Andrew N. Ostrovsky

MORPHOLOGICAL DIFFERENTIATION OF AVICULARIA AND THE PROLIFERATION OF SPECIES IN MID-CRETACEOUS WILBERTOPORA CHEETHAM, 1954 (BRYOZOA: CHEILOSTOMATA)

Abstract Discovery of avicularium-like polymorphs in Wilbertopora mutabilis Cheetham, 1954 has provided not only a new opportunity for revising the genus Wilbertopora Cheetham, 1954, but also a more detailed basis for documenting the series of morphological changes by which avicularia differentiated from ordinary feeding zooids in what appears to be the first occurrence of these characteristic cheilostome bryozoan structures in the fossil record. Eighteen of a total 60 quantitative characters measured on avicularia and ordinary and ovicell-bearing autozooids were sufficient to distinguish eight species of Wilbertopora by discriminant function analysis of zooid data from 93 colonies from the mid-Cretaceous (Albian–Cenomanian) Washita Group in northeastern Texas and southeastern Oklahoma. Eighteen of a total of 20 of the quantitative characters that could be statistically coded for cladistic analysis proved to be informative with respect to parsimony, providing two maximally parsimonious trees for the eight species. Two-thirds of the diagnostic characters involve avicularia. An additional 55 colonies too poorly preserved for morphometric analysis could then be assigned to species qualitatively, with 170 more colonies lacking species-diagnostic characters. The cladistic trees strongly suggest that most or all of the species diverged before the end of the Albian, but stratigraphic resolution is insufficient to test this hypothesis. Nevertheless, the series of morphological changes differentiating avicularia from ordinary autozooids in these species, based on the cladistic relationships, is highly significant statistically, and may be a pattern later repeated in other cheilostomes. Wilbertopora and W. mutabilis are emended, and seven new species are described: W. listokinae, W. tappanae, W. spatulifera, W. attenuata, W. improcera, W. acuminata, and W. hoadleyae.

Individual autozooidal behaviour and feeding in marine bryozoans

Abstract The article is devoted to individual behaviour of autozooids (mainly connected with feeding and cleaning) in 40 species and subspecies of marine bryozoans from the White Sea and the Barents Sea. We present comparative descriptions of the observations and for the first time describe some of autozooidal activities (e.g. cleaning of the colony surface by a reversal of tentacular ciliature beating, variants of testing-position, and particle capture and rejection). Non-contradictory aspects from the main hypotheses on bryozoan feeding have been used to create a model of feeding mechanism. Flicking activity in the absence of previous mechanical contact between tentacle and particle leads to the inference that polypides in some species can detect particles at some distance. The discussion deals with both normal and “spontaneous” reactions, as well as differences and similarities in autozooidal behaviour and their probable causes. Approaches to classification of the diversity of bryozoan behaviour (functional and morphological) are considered. Behavioural reactions recorded are classified using a morphological approach based on the structure (tentacular ciliature, tentacles and entire polypide) performing the reaction. We suggest that polypide protrusion and retraction might be the basis of the origin of some other individual activities. Individual autozooidal behaviour is considered to be a flexible and sensitive system of reactions in which the activities can be performed in different combinations and successions and can be switched depending on the situation.

Matrotrophy and placentation in invertebrates: a new paradigm

Matrotrophy, the continuous extra‐vitelline supply of nutrients from the parent to the progeny during gestation, is one of the masterpieces of nature, contributing to offspring fitness and often correlated with evolutionary diversification. The most elaborate form of matrotrophy—placentotrophy—is well known for its broad occurrence among vertebrates, but the comparative distribution and structural diversity of matrotrophic expression among invertebrates is wanting. In the first comprehensive analysis of matrotrophy across the animal kingdom, we report that regardless of the degree of expression, it is established or inferred in at least 21 of 34 animal phyla, significantly exceeding previous accounts and changing the old paradigm that these phenomena are infrequent among invertebrates. In 10 phyla, matrotrophy is represented by only one or a few species, whereas in 11 it is either not uncommon or widespread and even pervasive. Among invertebrate phyla, Platyhelminthes, Arthropoda and Bryozoa dominate, with 162, 83 and 53 partly or wholly matrotrophic families, respectively. In comparison, Chordata has more than 220 families that include or consist entirely of matrotrophic species. We analysed the distribution of reproductive patterns among and within invertebrate phyla using recently published molecular phylogenies: matrotrophy has seemingly evolved at least 140 times in all major superclades: Parazoa and Eumetazoa, Radiata and Bilateria, Protostomia and Deuterostomia, Lophotrochozoa and Ecdysozoa. In Cycliophora and some Digenea, it may have evolved twice in the same life cycle. The provisioning of developing young is associated with almost all known types of incubation chambers, with matrotrophic viviparity more widespread (20 phyla) than brooding (10 phyla). In nine phyla, both matrotrophic incubation types are present. Matrotrophy is expressed in five nutritive modes, of which histotrophy and placentotrophy are most prevalent. Oophagy, embryophagy and histophagy are rarer, plausibly evolving through heterochronous development of the embryonic mouthparts and digestive system. During gestation, matrotrophic modes can shift, intergrade, and be performed simultaneously. Invertebrate matrotrophic adaptations are less complex structurally than in chordates, but they are more diverse, being formed either by a parent, embryo, or both. In a broad and still preliminary sense, there are indications of trends or grades of evolutionarily increasing complexity of nutritive structures: formation of (i) local zones of enhanced nutritional transport (placental analogues), including specialized parent–offspring cell complexes and various appendages increasing the entire secreting and absorbing surfaces as well as the contact surface between embryo and parent, (ii) compartmentalization of the common incubatory space into more compact and ‘isolated’ chambers with presumably more effective nutritional relationships, and (iii) internal secretory (‘milk’) glands. Some placental analogues in onychophorans and arthropods mimic the simplest placental variants in vertebrates, comprising striking examples of convergent evolution acting at all levels—positional, structural and physiological.

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.

FROM INCIPIENT TO SUBSTANTIAL: EVOLUTION OF PLACENTOTROPHY IN A PHYLUM OF AQUATIC COLONIAL INVERTEBRATES

Matrotrophy has long been known in invertebrates, but it is still poorly understood and has never been reviewed. A striking example of matrotrophy (namely, placentotrophy) is provided by the Bryozoa, a medium‐sized phylum of the aquatic colonial filter feeders. Here I report on an extensive anatomical study of placental analogues in 21 species of the bryozoan order Cheilostomata, offering the first review on matrotrophy among aquatic invertebrates. The first anatomical description of incipient placentotrophy in invertebrates is presented together with the evidence for multiple independent origins of placental analogues in this order. The combinations of contrasting oocytic types (macrolecithal or microlecithal) and various degrees of placental development and embryonic enlargement during incubation, found in different bryozoan species, are suggestive of a transitional series from the incipient to the substantial placentotrophy accompanied by an inverse change in oogenesis, a situation reminiscent of some vertebrates. It seems that matrotrophy could trigger the evolution of sexual zooidal polymorphism in some clades. The results of this study show that this phylum, with its wide variety of reproductive patterns, incubation devices, and types of the simple placenta‐like systems, offers a promising model for studying parallel evolution of placentotrophy in particular, and matrotrophy in general.

Scorpiodinipora costulata (Canu & Bassler, 1929) (Bryozoa, Cheilostomata), a taxonomic and biogeographic dilemma: complex of cryptic species or human-mediated cosmopolitan colonizer?

ABSTRACT Despite implausible cosmopolitanism, the species Scorpiodinipora costulata (Canu & Bassler, 1929) has been attributed with reservations to small encrusting colonies with similar morphological features whose known distribution is scattered in tropical and subtropical seas: Pacific Ocean (Philippines), Indian Ocean (Oman), Red Sea, SE Mediterranean, SE Atlantic (Ghana) and SW Atlantic (Brazil). This material raised questions about its generic assignment. The genus Scorpiodinipora Balavoine, 1959 is redescribed with Schizoporella costulata Canu & Bassler, 1929, from the Philippines as the type species, as Balavoine misidentified the specimens to define the genus as Cellepora bernardii Audouin, 1826. Moreover, SEM examination of the cotypes of S. costulata showed that Canu & Bassler confused two genera among them. A lectotype and paralectotype were thus chosen from Canu & Basslers syntypes corresponding with the present morphotype. Hippodiplosia ottomuelleriana var. parva Marcus, 1938, from Brazil, which presents the same morphotype, is provisionally considered as the junior synonym of S. costulata. Considering the broad allopatric distribution of this morphotype across the oceans and the low capacity of dispersal of species with short-lived larvae, it is likely that this material includes several sibling species. However, the role of man-mediated dispersal is not excluded, at least in regions with high shipping activity, such as that comprising the Suez Canal.

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

BackgroundMatrotrophy or extraembryonic nutrition – transfer of nutrients from mother to embryo during gestation – 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.ResultsFollicular 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.ConclusionsThe 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.

The Internal-Brooding Apparatus in the Bryozoan Genus Cauloramphus (Cheilostomata: Calloporidae) and Its Inferred Homology to Ovicells

Abstract We studied by SEM the external morphology of the ooecium in eight bryozoans of the genus Cauloramphus Norman, 1903 (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.

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.

Systematics of some Antarctic Idmidronea and Exidmonea (Bryozoa: Cyclostomata)

Descriptions are given of seven Antarctic species of cyclostome bryozoans belonging to the genera Idmidronea and Exidmonea, of which I. fraudulenta, I. pellucida and E. arcuata are new. The gonozooids of I. pseudocrisina Borg are described for the first time, and all species are newly illustrated using SEM. The large sample size available has permitted particular attention to be given to intraspecific variability, especially of the ooeciostome which is shown to be more variable than has been previously acknowledged.