Biol. Rev. (2015), 90, pp. 1118–1150. doi: 10.1111/brv.12148
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Biomineralization in bryozoans: present, past and future Paul D. Taylor1,∗ , Chiara Lombardi2 and Silvia Cocito2 1
Department of Earth Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, U.K. Environment and Sustainable Development Unit ENEA, PO Box 224, 19100 La Spezia, Italy
2 Marine
ABSTRACT Many animal phyla have the physiological ability to produce biomineralized skeletons with functional roles that have been shaped by natural selection for more than 500 million years. Among these are bryozoans, a moderately diverse phylum of aquatic invertebrates with a rich fossil record and importance today as bioconstructors in some shallow-water marine habitats. Biomineralizational patterns and, especially, processes are poorly understood in bryozoans but are conventionally believed to be similar to those of the related lophotrochozoan phyla Brachiopoda and Mollusca. However, bryozoan skeletons are more intricate than those of these two phyla. Calcareous skeletons have been acquired independently in two bryozoan clades – Stenolaemata in the Ordovician and Cheilostomata in the Jurassic – providing an evolutionary replicate. This review aims to highlight the importance of biomineralization in bryozoans and focuses on their skeletal ultrastructures, mineralogy and chemistry, the roles of organic components, the evolutionary history of bimineralization in bryozoans with respect to changes in seawater chemistry, and the impact of contemporary global changes, especially ocean acidification, on bryozoan skeletons. Bryozoan skeletons are constructed from three different wall types (exterior, interior and compound) differing in the presence/absence and location of organic cuticular layers. Skeletal ultrastructures can be classified into wall-parallel (i.e. laminated) and wall-perpendicular (i.e. prismatic) fabrics, the latter apparently found in only one of the two biomineralizing clades (Cheilostomata), which is also the only clade to biomineralize aragonite. A plethora of ultrastructural fabrics can be recognized and most occur in combination with other fabrics to constitute a fabric suite. The proportion of aragonitic and bimineralic bryozoans, as well as the Mg content of bryozoan skeletons, show a latitudinal increase into the warmer waters of the tropics. Responses of bryozoan mineralogy and skeletal thickness to oscillations between calcite and aragonite seas through geological time are equivocal. Field and laboratory studies of living bryozoans have shown that predicted future changes in pH (ocean acidification) combined with global warming are likely to have detrimental effects on calcification, growth rate and production of polymorphic zooids for defence and reproduction, although some species exhibit reasonable levels of resilience. Some key questions about bryozoan biomineralization that need to be addressed are identified. Key words: biomineralization, Bryozoa, skeletal ultrastructure, evolution, fossil record, climate change. CONTENTS I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1119 II. What are bryozoans? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1120 (1) Basic bryozoan biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1120 (2) Phylogeny . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1121 III. Inorganic components of the bryozoan skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1121 (1) Macroskeletal structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1121 (2) Skeletal ultrastructure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1123 (a) History of study and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1123 (b) Ultrastructural fabrics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1124 (c) Fabric suites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1128 (d) Spines and spicules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1128 * Address for correspondence (Tel: 0207 942 5673; E-mail: [email protected]).
Biological Reviews 90 (2015) 1118–1150 © 2014 Natural History Museum. Biological Reviews © 2014 Cambridge Philosophical Society
Bryozoan biomineralization
IV.
V.
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VII. VIII. IX.
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(3) Mineralogy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1129 (4) Geochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1130 (a) Magnesium in bryozoan calcite . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1130 (b) Stable isotopes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1132 Organic components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1132 (1) Study methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1132 (2) Cuticle: origin, structure and function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1132 (3) Biomineral formation in bryozoans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1133 Evolutionary history of bryozoan biomineralization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1135 (1) Bryozoan fossil record and skeletal ultrastructures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1135 (a) Stenolaemate fossil record . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1135 (b) Fossil stenolaemate skeletons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1136 (c) Cheilostome fossil record . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1137 (d) Fossil cheilostome skeletons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1137 (2) Mineralogy and geochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1137 (a) Mineralogy of fossil bryozoans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1137 (b) Seawater chemistry and mineralogical evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1138 (3) Elemental and isotopic composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1138 (4) Bryozoan skeletons and ocean acidification in the geological past . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1139 The future . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1139 (1) Future oceans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1139 (2) Bryomineralizers in oceans of the future . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1140 (a) In situ experiments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1141 (b) Laboratory experiments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1143 (3) Future scenarios for marine biomineralizers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1143 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1144 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1144 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 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I. INTRODUCTION Physiological pathways by which organisms precipitate skeletal biominerals and the roles of these biominerals in the functional morphology of the skeleton have been shaped by natural selection through the vastness of geological time. Biomineralized skeletons are first evident in the fossil record about 740 million years ago (Ma) in the Neoproterozoic (Knoll, 2003), but it was not until the Cambrian (540 Ma) that biominerals appeared in great abundance (Kouchinsky et al., 2012). Indeed, the famous Cambrian Explosion is due at least in part to the convergent evolution of biomineralized skeletons in organisms belonging to many different phyla (Murdock & Donoghue, 2011). More than 60 different minerals are known in modern organisms (Knoll, 2003), and new biominerals continue to be discovered. Biomineralized skeletons are composite materials combining organic and inorganic phases (Dove, DeYoreo & Weiner, 2003). The interplay between these two phases, along with the structure and formation of the mineral phases and of the macromolecular organic matrix, accounts for many aspects of biomineral complexity. About half of all known biominerals are calcium bearing, which may reflect the key functional role of calcium in cellular metabolism. Calcium carbonate minerals are the most abundant biominerals, both in terms of quantity and broad distribution across different taxa (Lowenstam & Weiner, 1989). Among calcium carbonate biomineralizers are cyanobacteria, coccolithophores,
coralline algae, foraminifera, corals, molluscs, echinoderms, brachiopods, arthropods and bryozoans. The last of these groups, the Bryozoa, is an exclusively colonial phylum in which the great majority of species secrete calcareous skeletons, which accounts for their good fossil record. The aim of this paper is to review our knowledge of bryozoan biomineralization, identify significant gaps in understanding, and highlight the potential for bryozoans to contribute to biomineralization studies, especially in the light of the impact of climatic changes including ocean acidification. Bryozoans are worthy subjects for biomineralogical research for several reasons. First, the phylum has a fossil record stretching back to the Early Ordovician [Taylor & Ernst (2004); note that Pywackia, a fossil from the Late Cambrian originally claimed by Landing, English & Keppie (2010) to be a bryozoan, has been re-interpreted as an octocoral by Taylor, Berning & Wilson (2013)]. Secondly, calcified bryozoan colonies create habitats for many other marine animals (e.g. Rao & Ganapati, 1980; Batson & Probert, 2000; Cocito, 2004; Wood et al., 2012; Lombardi, Taylor & Cocito, 2013; Morrison et al., 2014), including commercial species of fishes and crustaceans. Thirdly, bryozoans are capable of producing copious quantities of carbonate sediment after death (e.g. Bone & James, 1993; Rao, 1993; Hageman, James & Bone, 2000; Thomas, Hardy & Rashid, 2003; Taylor & James, 2013). Finally, bryozoans acquired calcareous skeletons de novo from soft-bodied ancestors twice (Taylor,
Biological Reviews 90 (2015) 1118–1150 © 2014 Natural History Museum. Biological Reviews © 2014 Cambridge Philosophical Society
1120 Vinn & Wilson, 2010), providing a replicate record of the evolution of biomineralized skeletons in two clades that are closely related and have very similar ecologies. Despite the great interest and numerous studies published on the biomineralized skeletons of animals and plants, enormous gaps still exist in our understanding of the processes involved in their formation (Skinner & Jaren, 2003; Smith, 2014). These gaps are more profound for some groups of organisms, including bryozoans, than they are for other groups such as molluscs and corals that have been far more intensively studied (e.g. Cusack & Freer, 2008; Tambutt´e et al., 2012). Indeed, a recent book on biomineralization (Cuif, Dauphin & Sorauf, 2011) failed to mention bryozoans at all, and earlier standard books on this subject (Lowenstam & Weiner, 1989; Simkiss & Wilbur, 1989; Mann, 2001) gave them no more than a passing mention. It is our hope that the present review will serve as a baseline for future studies and that the gaps identified and questions posed will help to stimulate further research on bryozoan biomineralization.
II. WHAT ARE BRYOZOANS? (1) Basic bryozoan biology Bryozoans are a phylum of diverse aquatic animals, numbering an estimated 5869 living species (Bock & Gordon, 2013). Most bryozoan species live in the sea but a small number inhabit freshwater environments. They are the only phylum among invertebrates in which all species are colonial. Colonies consist of conjoined clonal individuals known as zooids (Fig. 1). In evolutionary terms, each zooid is homologous to an individual of a unitary species, but the genetic individual is the entire colony and it can contain tens to many thousands of zooids. Most bryozoan colonies are benthic and sessile, typically attached to rocks, shells, seaweeds or other firm substrates (see Ryland, 1970, for a simple introduction to the phylum).
Fig. 1. Basic bryozoan morphology as seen in an oblique view of four autozooids from a cheilostome bryozoan colony. Only the zooid on the right has its lophophore expanded for feeding; in the other three, the lophophore is retracted into the security of the box-like skeleton. After Brusca & Brusca (1990).
P. D. Taylor and others All are active suspension feeders, the cilia on the tentacles of the zooidal lophophores beating to create a feeding current that drives phytoplankton towards the mouth. Colony shape varies considerably among species (e.g. Taylor & James, 2013) and may also show ecophenotypic variability within a species. Many species are encrusting and take the form of sheets that spread across the surface of a substrate. Other bryozoans are erect, producing tree-like colonies with bifurcating cylindrical branches, or having flattened fronds that may be entire or perforated by holes (fenestrules). The mechanical demands on the skeleton differ considerably between encrusting and erect species as the latter must be self-supporting. Despite their common genotype, not all of the zooids within a colony are necessarily identical morphologically: zooids can differ in appearance according to their own developmental stage (ontogeny), the developmental stage of the colony at the time that they were formed by budding (astogeny), or as a result of functional differentiation (polymorphism). With regard to polymorphism, all bryozoans possess feeding zooids (autozooids), which may be supplemented by brooding zooids (gonozooids), defensive zooids (avicularia), structural zooids (kenozooids), and various other polymorphs, depending on the species (Sil´en, 1977; Lidgard et al., 2012). Non-feeding polymorphs are possible in bryozoans because of the presence of the funicular system, a network extending through the mural pores of skeletal walls separating adjacent zooids that can transport metabolic products both within and among zooids, thus allowing feeding zooids to provision non-feeding zooids. Each bryozoan zooid can be subdivided into two component parts: cystid and polypide. The cystid includes the outer cuticle and mineralized skeleton, as well as the associated epithelia lining the body cavity. Biomineralization, when present, occurs within the cystid, not the polypide. Note that the terms zooecium and zoarium are often used in the palaeontological literature to refer, respectively, to the biomineralized skeletons of the zooid and the colony as a whole. The polypide comprises the lophophore, which is generally inverted cone- or bell-shaped, tentacle sheath, gut and associated muscles. Compared to the cystid, the polypide is ephemeral: polypides may regress, break down and be replaced one or more times during the life of the zooid. Some of the breakdown products are resorbed, but others are not and form brown bodies that can be enclosed by the developing gut of the new polypide and eventually expelled, or alternatively accumulate within the cystid. The U-shaped gut comprises a short pharynx, a slender oesophagus, a stomach, and a narrow intestine that passes to a short rectum, which opens at a dorsally situated anus on the outside of the base of the lophophore. The life cycle of bryozoans has two principal phases: (i) growth of the colony by asexual budding of new zooids, usually at well-defined growing edges at the colony perimeter; and (ii) formation of new colonies by sexually produced larvae which can swim away from the parent colony and settle on a hard substrate elsewhere. However, new colonies can also
Biological Reviews 90 (2015) 1118–1150 © 2014 Natural History Museum. Biological Reviews © 2014 Cambridge Philosophical Society
Bryozoan biomineralization be formed by asexual fragmentation of existing colonies, a process that propagates the maternal genomes (McKinney & Jackson, 1989). Whether a new colony forms sexually or by fragmentation, subsequent growth occurs by addition of modular clonal zooids. (2) Phylogeny The precise phylogenetic position of bryozoans among metazoan phyla has yet to be determined. Traditionally, Bryozoa is united with Brachiopoda and Phoronida in the ‘superphylum’ Lophophorata (e.g. Valentine, 1973), although some biologists have interpreted bryozoans to be more closely related to Entoprocta (Nielsen, 2002). Molecular phylogenies overwhelmingly consider Bryozoa to be lophotrochozoans closely related not only to Brachiopoda and Phoronida, but also to Mollusca and Annelida. From the standpoint of biomineralization, resolving the phylogenetic position of Bryozoa is important as this will allow determination of the degree of homology between the skeletons of bryozoans and other phyla. For example, did bryozoans inherit their calcareous skeleton directly from a non-bryozoan ancestor with a calcareous skeleton (e.g. a brachiopod), did they inherit only the genetic tool-kit needed to build a calcareous skeleton, or did this evolve convergently? Current evidence favours de-novo origin of the biomineralized skeleton in bryozoans. Recent advances in molecular phylogenetics have allowed the relationships between major subgroups of bryozoans to be resolved (Waeschenbach, Taylor & Littlewood, 2012), with important implications for the origin of biomineralized skeletons in the phylum. The most basal extant class is Phylactolaemata. Phylactolaemates are entirely freshwater animals, lack biomineralized skeletons and consequently have no significant fossil record, although phylactolaemate statoblasts (chitinous asexual dispersive and resting bodies) have been found as fossils back to the Permian (Vinogradov, 1996). The two predominantly marine classes Stenolaemata and Gymnolaemata constitute the sister-group of Phylactolaemata. Stenolaemata today is an exclusively marine class in which all known species possess biomineralized skeletons. The rich fossil record of stenolaemates extends back to the Early Ordovician in the guise of one extant (Cyclostomata) and five extinct orders (Cryptostomata, Cystoporata, Esthonioporina, Fenestrata, Trepostomata). Zooidal skeletons of stenolaemates are generally tubular in shape, each tube being narrow initially but broadening with growth and typically bending through 90◦ towards a terminal aperture from which the lophophore of the zooid is protruded at the colony surface. Gymnolaemata comprise the paraphyletic order Ctenostomata, which is entirely soft-bodied but can be traced back to the Early Ordovician in the form of borings in calcareous substrates (Taylor & Ernst, 2004), and Cheilostomata, an order of species with calcareous skeletons which first appeared in the fossil record comparatively recently in the Late Jurassic (Taylor, 1994) but is today the overwhelmingly dominant group of bryozoans. In contrast
1121 to stenolaemates, skeletons of cheilostome zooids tend to be box-shaped, with the orifice through which the lophophore is protruded located on the frontal surface of the zooid close to its distal end. As both morphological data and the fossil record (see Section V.1) generally support the emerging molecular phylogeny of major bryozoan groups, it provides a reliable framework onto which characters such as biomineralization can be mapped. The most parsimonious interpretation based on this phylogeny is that biomineralization has evolved twice during the evolutionary history of bryozoans: (i) during the Early Ordovician in the Stenolaemata; and (ii) during the Late Jurassic in the Cheilostomata.
III. INORGANIC COMPONENTS OF THE BRYOZOAN SKELETON (1) Macroskeletal structure The macrostructure of bryozoan skeletons is typically intricate, surpassing that of closely related lophotrochozoans such as molluscs and brachiopods. This intricacy must be understood before meaningful studies can be undertaken of biomineralization patterns as incorrect identification of macrostructural components can seriously compromise interpretations at micro- and ultrastructural levels. Much of the skeletal complexity in bryozoans is linked to their colonial organization. For example, walls can be secreted by the tissues of a single zooid or jointly by two adjacent zooids. In addition, bryozoans build a greater variety of skeletal structures (e.g. the embryonic brood chambers called ovicells and spines of cheilostomes) than is typical for many other biomineralized phyla, and at the largest scale are capable of producing numerous colony-forms having widely differing shapes. In order to appreciate bryozoan skeletal complexity it is useful to classify bryozoan walls in two ways: (i) topologically with respect to the zooid; and (ii) structurally according to the locations of secretory epithelia, mineralized skeleton and organic cuticle. Topologically, there are three types of zooidal walls: basal, vertical and frontal (Fig. 2). Basal walls form the floor of the zooid and, in the case of encrusting colony-forms, are adpressed to the substratum on which the colony grows. Vertical walls are oriented approximately at right angles to basal walls and give depth to the zooid. In cheilostomes with box-shaped zooids, the vertical walls may be further classified into lateral walls oriented parallel to growth direction, and transverse walls oriented at right angles to growth direction. Finally, frontal walls are oriented parallel (or subparallel) to the basal walls of the zooids, forming the roofs of the zooids. The fact that most of the skeletal characters used in bryozoan taxonomy reside in the frontal walls of the zooids betrays the inherent complexity of these walls. For example, even in the relatively simple zooids of tubuliporine cyclostomes the frontal wall complex may include a flat frontal wall sensu stricto,
Biological Reviews 90 (2015) 1118–1150 © 2014 Natural History Museum. Biological Reviews © 2014 Cambridge Philosophical Society
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Fig. 2. Stylized vertical section through the base and stem of a hypothetical bryozoan illustrating some of the main types of skeletal walls. Based loosely on the cyclostome Erksonea, the biomineralized skeleton is in blue, cuticle in red, and epithelium potentially capable of secreting the skeleton is shown as a dashed line. The colony has a basal exterior wall from which arises a compound wall with autozooids budding on the left side and kenozooids on the right side, the former developing frontal exterior walls which are lacking in the latter.
an upright outgrowth around the aperture called a peristome, and in older zooids that have ceased to feed, a cap called a terminal diaphragm sealing the aperture. Each of these components can exhibit a different pattern of biomineralization. Structurally, walls can be classified into interior walls and exterior walls, plus a variant of the latter called compound walls (Figs 2 and 3). Exterior walls most closely resemble the shells of molluscs and brachiopods in accreting from a secretory epithelium along their outer edges and from one side only. The calcified skeletal layer is sandwiched between the secretory epithelium and an organic cuticle (see Section IV.2). Resembling the periostraca of brachiopods and molluscs, the cuticle is the first-formed part of the skeleton and is located at the interface between the bryozoan and the external environment. By contrast, interior walls are internal partitions that subdivide the body cavity and include those walls shared between adjacent zooids in the colony. They have secretory epithelia on both sides and lack a layer of cuticle. Compound walls comprise two exterior walls back-to-back with their cuticles juxtaposed at the centre of the wall. All wall types may be imperforate or porous. In the case of interior walls, the pores pass through the entire thickness of the wall, whereas in exterior walls they pass through the calcified layers only and are covered by the cuticle, hence the name ‘pseudopore’ (note that this term is used inconsistently across the Bryozoa as certain complete pores in cheilostome frontal walls are somewhat confusingly referred to as pseudopores because they connect the hypostegal and visceral coeloms of the zooid). Pores in bryozoan walls may be constricted by minute spines growing inwards from their rims in cyclostomes, or contain plates perforated by one or
P. D. Taylor and others
Fig. 3. Compound skeletal walls. (A) Scanning electron micrograph of surface of split corrugated compound wall between two subcolonies of the Pliocene cyclostome Blumenbachium globosum. (B) Scanning electron micrograph of polished and etched section of a compound wall between two zooids of the Cretaceous cheilostome Chiplonkarina dimorphopora showing the sinuous remnants of the cuticle in the centre of the wall. In both cases the distal growth direction of the walls is from bottom to top. Scale bars: A = 100 μm; B = 10 μm.
more smaller perforations in the case of the uniporous and multiporous septulae, respectively, of cheilostomes. As already noted, recognition of wall type is critical when studying patterns of biomineralization in bryozoans. Whereas determination of the topological wall type is relatively straightforward when the orientation and growth direction of the zooid can be established, the distinction between exterior and interior walls can usually be made in dried or fossil skeletons from the microstructure of the wall surfaces. Outer surfaces of exterior walls tend to appear smooth, apart from transverse growth lines and wrinkles (Fig. 4A), whereas inner surfaces of exterior walls are typically undulose and may be covered by pustules or spines. The two opposite surfaces of interior walls tend to be identical and resemble the inner surfaces of exterior walls. Under scanning electron microscopy (SEM) the outer surface of exterior walls in both cheilostomes and stenolaemates often has a distinctive fabric termed ‘planar spherulitic’ by Sandberg (1971, 1973, 1976, 1983b). This fabric consists of flat, fan-like arrays of spherulites that were deposited in juxtaposition with the outer cuticle of the wall. By contrast, SEM examination of inner surfaces of exterior walls and the two opposite surfaces of interior walls in most stenolaemates and some cheilostomes shows these surfaces to be covered by imbricated, lath-like or platy crystallites oriented subparallel to the wall surface. The edges of the crystallites are sites of skeletal accretion and often exhibit distinct crystal faces with sharp interfacial angles (see Section III.2b). Some cheilostomes with walls comprising fibrous crystallites oriented perpendicular to the wall surface
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Fig. 4. Examples of crystallites and skeletal ultrastructural fabrics from stenolaemate (A–C, E–H, J–L) and cheilostome (D, I) bryozoans. (A–D) Planar spherulitic fabrics characteristic of the outer surfaces of exterior walls; (A) frontal wall of Crisia sigmoidea showing strips of calcification with slit-like pseudopores located at their contacts (growth direction from bottom to top); (B, C) pseudoporous terminal diaphragm occluding the aperture of a zooid of Diaperoecia purpurascens with fans of planer spherulitic calcification growing inwards from the edge (C); (D) strips of planar spherulitic calcification from the costal spine of Aspidelectra melolontha (spine growth direction is from bottom left to top right). (E, F) Hexagonal semi-nacreous fabric in Platonea stoechas; (E) semi-nacre (right) overlying granular fabric (left); (F) sectored tablet with alternating heavily and lightly etched faces. (G, H) Transversely fibrous fabrics; (G) broad fibres on the edge of the aperture of a kenozooid of Heteropora cf. neozelanica; (H) narrow, converging fibres in Cinctipora elegans (small arrows point to junction between fibres growing from the left and from the right). (I) Spindle-shaped crystallites from Jellyella eburnea. (J, K) Fabric of imbricated, foliated crystallites from Fasciculipora ramosa; (J) scalloped edge of interior wall growing towards the top; (K) detail of crystallites with well-defined crystal faces. (L) Internal surface of an exterior frontal wall of Crisia sigmoidea (compare with A), showing pseudopore and fabric of foliated crystallites surrounding it. Scale bars: A, B, G, J = 50 μm; C–E, H, L = 5 μm; F, I, K = 1 μm.
have a smoother appearance, making interior wall surfaces more difficult to distinguish from the outer surfaces of exterior walls. Compound walls are often crenulated at the suture formed between the two back-to-back exterior walls (Fig. 3). The presence of cuticle in the compound walls between zooidal rows in many cheilostomes means that specimens bleached for the study of skeletal morphology sometimes split apart along these planes. In fossils the degraded cuticle may be represented by a thin brown layer in this same position. Combining the topological and interior/exterior/ compound classifications of bryozoan skeletal walls yields a matrix of nine theoretically possible wall types (Table 1). Eight of these nine combinations are known to exist in
bryozoans, the apparent exception being frontal walls that are compound. (2) Skeletal ultrastructure (a) History of study and methods With the advent of electron microscopy, the micron-scale, ‘ultrastructure’ of bryozoan skeletons first became available for detailed study. Prior to this time, the best information on the fine structure of bryozoan skeletons came from petrographical thin sections prepared mostly, although not entirely, for the study of fossil stenolaemate bryozoans (see Boardman, 2008). More sophisticated methods of thin
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1124 Table 1. Bryozoan skeletal wall types classified topologically and according to the locations of secretory epithelia, mineralized wall and organic cuticle. The incidence of each of the nine possible categories is given for both stenolaemate and cheilostome bryozoans
Basal wall Vertical wall Frontal wall
Stenolaemates Cheilostomes Stenolaemates Cheilostomes Stenolaemates Cheilostomes
Interior wall
Exterior wall
Compound wall
•• •• ••• •• •• •••
••• •••
• •• • •••
x
•• •• ••
x x
Key: x = unknown; • = rare; •• = common; ••• = typical.
sectioning of combined hard and soft tissues were developed in the 1970s (Nye, Dean & Hinds, 1972), and ultrathin sectioning a little later (e.g. Bigey & Lafuste, 1982). Thin sections provide particularly clear indications of structural discontinuities in skeletal walls, including growth checks, laminations and layers containing different organic contents; see Boardman (1983) for good examples. They are also useful in determining crystallographic orientations and carbonate mineralogy. However, a fuller appreciation of bryozoan skeletal ultrastructure requires SEM. Scanning electron microscopy has been used at essentially two levels for the study of bryozoans. Whereas SEM has become a routine and necessary tool for the investigation and illustration of zooidal morphology in taxonomic and other studies (e.g. Taylor, 1990b), fewer studies have used it to investigate the ultrastructure of bryozoan skeletons. Nevertheless, early applications of SEM to bryozoans (e.g. Tavener-Smith & Williams, 1972; see also Williams, 1990) focused on skeletal ultrastructures and these were preceded by a few studies that employed transmission electron microscopy (TEM) to examine cellulose acetate replicas of sectioned walls (Tavener-Smith, 1969a,b). The upsurge of studies on bryozoan skeletal ultrastructure that followed the availability of SEM was, unfortunately, not sustained and there is still considerable need for further research. Papers dealing with cheilostome ultrastructure include: Sandberg (1971, 1976, 1977, 1983b), Ristedt (1977), Bigey (1981), Weedon & Taylor (2000), Bader & Sch¨afer (2004), Sch¨afer & Bader (2008) and Smith & Girvan (2010). Relative to their smaller present-day diversity, the ultrastructure of stenolaemate bryozoans has been more fully investigated, notably in the following papers: Brood (1970, 1972, 1976), Ross (1975, 1976, 1977), Bigey (1982), Boardman, McKinney & Taylor (1992), Taylor & Jones (1993), Taylor & Weedon (1996, 2000), Taylor, Weedon & Jones (1995), Weedon (1997, 1998), and Weedon & Taylor (1995, 1996, 1997, 1998). Utilizing SEM to resolve bryozoan skeletal ultrastructures can involve the observation of: (i) bleached wall surfaces (e.g. Taylor & Weedon, 2000); (ii) fractured walls (e.g. Bigey, 1981); or (iii) sectioned, polished and etched walls (e.g. Brood,
1975). Each has its advantages and drawbacks. Wall surfaces reveal the three-dimensional shapes of the exposed parts of the crystallites, including their growing edges. They are particularly instructive in the case of walls having laminated microstructures, but may be of limited value for walls comprising crystallites oriented perpendicularly to the wall surface. In the case of walls with laminated ultrastructures, a good appreciation of developmental changes in wall ultrastructure can be obtained by traversing in a proximal direction from the very distal edge of the wall, which shows the most recently formed ultrastructures, to reveal successively more mature surfaces. Fractured walls are generally more informative for the study of prismatic ultrastructures but the fracturing process is difficult to control and may potentially introduce artefacts. The orientation of polished and etched sections can be controlled more precisely than fractured sections but the amount of etching required for an optimal result varies and the degree of etching achieved can depend as much on the local chemistry of the skeleton as it does on the target ultrastructure. Reagents used for etching bryozoan walls have included formic and acetic acids (e.g. Sandberg, 1971), and ethylenediaminetetraacetic acid (EDTA) (e.g. Tavener-Smith & Williams, 1972). (b) Ultrastructural fabrics The calcareous skeletons of bryozoans, like those of molluscs and most other invertebrates, are microcrystalline, comprising aggregates of micron-scale crystallites. Variations in the morphology, arrangement and growth direction of the crystallites define different ultrastructural fabrics. Two or more ultrastructural fabrics may be found together in a single wall to define a fabric suite. A fundamental distinction can be made between fabrics where the crystallites are oriented more or less perpendicularly to the surface of the wall, and those in which they are oriented subparallel to the wall surface. Wall-perpendicular fabrics produce wall surfaces with relatively little microrelief, whereas wall-parallel fabrics endow wall surfaces with a stepped microrelief, the layers of crystallites often imbricated in a tile-like arrangement. Table 2 summarizes the major ultrastructural fabrics described in bryozoans, and Figs 4 and 5 show examples from a range of stenolaemate and cheilostome bryozoans. While the full taxonomic distribution of these fabrics is still incompletely known, it is clear that some types of fabrics are present in the independently evolved skeletons of stenolaemate and cheilostome bryozoans, whereas others occur in only one of these clades. Of particular note is that wall-perpendicular fabrics (Fig. 5A), which can comprise either calcite or aragonite, have been found only in cheilostomes to date. The near-ubiquity and presence in well-preserved specimens of early genera of cheilostomes, such as Wawalia, suggests that wall-perpendicular fabrics represent the primitive condition for this clade (Weedon & Taylor, 2000). By contrast, stenolaemate skeletons consist only of wall-parallel fabrics, giving the characteristically lamellar skeletons evident across the entire class and throughout its Ordovician–Recent geological history (see
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Table 2. Main skeletal ultrastructural fabrics found in bryozoans, categorized according to whether they are wall-perpendicular or wall-parallel. Note that granular and triangular wedge fabrics do not fit easily into either of these major categories but tend to form thin layers closer to wall-parallel than wall-perpendicular fabrics Fabric
Description
Occurrence
References
Wall-perpendicular fabric
Prismatic
Widely distributed in cheilostomes, often representing the principal fabric in both interior and exterior walls
Ristedt (1977), Sandberg (1983b) and Weedon & Taylor, 2000
Wall-parallel fabrics (laminated)
Granular
Densely packed crystallites (about 0.05–0.1 μm in diameter) oriented perpendicularly to wall surfaces, the crystallites often in fan-like bundles sometimes forming multiple layers Minute (50%); hard parts are reduced, probably due to evolutionary adaptation to fresh water and brackish water, where CaCO3 is usually undersaturated. Group II, including a few genera of Cheilostomata, has from 25 to 50% of organic matter, with appreciable amounts of iron and phosphorus within the skeletons (>0.4% Fe2 O3 ,
1118
Biomineralization in bryozoans: present, past and future Paul D. Taylor1,∗ , Chiara Lombardi2 and Silvia Cocito2 1
Department of Earth Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, U.K. Environment and Sustainable Development Unit ENEA, PO Box 224, 19100 La Spezia, Italy
2 Marine
ABSTRACT Many animal phyla have the physiological ability to produce biomineralized skeletons with functional roles that have been shaped by natural selection for more than 500 million years. Among these are bryozoans, a moderately diverse phylum of aquatic invertebrates with a rich fossil record and importance today as bioconstructors in some shallow-water marine habitats. Biomineralizational patterns and, especially, processes are poorly understood in bryozoans but are conventionally believed to be similar to those of the related lophotrochozoan phyla Brachiopoda and Mollusca. However, bryozoan skeletons are more intricate than those of these two phyla. Calcareous skeletons have been acquired independently in two bryozoan clades – Stenolaemata in the Ordovician and Cheilostomata in the Jurassic – providing an evolutionary replicate. This review aims to highlight the importance of biomineralization in bryozoans and focuses on their skeletal ultrastructures, mineralogy and chemistry, the roles of organic components, the evolutionary history of bimineralization in bryozoans with respect to changes in seawater chemistry, and the impact of contemporary global changes, especially ocean acidification, on bryozoan skeletons. Bryozoan skeletons are constructed from three different wall types (exterior, interior and compound) differing in the presence/absence and location of organic cuticular layers. Skeletal ultrastructures can be classified into wall-parallel (i.e. laminated) and wall-perpendicular (i.e. prismatic) fabrics, the latter apparently found in only one of the two biomineralizing clades (Cheilostomata), which is also the only clade to biomineralize aragonite. A plethora of ultrastructural fabrics can be recognized and most occur in combination with other fabrics to constitute a fabric suite. The proportion of aragonitic and bimineralic bryozoans, as well as the Mg content of bryozoan skeletons, show a latitudinal increase into the warmer waters of the tropics. Responses of bryozoan mineralogy and skeletal thickness to oscillations between calcite and aragonite seas through geological time are equivocal. Field and laboratory studies of living bryozoans have shown that predicted future changes in pH (ocean acidification) combined with global warming are likely to have detrimental effects on calcification, growth rate and production of polymorphic zooids for defence and reproduction, although some species exhibit reasonable levels of resilience. Some key questions about bryozoan biomineralization that need to be addressed are identified. Key words: biomineralization, Bryozoa, skeletal ultrastructure, evolution, fossil record, climate change. CONTENTS I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1119 II. What are bryozoans? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1120 (1) Basic bryozoan biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1120 (2) Phylogeny . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1121 III. Inorganic components of the bryozoan skeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1121 (1) Macroskeletal structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1121 (2) Skeletal ultrastructure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1123 (a) History of study and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1123 (b) Ultrastructural fabrics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1124 (c) Fabric suites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1128 (d) Spines and spicules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1128 * Address for correspondence (Tel: 0207 942 5673; E-mail: [email protected]).
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IV.
V.
VI.
VII. VIII. IX.
1119
(3) Mineralogy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1129 (4) Geochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1130 (a) Magnesium in bryozoan calcite . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1130 (b) Stable isotopes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1132 Organic components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1132 (1) Study methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1132 (2) Cuticle: origin, structure and function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1132 (3) Biomineral formation in bryozoans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1133 Evolutionary history of bryozoan biomineralization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1135 (1) Bryozoan fossil record and skeletal ultrastructures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1135 (a) Stenolaemate fossil record . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1135 (b) Fossil stenolaemate skeletons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1136 (c) Cheilostome fossil record . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1137 (d) Fossil cheilostome skeletons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1137 (2) Mineralogy and geochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1137 (a) Mineralogy of fossil bryozoans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1137 (b) Seawater chemistry and mineralogical evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1138 (3) Elemental and isotopic composition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1138 (4) Bryozoan skeletons and ocean acidification in the geological past . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1139 The future . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1139 (1) Future oceans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1139 (2) Bryomineralizers in oceans of the future . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1140 (a) In situ experiments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1141 (b) Laboratory experiments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1143 (3) Future scenarios for marine biomineralizers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1143 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1144 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1144 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 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I. INTRODUCTION Physiological pathways by which organisms precipitate skeletal biominerals and the roles of these biominerals in the functional morphology of the skeleton have been shaped by natural selection through the vastness of geological time. Biomineralized skeletons are first evident in the fossil record about 740 million years ago (Ma) in the Neoproterozoic (Knoll, 2003), but it was not until the Cambrian (540 Ma) that biominerals appeared in great abundance (Kouchinsky et al., 2012). Indeed, the famous Cambrian Explosion is due at least in part to the convergent evolution of biomineralized skeletons in organisms belonging to many different phyla (Murdock & Donoghue, 2011). More than 60 different minerals are known in modern organisms (Knoll, 2003), and new biominerals continue to be discovered. Biomineralized skeletons are composite materials combining organic and inorganic phases (Dove, DeYoreo & Weiner, 2003). The interplay between these two phases, along with the structure and formation of the mineral phases and of the macromolecular organic matrix, accounts for many aspects of biomineral complexity. About half of all known biominerals are calcium bearing, which may reflect the key functional role of calcium in cellular metabolism. Calcium carbonate minerals are the most abundant biominerals, both in terms of quantity and broad distribution across different taxa (Lowenstam & Weiner, 1989). Among calcium carbonate biomineralizers are cyanobacteria, coccolithophores,
coralline algae, foraminifera, corals, molluscs, echinoderms, brachiopods, arthropods and bryozoans. The last of these groups, the Bryozoa, is an exclusively colonial phylum in which the great majority of species secrete calcareous skeletons, which accounts for their good fossil record. The aim of this paper is to review our knowledge of bryozoan biomineralization, identify significant gaps in understanding, and highlight the potential for bryozoans to contribute to biomineralization studies, especially in the light of the impact of climatic changes including ocean acidification. Bryozoans are worthy subjects for biomineralogical research for several reasons. First, the phylum has a fossil record stretching back to the Early Ordovician [Taylor & Ernst (2004); note that Pywackia, a fossil from the Late Cambrian originally claimed by Landing, English & Keppie (2010) to be a bryozoan, has been re-interpreted as an octocoral by Taylor, Berning & Wilson (2013)]. Secondly, calcified bryozoan colonies create habitats for many other marine animals (e.g. Rao & Ganapati, 1980; Batson & Probert, 2000; Cocito, 2004; Wood et al., 2012; Lombardi, Taylor & Cocito, 2013; Morrison et al., 2014), including commercial species of fishes and crustaceans. Thirdly, bryozoans are capable of producing copious quantities of carbonate sediment after death (e.g. Bone & James, 1993; Rao, 1993; Hageman, James & Bone, 2000; Thomas, Hardy & Rashid, 2003; Taylor & James, 2013). Finally, bryozoans acquired calcareous skeletons de novo from soft-bodied ancestors twice (Taylor,
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1120 Vinn & Wilson, 2010), providing a replicate record of the evolution of biomineralized skeletons in two clades that are closely related and have very similar ecologies. Despite the great interest and numerous studies published on the biomineralized skeletons of animals and plants, enormous gaps still exist in our understanding of the processes involved in their formation (Skinner & Jaren, 2003; Smith, 2014). These gaps are more profound for some groups of organisms, including bryozoans, than they are for other groups such as molluscs and corals that have been far more intensively studied (e.g. Cusack & Freer, 2008; Tambutt´e et al., 2012). Indeed, a recent book on biomineralization (Cuif, Dauphin & Sorauf, 2011) failed to mention bryozoans at all, and earlier standard books on this subject (Lowenstam & Weiner, 1989; Simkiss & Wilbur, 1989; Mann, 2001) gave them no more than a passing mention. It is our hope that the present review will serve as a baseline for future studies and that the gaps identified and questions posed will help to stimulate further research on bryozoan biomineralization.
II. WHAT ARE BRYOZOANS? (1) Basic bryozoan biology Bryozoans are a phylum of diverse aquatic animals, numbering an estimated 5869 living species (Bock & Gordon, 2013). Most bryozoan species live in the sea but a small number inhabit freshwater environments. They are the only phylum among invertebrates in which all species are colonial. Colonies consist of conjoined clonal individuals known as zooids (Fig. 1). In evolutionary terms, each zooid is homologous to an individual of a unitary species, but the genetic individual is the entire colony and it can contain tens to many thousands of zooids. Most bryozoan colonies are benthic and sessile, typically attached to rocks, shells, seaweeds or other firm substrates (see Ryland, 1970, for a simple introduction to the phylum).
Fig. 1. Basic bryozoan morphology as seen in an oblique view of four autozooids from a cheilostome bryozoan colony. Only the zooid on the right has its lophophore expanded for feeding; in the other three, the lophophore is retracted into the security of the box-like skeleton. After Brusca & Brusca (1990).
P. D. Taylor and others All are active suspension feeders, the cilia on the tentacles of the zooidal lophophores beating to create a feeding current that drives phytoplankton towards the mouth. Colony shape varies considerably among species (e.g. Taylor & James, 2013) and may also show ecophenotypic variability within a species. Many species are encrusting and take the form of sheets that spread across the surface of a substrate. Other bryozoans are erect, producing tree-like colonies with bifurcating cylindrical branches, or having flattened fronds that may be entire or perforated by holes (fenestrules). The mechanical demands on the skeleton differ considerably between encrusting and erect species as the latter must be self-supporting. Despite their common genotype, not all of the zooids within a colony are necessarily identical morphologically: zooids can differ in appearance according to their own developmental stage (ontogeny), the developmental stage of the colony at the time that they were formed by budding (astogeny), or as a result of functional differentiation (polymorphism). With regard to polymorphism, all bryozoans possess feeding zooids (autozooids), which may be supplemented by brooding zooids (gonozooids), defensive zooids (avicularia), structural zooids (kenozooids), and various other polymorphs, depending on the species (Sil´en, 1977; Lidgard et al., 2012). Non-feeding polymorphs are possible in bryozoans because of the presence of the funicular system, a network extending through the mural pores of skeletal walls separating adjacent zooids that can transport metabolic products both within and among zooids, thus allowing feeding zooids to provision non-feeding zooids. Each bryozoan zooid can be subdivided into two component parts: cystid and polypide. The cystid includes the outer cuticle and mineralized skeleton, as well as the associated epithelia lining the body cavity. Biomineralization, when present, occurs within the cystid, not the polypide. Note that the terms zooecium and zoarium are often used in the palaeontological literature to refer, respectively, to the biomineralized skeletons of the zooid and the colony as a whole. The polypide comprises the lophophore, which is generally inverted cone- or bell-shaped, tentacle sheath, gut and associated muscles. Compared to the cystid, the polypide is ephemeral: polypides may regress, break down and be replaced one or more times during the life of the zooid. Some of the breakdown products are resorbed, but others are not and form brown bodies that can be enclosed by the developing gut of the new polypide and eventually expelled, or alternatively accumulate within the cystid. The U-shaped gut comprises a short pharynx, a slender oesophagus, a stomach, and a narrow intestine that passes to a short rectum, which opens at a dorsally situated anus on the outside of the base of the lophophore. The life cycle of bryozoans has two principal phases: (i) growth of the colony by asexual budding of new zooids, usually at well-defined growing edges at the colony perimeter; and (ii) formation of new colonies by sexually produced larvae which can swim away from the parent colony and settle on a hard substrate elsewhere. However, new colonies can also
Biological Reviews 90 (2015) 1118–1150 © 2014 Natural History Museum. Biological Reviews © 2014 Cambridge Philosophical Society
Bryozoan biomineralization be formed by asexual fragmentation of existing colonies, a process that propagates the maternal genomes (McKinney & Jackson, 1989). Whether a new colony forms sexually or by fragmentation, subsequent growth occurs by addition of modular clonal zooids. (2) Phylogeny The precise phylogenetic position of bryozoans among metazoan phyla has yet to be determined. Traditionally, Bryozoa is united with Brachiopoda and Phoronida in the ‘superphylum’ Lophophorata (e.g. Valentine, 1973), although some biologists have interpreted bryozoans to be more closely related to Entoprocta (Nielsen, 2002). Molecular phylogenies overwhelmingly consider Bryozoa to be lophotrochozoans closely related not only to Brachiopoda and Phoronida, but also to Mollusca and Annelida. From the standpoint of biomineralization, resolving the phylogenetic position of Bryozoa is important as this will allow determination of the degree of homology between the skeletons of bryozoans and other phyla. For example, did bryozoans inherit their calcareous skeleton directly from a non-bryozoan ancestor with a calcareous skeleton (e.g. a brachiopod), did they inherit only the genetic tool-kit needed to build a calcareous skeleton, or did this evolve convergently? Current evidence favours de-novo origin of the biomineralized skeleton in bryozoans. Recent advances in molecular phylogenetics have allowed the relationships between major subgroups of bryozoans to be resolved (Waeschenbach, Taylor & Littlewood, 2012), with important implications for the origin of biomineralized skeletons in the phylum. The most basal extant class is Phylactolaemata. Phylactolaemates are entirely freshwater animals, lack biomineralized skeletons and consequently have no significant fossil record, although phylactolaemate statoblasts (chitinous asexual dispersive and resting bodies) have been found as fossils back to the Permian (Vinogradov, 1996). The two predominantly marine classes Stenolaemata and Gymnolaemata constitute the sister-group of Phylactolaemata. Stenolaemata today is an exclusively marine class in which all known species possess biomineralized skeletons. The rich fossil record of stenolaemates extends back to the Early Ordovician in the guise of one extant (Cyclostomata) and five extinct orders (Cryptostomata, Cystoporata, Esthonioporina, Fenestrata, Trepostomata). Zooidal skeletons of stenolaemates are generally tubular in shape, each tube being narrow initially but broadening with growth and typically bending through 90◦ towards a terminal aperture from which the lophophore of the zooid is protruded at the colony surface. Gymnolaemata comprise the paraphyletic order Ctenostomata, which is entirely soft-bodied but can be traced back to the Early Ordovician in the form of borings in calcareous substrates (Taylor & Ernst, 2004), and Cheilostomata, an order of species with calcareous skeletons which first appeared in the fossil record comparatively recently in the Late Jurassic (Taylor, 1994) but is today the overwhelmingly dominant group of bryozoans. In contrast
1121 to stenolaemates, skeletons of cheilostome zooids tend to be box-shaped, with the orifice through which the lophophore is protruded located on the frontal surface of the zooid close to its distal end. As both morphological data and the fossil record (see Section V.1) generally support the emerging molecular phylogeny of major bryozoan groups, it provides a reliable framework onto which characters such as biomineralization can be mapped. The most parsimonious interpretation based on this phylogeny is that biomineralization has evolved twice during the evolutionary history of bryozoans: (i) during the Early Ordovician in the Stenolaemata; and (ii) during the Late Jurassic in the Cheilostomata.
III. INORGANIC COMPONENTS OF THE BRYOZOAN SKELETON (1) Macroskeletal structure The macrostructure of bryozoan skeletons is typically intricate, surpassing that of closely related lophotrochozoans such as molluscs and brachiopods. This intricacy must be understood before meaningful studies can be undertaken of biomineralization patterns as incorrect identification of macrostructural components can seriously compromise interpretations at micro- and ultrastructural levels. Much of the skeletal complexity in bryozoans is linked to their colonial organization. For example, walls can be secreted by the tissues of a single zooid or jointly by two adjacent zooids. In addition, bryozoans build a greater variety of skeletal structures (e.g. the embryonic brood chambers called ovicells and spines of cheilostomes) than is typical for many other biomineralized phyla, and at the largest scale are capable of producing numerous colony-forms having widely differing shapes. In order to appreciate bryozoan skeletal complexity it is useful to classify bryozoan walls in two ways: (i) topologically with respect to the zooid; and (ii) structurally according to the locations of secretory epithelia, mineralized skeleton and organic cuticle. Topologically, there are three types of zooidal walls: basal, vertical and frontal (Fig. 2). Basal walls form the floor of the zooid and, in the case of encrusting colony-forms, are adpressed to the substratum on which the colony grows. Vertical walls are oriented approximately at right angles to basal walls and give depth to the zooid. In cheilostomes with box-shaped zooids, the vertical walls may be further classified into lateral walls oriented parallel to growth direction, and transverse walls oriented at right angles to growth direction. Finally, frontal walls are oriented parallel (or subparallel) to the basal walls of the zooids, forming the roofs of the zooids. The fact that most of the skeletal characters used in bryozoan taxonomy reside in the frontal walls of the zooids betrays the inherent complexity of these walls. For example, even in the relatively simple zooids of tubuliporine cyclostomes the frontal wall complex may include a flat frontal wall sensu stricto,
Biological Reviews 90 (2015) 1118–1150 © 2014 Natural History Museum. Biological Reviews © 2014 Cambridge Philosophical Society
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Fig. 2. Stylized vertical section through the base and stem of a hypothetical bryozoan illustrating some of the main types of skeletal walls. Based loosely on the cyclostome Erksonea, the biomineralized skeleton is in blue, cuticle in red, and epithelium potentially capable of secreting the skeleton is shown as a dashed line. The colony has a basal exterior wall from which arises a compound wall with autozooids budding on the left side and kenozooids on the right side, the former developing frontal exterior walls which are lacking in the latter.
an upright outgrowth around the aperture called a peristome, and in older zooids that have ceased to feed, a cap called a terminal diaphragm sealing the aperture. Each of these components can exhibit a different pattern of biomineralization. Structurally, walls can be classified into interior walls and exterior walls, plus a variant of the latter called compound walls (Figs 2 and 3). Exterior walls most closely resemble the shells of molluscs and brachiopods in accreting from a secretory epithelium along their outer edges and from one side only. The calcified skeletal layer is sandwiched between the secretory epithelium and an organic cuticle (see Section IV.2). Resembling the periostraca of brachiopods and molluscs, the cuticle is the first-formed part of the skeleton and is located at the interface between the bryozoan and the external environment. By contrast, interior walls are internal partitions that subdivide the body cavity and include those walls shared between adjacent zooids in the colony. They have secretory epithelia on both sides and lack a layer of cuticle. Compound walls comprise two exterior walls back-to-back with their cuticles juxtaposed at the centre of the wall. All wall types may be imperforate or porous. In the case of interior walls, the pores pass through the entire thickness of the wall, whereas in exterior walls they pass through the calcified layers only and are covered by the cuticle, hence the name ‘pseudopore’ (note that this term is used inconsistently across the Bryozoa as certain complete pores in cheilostome frontal walls are somewhat confusingly referred to as pseudopores because they connect the hypostegal and visceral coeloms of the zooid). Pores in bryozoan walls may be constricted by minute spines growing inwards from their rims in cyclostomes, or contain plates perforated by one or
P. D. Taylor and others
Fig. 3. Compound skeletal walls. (A) Scanning electron micrograph of surface of split corrugated compound wall between two subcolonies of the Pliocene cyclostome Blumenbachium globosum. (B) Scanning electron micrograph of polished and etched section of a compound wall between two zooids of the Cretaceous cheilostome Chiplonkarina dimorphopora showing the sinuous remnants of the cuticle in the centre of the wall. In both cases the distal growth direction of the walls is from bottom to top. Scale bars: A = 100 μm; B = 10 μm.
more smaller perforations in the case of the uniporous and multiporous septulae, respectively, of cheilostomes. As already noted, recognition of wall type is critical when studying patterns of biomineralization in bryozoans. Whereas determination of the topological wall type is relatively straightforward when the orientation and growth direction of the zooid can be established, the distinction between exterior and interior walls can usually be made in dried or fossil skeletons from the microstructure of the wall surfaces. Outer surfaces of exterior walls tend to appear smooth, apart from transverse growth lines and wrinkles (Fig. 4A), whereas inner surfaces of exterior walls are typically undulose and may be covered by pustules or spines. The two opposite surfaces of interior walls tend to be identical and resemble the inner surfaces of exterior walls. Under scanning electron microscopy (SEM) the outer surface of exterior walls in both cheilostomes and stenolaemates often has a distinctive fabric termed ‘planar spherulitic’ by Sandberg (1971, 1973, 1976, 1983b). This fabric consists of flat, fan-like arrays of spherulites that were deposited in juxtaposition with the outer cuticle of the wall. By contrast, SEM examination of inner surfaces of exterior walls and the two opposite surfaces of interior walls in most stenolaemates and some cheilostomes shows these surfaces to be covered by imbricated, lath-like or platy crystallites oriented subparallel to the wall surface. The edges of the crystallites are sites of skeletal accretion and often exhibit distinct crystal faces with sharp interfacial angles (see Section III.2b). Some cheilostomes with walls comprising fibrous crystallites oriented perpendicular to the wall surface
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Fig. 4. Examples of crystallites and skeletal ultrastructural fabrics from stenolaemate (A–C, E–H, J–L) and cheilostome (D, I) bryozoans. (A–D) Planar spherulitic fabrics characteristic of the outer surfaces of exterior walls; (A) frontal wall of Crisia sigmoidea showing strips of calcification with slit-like pseudopores located at their contacts (growth direction from bottom to top); (B, C) pseudoporous terminal diaphragm occluding the aperture of a zooid of Diaperoecia purpurascens with fans of planer spherulitic calcification growing inwards from the edge (C); (D) strips of planar spherulitic calcification from the costal spine of Aspidelectra melolontha (spine growth direction is from bottom left to top right). (E, F) Hexagonal semi-nacreous fabric in Platonea stoechas; (E) semi-nacre (right) overlying granular fabric (left); (F) sectored tablet with alternating heavily and lightly etched faces. (G, H) Transversely fibrous fabrics; (G) broad fibres on the edge of the aperture of a kenozooid of Heteropora cf. neozelanica; (H) narrow, converging fibres in Cinctipora elegans (small arrows point to junction between fibres growing from the left and from the right). (I) Spindle-shaped crystallites from Jellyella eburnea. (J, K) Fabric of imbricated, foliated crystallites from Fasciculipora ramosa; (J) scalloped edge of interior wall growing towards the top; (K) detail of crystallites with well-defined crystal faces. (L) Internal surface of an exterior frontal wall of Crisia sigmoidea (compare with A), showing pseudopore and fabric of foliated crystallites surrounding it. Scale bars: A, B, G, J = 50 μm; C–E, H, L = 5 μm; F, I, K = 1 μm.
have a smoother appearance, making interior wall surfaces more difficult to distinguish from the outer surfaces of exterior walls. Compound walls are often crenulated at the suture formed between the two back-to-back exterior walls (Fig. 3). The presence of cuticle in the compound walls between zooidal rows in many cheilostomes means that specimens bleached for the study of skeletal morphology sometimes split apart along these planes. In fossils the degraded cuticle may be represented by a thin brown layer in this same position. Combining the topological and interior/exterior/ compound classifications of bryozoan skeletal walls yields a matrix of nine theoretically possible wall types (Table 1). Eight of these nine combinations are known to exist in
bryozoans, the apparent exception being frontal walls that are compound. (2) Skeletal ultrastructure (a) History of study and methods With the advent of electron microscopy, the micron-scale, ‘ultrastructure’ of bryozoan skeletons first became available for detailed study. Prior to this time, the best information on the fine structure of bryozoan skeletons came from petrographical thin sections prepared mostly, although not entirely, for the study of fossil stenolaemate bryozoans (see Boardman, 2008). More sophisticated methods of thin
Biological Reviews 90 (2015) 1118–1150 © 2014 Natural History Museum. Biological Reviews © 2014 Cambridge Philosophical Society
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1124 Table 1. Bryozoan skeletal wall types classified topologically and according to the locations of secretory epithelia, mineralized wall and organic cuticle. The incidence of each of the nine possible categories is given for both stenolaemate and cheilostome bryozoans
Basal wall Vertical wall Frontal wall
Stenolaemates Cheilostomes Stenolaemates Cheilostomes Stenolaemates Cheilostomes
Interior wall
Exterior wall
Compound wall
•• •• ••• •• •• •••
••• •••
• •• • •••
x
•• •• ••
x x
Key: x = unknown; • = rare; •• = common; ••• = typical.
sectioning of combined hard and soft tissues were developed in the 1970s (Nye, Dean & Hinds, 1972), and ultrathin sectioning a little later (e.g. Bigey & Lafuste, 1982). Thin sections provide particularly clear indications of structural discontinuities in skeletal walls, including growth checks, laminations and layers containing different organic contents; see Boardman (1983) for good examples. They are also useful in determining crystallographic orientations and carbonate mineralogy. However, a fuller appreciation of bryozoan skeletal ultrastructure requires SEM. Scanning electron microscopy has been used at essentially two levels for the study of bryozoans. Whereas SEM has become a routine and necessary tool for the investigation and illustration of zooidal morphology in taxonomic and other studies (e.g. Taylor, 1990b), fewer studies have used it to investigate the ultrastructure of bryozoan skeletons. Nevertheless, early applications of SEM to bryozoans (e.g. Tavener-Smith & Williams, 1972; see also Williams, 1990) focused on skeletal ultrastructures and these were preceded by a few studies that employed transmission electron microscopy (TEM) to examine cellulose acetate replicas of sectioned walls (Tavener-Smith, 1969a,b). The upsurge of studies on bryozoan skeletal ultrastructure that followed the availability of SEM was, unfortunately, not sustained and there is still considerable need for further research. Papers dealing with cheilostome ultrastructure include: Sandberg (1971, 1976, 1977, 1983b), Ristedt (1977), Bigey (1981), Weedon & Taylor (2000), Bader & Sch¨afer (2004), Sch¨afer & Bader (2008) and Smith & Girvan (2010). Relative to their smaller present-day diversity, the ultrastructure of stenolaemate bryozoans has been more fully investigated, notably in the following papers: Brood (1970, 1972, 1976), Ross (1975, 1976, 1977), Bigey (1982), Boardman, McKinney & Taylor (1992), Taylor & Jones (1993), Taylor & Weedon (1996, 2000), Taylor, Weedon & Jones (1995), Weedon (1997, 1998), and Weedon & Taylor (1995, 1996, 1997, 1998). Utilizing SEM to resolve bryozoan skeletal ultrastructures can involve the observation of: (i) bleached wall surfaces (e.g. Taylor & Weedon, 2000); (ii) fractured walls (e.g. Bigey, 1981); or (iii) sectioned, polished and etched walls (e.g. Brood,
1975). Each has its advantages and drawbacks. Wall surfaces reveal the three-dimensional shapes of the exposed parts of the crystallites, including their growing edges. They are particularly instructive in the case of walls having laminated microstructures, but may be of limited value for walls comprising crystallites oriented perpendicularly to the wall surface. In the case of walls with laminated ultrastructures, a good appreciation of developmental changes in wall ultrastructure can be obtained by traversing in a proximal direction from the very distal edge of the wall, which shows the most recently formed ultrastructures, to reveal successively more mature surfaces. Fractured walls are generally more informative for the study of prismatic ultrastructures but the fracturing process is difficult to control and may potentially introduce artefacts. The orientation of polished and etched sections can be controlled more precisely than fractured sections but the amount of etching required for an optimal result varies and the degree of etching achieved can depend as much on the local chemistry of the skeleton as it does on the target ultrastructure. Reagents used for etching bryozoan walls have included formic and acetic acids (e.g. Sandberg, 1971), and ethylenediaminetetraacetic acid (EDTA) (e.g. Tavener-Smith & Williams, 1972). (b) Ultrastructural fabrics The calcareous skeletons of bryozoans, like those of molluscs and most other invertebrates, are microcrystalline, comprising aggregates of micron-scale crystallites. Variations in the morphology, arrangement and growth direction of the crystallites define different ultrastructural fabrics. Two or more ultrastructural fabrics may be found together in a single wall to define a fabric suite. A fundamental distinction can be made between fabrics where the crystallites are oriented more or less perpendicularly to the surface of the wall, and those in which they are oriented subparallel to the wall surface. Wall-perpendicular fabrics produce wall surfaces with relatively little microrelief, whereas wall-parallel fabrics endow wall surfaces with a stepped microrelief, the layers of crystallites often imbricated in a tile-like arrangement. Table 2 summarizes the major ultrastructural fabrics described in bryozoans, and Figs 4 and 5 show examples from a range of stenolaemate and cheilostome bryozoans. While the full taxonomic distribution of these fabrics is still incompletely known, it is clear that some types of fabrics are present in the independently evolved skeletons of stenolaemate and cheilostome bryozoans, whereas others occur in only one of these clades. Of particular note is that wall-perpendicular fabrics (Fig. 5A), which can comprise either calcite or aragonite, have been found only in cheilostomes to date. The near-ubiquity and presence in well-preserved specimens of early genera of cheilostomes, such as Wawalia, suggests that wall-perpendicular fabrics represent the primitive condition for this clade (Weedon & Taylor, 2000). By contrast, stenolaemate skeletons consist only of wall-parallel fabrics, giving the characteristically lamellar skeletons evident across the entire class and throughout its Ordovician–Recent geological history (see
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Table 2. Main skeletal ultrastructural fabrics found in bryozoans, categorized according to whether they are wall-perpendicular or wall-parallel. Note that granular and triangular wedge fabrics do not fit easily into either of these major categories but tend to form thin layers closer to wall-parallel than wall-perpendicular fabrics Fabric
Description
Occurrence
References
Wall-perpendicular fabric
Prismatic
Widely distributed in cheilostomes, often representing the principal fabric in both interior and exterior walls
Ristedt (1977), Sandberg (1983b) and Weedon & Taylor, 2000
Wall-parallel fabrics (laminated)
Granular
Densely packed crystallites (about 0.05–0.1 μm in diameter) oriented perpendicularly to wall surfaces, the crystallites often in fan-like bundles sometimes forming multiple layers Minute (50%); hard parts are reduced, probably due to evolutionary adaptation to fresh water and brackish water, where CaCO3 is usually undersaturated. Group II, including a few genera of Cheilostomata, has from 25 to 50% of organic matter, with appreciable amounts of iron and phosphorus within the skeletons (>0.4% Fe2 O3 ,
