Comparative anatomical study of internal brooding in three anascan bryozoans (Cheilostomata) and its taxonomic and evolutionary implications

Abstract

The anatomical structure of internal sacs for embryonic incubation was studied using SEM and light microscopy in three cheilostome bryozoans-Nematoflustra flagellata (Waters,1904), Gontarella sp., and Biflustra perfragilis MacGillivray, 1881. In all these species the brood sac is located in the distal half of the maternal (egg-producing) autozooid, being a conspicuous invagination of the body wall. It consists of the main chamber and a passage (neck) to the outside that opens independently of the introvert. There are several groups of muscles attached to the thin walls of the brood sac and possibly expanding it during oviposition and larval release. Polypide recycling begins after oviposition in Gontarella sp., and the new polypide bud is formed by the beginning of incubation. Similarly, polypides in brooding zooids degenerate in N. flagellata and, sometimes, in B. perfragilis. In the evolution of brood chambers in the Cheilostomata, such internal sacs for embryonic incubation are considered a final step, being the result of immersion of the brooding cavity into the maternal zooid and reduction of the protecting fold (ooecium). Possible reasons for this transformation are discussed, and the hypothesis of Santagata and Banta (Santagata and Banta1996) that internal brooding evolved prior to incubation in ovicells is rejected.

The Internal-Brooding Apparatus in the Bryozoan Genus Cauloramphus (Cheilostomata: Calloporidae) and Its Inferred Homology to Ovicells

“…These similarities, along with the simple zooidal morphology and encrusting growth form of Gontarella, suggest that Gontarella might belong in the Calloporidae rather than in the Flustridae as Ostrovsky et al (2006) previously suggested. This is supported by the observation (Ostrovsky et al, 2006) that the internal brood sacs of Cauloramphus and Gontarella differ from those in representative species of the flustrid genera Nematoflustra and Biflustra, which have a different muscle arrangement and a shorter neck. In Gontarella, there is no trace of a kenozooidal ooecium, nor of a vestigial sclerite of the ooecial vescicle.…”

“…The internal brood sac in the genus Gontarella (Grischenko et al, 2002;Ostrovsky et al, 2006) is quite similar to that in Cauloramphus, in terms of the structure of the sac, the positions of its attached muscle bands, and the long neck. These similarities, along with the simple zooidal morphology and encrusting growth form of Gontarella, suggest that Gontarella might belong in the Calloporidae rather than in the Flustridae as Ostrovsky et al (2006) previously suggested.…”

“…The internal brood sac in the genus Gontarella (Grischenko et al, 2002;Ostrovsky et al, 2006) is quite similar to that in Cauloramphus, in terms of the structure of the sac, the positions of its attached muscle bands, and the long neck. These similarities, along with the simple zooidal morphology and encrusting growth form of Gontarella, suggest that Gontarella might belong in the Calloporidae rather than in the Flustridae as Ostrovsky et al (2006) previously suggested. This is supported by the observation (Ostrovsky et al, 2006) that the internal brood sacs of Cauloramphus and Gontarella differ from those in representative species of the flustrid genera Nematoflustra and Biflustra, which have a different muscle arrangement and a shorter neck.…”

“…Hyperstomial ovicells are the most common type of brood chamber in cheilostome bryozoans and consist of the following elements: 1) the ooecium, a double-walled, often hemispherical outgrowth, produced either by the maternal (egg-producing) zooid or the distal auto-or kenozooid, containing an enclosed coelomic lumen that connects with the zooid of origin through one or more pores; 2) a component of non-calcified distal wall from the maternal zooid, often in the form of an ooecial vesicle (=ooecial plug), and 3) a brood chamber (brooding cavity) bounded by the ooecial and maternal-wall components (Ryland, 1976;Ryland and Hayward, 1977;Reed, 1991;Ostrovsky, 1998;Ostrovsky et al, , 2006. The brooding apparatus in Cauloramphus contains all these elements (all maternally derived) and thus shows homology with cheilostome hyperstomial ovicells, though highly modified in form.…”

“…Ostrovsky et al (2006) proposed several hypotheses (not mutually exclusive) to explain this transition: (1) reduction of ooecia could conserve energy for somatic growth and reproduction; (2) internal brooding cavities may be more spacious than ovicells, allowing the brooding of larger larvae; and (3) internal brooding may be an evolutionary response to the evolution of predators that feed on embryos held in ovicells. In any case, the numerous internal brooders known among different cheilostome families shows that the internalization of brooding is a novelty that allows them to successfully compete with relatives possessing ooecia in the form of prominent protective hoods.…”