Ultrastructural and elemental characterization of the extracorporeal tube of the sessile rotifer Floscularia conifera (Rotifera: Gnesiotrocha)

Abstract

Rotifers are aquatic microinvertebrates that live in the plankton or in the benthos, which may include a variety of macrophytes. Among these periphytic forms of rotifers, some have taken up a sessile existence and secrete protective tubes around their bodies. One type of tube common to species of Floscularia is made of small round pellets. To date, the building process and some fine structural details are known for Floscularia ringens, but many questions about the composition of the tube and its ultrastructure still remain unanswered. Here, we use transmission electron microscopy and scanning electron microscopy-energy dispersive X-ray spectroscopy (SEM-EDS) to study the ultrastructure of the pellets and their elemental composition, respectively, in the putative sister species, Floscularia conifera. We revealed several new details that add important information about the physiology of tubemaking in species of Floscularia. First, we note an inner secretory membrane that is thin, electron lucent, and supports the external pellets. The pellets are relatively consistent in size and have a small depression on their inner surface. All pellets are individually wrapped in a secretory membrane that completely encapsulates suspended materials collected from the surrounding water. Elemental signatures of pellets reveal they consist mostly of carbon (C), nitrogen (N), and oxygen (O), with some silicon (Si) content that is likely the result of diatom shells. Other trace elements such as iron (Fe) and sodium (Na) are also present and likely the result of incorporated bacteria and suspended materials. When larval rotifers are cultured in filtered pond water, the pellets consist mostly of C and O, with little N and no Si; Fe is present in smaller amounts. These new discoveries provide a better understanding of the physiology of rotifer tube construction and tube composition, and their future utility in understanding if and how changes in freshwater environments might impact these factors. K E Y W O R D S allochthonous, pellets, secretion, sessile, silicon

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

“…In species with a hardened, cement‐like matrix such as Limnias melicerta , or in species with a pellet‐like tube such as Floscularia conifera , there is always a layer of hydrogel‐like matrix beneath them that appears to be secreted at the base of the foot and probably functions as a form of mortar to hold the more solid, external pieces in place. Importantly, both the cement‐like matrix (Yang & Hochberg, 2018a) and the pellets (Fontaneto et al, 2003; Yang & Hochberg, 2018b) are derived from a specialized integumental region in the trunk (syncytial glandular regions) or a modified organ on the corona (modulus), respectively, suggesting that the origins of the hardened secretions and the hydrogel matrices are different.…”

“…The sessile species are known to secrete soft hydrogels (Wright, 1959), hardened pipes (Wright, 1954), and chimney‐like pipes of pellets (Wright, 1950), but regardless of their external appearance, all appear to have a hydrogel component (Yang & Hochberg, 2018a, 2018b). For example, Limnias melicerta Weisse 1848 secretes a hardened pipe derived from multiple ring‐like secretions that have a gelatinous foundation (Yang & Hochberg, 2018a), whereas Floscularia conifera ( Hudson 1886) secretes a gelatinous base around its foot and slowly adds pellets onto the base, eventually producing a chimney‐like structure (Yang & Hochberg, 2018b). Other rotifers appear to secrete only a gel, which takes the form of a soft, cushion‐like matrix that is somewhat elastic and semi‐opaque (Wallace et al, 2015; Wright, 1959).…”

Key to sessile gnesiotrochan rotifers: Floscularia (Monogononta; Flosculariidae)

“…These are then laid one upon another-like a brick layer might do-to form a tubular wall resembling the turret of a medieval castle (Remane 1929(Remane -1933Wright 1950). The inside of these tubes is apparently lined with a membranous coat (Fontaneto et al 2003;Yang & Hochberg 2018a). Differences in suspended particles may alter the color of the pellets (see below) (Edmondson 1945;Hudson & Gosse 1886).…”

“…Identification of sessile rotifers is based on relatively simple characters, including shape of the corona, presence of sensory and other morphological structures in the apical field, body size, propensity to form colonies, and the fact that many species form extracorporeal coverings that surround their bodies (Yang & Hochberg 2018a, 2018bYang et al 2021). Indeed, because these coverings vary in their construction to include gelatinous matrices, flexible, hardened tubes, and pipe-like tubes composed of pellets, their composition is a convenient characteristic on which keys to the genera and even species may be based (Davies et al 2024;Edmondson 1959;Koste 1978).…”

Sessile rotifers (Rotifera) exhibit strong seasonality in a shallow, eutrophic Ramsar site in Mexico

“…Several other studies have only focused on one or at best a few species at a time (Bevington, White, & Wallace, ; Sarma, Jiménez‐Santos, Nandini, & Wallace, ; Sarma & Rao, ; Wallace, ; Wallace, Cipro, & Grubbs, ; Wallace & Edmondson, ; Wallace & Starkweather, , ). The paucity of information on these sessile organisms is not surprising because when preserved, these illoricate species contract into a nearly unidentifiable lump of tissue (Wallace, Snell, & Smith, ; Yang & Hochberg, ). Similar to planktonic taxa, sessile rotifers have a global distribution (Koste, ; Segers, ) and are found in a wide range of environmental conditions (Edmondson, ; Sládeček, ), including acid bog ponds (Wallace, ), arid lands (Jersabek & Bolortsetseg, ; Walsh, Arroyo, Schröder, & Wallace, ), and the Antarctic (Fontaneto, Iakovenko, & De Smet, ).…”