Systematics of Upper Cretaceous calloporid bryozoans with primitive spinose ovicells

The majority of fossil and Recent cheilostome bryozoans brood their larvae in ovicells. These double-walled, hood-like skeletal structures are thought to have arisen through modification of spines belonging to the zooid distal of the maternal zooid. Support for this hypothesis comes from the existence of ovicells constructed of multiple spines in a few Upper Cretaceous species belonging to two groups, microporids and cribrimorphs. Here we report the discovery of similar multispinose ovicells in a third group, calloporids, which are closely related to primitive cheilostomes that do not brood their larvae. The genus Distelopora Lang, 1915 from the Cenomanian ('Chalk Marl') of Cambridge is taken out of synonymy and shown to comprise the type species ( D. bipilata ) and two new species ( D. langi and D. spinifera ) of multiserial calloporids. Between 5 and 15 spine bases are arranged in a crescent on the gymnocyst of the zooid distal of each maternal (egg-producing) zooid in Distelopora . This indicates the presence of an ovicell formed by a cage of basally articulated spines. Similar ovicells represented by 18–19 spine bases occur in a uniserial calloporid from the German Campanian Allantopora krauseae Voigt and Schneemilch, 1986, which is made the type species of the new genus Unidistelopora . Another calloporid from the Cambridge Cenomanian has ovicells constructed by two claw-like, flattened, non-articulated and laterally juxtaposed spines. Described as Gilbertopora larwoodi gen. et sp. nov., this multiserial species provides a link between Distelopora and more typical cheilostome ovicells. The spines forming primitive ovicells provide a good example of exaptations, co-opted from their original function protecting the polypide of the distal zooid.     

Ultrastructure and Development of the Ooecial Walls in Some Calloporid Bryozoans (Gymnolaemata: Cheilostomata)

In the brood chambers (ovicells) of six calloporid cheilostomes studied each skeletal wall consists of four calcified layers: (1) a very thin superficial layer of planar spherulitic crystallites, (2) an upper (outer) layer with wall-perpendicular prismatic ultrastructure, (3) an intermediate lamellar layer, and (4) a lower (inner) wall-perpendicular prismatic layer. Comparative studies of both the ovicell wall ultrastructure and early ovicell formation showed a hypothetical opportunity for evolving complex (multilayered) skeletal walls by fusion of the initially separated gymnocystal and cryptocystal calcifications in Cheilostomata. In two species studied, a bilobate pattern in the final stage of the formation of the ooecial roof was encountered in specimens with the cuticle preserved. A possible explanation to this finding is discussed – the bilobate pattern is suggestive of the hypothetical origin of the brood chamber from (1) two flattened spines, or (2) reduction in spine number of an originally multispinous ovicell.     

A new cheilostome bryozoan with gigantic zooids from the North-West Pacific

Gontarella gigantea gen. et sp. nov. is described from two stations, one in the Sea of Okhotsk and the second on the Pacific side of the Small Kuril Arc. This membraniporiform anascan cheilostome bryozoan has very large zooids, the largest known among extant sheet-like encrusting anascans. Comparative data on similar sheet-like cheilostomes gathered from the literature shows that the new species represents a conspicuous outlier in size, with the surface area of the zooid being approximately twice that of the next largest species. Skeletal evidence, including the lack of ovicells, indicates that G. gigantea belongs within the malacostegan family Electridae. The gigantic ancestrula suggests that the species has a cyphonautes larva about 1 mm in maximum dimension.     

Comparative anatomy of internal incubational sacs in cupuladriid bryozoans and the evolution of brooding in free‐living cheilostomes

Numerous gross morphological attributes are shared among unrelated free‐living bryozoans revealing convergent evolution associated with functional demands of living on soft sediments. Here, we show that the reproductive structures across free‐living groups evolved convergently. The most prominent convergent traits are the collective reduction of external brood chambers (ovicells) and the acquisition of internal brooding. Anatomical studies of four species from the cheilostome genera Cupuladria and Discoporella (Cupuladriidae) show that these species incubate their embryos in internal brooding sacs located in the coelom of the maternal nonpolymorphic autozooids. This sac consists of a main chamber and a narrow neck communicating to the vestibulum. The distal wall of the vestibulum possesses a cuticular thickening, which may further isolate the brood cavity. The presence of this character in all four species strongly supports grouping Cupuladria and Discoporella in one taxon. Further evidence suggests that the Cupuladriidae may be nested within the Calloporidae. Based on the structure of brooding organs, two scenarios are proposed to explain the evolution of the internal brooding in cupuladriids. The evolution of brood chambers and their origin in other free‐living cheilostomes is discussed. Unlike the vast majority of Neocheilostomina, almost all free‐living cheilostomes possess nonprominent chambers for embryonic incubation, either endozooidal and immersed ovicells or internal brooding sacs, supporting the idea that internal embryonic incubation is derived. We speculate that prominent skeletal brood chambers are disadvantageous to a free‐living mode of life that demands easy movement through sediment in instable sea‐floor settings. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Gametogenesis and embryonic brooding in the cheilostome bryozoan Celleporella hyalina

Celleporella hyalina (L.) is unusual among cheilostomes in producing sexually dimorphic gonozooids which are frontally budded from a layer of sterile autozooids, and also in the possession of a placental system for extracoelomic nutrition of the developing embryo. This paper investigates these two aspects of the reproductive strategy, combining observations of living colonies with ultrastructural study of preserved material. The formation of the male and female gonozooids is described. Female zooids underwent a maximum of four successive reproductive cycles before senescence. About 29% of embryos failed to develop to completion and were prematurely expelled from the ovicell. Spermatogenesis follows the typical cheilostome pattern. Fertilization is internal, and probably occurs during vitellogenesis of the oocyte. Oogenesis involves the activity of a nurse cell. The telolecithal egg increases in volume approximately 15–fold after transfer to the ovicell, and is nourished by a relatively simple placental system formed by the distal epithelium of the maternal zooid.     

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

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

The internal-brooding apparatus in the bryozoan genus Cauloramphus (Cheilostomata: Calloporidae) and its inferred homology to ovicells

We studied by SEM the external morphology of the ooecium in eight bryozoans of the genus Cauloramphus (Cheilostomata, Calloporidae): C. spinifer, C. variegatus, C. magnus, C. multiavicularia, C. tortilis, C. cryptoarmatus, C. niger, and C. multispinosus, and by sectioning and light microscopy the anatomy of the brooding apparatus of C. spinifer, C. cryptoarmatus, and C. niger. These species all have a brood sac, formed by invagination of the non-calcified distal body wall of the maternal zooid, located in the distal half of the maternal (egg-producing) autozooid, and a vestigial, maternally budded kenozooidal ooecium. The brood sac comprises a main chamber and a long passage (neck) opening externally independently of the introvert. The non-calcified portion of the maternal distal wall between the neck and tip of the zooidal operculum is involved in closing and opening the brood sac, and contains both musculature and a reduced sclerite that suggest homology with the ooecial vesicle of a hyperstomial ovicell. We interpret the brooding apparatus in Cauloramphus as a highly modified form of cheilostome hyperstomial ovicell, as both types share 1) a brood chamber bounded by 2) the ooecium and 3) a component of the distal wall of the maternal zooid. We discuss Cauloramphus as a hypothetical penultimate stage in ovicell reduction in calloporid bryozoans. We suggest that the internal-brooding genus Gontarella, of uncertain taxonomic affinities, is actually a calloporid and represents the ultimate stage in which no trace of the ooecium remains. Internal brooding apparently evolved several times independently within the Calloporidae.     

Body wall morphology of Pentapora foliacea (Ellis and Solander) (Bryozoa,Cheilostomata)

The ascophoran Pentapora foliacea was studied from epoxy sections of skeletal and soft (hard-soft) tissues. The basal wall is double, indicating the colony grew as two independent layers, back to back. The structure of the vertical walls and interzooidal communication organs indicates that zooids were budded in the usual way as in most encrusting cheilostomes. Secondary layers of the frontal wall are of acicular aragonite. The ovicell develops as a flattened cuticular bladder in early ontogeny; the aragonitic layer of the frontal wall later engulfs it. A median vesicle, an evagination of the vestibular wall, is present but the eggs may be supplied with sufficient yolk to nurture the embryo. The overall ovicell structure is similar to that of hyperstomial ovicells in other cheilostomes.     

Ovicell structure in Callopora dumerilii and C. lineata (Bryozoa: Cheilostomatida)

Anatomical and SEM-studies of the brood-chambers (ovicells) in two bryozoans (Callopora dumerilii and C. lineata) were undertaken to resolve a long-term controversy existing in the literature about the origin of the ovicells. In contrast with the interpretation of Silén (1945 ), both species investigated possess hyperstomial ovicells with the ooecium formed by the distal (daughter) zooid. The ooecial coelomic cavity communicates with the zooidal coelom through a pore-like canal or canals remaining after the closure of an arch-shaped slit. The slit forms during ovicellogenesis. The communication canals are normally plugged by epithelial cells, however incompletely closed canals were also found in Callopora lineata. SEM-studies of noncleaned, air-dried specimens showed a relationship between membranous and calcified parts during early ovicellogenesis. It starts from a transverse wall as the calcification of the proximal part of the daughter zooid frontal wall, and has the shape of two flat rounded plates. There are no knobs or any other outgrowths. Conditions and phenomenology of hyperstomial ovicell formation are discussed.     

Diversity of brood chambers in calloporid bryozoans (Gymnolaemata,Cheilostomata): comparative anatomy and evolutionary trends

Comparative anatomical studies of 12 species from 10 genera (Callopora, Tegella, Amphiblestrum, Parellisina, Corbulella, Crassimarginatella, Valdemunitella, Bryocalyx, Concertina, Cauloramphus) belonging to one of the largest and most diverse bryozoan taxa, the Calloporidae, and one species from the genus Akatopora belonging to the related taxon Antroporidae, were undertaken to elucidate the morphological diversity of brooding structures and to recognize main trends in their evolution. Most of the species studied possess ovicells (specialized brooding receptacles) formed by the distal and maternal (egg-producing) autozooids. The distal zooid can be an autozooid, a vicarious avicularium or a kenozooid. The calcified protective hood (ooecium) is an outgrowth from the distal zooid. Hyperstomial or prominent ovicells are most common. They were found in species of the genera Callopora, Tegella, Amphiblestrum, Parellisina, Corbulella, Bryocalyx and Concertina. Subimmersed ovicells were found in Valdemunitella, and immersed ovicells in Crassimarginatella and Akatopora. Cauloramphus has an internal brooding sac and a vestigial kenozooidal ooecium, budded by the maternal zooid. Based on the structure of the brooding organs, the following evolutionary trends can be recognized within the group: (1) reduction of the distal (ooecium-producing) zooid, (2) immersion of the brooding cavity correlated with a reduction of the ooecium and ooecial vesicle and with changes in the ovicell closure and the structure of the brood chamber floor, (3) reduction of the calcification of the ectooecium, and (4) transition from bilobate to entire ooecium. The trend towards immersion of the brooding cavity could have evolved repeatedly within the Calloporidae. Transition from bilobate to entire ooecium is characteristic of the related taxon Cribrilinidae, showing a good example of parallel evolution of the ooecium in two closely related clades. Possible causes for the transformations described are discussed.     

a new ichnogenus for etchings made by cheilostome bryozoans into calcareous substrates

Some encrusting cheilostome bryozoans etch a pattern of small pits into hard calcareous substrates, especially calcitic and aragonitic shells of molluscs. These patterns, herein described as Leptichnus ichnogen. nov., comprise pits which are sub-circular to elongate in cross section and are found in either uniserial ( L. dromeus isp. nov.) or multiserial arrangements ( L. peristroma isp. nov., the type species). Each pit corresponds to the location of a single zooid in the bryozoan colony. The oldest known Leptichnus is Late Cretaceous (Maastrichtian), the trace fossil first becomes common in the Cenozoic, and at least nine modern cheilostome genera produce incipient Leptichnus. Leptichnus can be the only evidence remaining of encrusting cheilostomes following taphonomic or diagenetic loss of their calcareous skeletons. The mechanism by which bryozoans etch into their calcareous substrates is unknown but is almost certain to be chemical and necessitates having windows in the basal walls of the zooids which permit contact with the substratum beneath. Etching may result in better adherence to the substrate, giving protection from abrasion and bioerosion.     

Cope's Rule in a modular organism: Directional evolution without an overarching macroevolutionary trend

Cope's Rule describes increasing body size in evolutionary lineages through geological time. This pattern has been documented in unitary organisms but does it also apply to module size in colonial organisms? We address this question using 1169 cheilostome bryozoans ranging through the entire 150 million years of their evolutionary history. The temporal pattern evident in cheilostomes as a whole shows no overall change in zooid (module) size. However, individual subclades show size increases: within a genus, younger species often have larger zooids than older species. Analyses of (paleo)latitudinal shifts show that this pattern cannot be explained by latitudinal effects (Bergmann's Rule) coupled with younger species occupying higher latitudes than older species (an “out of the tropics” hypothesis). While it is plausible that size increase was linked to the advantages of large zooids in feeding, competition for trophic resources and living space, other proposed mechanisms for Cope's Rule in unitary organisms are either inapplicable to cheilostome zooid size or cannot be evaluated. Patterns and mechanisms in colonial organisms cannot and should not be extrapolated from the better‐studied unitary organisms. And even if macroevolution simply comprises repeated rounds of microevolution, evolutionary processes occurring within lineages are not always detectable from macroevolutionary patterns.     

The placental analogue and the pattern of sexual reproduction in the cheilostome bryozoan Bicellariella ciliata (Gymnolaemata)

Background

Matrotrophy or extraembryonic nutrition ?C transfer of nutrients from mother to embryo during gestation ?C is well known and thoroughly studied among vertebrates, but still poorly understood in invertebrates. The current paper focuses on the anatomy and ultrastructure of the oogenesis and placentotrophy as well as formation of the brood chamber (ovicell) in the cheilostome bryozoan Bicellariella ciliata (Linnaeus, 1758). Our research aimed to combine these aspects of the sexual reproduction into an integral picture, highlighting the role of the primitive placenta-like system in the evolution of bryozoan reproductive patterns.

Results

Follicular and nutrimentary provisioning of the oocyte occur during oogenesis. Small macrolecithal oocytes are produced, and embryos are nourished in the ovicell via a simple placental analogue (embryophore). Every brooding episode is accompanied by the hypertrophy of the embryophore, which collapses after larval release. Nutrients are released and uptaken by exocytosis (embryophore) and endocytosis (embryo). Embryos lack specialized area for nutrient uptake, which occurs through the whole epidermal surface. The volume increase between the ripe oocyte and the larva is ca. 10-fold.

Conclusions

The ovicell is a complex organ (not a special polymorph as often thought) consisting of an ooecium (protective capsule) and an ooecial vesicle (plugging the entrance to the brooding cavity) that develop from the distal and the fertile zooid correspondingly. Combination of macrolecithal oogenesis and extraembryonic nutrition allows attributing B. ciliata to species with reproductive pattern IV. However, since its oocytes are small, this species represents a previously undescribed variant of this pattern, which appears to represent a transitional state from the insipient matrotrophy (with large macrolecithal eggs) to substantial one (with small microlecithal ones). Altogether, our results substantially added and corrected the data obtained by the previous authors, providing a new insight in our understanding of the evolution of matrotrophy in invertebrates.     

DO CONSTANT ENVIRONMENTS PROMOTE COMPLEXITY OF FORM?: THE DISTRIBUTION OF BRYOZOAN POLYMORPHISM AS A TEST OF HYPOTHESES

The distribution of cheilostome bryozoans on the Caribbean reefs of Panama was surveyed to test the hypothesis that physically constant environments favor increased morphologic complexity, expressed as the number of zooid types within a colony. The proportion of species within defined grades of complexity did not vary significantly with locality, depth, or substratum. Some differences were found in grade-specific ecological success, measured by colony abundance and spatial cover, but these were not consistently related to habitat type. There was no inverse correlation between morphologic complexity and range of distribution: morphologically specialized cheilostomes were not more stenotopic than generalized forms. Patterns of distribution and total space occupation indicate a sensitivity to local habitat conditions, but relative success of species was not correlated with level of polymorphism. In a bryozoan fauna from Florida, the frequency of polymorphic species was weakly associated with constancy of habitat. In estuaries, polymorphic cheilostomes are almost absent at salinities below 18‰, but this pattern is strongly confounded taxonomically. All species tolerant of low salinities are encrusting anascans; within this group, polymorphism does not decrease significantly with declining salinity. Bryozoan faunas from different biogeographic zones may vary in frequency of avicularian polymorphism, but not along a simple latitudinal cline. These large-scale comparisons may be strongly biased historically and taxonomically. The distribution of cheilostome polymorphism on a local and geographic scale provides no evidence for a causal relationship between habitat constancy and morphologic specialization at the zooidal level. This is in striking contrast to the strong habitat dependence of colony form, which suggests that selective processes may operate differently at the zooidal and colonial levels.     

Major radiation of cheilostome bryozoans: Triggered by the evolution of a new larval type?

A macroevolutionary model is developed to account for the “adaptive radiation”; of cheilostome bryozoans that commenced in the Cenomanian after a long phase of low diversity. Living cheilostome species possess one of two types of larvae; planktotrophic (cyphonautes) larvae of relatively long duration, and brooded non‐planktotrophic (coronate) larvae of short duration. Planktotrophic larvae characterize the paraphyletic “malacostegans”; from which “advanced”; cheilostomes with non‐planktotrophic larvae are thought to have evolved monophyletically. Research on other marine invertebrates suggests that gene flow within and between populations is likely to be poorer in species having non‐planktotrophic larvae, and hence the frequency of allopatric and quasi‐sympatric speciation may be greater. Skeletal evidence of larval brooding in the cheilostomes first appears in the late Albian, immediately before their adaptive radiation, and the evolution of non‐planktotrophy with associated increase in speciation rate is proposed to have triggered this radiation.     

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

Rendering developmental and ecological processes into macroevolutionary events and trends has proved to be a difficult undertaking, not least because processes and outcomes occur at different scales. Here we attempt to integrate comparative analyses that bear on this problem, drawing from a system that has seldom been used in this way: the co-occurrence of alternate phenotypes within genetic individuals, and repeated evolution of distinct categories of these phenotypes. In cheilostome bryozoans, zooid polymorphs (avicularia) and some skeletal structures (several frontal shield types and brood chambers) that evolved from polymorphs have arisen convergently at different times in evolutionary history, apparently reflecting evolvability inherent in modular organization of their colonial bodies. We suggest that division of labor evident in the morphology and functional capacity of polymorphs and other structural modules likely evolved, at least in part, in response to the persistent, diffuse selective influence of predation by small motile invertebrate epibionts.     

Colony Growth Pattern in Electra pilosa (Linnaeus) and Comparable Encrusting Cheilostome Bryozoans

Colony growth pattern is described in E. pilosa, an abundant cheilostome bryozoan commonly found as an epiphyte of Laminaria. Each zooid has 4 potential budding loci—one distal, two lateral and one proximal. The ancestrula buds daughter zooids from all of these loci; the two lateral buds appear first, followed by the distal bud and, after a long delay, the proximal bud. The laterally budded zooids curve inwards as they grow to form a triad with their distally budded sibling zooid. ‘Mature’ multiserial colonies growing on flat substrata consist of a series of radially diverging sectors. Each sector has an axis, generally of 3 parallel rows of zooids, flanked by wings consisting of rows of zooids originating as lateral buds from the section axis which infills the area between the axes. Occasional colonies occur with uniserial or semiuniserial growth patterns. These resemble colonies of the obligatory uniserial species Pyripora catenularia and poorly fed colonies of the related Conopeum tenuissimum, which is normally multiserial like E. pilosa. The ‘composite multiserial’ colonies of E. pilosa differ in several respects from ‘unitary multiserial’ colonies characteristic of most sheet-like cheilostomes, including the well-known Membranipora membranacea. Composite and unitary multiserial growth patterns may have evolved independently from uniserial ancestors.     

Early Colony Development in Aetea (Bryozoa)

External structures on the erect parts of zooids of Aetea havebeen demonstrated to be brood chambers by observation of release,settlement and metamorphosis of larvae from the chambers. Theancestrula is smaller than, but very similar to succeeding zooidsin the primary zone of astogenetic change, which do not showtubular connections. Sections through brood chambers and zooidsshow that part of the brood chamber wall may be slightly calcified.Brood chambers appear to be products of the external zooid walland not diverticula derived from the tentacle sheath.     

Comparative Studies of Ovicell Anatomy and Reproductive Patterns in Cribrilina annulata and Celleporella hyalina (Bryozoa: Cheilostomatida)

Investigations of the common boreal-arctic cheilostomate bryozoans Cribrilina annulata and Celleporella hyalina have shown that the two species possess similar ovicell structures and reproductive patterns. Both species are characterized by frontal dwarf ovicellate zooids, that are female autozooidal polymorphs in C. hyalina and simultaneous hermaphroditic autozooids in C. annulata. The latter species in addition has ovicellate autozooids of the usual type. Each ovicell is formed from a maternal zooid only, and its cavity is lined by the outer hemispherical fold (ooecium) and the distal zooidal wall. The coelomic cavity of the ooecium is separated from the body cavity of the maternal zooid by a transverse wall with simple pores. Each pore is closed by a cell plug, and the ooecia may be considered as kenozooids. Each oocyte is accompanied by a single nurse cell that degenerates after ovulation. The eggs are macrolecithal in C. annulata and microlecithal in C. hyalina, and the former species is a non-placental brooder whereas the latter forms a placenta. Fertilization is precocious. Possible mechanisms of sperm entry as well as oviposition are discussed. The literature concerning ovicell structure and development in cheilostomates is analysed. It is proposed that the brood chamber of cribrimorphs evolved by a fusion of costae and a reduction of the daughter zooid in ancestral forms. © 1998 The Royal Swedish Academy of Sciences. Published by Elsevier Science Ltd. All rights reserved