Developmental Process of a Heterozooid: Avicularium Formation in a Bryozoan, Bugulina californica.

In bryozoans (phylum Bryozoa), representative colonial animals mostly found in marine environments, some species possess different types of individuals (heterozooids) specialized in different functions such as defense or structural support for their colonies. Among them, the best-known heterozooids are the avicularia, known to function as defenders. The differentiation processes of heterozooids, including avicularia, should be important keys to understand the evolutionary significance of bryozoans. However, the developmental process of avicularium formation remains to be fully understood. In this study, therefore, in order to understand the detailed developmental process and timing of avicularium formation, extensive observations were carried out in a bryozoan species, Bugulina californica (Cheilostomata, Bugulidae), that possesses adventitious avicularia, by performing stereomicroscopy on live materials, in addition to scanning electron microscopy and histological observations. The whole process can be divided into seven stages based on developmental events. Especially notably, at the earlier stages, there are three major budding events that produce proliferating cell masses corresponding to primordial tissues: (1) budding of the peduncle cushion at the outer margin of the distal part of a young autozooid, (2) budding of the head-part primordium from the peduncle cushion, and (3) budding of the polypide inside the head part. Experimental control of temperature showed that 20°C would be the best to maintain B. californica colonies.

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.

Megabenthic communities of the Ligurian deep continental shelf and shelf break (NW Mediterranean Sea).

The Ligurian Sea is one of the most studied Mediterranean basins. Since the beginning of the last century, many research expeditions have characterized its benthic and pelagic fauna through scuba diving and trawl surveys. However, a large knowledge gap exists about the composition of benthic communities extending into the so-called mesophotic or twilight depth range, currently under intense pressure from commercial and recreational fishing. A series of visual surveys, carried out by means of remotely operated vehicles between 2012 and 2018, were conducted along the Ligurian deep continental shelf and shelf break, between 30 and 210 m depth, in order to characterize the main benthic biocoenoses dwelling at this depth range and to determine the most relevant environmental factors that explain their spatial distribution. Deep circalittoral communities of the Ligurian Sea were represented by a mixture of species belonging to the deepest extension of shallow-water habitats and deep circalittoral ones. Twelve major biocoenoses were identified, each one characterized by specific preferences in depth range, substrate type and seabed slope. Those biocoenoses included gorgonian and hydrozoan forests, dense keratose sponge grounds, Dendrophyllia cornigera gardens, bryozoan beds and soft-bottom meadows of sabellid polychaetes and soft-corals. Other less common aggregations included six forests of black corals and two populations of Paramuricea macrospina. A georeferenced database has been created in order to provide information to managers and stakeholders about the location of the identified communities and high-diversity areas, aiming to facilitate sustainable long-term conservation of the Ligurian benthic ecosystem.

Assemblage of encrusting organisms on floating anthropogenic debris along the northern coast of the Persian Gulf.

Global concern about floating marine debris and its fundamental role in shaping coastal biodiversity is growing, yet there is very little knowledge about debris-associated rafting communities in many areas of the world's oceans. In the present study, we examined the encrusting assemblage on different types of stranded debris (wood, plastic, glass, and metal cans) along the Iranian coast of the Persian Gulf. In total, 21 taxa were identified on 132 items. The average frequency of occurrence (±SE) across all sites and stranded debris showed that the barnacle Amphibalanus amphitrite (68.9 ±â€¯1.1%), the oyster Saccostrea cucullata (40.9 ±â€¯0.7%), the polychaete Spirobranchus kraussii (27.3 ±â€¯0.5%), green algae (22 ±â€¯0.5%) and the coral Paracyathus stokesii (14.4 ±â€¯0.7%) occurred most frequently. Relative substratum coverage was highest for A. amphitrite (44.3 ±â€¯2.7%), followed by green algae (14.4 ±â€¯1.5%), Spirobranchus kraussii (9.3 ±â€¯1.3%), Saccostrea cucullata (7.6 ±â€¯1.3%) and the barnacle Microeuraphia permitini (5.8 ±â€¯0.9%). Despite the significant difference in coverage of rafting species on plastic items among different sites, there was no clear and consistent trend of species richness and coverage from the eastern (Strait of Hormuz) to the western part of the Persian Gulf. Some rafting species (bryozoans and likely barnacles) were found to be non-indigenous species in the area. As floating marine debris can transport non-indigenous species and increase the risk of bio-invasions to this already naturally- and anthropogenically-stressed water body, comprehensive monitoring efforts should be made to elucidate the vectors and arrival of new invasive species to the region.

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.

Metal pollution affects both native and non-indigenous biofouling recruitment in a subtropical island system.

Hull fouling has been a driving force behind the development of most modern marine antifouling coatings that mainly contain copper based biocides to inhibit growth of fouling organisms. Despite these efforts, several non-indigenous species continue to be transferred via hull-fouling worldwide. In this study we designed a disturbance gradient with three commercial antifouling paints applied to PVC settling plates with different concentrations of copper oxide and allowed colonization of fouling communities in four marinas located at the Madeira Archipelago (NE Atlantic). Overall, the antifouling treatments were effective in decreasing the diversity of fouling communities and spatial variability across marinas was observed. Increasing exposure to metal pollutants decreases both species cover and total diversity, independently of their native or NIS condition. However, evidences found suggest that long-term effects of copper based antifouling coatings can be modulated by metal-resistant species allowing a secondary substrate for the epibiosis of other species to establish.

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.

Diversity and Dynamics of "Candidatus Endobugula" and Other Symbiotic Bacteria in Chinese Populations of the Bryozoan, Bugula neritina.

Bugula neritina is a common invasive cosmopolitan bryozoan that harbors (like many sessile marine invertebrates) a symbiotic bacterial (SB) community. Among the SB of B. neritina, "Candidatus Endobugula sertula" continues to receive the greatest attention, because it is the source of bryostatins. The bryostatins are potent bioactive polyketides, which have been investigated for their therapeutic potential to treat various cancers, Alzheimer's disease, and AIDS. In this study, we compare the metagenomics sequences for the 16S ribosomal RNA gene of the SB communities from different geographic and life cycle samples of Chinese B. neritina. Using a variety of approaches for estimating alpha/beta diversity and taxonomic abundance, we find that the SB communities vary geographically with invertebrate and fish mariculture and with latitude and environmental temperature. During the B. neritina life cycle, we find that the diversity and taxonomic abundances of the SB communities change with the onset of host metamorphosis, filter feeding, colony formation, reproduction, and increased bryostatin production. "Ca. Endobugula sertula" is confirmed as the symbiont of the Chinese "Ca. Endobugula"/B. neritina symbiosis. Our study extends our knowledge about B. neritina symbiosis from the New to the Old World and offers new insights into the environmental and life cycle factors that can influence its SB communities, "Ca. Endobugula," and bryostatins more globally.

HSP90 regulates larval settlement of the bryozoan Bugula neritina through the nitric oxide pathway.

The larvae of many sessile marine invertebrates go through a settlement process, during which planktonic larvae attach to a substrate and metamorphose into sessile juveniles. Larval attachment and metamorphosis (herein defined as 'settlement') are complex processes mediated by many signalling pathways. Nitric oxide (NO) signalling is one of the pathways that inhibits larval settlement in marine invertebrates across different phyla. NO is synthesized by NO synthase (NOS), which is a client of the molecular chaperone heat shock protein 90 (HSP90). In the present study, we provide evidence that NO, a gaseous messenger, regulates larval settlement of Bugula neritina By using pharmacological bioassays and western blotting, we demonstrated that NO inhibits larval settlement of B. neritina and that NO signals occur mainly in the sensory organ of swimming larvae. The settlement rate of B. neritina larvae decreased after heat shock treatment. Inhibition of HSP90 induced larval settlement, and attenuated the inhibition of NO donors during larval settlement. In addition, the expression level of both HSP90 and NOS declined upon settlement. These results demonstrate that HSP90 regulates the larval settlement of B. neritina by interacting with the NO pathway.

Warming by 1°C Drives Species and Assemblage Level Responses in Antarctica's Marine Shallows.

Forecasting assemblage-level responses to climate change remains one of the greatest challenges in global ecology [1, 2]. Data from the marine realm are limited because they largely come from experiments using limited numbers of species [3], mesocosms whose interior conditions are unnatural [4], and long-term correlation studies based on historical collections [5]. We describe the first ever experiment to warm benthic assemblages to ecologically relevant levels in situ. Heated settlement panels were used to create three test conditions: ambient and 1°C and 2°C above ambient (predicted in the next 50 and 100 years, respectively [6]). We observed massive impacts on a marine assemblage, with near doubling of growth rates of Antarctic seabed life. Growth increases far exceed those expected from biological temperature relationships established more than 100 years ago by Arrhenius. These increases in growth resulted in a single "r-strategist" pioneer species (the bryozoan Fenestrulina rugula) dominating seabed spatial cover and drove a reduction in overall diversity and evenness. In contrast, a 2°C rise produced divergent responses across species growth, resulting in higher variability in the assemblage. These data extend our ability to expand, integrate, and apply our knowledge of the impact of temperature on biological processes to predict organism, species, and ecosystem level ecological responses to regional warming.

Ecologically relevant levels of multiple, common marine stressors suggest antagonistic effects.

Stressors associated with global change will be experienced simultaneously and may act synergistically, so attempts to estimate the capacity of marine systems to cope with global change requires a multi-stressor approach. Because recent evidence suggests that stressor effects can be context-dependent, estimates of how stressors are experienced in ecologically realistic settings will be particularly valuable. To enhance our understanding of the interplay between environmental effects and the impact of multiple stressors from both natural and anthropogenic sources, we conducted a field experiment. We explored the impact of multiple, functionally varied stressors from both natural and anthropogenic sources experienced during early life history in a common sessile marine invertebrate, Bugula neritina. Natural spatial environmental variation induced differences in conspecific densities, allowing us to test for density-driven context-dependence of stressor effects. We indeed found density-dependent effects. Under high conspecific density, individual survival increased, which offset part of the negative effects of experiencing stressors. Experiencing multiple stressors early in life history translated to a decreased survival in the field, albeit the effects were not as drastic as we expected: our results are congruent with antagonistic stressor effects. We speculate that when individual stressors are more subtle, stressor synergies become less common.

Interactive effects of temperature, food and skeletal mineralogy mediate biological responses to ocean acidification in a widely distributed bryozoan.

Marine invertebrates with skeletons made of high-magnesium calcite may be especially susceptible to ocean acidification (OA) due to the elevated solubility of this form of calcium carbonate. However, skeletal composition can vary plastically within some species, and it is largely unknown how concurrent changes in multiple oceanographic parameters will interact to affect skeletal mineralogy, growth and vulnerability to future OA. We explored these interactive effects by culturing genetic clones of the bryozoan Jellyella tuberculata (formerly Membranipora tuberculata) under factorial combinations of dissolved carbon dioxide (CO2), temperature and food concentrations. High CO2 and cold temperature induced degeneration of zooids in colonies. However, colonies still maintained high growth efficiencies under these adverse conditions, indicating a compensatory trade-off whereby colonies degenerate more zooids under stress, redirecting energy to the growth and maintenance of new zooids. Low-food concentration and elevated temperatures also had interactive effects on skeletal mineralogy, resulting in skeletal calcite with higher concentrations of magnesium, which readily dissolved under high CO2 For taxa that weakly regulate skeletal magnesium concentration, skeletal dissolution may be a more widespread phenomenon than is currently documented and is a growing concern as oceans continue to warm and acidify.

Ocean acidification increases larval swimming speed and has limited effects on spawning and settlement of a robust fouling bryozoan, Bugula neritina.

Few studies to date have investigated the effects of ocean acidification on non-reef forming marine invertebrates with non-feeding larvae. Here, we exposed adults of the bryozoan Bugula neritina and their larvae to lowered pH. We monitored spawning, larval swimming, settlement, and post-settlement individual sizes at two pHs (7.9 vs. 7.6) and settlement dynamics alone over a broader pH range (8.0 down to 6.5). Our results show that spawning was not affected by adult exposure (48h at pH7.6), larvae swam 32% faster and the newly-settled individuals grew significantly larger (5%) at pH7.6 than in the control. Although larvae required more time to settle when pH was lowered, reduced pH was not lethal, even down to pH6.5. Overall, this fouling species appeared to be robust to acidification, and yet, indirect effects such as prolonging the pelagic larval duration could increase predation risk, and might negatively impact population dynamics.

Anti-HSV-1, antioxidant and antifouling phenolic compounds from the deep-sea-derived fungus Aspergillus versicolor SCSIO 41502.

Chemical investigation of the deep-sea-derived fungus Aspergillus versicolor SCSIO 41502 resulted in the isolation of three new anthraquinones, aspergilols G-I (1-3), one new diphenyl ether, 4-carbglyceryl-3,3'-dihydroxy-5,5'-dimethyldiphenyl ether (4), and one new benzaldehyde derivative, 2,4-dihydroxy-6-(4-methoxy-2-oxopentyl)-3-methylbenzaldehyde (5), along with 23 known phenolic compounds (6-28). The structures of new compounds were elucidated by extensive spectroscopic analysis. The absolute configuration of 3 was established by CD spectrum and the modified Mosher method. Compounds 2, 3 and 9 had evident antiviral activity towards HSV-1 with EC50 values of 4.68, 6.25, and 3.12µM, respectively. Compounds 15, 18, 20 and 22-24 showed more potent antioxidant activity than l-ascorbic acid with IC50 values of 18.92-52.27µM towards DPPH radicals. Comparison of the structures and antioxidant activities of 1-28 suggests that the number of phenolic hydroxyl group that can freely rotate can significantly affect the antioxidant activity of phenolic compounds. In addition, 4, 22-24 and 27 had significant antifouling activity against Bugula neritina larval settlement with EC50 values of 1.28, 2.61, 5.48, 1.59, and 3.40µg/ml, respectively.

Factors influencing the en route survivorship and post-voyage growth of a common ship biofouling organism, Bugula neritina.

The likelihood that viable non-indigenous biofouling species will survive a voyage on a vessel is influenced by a range of factors, including the speed, duration, and route of the voyage and the amount of time the vessel spends in port. In this study, a land-based dynamic flow device was used to test the effect of recruit age, vessel speed and voyage duration on the survivorship and growth of the bryozoan Bugula neritina. In the experiment, one-week-old recruits had a higher likelihood (100%) of surviving voyages than older (one-month-old, 90%) or younger (one-day-old, 79%) recruits, but survival was not influenced by vessel speed (6 and 18 knots) or voyage duration (two and eight days). The results suggest that the non-indigenous species B. neritina can be effectively transferred at a range of ages but one-week-old recruits are more likely to survive the translocation process and survive in the recipient environment.

Recyclable plastics as substrata for settlement and growth of bryozoans Bugula neritina and barnacles Amphibalanus amphitrite.

Plastics are common and pervasive anthropogenic debris in marine environments. Floating plastics provide opportunities to alter the abundance, distribution and invasion potential of sessile organisms that colonize them. We selected plastics from seven recycle categories and quantified settlement of (i) bryozoans Bugula neritina (Linnaeus, 1758) in the lab and in the field, and of (ii) barnacles Amphibalanus (= Balanus) amphitrite (Darwin, 1854) in the field. In the laboratory we cultured barnacles on the plastics for 8 weeks and quantified growth, mortality, and breaking strength of the side plates. In the field all recyclable plastics were settlement substrata for bryozoans and barnacles. Settlement depended on the type of plastic. Fewer barnacles settled on plastic surfaces compared to glass. In the lab and in the field, bryozoan settlement was higher on plastics than on glass. In static laboratory rearing, barnacles growing on plastics were initially significantly smaller than on glass. This suggested juvenile barnacles were adversely impacted by materials leaching from the plastics. Barnacle mortality was not significantly different between plastic and glass surfaces, but breaking strength of side plates of barnacles on polyvinyl chloride (PVC) and polycarbonate (PC) were significantly lower than breakage strength on glass. Plastics impact marine ecosystems directly by providing new surfaces for colonization with fouling organisms and by contaminants shown previously to leach out of plastics and impact biological processes.

Two new species of the genus Turbicellepora Ryland, 1963 (Bryozoa: Celleporidae) found on Lophelia coral from the Greenland slope.

The genus Turbicellepora was established by Ryland (1963) in the course of his work on the Norwegian bryozoan fauna. At present, the genus includes 71 recent and fossil species, which have been reported from all continents and seas (Bock & Gordon 2014). The distinctive characteristics of the genus include a multiporous ooecium, proximal orificial sinus, an asymmetrically placed peristomial avicularium and enlarged or vicarious avicularia (Ryland 1963). Occasionally, an additional pre-oral avicularium is also present (Hayward 1978). Colonies have a changeable form. They can be massive and branching or have the form of a mound or flat crust. The most comprehensive comparative study of European species of the genus, with detailed descriptions of 13 taxa, was carried out by Hayward (1978), who noted that the genus seemed to be centred in the Atlanto-Mediterranean region.

Systematics and diversity of deep-water Cheilostomata (Bryozoa) from Galicia Bank (NE Atlantic).

Galicia Bank is a large seamount situated c. 200 km off NW Iberia with a minimum depth of 600 m. It was recently included in Natura 2000, an EU-wide network of nature protection areas. We here present the first taxonomic descriptions of cheilostome bryozoans from this bank. The specimens were collected through the Spanish project INDEMARES (during BANGAL 0811 cruise conducted in 2011) and during two previous campaigns, the French Seamount 1 in 1987 and the German Victor Hensen in 1997). Twenty-five species were found, including 12 that are new to science, while five species remain in open nomenclature. Three new cheilostome genera (Breoganipora, Galiciapora and Placidoporella) are described. A lectotype is designated for Setosella vulnerata (Busk), and Palmicellaria tenuis Calvet is transferred to the genus Porella [as Porella tenuis (Calvet) n. comb.]. Additionally, our study shows that 48-60% of the bryozoan species are endemic to Galicia Bank. The degree of endemism of the Cheilostomata is thus the highest among all orders present on this seamount.

Bryozoa of Floridan Oculina reefs.

The deep-water Oculina coral reefs on the continental shelf off the east central coast of Florida are a unique protected marine habitat. A complete inventory of the Oculina-associated fauna is important to support its conservation. This paper provides an inventory of the bryozoans of the Oculina reef area. Unusually, the bryozoan fauna is dominated by encrusting cribrilinid bryozoans. These include two new species of Puellina and three other Floridan-Atlantic shelf Puellina only recently described. Additional cribrilinid species belong to the genera Klugerella and Rosulapelta. Other bryozoans found in the habitat include 38 encrusting cheilostome species, six of them new to science, belonging to the genera Callopora, Parasmittina, Parasmittina, Smittina, Microporella and Stephanollona. Cyclostomes were only sparsely represented, comprising three encrusting taxa.