How modularity and heterotrophy complicate the understanding of the causes of thermal performance curves: the case of feeding rate in a filter-feeding animal.

Warming global temperatures have consequences for biological rates. Feeding rates reflect the intake of energy that fuels survival, growth and reproduction. However, temperature can also affect food abundance and quality, as well as feeding behavior, which all affect feeding rate, making it challenging to understand the pathways by which temperature affects the intake of energy. Therefore, we experimentally assessed how clearance rate varied across a thermal gradient in a filter-feeding colonial marine invertebrate (the bryozoan Bugula neritina). We also assessed how temperature affects phytoplankton as a food source, and zooid states within a colony that affect energy budgets and feeding behavior. Clearance rate increased linearly from 18°C to 32°C, a temperature range that the population experiences most of the year. However, temperature increased algal cell size, and decreased the proportion of feeding zooids, suggesting indirect effects of temperature on clearance rates. Temperature increased polypide regression, possibly as a stress response because satiation occurred quicker, or because phytoplankton quality declined. Temperature had a greater effect on clearance rate per feeding zooid than it did per total zooids. Together, these results suggest that the effect of temperature on clearance rate at the colony level is not just the outcome of individual zooids feeding more in direct response to temperature but also emerges from temperature increasing polypide regression and the remaining zooids increasing their feeding rates in response. Our study highlights some of the challenges for understanding why temperature affects feeding rates, especially for understudied, yet ecologically important, marine colonial organisms.

To be a transit link: Similarity in the structure of colonial system of integration and communication pores in autozooids and avicularia of Terminoflustra membranaceotruncata (Bryozoa: Cheilostomata).

Bryozoan colonies consist of zooids, which can differ in structure and function. Most heteromorphic zooids are unable to feed and autozooids supply them with nutrients. The structure of the tissues providing nutrient transfer is poorly investigated. Here, I present a detailed description of the colonial system of integration (CSI) and communication pores in autozooids and avicularia of the cheilosome bryozoan Terminoflustra membranaceotruncata. The CSI is the nutrient transport and distribution system in the colony. In both autozooids and avicularia it consists of a single cell type, that is, elongated cells, and has a variable branching pattern, except for the presence of a peripheral cord. The general similarity in the CSI structure in avicularia and autozooids is probably due to the interzooidal type of the avicularium. Interzooidal avicularia are likely to consume only a part of the nutrients delivered to them by the CSI, and they transit the rest of the nutrients further. The variability and irregularity of branching pattern of the CSI may be explained by the presence of single communication pores and their varying number. The structure of communication pores is similar regardless of their location (in the transverse or lateral wall) and the type of zooid in contact. Rosette complexes include a cincture cell, a few special cells, and a few limiting cells. Along each zooidal wall, there are communication pores with both unidirectional and bidirectional polarity of special cells. However, the total number of nucleus-containing lobes of special cells is approximately the same on each side of any zooidal wall. Supposing the polarity of special cells reflects the direction of nutrient transport, the pattern of special cells polarity is probably related to the need for bidirectional transport through each zooidal wall. The possibility for such transport is important in large perennial colonies with wide zones of autozooids undergoing polypide degeneration.

Planktonic Duration of the Bryozoan Cyphonautes Larva and Limits on Growth Rate Imposed by Its Form-Limited Maximum Clearance Rate.

AbstractThe form of the cyphonautes larva of bryozoans changes little during development. The ciliated band that generates the feeding current increases nearly in proportion to body length, so that the maximum rate of clearing planktonic food from a volume of water becomes increasingly low relative to body protein. This development is unlike the other larvae that produce a feeding current with bands of simple cilia. The cyphonautes' growth rate has therefore been predicted to be unusually low when food is scarce. As predicted, cyphonautes larvae of a species of Membranipora starved at concentrations of food that supported growth of pluteus larvae. Comparisons between the cyphonautes and plutei of a sand dollar were for growth from first feeding to metamorphosis, with a mix of two algal species. Another comparison was for growth of cyphonautes at an advanced stage and plutei of a regular sea urchin at an early stage, with food in seawater at a reduced concentration. The low maximum clearance rate did not prevent rapid growth and development of some cyphonautes from egg through metamorphosis when food was abundant. Twenty-nine days for development to metamorphosis in the laboratory with abundant food was close to Yoshioka's estimate of larval duration from the time lag between adult zooid density and larval abundance in a population in the Southern California Bight. Despite individual variation in growth rates and other physiological and environmental influences, simple measures of larval form predicted the differences in larval performance: scarce food extended larval duration for the cyphonautes more than for plutei.

Further species and range extensions of Amazonian bryozoans: chipping away at the iceberg.

A bryozoan survey conducted in the Amazon Basin in the vicinities of Manaus and Santarm during the high water season (May, 2018) revealed four new species described here: Fredericella adrianoi n. sp., Plumatella divae n. sp., Plumatella hartikainenae n. sp., and Plumatella spencerjonesae n. sp. Two of these species were encountered only once, suggesting that other undescribed species are likely to occur in the area. Range extensions were determined for two additional species: Plumatella pirassununga and Timwoodiellina natans. In addition, colonies were collected for the first time for two species previously known only by their statoblasts: Plumatella siolii and Plumatella marcusi. Statoblasts of Tapajosella elongata were encountered near Manaus, but the colonies remained elusive. The discovery of new species collected during two expeditions to the Amazon Basin in different seasons and years suggests that further diversity remains undetected in this and other poorly studied regions of the world. With few exceptions, plumatellid colonies described so far from the Amazon Basin are very similar in appearance, with branches wholly attached to the substratum and body walls that are soft, colorless, and transparent.

Metabolism drives demography in an experimental field test.

Metabolism should drive demography by determining the rates of both biological work and resource demand. Long-standing "rules" for how metabolism should covary with demography permeate biology, from predicting the impacts of climate change to managing fisheries. Evidence for these rules is almost exclusively indirect and in the form of among-species comparisons, while direct evidence is exceptionally rare. In a manipulative field experiment on a sessile marine invertebrate, we created experimental populations that varied in population size (density) and metabolic rate, but not body size. We then tested key theoretical predictions regarding relationships between metabolism and demography by parameterizing population models with lifetime performance data from our field experiment. We found that populations with higher metabolisms had greater intrinsic rates of increase and lower carrying capacities, in qualitative accordance with classic theory. We also found important departures from theory-in particular, carrying capacity declined less steeply than predicted, such that energy use at equilibrium increased with metabolic rate, violating the long-standing axiom of energy equivalence. Theory holds that energy equivalence emerges because resource supply is assumed to be independent of metabolic rate. We find this assumption to be violated under real-world conditions, with potentially far-reaching consequences for the management of biological systems.

Bryozoa from the reefs off the Amazon River mouth: checklist, thirteen new species, and notes on their ecology and distribution.

The reef system off the Amazon River mouth extends from Amapá state to Maranhão state along the Brazilian Equatorial Margin, encompassing more than 10,000 km2 of rhodolith beds and high-relief hard structures on the outer shelf and upper slope. This unique hard bottom mosaic is remarkable for being influenced by the turbid and hyposaline plume from the world's largest river, and also for representing a connectivity corridor between the Caribbean and Brazil. Bryozoans were recently recognized as major reef builders in the Southwestern Atlantic, but their diversity off the Amazon River mouth remained unknown. Here, we report on recent collections obtained from 23 to 120 m depth in Northern Brazil. Sixty-five bryozoan taxa were characterized using scanning electron microscopy, including 57, five and three taxa of Cheilostomatida, Cyclostomatida and Ctenostomatida, respectively. Cribrilaria smitti and three genera (Cranosina, Glabrilaria and Thornelya) are new records for Brazil, and 13 new species are herein described: Antropora cruzeiro n. sp., Cranosina gilbertoi n. sp., Cribrilaria lateralis n. sp., Crisia brasiliensis n. sp., Glabrilaria antoniettae n. sp., Micropora amapaensis n. sp., Parasmittina amazonensis n. sp., Plesiocleidochasma arcuatum n. sp., Poricella bifurcata n. sp., Pourtalesella duoavicularia n. sp., Stephanollona domuspusilla n. sp., Therenia dianae n. sp., and Thornelya atlanticoensis n. sp. Our results highlight the biodiversity significance of the Amazon reefs and the need for more comprehensive sampling to clarify the role of bryozoans in modern turbid-zone reefs and rhodolith beds.

Peculiarities of Tentacle Innervation of Flustrellidra hispida and Evolution of Lophophore in Bryozoa.

The study of the lophophore organization is of great importance for the reconstruction of lophophorate phylogeny and for understanding the evolutionary transformation in each phylum of Lophophorata. The innervation of the lophophore in ctenostome bryozoan Flustrellidra hispida was studied using immunocytochemistry and confocal laser scanning microscopy. It has been demonstrated that this species has an outer nerve ring giving rise to the tentacle nerves. The outer nerve ring was earlier described in some ctenostomates and cyclostomates, but not as connected with nerves. The discovered feature of lophophore innervation in F. hispida suggests the evolutionary transformation from a hypothetical phoronida-like ancestor lophophore bearing a prominent outer nerve ring with numerous tentacle nerves emanating from it, to the complex bell-shaped lophophore of F. hispida with a well-pronounced outer nervous ring bearing a few tentacle nerves. The next one in this hypothetical row is the lophophore of the other ctenostomates and some cyclostomates with no ring-nerve connection and cheilostomates lophophore with no outer nerve ring at all.

Artificial habitats induce plasticity in colonies of the marine bryozoan Schizoporella errata.

Modular organization provides flexibility for colonial animals to deal with variable and unpredictable environmental conditions since each module has specific tasks within the colony, such as feeding, defending or reproducing. Depending on the selecting pressures, sessile organisms may phenotypically adjust the morphology of each module or modify their density, increasing individual fitness. Here we used the marine bryozoan Schizoporella errata (Cheilostomata, Schizoporellidae) to test how the divergent conditions between two artificial habitats, the location inside a marina (IM) and the external wall of the breakwater (BW), affect colony size and the density of the distinct modules. The density of avicularia and ovicells, modules related to defense and reproduction, respectively, did not differ between habitats. However, colonies growing in the turbulent waters of BW were, in general, larger and had higher density of feeding autozooids than those at IM. Reciprocal transplants of bryozoan clones indicated that trait variation is genotype-dependent but varies according to the environmental conditions at the assigned location. The occurrence of larger colonies with more zooids in BW is probably linked to the easier feeding opportunity offered by the small diffusive boundary layer around the colony at this location. Since in colonial polymorphic organisms each module (zooid) performs a specific function, the phenotypic response is not uniform across colonies, affecting only those modules that are susceptible to variations in the main selective pressures. Understanding the importance of colony-level plasticity is relevant to predict how modularity will contribute to organisms to deal with human-induced environmental changes in coastal habitats.

Global Distribution and Variation of the Invasive Cheilostome Bryozoan Cribrilina mutabilis.

Viable populations of the cheilostome bryozoan Cribrilina mutabilis Ito, Onishi & Dick exist in the NW Pacific (Russian Far East and northern Japan), NE Atlantic (Scandinavia and Scotland), and NW Atlantic (Maine, USA). The first NE and NW Atlantic records are from Norway (2008) and Casco Bay, Maine, USA (2018), respectively, indicating a relatively recent introduction to the region. Mitochondrial COI gene sequences from North Atlantic populations (Sweden, Norway, and Maine) showed two haplotypes differing by one substitution, but differed from two haplotypes from Akkeshi, northern Japan, by 6-8 substitutions. North Atlantic populations differed morphologically from the Akkeshi population in that some zooids formed a suboral projection, and frontal zooids were more common. While C. mutabilis in northern Japan has been found only on natural or artificial eelgrass (Zostera marina), across its range it has been found on several species of algae, plastic panels and strips, several species of Zostera, and mollusc shells. Similar frequencies of heteromorphic zooids with differing degree of frontal wall calcification, i.e., R (rib)-, I (intermediate)-, and S (shield)-type zooids, in colonies on eelgrass at comparable times of the season and across populations suggest an innate response to seasonal environmental fluctuations, although zooid frequencies were different on non-eelgrass substrates. The increase in trans-Arctic shipping along the Northern Sea Route in recent decades, and previous documentation of C. mutabilis on ship hulls in the Sea of Japan, indicate a clear mechanism for anthropogenic introduction from the Far East to Europe in recent decades.

Key novelties in the evolution of the aquatic colonial phylum Bryozoa: evidence from soft body morphology.

Molecular techniques are currently the leading tools for reconstructing phylogenetic relationships, but our understanding of ancestral, plesiomorphic and apomorphic characters requires the study of the morphology of extant forms for testing these phylogenies and for reconstructing character evolution. This review highlights the potential of soft body morphology for inferring the evolution and phylogeny of the lophotrochozoan phylum Bryozoa. This colonial taxon comprises aquatic coelomate filter-feeders that dominate many benthic communities, both marine and freshwater. Despite having a similar bauplan, bryozoans are morphologically highly diverse and are represented by three major taxa: Phylactolaemata, Stenolaemata and Gymnolaemata. Recent molecular studies resulted in a comprehensive phylogenetic tree with the Phylactolaemata sister to the remaining two taxa, and Stenolaemata (Cyclostomata) sister to Gymnolaemata. We plotted data of soft tissue morphology onto this phylogeny in order to gain further insights into the origin of morphological novelties and character evolution in the phylum. All three larger clades have morphological apomorphies assignable to the latest molecular phylogeny. Stenolaemata (Cyclostomata) and Gymnolaemata were united as monophyletic Myolaemata because of the apomorphic myoepithelial and triradiate pharynx. One of the main evolutionary changes in bryozoans is a change from a body wall with two well-developed muscular layers and numerous retractor muscles in Phylactolaemata to a body wall with few specialized muscles and few retractors in the remaining bryozoans. Such a shift probably pre-dated a body wall calcification that evolved independently at least twice in Bryozoa and resulted in the evolution of various hydrostatic mechanisms for polypide protrusion. In Cyclostomata, body wall calcification was accompanied by a unique detachment of the peritoneum from the epidermis to form the hydrostatic membraneous sac. The digestive tract of the Myolaemata differs from the phylactolaemate condition by a distinct ciliated pylorus not present in phylactolaemates. All bryozoans have a mesodermal funiculus, which is duplicated in Gymnolaemata. A colonial system of integration (CSI) of additional, sometimes branching, funicular cords connecting neighbouring zooids via pores with pore-cell complexes evolved at least twice in Gymnolaemata. The nervous system in all bryozoans is subepithelial and concentrated at the lophophoral base and the tentacles. Tentacular nerves emerge intertentacularly in Phylactolaemata whereas they partially emanate directly from the cerebral ganglion or the circum-oral nerve ring in myolaemates. Overall, morphological evidence shows that ancestral forms were small, colonial coelomates with a muscular body wall and a U-shaped gut with ciliary tentacle crown, and were capable of asexual budding. Coloniality resulted in many novelties including the origin of zooidal polymorphism, an apomorphic landmark trait of the Myolaemata.

Invasive marine species discovered on non-native kelp rafts in the warmest Antarctic island.

Antarctic shallow coastal marine communities were long thought to be isolated from their nearest neighbours by hundreds of kilometres of deep ocean and the Antarctic Circumpolar Current. The discovery of non-native kelp washed up on Antarctic beaches led us to question the permeability of these barriers to species dispersal. According to the literature, over 70 million kelp rafts are afloat in the Southern Ocean at any one time. These living, floating islands can play host to a range of passenger species from both their original coastal location and those picked in the open ocean. Driven by winds, currents and storms towards the coast of the continent, these rafts are often cited as theoretical vectors for the introduction of new species into Antarctica and the sub-Antarctic islands. We found non-native kelps, with a wide range of "hitchhiking" passenger organisms, on an Antarctic beach inside the flooded caldera of an active volcanic island. This is the first evidence of non-native species reaching the Antarctic continent alive on kelp rafts. One passenger species, the bryozoan Membranipora membranacea, is found to be an invasive and ecologically harmful species in some cold-water regions, and this is its first record from Antarctica. The caldera of Deception Island provides considerably milder conditions than the frigid surrounding waters and it could be an ideal location for newly introduced species to become established. These findings may help to explain many of the biogeographic patterns and connections we currently see in the Southern Ocean. However, with the impacts of climate change in the region we may see an increase in the range and number of organisms capable of surviving both the long journey and becoming successfully established.

How colonial animals evolve.

The evolution of modular colonial animals such as reef corals and bryozoans is enigmatic because of the ability for modules to proliferate asexually as whole colonies reproduce sexually. This reproductive duality creates an evolutionary tension between modules and colonies because selection operates at both levels. To understand how this evolutionary conflict is resolved, we compared the evolutionary potential of module- and colony-level traits in two species of the bryozoan Stylopoma, grown and bred in a common garden experiment. We find quantitatively distinct differences in the evolutionary potential of modular and colony traits. Contrary to solitary organisms, individual traits are not heritable from mother to daughter modules, but colony traits are strongly heritable from parent to offspring colonies. Colony-level evolution therefore dominates because no evolutionary change can accumulate among its modules.

Architecture of Anoteropora latirostris (Bryozoa, Cheilostomata) and implications for their biomineralization.

Cheilostome Bryozoa Anoteropora latirostris, a colonial marine invertebrate, constructs its skeleton from calcite and aragonite. This study presents firstly correlated multi-scale electron microscopy, micro-computed tomography, electron backscatter diffraction and NanoSIMS mapping. We show that all primary, coarse-grained platy calcitic lateral walls are covered by fine-grained fibrous aragonite. Vertical lateral walls separating autozooid chambers have aragonite only on their distal side. This type of asymmetric mineralization of lateral walls results from the vertical arrangement of the zooids at the growth margins of the colony and represents a type of biomineralization previously unknown in cheilostome bryozoans. NanoSIMS mapping across the aragonite-calcite interface indicates an organic layer between both mineral phases, likely representing an organic template for biomineralization of aragonite on the calcite layer. Analysis of crystallographic orientations show a moderately strong crystallographic preferred orientation (CPO) for calcite (7.4 times random orientation) and an overall weaker CPO for aragonite (2.4 times random orientation) with a high degree of twinning (45%) of the aragonite grains. The calculated Young's modulus for the CPO map shows a weak mechanical direction perpendicular to the colony's upper surface facilitating this organism's strategy of clonal reproduction by fragmentation along the vertical zooid walls.

Can competitive asymmetries maintain offspring size variation? A manipulative field test.

Offspring sizes vary within populations but the reasons are unclear. Game-theoretic models predict that selection will maintain offspring-size variation when large offspring are superior competitors (i.e., competition is asymmetric), but small offspring are superior colonizers. Empirical tests are equivocal, however, and typically rely on interspecific comparisons, whereas explicit intraspecific tests are rare. In a field study, we test whether offspring size affects competitive asymmetries using the sessile marine invertebrate, Bugula neritina. Surprisingly, we show that offspring size determines whether interactions are competitive or facilitative-large neighbors strongly facilitated small offspring, but also strongly competed with large offspring. These findings contradict the assumptions of classic theory-that is, large offspring were not superior competitors. Instead, smaller offspring actually benefit from interactions with large offspring-suggesting that asymmetric facilitation, rather than asymmetric competition, operates in our system. We argue that facilitation of small offspring may be more widespread than currently appreciated, and may maintain variation in offspring size via negative frequency-dependent selection. Offspring size theory has classically viewed offspring interactions through the lens of competition alone, yet our results and those of others suggest that theory should accommodate positive interactions in explorations of offspring-size variation.

Body cavities in bryozoans: Functional and phylogenetic implications.

Based on morphological evidence, Bryozoa together with Phoronida and Brachiopoda are traditionally combined in the group Lophophorata, although this view has been recently challenged by molecular studies. The core of the concept lies in the presence of the lophophore as well as the nature and arrangement of the body cavities. Bryozoa are the least known in this respect. Here, we focused on the fine structure of the body cavity in 12 bryozoan species: 6 gymnolaemates, 3 stenolaemates and 3 phylactolaemates. In gymnolaemates, the complete epithelial lining of the body cavity is restricted to the lophophore, gut walls, and tentacle sheath. By contrast, the cystid walls are composed only of the ectocyst-producing epidermis without a coelothelium, or an underlying extracellular matrix; only the storage cells and cells of the funicular system contact the epidermis. The nature of the main body cavity in gymnolaemates is unique and may be considered as a secondarily modified coelom. In cyclostomes, both the lophophoral and endosaccal cavities are completely lined with coelothelium, while the exosaccal cavity only has the epidermis along the cystid wall. In gymnolaemates, the lophophore and trunk cavities are divided by an incomplete septum and communicate through two pores. In cyclostomes, the septum has a similar location, but no openings. In Phylactolaemata, the body cavity is undivided: the lophophore and trunk coeloms merge at the bases of the lophophore arms, the epistome cavity joins the trunk, and the forked canal opens into the arm coelom. The coelomic lining of the body is complete except for the epistome, lophophoral arms, and the basal portions of the tentacles, where the cells do not interlock perfectly (this design probably facilitates the ammonia excretion). The observed partitioning of the body cavity in bryozoans differs from that in phoronids and brachiopods, and contradicts the Lophophorata concept.

Impact of environmental variables on fouling bryozoan species in the Eastern Aegean Sea.

Bryozoans are the major component of marine macro-fouling communities. In the study, the relations between bryozoan species and environmental variables were investigated at seven stations along the Aegean coast in August and December 2015. Constant bryozoan species in both sampling periods were Bugula neritina, Amathia verticillata, Shizoporella errata, Cryptosula pallasiana and Celleporaria brunnea. Their relationship with physico-chemical variables (Temperature, salinity, pH, dissolved oxygen, ammonium, nitrite and nitrate nitrogen, orthophosphate phosphorous, total phosphate, chlorophyll-a) were analysed by means of logistic regression analysis. The result showed that temperature with B. neritina; NH4-N, oPO4-P and TPO4-P with A verticillata; dissolved oxygen concentrations with S. errata and C. brunnea were positively related (p < 0.05).

Text-mined fossil biodiversity dynamics using machine learning.

Documented occurrences of fossil taxa are the empirical foundation for understanding large-scale biodiversity changes and evolutionary dynamics in deep time. The fossil record contains vast amounts of understudied taxa. Yet the compilation of huge volumes of data remains a labour-intensive impediment to a more complete understanding of Earth's biodiversity history. Even so, many occurrence records of species and genera in these taxa can be uncovered in the palaeontological literature. Here, we extract observations of fossils and their inferred ages from unstructured text in books and scientific articles using machine-learning approaches. We use Bryozoa, a group of marine invertebrates with a rich fossil record, as a case study. Building on recent advances in computational linguistics, we develop a pipeline to recognize taxonomic names and geologic time intervals in published literature and use supervised learning to machine-read whether the species in question occurred in a given age interval. Intermediate machine error rates appear comparable to human error rates in a simple trial, and resulting genus richness curves capture the main features of published fossil diversity studies of bryozoans. We believe our automated pipeline, that greatly reduced the time required to compile our dataset, can help others compile similar data for other taxa.

Biodiversity and antifouling activity of fungi associated with two soft corals from the South China Sea.

Bacteria in corals have been studied in detail in the past decades. However, the biodiversity and bioactivity of fungi in corals are still poorly understood. This study investigated the biodiversity and antifouling activity of fungi in soft corals Cladiella krempfi and Sarcophyton tortuosum from the South China Sea. A high diverse and abundant fungal community was found in the two soft corals. Furthermore, five isolates shared 83-95% similarity with their closest relatives, indicating that they might be novel species in genera Phaeoshaeria and Mucor. In addition, approximately 50% of the representative isolates exhibited distinct antifouling activity. In particular, isolates Fungal sp. SCAU132 and Fungal sp. SCAU133 displayed very strong antifouling activity against Bugula neritina, suggesting they can provide a potential resource for further investigation on isolation of novel antifouling metabolites. To our knowledge, this study is the first report to investigate the biodiversity and antifouling activity of fungi in C. krempfi and S. tortuosum.

Marinas: An overlooked habitat for exploring the relation among polychaete assemblages and environmental factors.

The increasing number of anthropogenic areas in the marine environment results in significant impact to adjacent ecosystems. In fact, the presence of marinas modifies the original environmental conditions and ends up disturbing the faunal community. However, despite the essential role displayed by the macrofauna on marinas' fouling biota, certain taxa such as polychaetes have been poorly studied. The present study provides the first spatial characterization of the epibiont polychaete fauna associated with the bryozoan Bugula neritina in marinas along the Iberian Peninsula and the north of Morocco. A total of 32 polychaete species were identified, with Syllidae being the most diverse family. Furthermore, the environmental factors involved in the occurrence and abundance of the dominant species Salvatoria clavata were also analyzed by Generalized Linear Models; results showed that the highest predicted values of S. clavata abundance appeared at marinas with high levels of nutrient enrichment and of heavy metals concentration.

Sexual reproduction of the placental brooder Celleporella hyalina (Bryozoa, Cheilostomata) in the White Sea.

The evolution of parental care is a central field in many ecological and evolutionary studies, but integral approaches encompassing various life-history traits are not common. Else, the structure, development and functioning of the placental analogues in invertebrates are poorly understood. Here, we describe the life-history, sexual colony dynamics, oogenesis, fertilization and brooding in the boreal-Arctic cheilostome bryozoan Celleporella hyalina. This placental brooder incubates its progeny in calcified protective chambers (ovicells) formed by polymorphic sexual zooids. We conducted a detailed ultrastructural study of the ovary and oogenesis, and provide evidence of both auto- and heterosynthetic mechanisms of vitellogenesis. We detected sperm inside the early oocyte and within funicular strands, and discuss possible variants of fertilization. We also detail the development and functioning of the placental analogue (embryophore) in the various stages of embryonic incubation as well as embryonic histotrophic nourishment. In contrast to all known cheilostome placentas, the main part of embryophore of C. hyalina is not a single cell layer. Rather, it is a massive "nutritive tissue" whose basal part is associated with funicular strands presumably providing transport function. C. hyalina shows a mixture of reproductive traits with macrolecithal oogenesis and well-developed placenta. These features give it an intermediate position in the continuum of variation of matrotrophic provisioning between lecithotrophic and placentotrophic cheilostome brooders. The structural and developmental differences revealed in the placental analogue of C. hyalina, together with its position on the bryozoan molecular tree, point to the independent origin of placentation in the family Hippothoidae.