Boring systematics: A genome skimmed phylogeny of ctenostome bryozoans and their endolithic family Penetrantiidae with the description of one new species.

Ctenostomes are a group of gymnolaemate bryozoans with an uncalcified chitinous body wall having few external, skeletal characters. Hence, species identification is challenging and their systematics remain poorly understood, even more so when they exhibit an endolithic (boring) lifestyle. Currently, there are four Recent families of endolithic bryozoans that live inside mineralized substrates like mollusk shells. In particular, Penetrantiidae Silén, 1946 has received considerable attention and its systematic affinity to either cheilostomes or ctenostomes has been debated. Species delimitation of penetrantiids remains difficult, owing to a high degree of colonial and zooidal plasticity. Consequently, an additional molecular approach is essential to unravel the systematics of penetrantiids, their phylogenetic placement and their species diversity. We therefore sequenced the mitochondrial (mt) genomes and two nuclear markers of 27 ctenostome species including nine penetrantiids. Our phylogeny supports the Penetrantiidae as a monophyletic group placed as sister taxon to the remaining ctenostomes alongside paludicellids, arachnidioids and terebriporids. The boring family Terebriporidae d'Orbigny, 1847 were previously considered to be among vesicularioids, but our results suggest an arachnidioid affinity instead. Ctenostome paraphyly is supported by our data, as the cheilostomes nest within them. A Multiporata clade is also well supported, including the former victorelloid genus Sundanella. Altogether, this study provides new insights into ctenostome systematics, assists with species delimitation and contributes to our understanding of the bryozoan tree of life.

Multiple evolutionary transitions of reproductive strategies in a phylum of aquatic colonial invertebrates.

Parental care is considered crucial for the enhanced survival of offspring and evolutionary success of many metazoan groups. Most bryozoans incubate their young in brood chambers or intracoelomically. Based on the drastic morphological differences in incubation chambers across members of the order Cheilostomatida (class Gymnolaemata), multiple origins of incubation were predicted in this group. This hypothesis was tested by constructing a molecular phylogeny based on mitogenome data and nuclear rRNA genes 18S and 28S with the most complete sampling of taxa with various incubation devices to date. Ancestral character estimation suggested that distinct types of brood chambers evolved at least 10 times in Cheilostomatida. In Eucratea loricata and Aetea spp. brooding evolved unambiguously from a zygote-spawning ancestral state, as it probably did in Tendra zostericola, Neocheilostomata, and 'Carbasea' indivisa. In two further instances, brooders with different incubation chamber types, skeletal and non-skeletal, formed clades (Scruparia spp., Leiosalpinx australis) and (Catenicula corbulifera (Steginoporella spp. (Labioporella spp., Thalamoporella californica))), each also probably evolved from a zygote-spawning ancestral state. The modular nature of bryozoans probably contributed to the evolution of such a diverse array of embryonic incubation chambers, which included complex constructions made of polymorphic heterozooids, and maternal zooidal invaginations and outgrowths.

Effects of substratum type and orientation on the recruitment of bryozoans in an artificial area of the Western Atlantic.

Bryozoans are commonly associated with various artificial structures in marine environments and have been responsible for several bioinvasion events worldwide. Understanding the interactions between bryozoans and artificial structures is therefore essential to prevent the establishment and spread of potential bioinvaders. This study investigated bryozoan recruitment on four different substrates (PET, nautical ropes, metal, and PVC) placed in three orientations (vertical, horizontal facing down and facing up) in an area of the Western Atlantic. In total, 15 species of bryozoans were found. The results revealed significant variations in assemblages' richness, with bryozoans showing a preference for settling on PVC (14 species found) and on the underside of horizontal substrates (15 species found), resulting in the higher representativity observed in this study. Cryptogenic (nine species) and exotic (five species) bryozoans dominated the assemblages in all treatments, indicating that the type of substrate (especially artificial) and its orientation can favor the settlement of bryozoans, particularly non-native species. Therefore, the availability of multiple types of artificial substrates in marine environments should be treated as a cause for concern.

Stranding events of drift organisms (Arribadas) in southern Brazil and the spread of invasive bryozoan in South America.

The accumulation of drift organisms (Arribadas, constituted by benthic microalgae, macroalgae and bryozoans) on Central Beach in Balneário Camboriú (SC) has drawn attention since the early 2000s. However, historical surveys suggest an ancient phenomenon that has been increasing in intensity, promoted by urbanization and the eutrophication of the bay in recent years, leading to changes in the taxonomic composition. Previously, these Arribadas were comprised of two species of benthic microalgae (Amphitetras antediluviana and Biddulphia biddulphiana) and the bryozoan Arbocuspis ramosa. However, since 2019, a substantial increase in biomass has been observed on the beach and the dominance of the macroalgae Bryopsis plumosa strongly suggests an increase in the load of organic matter and nutrients in the bay. Recently (2022) the presence of a new invasive bryozoan species (Amathia alternata) was detected, highlighting the need to continue investigating the Arribadas to monitor the ecological evolution of this process.

Paleozoic origins of cheilostome bryozoans and their parental care inferred by a new genome-skimmed phylogeny.

Phylogenetic relationships and the timing of evolutionary events are essential for understanding evolution on longer time scales. Cheilostome bryozoans are a group of ubiquitous, species-rich, marine colonial organisms with an excellent fossil record but lack phylogenetic relationships inferred from molecular data. We present genome-skimmed data for 395 cheilostomes and combine these with 315 published sequences to infer relationships and the timing of key events among c. 500 cheilostome species. We find that named cheilostome genera and species are phylogenetically coherent, rendering fossil or contemporary specimens readily delimited using only skeletal morphology. Our phylogeny shows that parental care in the form of brooding evolved several times independently but was never lost in cheilostomes. Our fossil calibration, robust to varied assumptions, indicates that the cheilostome lineage and parental care therein could have Paleozoic origins, much older than the first known fossil record of cheilostomes in the Late Jurassic.

Ten new species of marine bryozoans (Gymnolaemata: Cheilostomatida) from Brazil.

Despite a recent increase in the number of taxonomic studies on the bryozoan fauna of northeastern Brazil, new discoveries and re-examination of museum specimens allow the continued recognition of new taxa. Here, we describe ten new cheilostome species from the northeastern continental shelf of Brazil based on different museum collections. The new species are: Thalamoporella tupinamba n. sp., Turbicellepora papula n. sp., Plesiocleidochasma brasiliensis n. sp., Plesiocleidochasma infundibulum n. sp., Rhynchozoon turgidum n. sp., Cribrilaria brasiliensis n. sp., Hippoporina titan n. sp., Crepidacantha fasciata n. sp., Crepidacantha browni n. sp., and Hippopodina inarmata n. sp. Some specimens previously reported from northeastern Brazil are here reassigned to the newly described taxa, and two new combinations, Cribrilaria caraguata (Winston Vieira, 2013) n. comb. and Cribrilaria tuba (Winston Vieira, 2013) n. comb., are proposed.

From the individual to the colony: Marine invertebrates as models to understand levels of biological organization.

The developmental and evolutionary principles of coloniality in marine animals remain largely unexplored. Although many common traits have evolved independently in different groups of colonial animals, questions about their significance for colonial life histories remain unanswered. In 2018 (Nov. 25 - Dec. 8), the inaugural course on the Evolution of Coloniality and Modularity took place at the Center for Marine Biology of the University of São Paulo (CEBIMAR-USP), Brazil. During the intensive two-week graduate-level course, we addressed some of the historical ideas about animal coloniality by focal studies in bryozoans, tunicates, cnidarians, and sponges. We discussed many historical hypotheses and ways to test these using both extant and paleontological data, and we carried direct observations of animal colonies in the different phyla to address questions about coloniality. We covered topics related to multi-level selection theory and studied colonial traits, including modular miniaturization, polymorphism, brooding, and allorecognition. Course participants carried out short research projects using local species of animals to address questions on allorecognition and regeneration in ascidians and sponges, fusion and chimerism in anthoathecate hydrozoans, and evolution of polymorphism in bryozoans. Although many questions remain unanswered, this course served as a foundation to continue to develop a developmental and evolutionary synthesis of clonal and modular development in colonial marine organisms.

The role of artificial habitats on fouling bryozoan fauna in the southwestern Atlantic.

Artificial habitats, such as harbours and marinas, are entry doors for the introduction and dispersal of species. Surveys on fouling community in these habitats help to understand preventing environmental impacts and management of invasive species. Thus, a survey on fouling bryozoan fauna was carried out along 17 artificial habitats (eight harbours and nine marinas) from three coastal stretches in Southwestern Atlantic. A total of 55 species were identified, including 13 non-native, 33 cryptogenic and nine native taxa. Only five bryozoan species were found in more than 75% of sampled sites. Our analysis revealed that bryozoan fouling communities in artificial habitats do not vary significantly between commercial and recreational localities. However, we also found that faunal assemblages varied significantly along Brazilian coastal stretches that are distinguished by environmental conditions, such as salinity and temperature.

Free-living bryozoans (Cheilostomatida, Cupuladriidae) from northeastern and northern Brazil.

Free-living bryozoans, unlike most cheilostomes, live unattached from the substratum on or within soft sedimentary bottoms. Bryozoans of the family Cupuladriidae Lagaaij, 1952 are probably the best-studied free-living representatives. In Brazil, eight species of cupuladriids have been reported to date, including some regarded as species complexes. This paper documents cupuladriid taxa from northeastern and northern Brazil based on the examination of 1236 colonies. Three species previously reported from Brazil are described: Cupuladria monotrema (Busk, 1884), Discoporella gemmulifera Winston Vieira, 2013 and Discoporella salvadorensis Winston, Vieira Woollacott, 2014. A new species, Cupuladria minuta n. sp., is erected; it differs from its congeners in having small, flat discoid colonies, with the central area up to the fifth astogenetic generation composed of vicarious avicularia with an auriform opesia, and quadrangular to rectangular basal sectors with 1-6 small openings per sector. Our results suggest that four species previously recorded from Brazil are doubtful-Cupuladria canariensis (Busk, 1859), Cupuladria biporosa Canu Bassler, 1923, Discoporella umbellata (Defrance, 1923) and Discoporella depressa (Conrad, 1841). Some Brazilian specimens previously assigned to Discoporella umbellata var. conica are re-assigned to D. salvadorensis. The species studied here frequently co-occur on mainly sandy and muddy bottoms at 8-130 m depth, as it is typical of most living populations of cupuladriids. The sedimentation rate, and thus the bottom composition, likely influence the distribution of cupuladriids in Brazil, with Cupuladria species being more common in stabler and coarser sea bottoms than Discoporella species, which tend to be more broadly distributed.

Revision of the European species of the genus Hincksina Norman, 1903 (Bryozoa, Cheilostomatida, Flustridae).

Four Atlantic species of the flustrid genus Hincksina Norman, 1903, which were introduced during the 19th and early 20th century, are redescribed and imaged: Hincksina flustroides (Hincks, 1877) from Great Britain, Hincksina sceletos (Busk, 1858) from Madeira as well as Hincksina neptuni (Jullien in Jullien Calvet, 1903) n. comb. and Hincksina alice (Jullien in Jullien Calvet, 1903) n. comb. from the Azores, the latter two of which were hitherto placed in the cribrilinid genus Membraniporella Smitt, 1873. Lectotypes are designated for all species. A new species, Hincksina synchysia n. sp., is introduced for the Mediterranean taxon previously referred to as Hincksina flustroides f. crassispinata Gautier, 1962. In contrast to species from the continental shelf, which have simple cylindrical or flattened spines, some of the species from the oceanic islands of Madeira and the Azores are particularly characterised by falciform and variably formed palmicorn spines. Moreover, whilst most Hincksina species have avicularia with a relatively short, (sub)rounded rostrum and mandible, the two Azorean species have elongated, curved and pointed avicularia. The relationship between Gregarinidra Barroso, 1949, which also has pointed avicularia, and Hincksina is commented upon. Based on several shared diagnostic characters, the genus Cribralaria Siln, 1941 is here transferred from the Cribrilinidae Hincks, 1879 to the Flustridae Fleming, 1828.

p class="ZootaxaTitle"Report of ciliate-bryozoan-crustacean hyperepibiosis on crab (Decapoda: Brachyura) from west coast of India, Arabian Sea.

Epibiosis is a common phenomenon, found in different taxa of aquatic animals. This relationship could occur as hyperepibiosis, when a basibiont being also an epibiont, providing a stable substrate for the hypersymbiont. Here we reported a ciliate-bryozoan-crustacean hyperepibiosis in Mandovi River mouth, Goa, West coast of India. We provided descriptions and characterization of the crab Atergatis sp., serving as basibiont for the bryozoan Triticella pedicellata (Alder, 1857), in turn colonized with (hyperepibionts) the ciliates Paracineta saifulae (Mereschkowsky, 1877) and Cothurnia ceramicola Kahl, 1933. Paracineta saifulae and Cothurnia ceramicola are reported here for first time from the Indian Ocean.

Influence of depth on bryozoan richness and distribution from the continental shelf of the northern coast of Bahia State, north-eastern Brazil.

Biological and abiotic processes influence ecosystem structure and species distribution. For bryozoan assemblages, depth, substratum and habitat structure are among the main factors influencing their distribution. Ecological studies on bryozoan fauna from Brazil are scarce and factors affecting the distribution and/or diversity of this common group are obscure. Here we attempted to verify the influence of bathymetry on bryozoan richness on the north shore of Bahia State, north-eastern Brazil. We identified 57 bryozoan taxa, comprising 35 families and 50 genera, all belonging to the Cheilostomata. Retevirgula multipunctata Winston, Vieira & Woollacott, 2014 and Tetraplaria dichotoma (Osburn, 1914) and the genus Aimulosia Jullien, 1888 were recorded for the first time from Bahia State. Species growing as encrusting sheets were dominant at all depths. There was a significant difference in richness among samples at different depths, with highest values of richness at 40 meters (Kruskal-Wallis Test). Analysis of similarities revealed a significant difference among the bryozoan assemblages, mainly when comparing assemblages from 10 and 20 meters with deeper ones. Also, shallower assemblages composition varied much than assemblages from 30 and 40 meters. Since depth is a proxy for several environmental parameters, further studies are needed to identify other factors influencing bryozoan distribution.

New species of Stylopoma (Bryozoa, Cheilostomata) from Bahia State, northeastern Brazil.

At date, seven species of Stylopoma Levinsen, 1909 are reported from the Brazilian coast, five of which are known from Bahia State in the northeastern region. Here we describe four new species of Stylopoma, all from Bahia State: Stylopoma corallinum n. sp., Stylopoma faceluciae n. sp., Stylopoma multiavicularia n. sp. and Stylopoma sinuata n. sp. Unlike the Caribbean species of Stylopoma, that mainly have rounded primary orifice and slit-like sinus, the morphology of the primary orifice of Brazilian taxa, including the new species presented here, is quite variable. In the newly described taxa, the sinus is drop-shaped in S. corallinum n. sp. and S. faceluciae n. sp., U-shaped in S. multiavicularia n. sp. and V-shaped in S. sinuata n. sp. Like congeners from the Caribe, S. corallinum n. sp., S. faceluciae n. sp. and S. multiavicularia n. sp. have avicularia on the surface of the ooecia. Remarks on the morphological characters currently used in Stylopoma taxonomy are provided, including a comparative table of all living species worldwide.

The Phylum Bryozoa: From Biology to Biomedical Potential.

Less than one percent of marine natural products characterized since 1963 have been obtained from the phylum Bryozoa which, therefore, still represents a huge reservoir for the discovery of bioactive metabolites with its ~6000 described species. The current review is designed to highlight how bryozoans use sophisticated chemical defenses against their numerous predators and competitors, and which can be harbored for medicinal uses. This review collates all currently available chemoecological data about bryozoans and lists potential applications/benefits for human health. The core of the current review relates to the potential of bryozoan metabolites in human diseases with particular attention to viral, brain, and parasitic diseases. It additionally weighs the pros and cons of total syntheses of some bryozoan metabolites versus the synthesis of non-natural analogues, and explores the hopes put into the development of biotechnological approaches to provide sustainable amounts of bryozoan metabolites without harming the natural environment.

A genome-skimmed phylogeny of a widespread bryozoan family, Adeonidae.

BACKGROUND: Understanding the phylogenetic relationships among species is one of the main goals of systematic biology. Simultaneously, credible phylogenetic hypotheses are often the first requirement for unveiling the evolutionary history of traits and for modelling macroevolutionary processes. However, many non-model taxa have not yet been sequenced to an extent such that statistically well-supported molecular phylogenies can be constructed for these purposes. Here, we use a genome-skimming approach to extract sequence information for 15 mitochondrial and 2 ribosomal operon genes from the cheilostome bryozoan family, Adeonidae, Busk, 1884, whose current systematics is based purely on morphological traits. The members of the Adeonidae are, like all cheilostome bryozoans, benthic, colonial, marine organisms. Adeonids are also geographically widely-distributed, often locally common, and are sometimes important habitat-builders. RESULTS: We successfully genome-skimmed 35 adeonid colonies representing 6 genera (Adeona, Adeonellopsis, Bracebridgia, Adeonella, Laminopora and Cucullipora). We also contributed 16 new, circularised mitochondrial genomes to the eight previously published for cheilostome bryozoans. Using the aforementioned mitochondrial and ribosomal genes, we inferred the relationships among these 35 samples. Contrary to some previous suggestions, the Adeonidae is a robustly supported monophyletic clade. However, the genera Adeonella and Laminopora are in need of revision: Adeonella is polyphyletic and Laminopora paraphyletically forms a clade with some Adeonella species. Additionally, we assign a sequence clustering identity using cox1 barcoding region of 99% at the species and 83% at the genus level. CONCLUSIONS: We provide sequence data, obtained via genome-skimming, that greatly increases the resolution of the phylogenetic relationships within the adeonids. We present a highly-supported topology based on 17 genes and substantially increase availability of circularised cheilostome mitochondrial genomes, and highlight how we can extend our pipeline to other bryozoans.

Exotic species dominate marinas between the two most populated regions in the southwestern Atlantic Ocean.

Human occupation of coastal areas promotes the establishment of non-native species but information on bioinvasions is usually biased toward the Northern Hemisphere. We assessed non-native species' importance in sessile communities at six marinas along the most urbanized area of the Southwestern Atlantic coastline. We found 67 species, of which 19 are exotic. The most frequent species was the exotic polychaete Branchiomma luctuosum, while the most abundant was the exotic bryozoan Schizoporella errata that monopolized the substrata in three marinas. Along with S. errata, the exotic polychaete Hydroides elegans and ascidian Styela plicata dominated space in the three remaining marinas, while native species were in general rare. We show that communities associated with artificial substrata along this Brazilian urbanized area are dominated by exotic species and that using abundance data along with species identity can improve our understanding of the importance of exotic species for the dynamics of biological communities.

Dismantling the Beania magellanica (Busk, 1852) species complex (Bryozoa, Cheilostomata): two new species from European waters.

New research on bryozoans has determined that formerly widespread species are in many cases complexes of similar, but distinct, species with more restricted distributions. Notwithstanding, the limits of distribution are still unresolved for many taxa, and occasionally a wide distribution is confirmed. Beania magellanica has been considered a widespread species, distributed throughout the Southern Hemisphere, parts of northern Pacific and Atlantic Oceans and the Mediterranean Sea. This study examines the Magellanic-type material, together with other historic samples and new specimens collected in the western Mediterranean and Adriatic, and for the first time, presents specimens from the European North Atlantic. Morphological comparisons and biometric analysis show the existence of three different species among the specimens studied. A redescription of B. magellanica based on the type specimen is presented, and two new species are described: B. serrata sp. nov. from the Northeast Atlantic and B. mediterranea sp. nov. from the Mediterranean Sea. These results indicate that B. magellanica s.l. is a large complex of species and that most specimens from different parts of the world must be revised.

Bryozoa on disarticulated bivalve shells from Todos os Santos Bay, northeastern Brazil, with the description of two new species.

As sessile organisms, bryozoans are among the commonest components of the encrusting communities on hard substrata. On unconsolidated bottoms, benthic animals and their carapaces, including mollusk shells, represent potential surfaces for encrustation. Here we describe the bryozoan fauna growing on disarticulated bivalve shells collected intertidally on Itaparica beach, Todos os Santos Bay, northeast Brazil. We examined a total of 382 valves representing seven species of bivalves, among which we found 82 valves of three bivalve species to be encrusted by bryozoans, with 109 bryozoan colonies detected overall. We identified 11 cheilostome bryozoan species, among which Phidoloporidae and Smittinidae were the most diverse, with four and two species, respectively. We redescribed two bryozoan species, Parasmittina loxoides and Rhynchozoon phrynoglossum, and describe another two, Pleurocodonellina marcusi n. sp. and Rhynchozoon itaparicaensis n. sp., as new. A new combination for Cribella triangulata Canu Bassler, 1928 is proposed, including Calyptotheca tenuata Harmer, 1957 as a new junior subjective synonym of Calyptotheca triangulata n. comb. All but one of the 11 species have encrusting colonies; Licornia aff. diadema, forms erect branching colonies. For seven of the bryozoans, ours are the first records of these species growing on shells. Although the majority of bryozoans we studied have also been reported on other substrata, Rhynchozoon brasiliensis and Parasmittina loxoides were predominant in the fauna, comprising 79 (72%) of all colonies inventoried. Due to the lack of information on the distribution of these species in northeastern Brazil, further studies are needed to determine whether they show any substratum preference.

Non-native marine bryozoans (Bryozoa: Gymnolaemata) in Brazilian waters: Assessment, dispersal and impacts.

Bryozoa is a phylum of aquatic invertebrates widely distributed around the world, including harbor areas. They have association to artificial structures as main mechanism of dispersal, including ships, which facilitates their introduction to new environments. The detection of exotic species is important to prevent new introductions and to propose management strategies of marine areas. Thus, after analyzing and discussing local and global criteria of exotic species, an account of exotic bryozoans from Brazil is presented, including 12 classified as exotic (six established and six detected) and 17 classified as potentially exotic (cryptogenic). Three species have been reported causing economic or environmental impacts worldwide. Of those, Membraniporopsis tubigera is known to cause economic impacts on the Brazilian coast. Hull fouling is the main dispersal mechanism for exotic bryozoans. The lacking of reliable data did not allow inferring on the exotic status on some fouling bryozoan species in Brazil.

Taxonomy of intertidal cheilostome Bryozoa of Maceió, northeastern Brazil. Part 1: Suborders Inovicellina, Malacostegina and Thalamoporellina.

Thirteen cheilostome bryozoan species from intertidal habitats of Maceió, Alagoas State, Brazil, are reported here. We describe four new species: Aetea cultrata n. sp., Biflustra marcusi n. sp., Biflustra sphinx n. sp. and Jellyella brasiliensis n. sp. Two other species of Inovicellina, Aetea arcuata Winston & Hayward, 2012, and Aetea curta Jullien, 1888, and four species of Malacostegina, Arbocuspis bellula (Hincks, 1881), Arbocuspis bicornis (Hincks, 1881), Arbocuspis ramosa (Osburn, 1940), and Jellyella tuberculata (Bosc, 1802), are reported on drift algae. Three species of Thalamoporellina are found for the first time in Maceió, Labioporella tuberculata Winston, Vieira & Woollacoot, 2014, Steginoporella           magnilabris (Busk, 1854) and Thalamoporella floridana Osburn, 1940.