Email updates

Keep up to date with the latest news and content from Frontiers in Zoology and BioMed Central.

Open Access Research

The placental analogue and the pattern of sexual reproduction in the cheilostome bryozoan Bicellariella ciliata (Gymnolaemata)

Martin Moosbrugger1, Thomas Schwaha1, Manfred G Walzl1, Matthias Obst2 and Andrew N Ostrovsky34*

Author Affiliations

1 Department of Integrative Zoology, Faculty of Life Sciences, University of Vienna, Althanstraße 14, A-1090, Vienna, Austria

2 Department of Biological and Environmental Sciences, University of Gothenburg, Box 463, SE-40530, Gothenburg, Sweden

3 Department of Palaeontology, Faculty of Earth Sciences, Geography and Astronomy, Geozentrum, University of Vienna, Althanstraße 14, A-1090, Vienna, Austria

4 Department of Invertebrate Zoology, Faculty of Biology and Soil Science, St. Petersburg State University, Universitetskaja nab. 7/9, 199034, St. Petersburg, Russia

For all author emails, please log on.

Frontiers in Zoology 2012, 9:29  doi:10.1186/1742-9994-9-29

Published: 25 October 2012

Abstract

Background

Matrotrophy or extraembryonic nutrition – transfer of nutrients from mother to embryo during gestation – is well known and thoroughly studied among vertebrates, but still poorly understood in invertebrates. The current paper focuses on the anatomy and ultrastructure of the oogenesis and placentotrophy as well as formation of the brood chamber (ovicell) in the cheilostome bryozoan Bicellariella ciliata (Linnaeus, 1758). Our research aimed to combine these aspects of the sexual reproduction into an integral picture, highlighting the role of the primitive placenta-like system in the evolution of bryozoan reproductive patterns.

Results

Follicular and nutrimentary provisioning of the oocyte occur during oogenesis. Small macrolecithal oocytes are produced, and embryos are nourished in the ovicell via a simple placental analogue (embryophore). Every brooding episode is accompanied by the hypertrophy of the embryophore, which collapses after larval release. Nutrients are released and uptaken by exocytosis (embryophore) and endocytosis (embryo). Embryos lack specialized area for nutrient uptake, which occurs through the whole epidermal surface. The volume increase between the ripe oocyte and the larva is ca. 10-fold.

Conclusions

The ovicell is a complex organ (not a special polymorph as often thought) consisting of an ooecium (protective capsule) and an ooecial vesicle (plugging the entrance to the brooding cavity) that develop from the distal and the fertile zooid correspondingly. Combination of macrolecithal oogenesis and extraembryonic nutrition allows attributing B. ciliata to species with reproductive pattern IV. However, since its oocytes are small, this species represents a previously undescribed variant of this pattern, which appears to represent a transitional state from the insipient matrotrophy (with large macrolecithal eggs) to substantial one (with small microlecithal ones). Altogether, our results substantially added and corrected the data obtained by the previous authors, providing a new insight in our understanding of the evolution of matrotrophy in invertebrates.

Keywords:
Matrotrophy; Oogenesis; Ovicell; Placental analogue; Bicellariella ciliata; Bryozoa