RESUMEN
Terebriporidae is one of the four extant endolithic ctenostome bryozoan families, with colonies immersed into carbonate substrates like molluscan shells. This monogeneric family comprises 17 species, with 11 extant and 6 fossil species. It is currently considered closely related to vesicularioid ctenostomes, a group characterized by colonies interconnected by polymorphic stolons and a distinct gizzard as part of their digestive systems. However, confusion persists regarding the correct species identities and affiliations of many terebriporid species, and even the description of the entire family is based solely on a few external features of their boring traces, rendering the family an ichnotaxon (trace fossil). Our molecular analysis does not support a vesicularioid affinity, but corroborate a close relationship to Immergentia, another genus of boring bryozoans. Consequently, this study aims to untangle the systematic confusion surrounding Terebriporidae by examining the tracemaker of the type species of the family, Terebripora ramosa from Chile, and investigating its morphology and histology using modern techniques. The current analysis could not confirm typical vesicularioid characters such as a gizzard or true polymorphic stolons. Instead, all characters point towards a closer relationship to Immergentiidae as suggested by a recent molecular phylogeny. In fact, these two taxa share several characters such as cystid appendages and duplicature bands, and appear closely related, with the only difference being a characteristic vane with tubulets present in the tracemaker of T. ramosa. The sister-group relationship of the tracemaker and the genus Immergentia infers that these borers share a common boring ancestor, but also emphasizes that additional species from the ichnogenus Terebripora need to be studied for more clarity.
Asunto(s)
Briozoos , Fósiles , Briozoos/anatomía & histología , Animales , Fósiles/anatomía & histología , FilogeniaRESUMEN
Immergentia is an endolithic genus of ctenostome bryozoans and the sole member of the Immergentiidae. Etchings of their typical spindled-shaped and sometimes enantiomorphic borehole aperture in calcium carbonate substrates are accomplished by chemical dissolution. The tentacle crown of the bryozoan is essentially the only body part that extends beyond the shell surface when protruded. Previously, species were mainly described using external colony and zooidal characteristics or whole mounts, with partial histological sections conducted on a single species in 1947. Modern approaches, however, are hitherto missing. We examined the soft body morphology of Immergentia from different locations with confocal laser scanning microscopy and the production of 3D reconstructions. In addition, zooidal characteristics such as tentacle number, size, tubulets, and interzooidal distances were used to distinguish and describe species. The combination of conventional and modern methods revealed the presence of a cardiac constrictor and intercalary kenozooids that can interpose between the cystid appendages, something not previously reported in immergentiids, thus necessitating an amendment of the family diagnosis. The polypide typically has eight to ten tentacles, and the anus is positioned in the low or mid-lophophoral area. In addition, sequence data, including the mitogenome and the nuclear ribosomal genes (18S and 28S) of four species from five locations, are presented for the first time. Based on molecular and morphological data, a novel intertidal immergentiid from France, Immergentia stephanieae sp. nov., and a subtidal species from New Zealand, I. pohowskii sp. nov., are described. This work supplements the rather sparse existing knowledge on Immergentiidae and proposes additional characteristics to complement existing descriptions in order to enhance future species identification. Supplementary Information: The online version contains supplementary material available at 10.1007/s13127-024-00645-y.
RESUMEN
Ctenostome bryozoans are a small group of gymnolaemates comprising less than 400 recent species. They are paraphyletic and ctenostome-grade ancestors gave rise to Cheilostomata, the most dominant and speciose taxon of Bryozoa in the present day. Investigations into ctenostomes are important for reconstructing character evolution among Gymnolaemata. As a continuation of studies on a morphological series of ctenostome bryozoans, we herein investigate six species of hislopiids, a small clade of three genera occurring in freshwater habitats. The general morphology of all species is similar in having primarily uniserial chains of encrusting zooids, which are mostly oval to ellipsoid and have a flattened frontobasal axis. Hislopia prolixa and Echinella placoides often have more slender zooids with a higher frontobasal axis. Apertures of hislopiids are quadrangular, lined by a thickened cuticle. Apertural spines are present in various lengths in E. placoides, Hislopia lacustris and Hislopia corderoi. The remaining cuticle is rather thin except at lateral areas, close to the pore-plates which are prominent in hislopiids because of abundant special and limiting cells. All species except H. corderoi and Timwoodiellina natans have a prominent collar obstructing the vestibulum, whereas the latter two species instead have an 'external collar' as cuticular, outer folds projecting over the aperture. Hislopiid lophophores carry eight, or more commonly 12-18 tentacles. The digestive tract is distinguished by an often highly elongated esophagus and/or cardia, with the latter always having a prominent bulbous part in the form of a proventriculus-or gizzard in E. placoides. The caecum is extensive in all species. In Hislopia the intestine is characteristically two-chambered with a proximal and distal part before entering an anal tube of various length. The latter is present in all species except T. natans and terminates in mid-lophophoral area. Oocytes in E. placoides are large and macrolecithal indicating brooding and the production of lecithotrophic larvae. Hislopia species produce small, oligolecithal ones, which suggests zygote spawning and planktotrophy. In general, the morphology is similar among the different hislopiids with characters of the gut aiding in delineating the genera Echinella and Timwoodiellina.
Asunto(s)
Briozoos , Animales , Briozoos/anatomía & histología , Canal Anal , Larva , Oocitos , Agua DulceRESUMEN
Ctenostome bryozoans are unmineralized and mostly marine. Their lack of calcified skeletal features requires other characters to be considered for systematic and phylogenetic considerations. As a continuation of an ongoing series of studies, we herein investigate the morphology of Amphibiobeania epiphylla, a unique bryozoan inhabiting mangrove leaves that are highly exposed to tidal cycles and regular dry events according to the tidal cycle. Besides this interesting mode of life, the species was originally interpreted to be a weakly mineralized cheilostome bryozoan, whereas molecular data place it among ctenostome bryozoans. To elucidate the systematic and phylogenetic position of the genus and also find morphological adaptations to an extreme habitat, we investigated the morphology of A. epiphylla in detail. Zooids show a lophophore with eight tentacles and a simple gut with a prominent caecum, lophophoral anus and most notably a distinct gizzard in the cardiac region. Gizzard teeth are multiple, simple homogeneous cuticular structures. The cuticle of the zooid is rather uniform and shows no respective thickenings into opercular flaps or folds. Likewise, apertural muscles are represented by a single pair of muscles. There are no specific closing muscles in the apertural area like the operculum occlusors of cheilostomes. Most prominent within zooids is a spongiose tissue filling most of the body cavity. Although not properly understood, this tissue may aid in keeping animals moist and hydrated during prolonged dry times. In summary, all morphological characters support a ctenostome rather than a cheilostome affinity, possibly with Vesicularioidea or Victorelloidea. In addition, we provide new molecular data that clearly supports such a closer relationship.
Asunto(s)
Briozoos , Animales , Filogenia , Briozoos/anatomía & histología , Ecosistema , Canal Anal , MúsculosRESUMEN
Ctenostome bryozoans are a small group of gymnolaemates that comprise only a few hundred described species. Soft-tissue morphology remains the most important source for analysing morphological characters and inferring relationships within this clade. The current study focuses on the genus Sundanella, for which morphological data is scarce to almost absent. We studied two species of the genus, including one new to science, using histology and three-dimensional reconstruction techniques and confocal laser scanning microscopy. Sundanella generally has a thick, sometimes arborescent cuticle and multiporous interzooidal pore plates. The lophophore is bilateral with an oral rejection tract and generally has 30 or 31 tentacles in both species. The digestive tract shows a large cardia in S. floridensis sp. nov. and an extremely elongated intestine in Sundanella sibogae. Both terminate via a vestibular anus. Only parietodiaphragmatic muscles are present and four to six duplicature bands. Both species show a large broad frontal duplicature band further splitting into four individual bands. The collar is vestibular. Sundanella sibogae shows highly vacuolated cells at the diaphragm, whereas S. floridensis sp. nov. has unique glandular pouches at the diaphragmal area of the tentacle sheath. Such apertural glands have never been encountered in other ctenostomes. Both species of Sundanella are brooders that brood embryos either in the vestibular or cystid wall. Taken together, the current analysis shows numerous characteristics that refute an assignment of Sundanella to victorellid ctenostomes, which only show superficial resemblance, but differ substantially in most of their soft-body morphological traits. Instead, a close relationship with other multiporate ctenostomes is evident and the families Pherusellidae, Flustrellidrae and Sundanellidae should be summarized as clade 'Multiporata' in the future.
Asunto(s)
Briozoos , Canal Anal , Animales , Briozoos/anatomía & histología , Tracto Gastrointestinal , Microscopía Confocal , Músculos/anatomía & histologíaRESUMEN
The genus Pierrella was originally created for a single fossil ctenostome bryozoan species from the Late Cretaceous, which is characterized by runner-like colonies, with zooids possessing a distinctive radial, folded aperture. Not long ago, a few specimens of a recent deep-sea congener, Pierrella plicata, were discovered and described from the Russian exploration area of the Clarion-Clipperton Fracture Zone, eastern Central Pacific Ocean. Owing to the lack of data on the internal morphology of this species, we investigated the soft-body morphology of P. plicata using serial sectioning and 3D-reconstruction in order to compare it to other more recently investigated ctenostome bryozoans and to infer the systematic position of the genus. The most striking peculiarity of the examined species is the radial aperture formed by multiple cuticular, pleated folds of the cystid wall. The cuticle is thickened into triangular-shaped folds in this area. An orifical sphincter underlies the folded aperture. Apertural muscles are present as a single pair of parieto-diaphragmatic muscles and four duplicature bands. The remaining polypide anatomy is mainly characterized by its miniature design: the lophophore has eight short tentacles and the digestive tract is one of the shortest and most compact ever observed in any bryozoan. A small intertentacular organ was detected at the lophophoral base. Taken together the genus Pierrella shows unique characters, such as the radial apertural folds that are closed by a series of orificial sphincter muscles, and its particularly small polypide. The general colony morphology resembles arachnidioidean ctenostomes whereas its internal morphology resembles alcyonidioidean species.
Asunto(s)
Briozoos , Animales , Fósiles , Tracto Gastrointestinal , Técnicas Histológicas , MúsculosRESUMEN
Ctenostome bryozoans are a small group of bryozoans whose soft-tissue morphology has received only little attention. The present study represents the third in a series of articles dealing with the morphology of this clade of bryozoans. The morphology of three genera of Alcyonidioidea, that is, Bockiella (Alcyonidiidae), Elzerina and Flustrellidra (both Flustrellidridae), are analyzed using histology and 3D-reconstruction techniques. The general zooidal morphology is similar and externally differs by the shape of the aperture. Zooids of Elzerina binderi are elongated in the fronto-basal axis, whereas the other two are more flattened in this axis. All species show multiple pore-complexes in their zooidal walls ranging from ~66 in E. binderi, to ~30 in F. hispida and to less than 10 in Bockiella. The aperture is bilabiate in flustrellidrids and roundish in Bockiella. Apertural muscles are present as parieto-diaphragmatic muscles. The flustrellidrids have a large frontal duplicature band that further splits into four separate bands. The collar is diaphragmatic in Bockiella, but vestibular in the flustrellidrids. Lophophores are similar among the investigated species with a rejection tract in the flustrellidrids. The digestive tract shows differences in the extent and proportions of the caecum, which is large in the flustrellidrids and small in Bockiella; the anus is vestibular in all species. A funicular muscle of variable location is present in each species. Elzerina binderi has additional thin strands emanating from the digestive tract to the body wall. The parietal muscles show a unique situation in E. binderi with five bundles being present, two laterals and one distal. Several features aid in defining characters for the entire superfamily and the families Flustrellidridae and Alcyonidiidae. Besides the shape of the aperture, the frontal duplicature band, the vestibular collar and the large caecum are important. The set of characters also confirms recent notions that Bockiella belongs to the Alcyonidiidae.
Asunto(s)
Briozoos , Canal Anal , Animales , Tracto Gastrointestinal , Técnicas Histológicas , MúsculosRESUMEN
The genus Haywardozoon represent a little known genus of ctenostome bryozoans that has only been found in the deep-sea. It forms small, mostly uniserial colonies lacking polymorphs. Zooids have a conspicuous apertural closure mechanism consisting of a cuticular lower lip that closes the aperture. The systematic placement of the genus remains uncertain, detailed morphological studies that include soft-body morphological traits are missing. Consequently, this is the first study analyzing H. pacificum by means of histological serial sections and 3d-reconstruction. Zooids are ovoid and in some cases solitary, that is, showing no interconnected zooids. Most prominent is the large vestibular wall that can be more than half of the total length of the zooid. Its vestibular wall is particularly lined by a complex, multilayered and branched cuticle. A single pair of lateral parieto-diaphragmatic muscles is present. The polypide is small and comprises about 17 tentacles. The digestive tract is short, has an elongated cardia, a vestigial caecum and a vestibular anus. An ovipositor/intertentacular organ and several oligolecithal oocytes were detected. Several aspects of zooidal morphology, including the structure of the bilateral aperture, parieto-diaphragmatic muscles, general structure of the gut and the thick cuticle, clearly indicate an association to the ctenostome superfamily Alcyonidioidea. Therefore, we reject the previous placement into Hislopioidea and suggest a possible association to pherusellid ctenostomes. New reproductive characters show that H. pacificum is a broadcaster contrary to some other deep-sea forms that are brooding. RESEARCH HIGHLIGHT: Morphology of ctenostome bryozoans remain little investigated. This contribution is the second of a series of detailed morphological analyses of this understudied clade of bryozoans. The morphological investigation of Haywardozoon pacificum revealed numerous characters that show a closer relationship to Flustrellididrae rather than Hislopiidae as previously assumed.