Skeletal resorption in bryozoans: occurrence, function and recognition

Abstract

Skeletal resorption – the physiological removal of mineralised parts by an organism – is an important morphogenetic process in bryozoans. Reports of its occurrence and function across the phylum are patchy, however, and have not previously been synthesised. Here we show that resorption occurs routinely across a wide range of bryozoan clades, colony sizes, growth forms, ontogenetic stages, body wall types, skeletal ultrastructures and mineralogies. Beginning in the early Paleozoic, different modes and functions of resorption have evolved convergently among disparate groups, highlighting its utility as a morphogenetic mode in this phylum. Its functions include branch renovation, formation of branch articulations, excavation of reproductive chambers, part‐shedding, and creation of access portals for budding beyond previously formed skeletal walls. Bryozoan skeletons can be altered by resorption at microscopic, zooidal and colony‐wide scales, typically with a fine degree of control and coordination. We classified resorption patterns in bryozoans according to the morphology and function of the resorption zone (window formation, abscission or excavation), timing within the life of the skeletal element resorbed (primary or secondary), and scale of operation (zooidal or multizooidal). Skeletal resorption is probably greatly underestimated in terms of its utility and role in bryozoan life history, and its prevalence across taxa, especially in fossil forms. It is reported proportionally more frequently in stenolaemates than in gymnolaemates. Some modes of resorption potentially alter or remove the spatial–temporal record of calcification preserved within a skeleton. Consequently, knowledge that resorption has occurred can be relevant for some common applications of skeletal analysis, such as palaeoenvironmental interpretation, or growth and ageing studies. To aid recognition we provide scanning electron microscopy, backscattered electron scanning electron microscopy and transmission electron microscopy examples of skeletal ultrastuctures modified by resorption.

Can colony resizing represent a strategy for octocorals to face climate warming? The case of the precious red coral Corallium rubrum

“…This structure demonstrated an active process of mineralization acting on the fragmented surfaces, as previously described under laboratory conditions by Russo et al (1997). The ability of autotomy and resorption of mineral and organic skeletal components is typical in most marine phyla, including Cnidaria (Batson et al 2020). In the red coral skeletome, various matrix metallopeptidases and collagen-like proteins have been found (Le Roy et al 2021), and, due to the role they play in remodelling and mineralization processes, they may be also involved in the scleraxis resorption.…”

Composite branch construction by dual autozooidal budding modes in hornerids (Bryozoa: Cyclostomatida)

“…Evidence supporting a hornerid origin of C. osheai includes: (1) eruption of occasional short functionally unilaminate branches, with distinct frontal and lateral autozooids (Figure 16a–c ); (2) lateral autozooids formed by exomural budding (Figure 16b,c ); (3) localized development of narrow, haphazard, branch‐like arrangements of autozooids seemingly “embedded” within the broader, roughly cylindrical main branch surfaces, surrounded by cancellate walls (Figure 16d ); and (4) in one case, an eruptive branch has a transversely oriented, incomplete skeletal abscission zone at its base (resorption‐mediated branch abscission is a near‐ubiquitous trait in other hornerids—Batson et al, 2020 ). If our interpretation is correct, the cancellus‐bearing orifice‐free walls surrounding the patches of autozooidal apertures may be homologous with the abfrontal wall of unilaminate hornerids.…”

Proof of concept for measuring growth of shelf marine calcifiers: ‘a Bryozoan odyssey’

“…The annual growth reported here for C. immersa requires the assumption that the colony grows continuously in length at the same rate throughout the year. This notion is unlikely to be true, because at times the colony may have to prioritise other important biological processes (Batson et al 2020;Smith and Key 2020), such that younger internodes have lower growth rates.…”

“…Newly formed internodes are likely to split their energy into primary calcification (i.e. calcium carbonate deposition distally), secondary calcification to strengthen the foundations of the new internode, skeletal resorption for the formation of the node and the formation and growth of the rhizooids (Batson et al 2020). Schafer et al (2006) stated that in the early stages of internode formation in C. sinuosa, the cryptocyst and interior walls are fully calcified, whereas the first zooid row on the new branch tends to be almost twice as long as the rest of the autozooids.…”