Reproductive biology, embryonic development and matrotrophy in the phylactolaemate bryozoan Plumatella casmiana

Abstract

Bryozoa is a phylum of aquatic, colonial suspension-feeders within the Lophotrochozoa. In the Phylactolaemata embryonic development occurs in an internal brood sac on the body wall accompanied by extraembryonic nutrition. Owing to previous contradictive descriptions, many aspects of their sexual reproduction require restudy. Consequently, this study analyses embryogenesis of the freshwater bryozoan Plumatella casmiana by serial sections, 3D reconstruction and transmission electron microscopy. Early embryos cleave and soon develop into blastulae with a small central cavity. The mesoderm forms by delamination starting from the distal side towards the proximal end. In later embryos two polypides form on the posterior side that ultimately will be covered by a ciliated mantle in the larva. Embryos increase in size during development and form temporary cell contacts to the embryo sac. Mesodermal cells of the embryo sac show signs of transcellular transport indicating that embryos are nourished by transferring nutrients from the maternal coelom towards the brood cavity. This study clarifies several details such as mesoderm formation and the onset of bud development. Embryos are connected to their respective embryo sacs by a variety of temporary cytoplasmic processes formed by both tissues during embryogenesis, including a ‘placental’ ring zone. Although ultrastructural data of these cell contacts are not entirely conclusive about their function, we suggest that embryos absorb nutrients via the entire surface. The close opposition of embryos to the embryo sac implies placentation as matrotrophic mode in phylactolaemate bryozoans, with embryo sacs acting as placental analogues.

Morphology of ctenostome bryozoans: 5. Sundanella, with description of a new species from the Western Atlantic and the Multiporata concept

“…So far, our knowledge is incomplete and inconclusive: our data on S. sibogae show multiple early embryos embedded into the thinned vestibular wall, whereas previous observations found embryos immersed in an invagination of the body wall forming a two‐layered embryo sac with a rather hypertrophied epithelium (Braem, 1939). This is, in fact, a situation resembling phylactolaemate bryozoans (Bibermair et al, 2021; Ostrovsky et al, 2009, 2016). While the brooding of embryos in the vestibular wall is not uncommon (Ström, 1977), it often occurs in victorellid bryozoans (Braem, 1951).…”

“…an invagination of the body wall forming a two-layered embryo sac with a rather hypertrophied epithelium (Braem, 1939). This is, in fact, a situation resembling phylactolaemate bryozoans (Bibermair et al, 2021;Ostrovsky et al, 2009Ostrovsky et al, , 2016. While the brooding of embryos in the vestibular wall is not uncommon (Ström, 1977), it often occurs in victorellid bryozoans (Braem, 1951).…”

Aboral (pallial) epithelium in bryozoan larvae: a comparative morpho-functional analysis

“…During development, the embryo of matrotrophic Amathia greatly increases occupying most of the brooding zooid (see, e.g., Schwaha et al, 2019); thus, the expanded locomotory corona could be a major 'tool' for larval release (Reed, 1988). many myolaemate lineages, the larval development was supplemented by extraembryonic nutrition, resulting in a considerable increase in larval size (e.g., Borg, 1926;Woollacott, Zimmer, 1975;Dyrynda, King, 1982;Hughes, 1987;Moosbrugger et al, 2012;Ostrovsky, 2013b;Schwaha et al, 2019;Nekliudova et al, 2021;Bibermair et al, 2021). Thus, the oocyte-larval large size could conflict with the size of the much smaller opening of incubation chamber.…”

“…The development of an extensive corona did not prevent the nutrient absorption and endocytosis in phylactolaemate, cyclostome, and some coronate larvae from the fluid of the incubation cavity during development. Although endocytosis occurs from all sides of the developing embryo via its superficial cells (Moosbrugger et al, 2012;Ostrovsky, 2013b;Schwaha et al, 2019;Nekliudova et al, 2019aNekliudova et al, , 2021Bibermair et al, 2021), the pallial epithelium probably is the least suited for this function, as it is either covered by a protective cuticle or shell, or immersed.…”

“…Bryozoa comprises two major clades -Phylactolaemata and Myolaemata . Phylactolaemata are exclusively freshwater, non-skeletal bryozoans with placental matrotrophy and highly modified sexual and asexual development (Bibermair et al, 2021). This class is not considered in this study.…”