) that might aid in maceration. We hypothesize that the thick glycocalyx might serve a protective function against the movements of live prey and/or against enzymes released from the rotifer's gastric glands that become regurgitated during feeding.

Substratum selection and feeding responses influence the demography of the sessile rotifer Cupelopagis vorax (Collothecacea: Atrochidae)

“…During predatory behaviour, Cupelopagis rotates on a short, flexible, pedal stalk and captures prey that come close to its infundibulum (Bevington et al, 1995). Thus, this species is the only rotifer known to exhibit specific attack behaviour (i.e., extending the corona) towards water currents produced by potential prey (Bevington et al, 1995; Hochberg et al, 2017); most sessile rotifers contract their corona when they detect vibrations (Sarma et al, 2020). Wright (1958) also describes how collothecid rotifers (e.g., C. ornata ) use their setae [which he terms cilia] to capture prey by flicking the prey (flagellates, small ciliates and rotifers) towards the base of the infundibulum; however, this action does not appear to be initiated, by vibrations made by prey.…”

Ultrastructure of extracorporeal secretions of four sessile species of Rotifera (Gnesiotrocha), with observations on the chemistry of the gelatinous tube

“…To our knowledge, this is the first detailed ultrastructural study of the extracorporeal tubes of rotifers. Previously, the only other secretion that has been documented in any detail is the glycocalyx, which is secreted by the syncytial integument and varies in both thickness and other properties across species (Clément, 1969; Koehler, 1965; Storch & Welsch, 1969; Brodie, 1970; Schramm, 1978; Clément & Wurdak, 1991; Hochberg et al, 2015; Hochberg, Walsh, et al, 2017; Hochberg, Yang, et al, 2017). The peduncle has never been examined before.…”

Remodeling of the nervous system of the indirectly developing rotifer Cupelopagis vorax (Gnesiotrocha, Collothecaceae)

“…To date, there is little information on the lifecycle dynamics or larvae of C. vorax (Evans, 1981; Koste, 1978), but several details exist on the morphology of the adult female (Cori, 1925; Gast, 1900; Hochberg et al., 2017; Koste, 1978; Leidy, 1857; Montgomery, 1903; Vasisht & Dawar, 1969). In particular, the study by Vasisht and Dawar (1969) provided comprehensive information on the adult female's nervous system, ultimately concluding that despite the species' unique appearance, it was very similar to that of other rotifers.…”

“…Food is processed by the mastax, where the trophi masticate it before being moved through the esophagus and into the stomach (Starkweather, 1996; Wallace et al., 2015). Variations in feeding behavior and digestive organization are present in specialized taxa (e.g., parasitic rotifers: May, 1989; Cupelopagis vorax (L eidy 1857): Bevington et al., 1995; Hochberg et al., 2017).…”

“…However, observations of several species of Collothecidae and Atrochidae, together forming the order Collothecaceae, have shown that this life stage goes through a dramatic metamorphosis. This transformation leads to a complete replacement of the larval head with a new adult head, called the infundibulum (Hochberg & Hochberg, 2015, 2017; Hochberg et al., 2017, 2019; Kutikova, 1995). Larvae do not feed but appear to survive on limited maternal reserves (Wallace, 1993; Young et al., 2019) and must, therefore, find a suitable substrate before expending their energy (Wallace, 1980).…”