Polymorphism and vestigiality: comparative anatomy and morphology of bryozoan avicularia

Abstract

Avicularia are polymorphic zooids characteristic of cheilostome bryozoans. Avicularia are assumed to have a defensive role yet ascertaining the presence of sensory structures to support this theory has been overlooked. We examine palatal morphology of the avicularia from five species of cheilostome bryozoans and compare the ultrastructural anatomy of the avicularia from two bugulid species from different habitats. SEM analysis revealed an array of palatal morphologies. Small tufts of cilia emerge from the orifice in the palate of the avicularia of Tricellaria catalinensis, Arachnopusia unicornis and Catenicella pseudoelegans. A ciliated vestigial polypide emerges from the orifice in the palate of Rhynchozoon zealandicum and comprises eleven papillae, or vestigial tentacles, seven of which are covered in microvilli. The vestigial polypide of the bird's head avicularium of the cosmopolitan Bugula flabellata consists of a mass of ciliated and unciliated cells containing numerous granular vesicles. The avicularium of B. flabellata is capable of detecting tactile stimulation by virtue of the tuft of sensory cilia and is proactive in the capture of invertebrate epibionts. In contrast, in the deep-sea Nordgaardia cornucopioides, the vestigial polypide consists of a ciliated vestigial tentacle encased by glandular secretory cells. Avicularia possess structures derived from a feeding autozooid, and we show how the homologous structures have evolved and suggest that avicularia have been modified to carry out a variety of specific functions.

Division of labor and recurrent evolution of polymorphisms in a group of colonial animals

“…3), strongly indicate that avicularia serve various functions across many taxa (Marcus 1939;Silén 1977;Winston 1984). Some avicularia can grasp and hold small motile invertebrates, often until death ensues (Nordmann 1840;Winston 1986Winston , 1991Winston , 2010Carter et al 2010a). Such behavior has led to the general consensus that many and perhaps most avicularia have a defensive function (Darwin 1872;Nordmann 1840;Johnston 1847;Kaufmann 1968Kaufmann , 1971Winston 1984Winston , 1986Winston , 1991, yet their capacity for such a role and their impact on potential threats to the colony have not been rigorously examined (Carter et al 2010b).…”

“…In contrast, the retractor muscles, responsible for retraction of the polypide in the autozooid, are reduced to a couple of single fibers in the avicularium (Carter et al in press). The vestigial polypide consists of a mass of ciliated cells, the remnant of the ciliated tentacles in autozooids (Carter et al 2010a). When the mandible is open, a tuft of cilia everts through the avicularian palate and is exposed to the external environment (Fig.…”

Functional innovation through vestigialization in a modular marine invertebrate

“…Nordmann (1840) noted the apparent lack of feeding and digestive organs and observed a bird's-head avicularium rapidly clamp down on a passing nematode, holding it for hours until the worm was eventually torn where it was clamped. This commenced the interpretation of a defensive function for the bird's-head avicularium (and some of the other avicularian types) that is now supported by a long historical sequence of studies (Busk, 1852;Hincks, 1880;Harmer, 1901;Kaufmann, 1968Kaufmann, , 1971Winston, 1984Winston, , 1986Winston, , 2010Carter, Gordon & Gardner, 2010b). This paper forms part of a larger study that revisits the bird's-head avicularium of B. flabellata and incorporates modern microscopic techniques to describe in detail the morphology and ultrastructural anatomy of the bird's-head avicularium (Carter et al, 2010b).…”

“…This commenced the interpretation of a defensive function for the bird's-head avicularium (and some of the other avicularian types) that is now supported by a long historical sequence of studies (Busk, 1852;Hincks, 1880;Harmer, 1901;Kaufmann, 1968Kaufmann, , 1971Winston, 1984Winston, , 1986Winston, , 2010Carter, Gordon & Gardner, 2010b). This paper forms part of a larger study that revisits the bird's-head avicularium of B. flabellata and incorporates modern microscopic techniques to describe in detail the morphology and ultrastructural anatomy of the bird's-head avicularium (Carter et al, 2010b). In this component of the study, we use laser scanning confocal microscopy to describe the occurrence of retractor and circular muscles in the bird's-head avicularium that were previously unreported.…”

Feeding deterrency in Antarctic marine organisms: bioassays with the omnivore amphipod Cheirimedon femoratus

“…The sea cucumber Peniagone vignioni, due to its ability to move and swim, may be less vulnerable to amphipod predation, and might not require chemical defenses (Galley et al 2008). Similarly, the bryozoan Isoschizoporella secunda uses alternative defense strategies in the form of a calcified structure (Winston & Bernheimer 1986) and avicularia that can act as traps for small crustaceans (Carter et al 2010), making unpalatability redundant. The extract from Cephalo discus nigrescens was inactive, even phagostimulatory (Fig.…”