Comparative Anatomical Study of Internal Brooding in
Three Anascan Bryozoans (Cheilostomata) and Its
Taxonomic and Evolutionary Implications
Andrew N. Ostrovsky,
1
Andrei V. Grischenko,
2
Paul D. Taylor,
3
* Phil Bock,
4
and
Shunsuke F. Mawatari
2
1
Department of Invertebrate Zoology, Faculty of Biology & Soil Science, St. Petersburg State University,
St. Petersburg 199034, Russia
2
Division of Biological Sciences, Graduate School of Science, Hokkaido University, Sapporo 060 0810, Japan
3
Department of Palaeontology, Natural History Museum, London SW7 5BD, UK
4
School of Ecology & Environment, Deakin University, Burwood, VIC 3125, Australia
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 re-
lease. Polypide recycling begins after oviposition in Gon-
tarella 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 incuba-
tion are considered a final step, being the result of immer-
sion of the brooding cavity into the maternal zooid and
reduction of the protecting fold (ooecium). Possible rea-
sons for this transformation are discussed, and the hy-
pothesis of Santagata and Banta (1996) that internal
brooding evolved prior to incubation in ovicells is rejected.
J. Morphol. 267:739 –749, 2006. © 2006 Wiley-Liss, Inc.
KEY WORDS: parental care; ovicells; internal brood sacs;
evolution; Cheilostomata; Bryozoa
The origin of parental care in the bryozoan order
Cheilostomata is considered one of the key evolu-
tionary innovations contributing to their success in
benthic marine communities from the mid-
Cretaceous to the present day (Taylor, 1988). Two
facts that favor this supposition are: 1) despite an-
tedating brooders, nonbrooders are represented by
very few fossil and Recent species, and most cheilos-
tomes instead hold their embryos in special embry-
onic chambers called ovicells; and 2) the earliest
known fossil ovicells coincide in time with the onset
of an explosive radiation of cheilostomes in the Late
Albian.
Incubation in the coelom (more precisely, in the
ovary) is restricted to one cheilostome family (Epis-
tomiidae). Only a few species, belonging to the prim-
itive genera Aetea (Aeteidae), Eucratea (Eucratei-
dae) and Leiosalpinx (Leiosalpingidae), brood their
embryos externally in a membranous sac. The over-
whelming majority of cheilostomes brood embryos in
chambers with calcified walls (ovicells), in which the
brood cavity is external with respect to the visceral
coelom. In species with internal brood sacs formed
by noncalcified zooidal walls, the brood cavity is also
external with respect to the coelomic cavity of the
maternal (egg-producing and brooding) zooid and
yet is completely immersed in the maternal zooid
and therefore often difficult to recognize (reviewed
in Hyman, 1959; Stro ¨m, 1977; Reed, 1991; Os-
trovsky, 2006a).
Internal brooding is known in both anascan (Sub-
order Flustrina) and ascophoran (Suborder Asco-
phora) cheilostomes. Among anascans it has been
reported in species assigned to the Flustridae, Can-
didae, Steginoporellidae, Poricellariidae, Chlidoni-
idae, and a few other families (see below), and
among ascophorans, in species of Adeonidae, Ad-
eonellidae, Watersiporidae, Cryptosulidae, and Eu-
Contract grant sponsor: Alexander von Humboldt Foundation, Ger-
many, and the Lise Meitner Foundation, Austria (postdoctoral fellow-
ships to A.N.O.); Contract grant sponsor: 21st Century Center of
Excellence (COE) Program on “Neo-Science of Natural History” (Pro-
gram Leader: H. Okada, Co-ordinator Dr. P. Gautam) at Hokkaido
University financed by the Ministry of Education, Culture, Sports,
Science, and Technology, Japan (research fellowship); Contract grant
sponsor: JSPS (fellowship to P.D.T.).
*Correspondence to: Dr. P.D. Taylor, Department of Palaeontology,
Natural History Museum, Cromwell Road, London SW7 5BD, UK.
E-mail: pdt@nhm.ac.uk
Published online 8 March 2006 in
Wiley InterScience (www.interscience.wiley.com)
DOI: 10.1002/jmor.10438
JOURNAL OF MORPHOLOGY 267:739 –749 (2006)
© 2006 WILEY-LISS, INC.