The impact of habitat complexity on the structure of marine sessile communities and larvae supply.

Coastal infrastructure replaces complex and heterogeneous natural habitats with flat, two-dimensional concrete walls, reducing refuges against predation, which modifies the composition and identity of the dominant species in sessile communities. This modification in the community structure can also change the reproductive propagules available in plankton, affecting the recruitment dynamics in communities from natural habitats nearby. Here, we tested the combined effects of the habitat type (simple vs. complex with holes) and predation on the diversity, larval production, and structure of sessile communities from a recreational marina. Complex substrates showed a larger biomass and a greater abundance of solitary organisms, mainly ascidians and bivalves, that benefited from refuges. Barnacles and calcified encrusting bryozoans dominated simple, flat substrates. The difference in dominance affected the pool of larvae produced by the communities. After eight months, communities growing on flat substrates produced more barnacle larvae than those from complex substrates, where larvae of ascidians were more abundant. However, this difference disappeared after 18 months of community development. The difference in the pool of larvae between simple and complex substrates did not affect the structure of the community on flat substrates nearby, which was determined by the predation regime. In the studied region, communities in artificial environments are under intense predation control, suppressing eventual recruitment differences in communities developing in flat substrates. Large interventions that modify habitat topography, creating refuges in the subtidal zone, can change the dynamic of the sessile communities in artificial habitats and, consequently, the larval supply in the vicinities. However, differences in larval supply will only translate in distinct sessile communities when the scale of intervention encompasses large areas, and other processes do not buffer the differences in recruitment.

The high biodiversity of benthic organisms in a coastal ecosystem revealed by an integrative approach / A alta biodiversidade de organismos bentônicos em um ecossistema costeiro revelada por uma abordagem integrativa

Abstract Increasing habitat modification and species loss demand consistent efforts to describe and understand biodiversity patterns. The BIOTA/FAPESP Program was created in this context and it has been a successful initiative to promote studies on biodiversity and conservation in Brazil. The BIOTA/Araçá is an interdisciplinary project that provided a detailed evaluation of the biodiversity of Araçá Bay, a coastal seascape located on the North coast of the state of São Paulo, Southeast Brazil. The bay encompasses multiple habitats, such as beaches, mangroves, rocky shores, and a tidal flat, and provides important ecosystem services. Unfortunately, the bay is the subject of complex social-environmental conflicts that oppose economic, social, and environmental demands (i.e., the expansion of neighboring harbor activities vs. small-scale artisanal fisheries and protection of biodiversity). The present study presents a survey of the benthic species occurring in the different habitats of Araçá Bay, including data obtained during the BIOTA/Araçá project and previous assessments of the area. The benthic species play an important role in marine environments and studying the diversity of these organisms that live associated with the bottom is indispensable for comprehending the environment's functioning. The macrofauna, meiofauna, and microorganisms associated with soft and hard bottom were listed, and additional information, such as the habitat and geographical distribution, were provided for each species. The checklist includes 826 species, almost 70% recorded during the BIOTA/Araçá project. The most speciose taxa were the annelids (225 spp.), mollusks (194 spp.), and crustaceans (177 spp.). Seven benthic species are endemic to Araçá Bay, 14 are considered threatened, and seven are economically exploited. Furthermore, the bay is the type locality of many taxa, and 11 new benthic species were described based on specimens sampled during the project. This project shows the importance of Araçá Bay as a unique biologically rich environment and highlights the need for conservation efforts in light of the current threats.

Resumo O aumento da modificação dos habitats e da perda de espécies demanda esforços consistentes para descrever e compreender os padrões de biodiversidade. O programa BIOTA/FAPESP foi criado nesse contexto e é uma iniciativa de sucesso para promover estudos em biodiversidade e conservação no Brasil. O BIOTA/Araçá é um projeto interdisciplinar que promoveu uma avaliação detalhada da biodiversidade da Baía do Araçá, um ecossistema costeiro localizado ao Norte do estado de São Paulo, Sudeste do Brasil. A baía engloba múltiplos habitats, tais como praias, manguezais, costões rochosos, e uma planície de maré, e também fornece importantes serviços ecossistêmicos. Infelizmente, a baía está sujeita à conflitos sócio-ambientais complexos que contrastam demandas econômicas, sociais e ambientais (i.e. a expansão das atividades do porto vizinho vs. a pesca artesanal de pequena escala e a proteção da biodiversidade). O presente estudo apresenta um levantamento das espécies bentônicas que ocorrem nos diferentes habitats da Baía do Araçá, incluindo dados obtidos durante o projeto BIOTA/Araçá e de investigações realizadas anteriormente na área. As espécies bentônicas desempenham um papel importante no ambiente marinho, e estudar a diversidade desses organismos que vivem associados ao fundo é indispensável para compreender o funcionamento do meio ambiente. A macrofauna, meiofauna, e microorganismos associados aos fundos consolidado e inconsolidado foram listados, e informações adicionais foram fornecidas para cada espécie, tais como a distribuição geográfica e nos habitats. O checklist inclui 826 espécies, quase 70% registradas durante o projeto BIOTA/Araçá. Os taxa mais especiosos foram os anelídeos (225 spp.), moluscos (194 spp.), e crustáceos (177 spp.). Entre as espécies bentônicas listadas, sete são endêmicas da Baía do Araçá, 14 são consideradas ameaçadas de extinção, e sete são exploradas economicamente. A baía é a localidade tipo de vários taxa, e 11 novas espécies bentônicas foram descritas com base em espécimes amostrados durante o projeto. Este projeto mostra a importância da Baía do Araçá como um ambiente de riqueza biológica única e demonstra a necessidade de esforços para a sua conservação considerando as atuais ameaças.

Characterization of Peptaibols Produced by a Marine Strain of the Fungus Trichoderma endophyticum via Mass Spectrometry, Genome Mining and Phylogeny-Based Prediction.

Trichoderma is recognized as a prolific producer of nonribosomal peptides (NRPs) known as peptaibols, which have remarkable biological properties, such as antimicrobial and anticancer activities, as well as the ability to promote systemic resistance in plants against pathogens. In this study, the sequencing of 11-, 14- and 15-res peptaibols produced by a marine strain of Trichoderma isolated from the ascidian Botrylloides giganteus was performed via liquid chromatography coupled to high-resolution tandem mass spectrometry (LC-MS/MS). Identification, based on multilocus phylogeny, revealed that our isolate belongs to the species T. endophyticum, which has never been reported in marine environments. Through genome sequencing and genome mining, 53 biosynthetic gene clusters (BGCs) were identified as being related to bioactive natural products, including two NRP-synthetases: one responsible for the biosynthesis of 11- and 14-res peptaibols, and another for the biosynthesis of 15-res. Substrate prediction, based on phylogeny of the adenylation domains in combination with molecular networking, permitted extensive annotation of the mass spectra related to two new series of 15-res peptaibols, which are referred to herein as "endophytins". The analyses of synteny revealed that the origin of the 15-module peptaibol synthetase is related to 18, 19 and 20-module peptaibol synthetases, and suggests that the loss of modules may be a mechanism used by Trichoderma species for peptaibol diversification. This study demonstrates the importance of combining genome mining techniques, mass spectrometry analysis and molecular networks for the discovery of new natural products.

Seeding artificial habitats with native benthic species can prevent the occurrence of exotic organisms.

Seeding native species on pillars and platforms of marinas and harbors has been suggested to reduce space availability and prevent the colonization of exotic nuisance species, which are usually associated with coastal urbanization. The efficacy of seeding, however, has been tested mainly on the intertidal zone. To test how seeding native species in the subtidal zone affects the subsequent colonization and spread of exotic species and the community diversity, we deployed 10 PVC plates seeded with adults of the native sponge Mycale angulosa, 10 with the native ascidian Symplegma rubra, both covering about 6% of the available substrate, and 10 plates free of any intervention in a recreational marina from the Southwestern Atlantic Ocean. We then assessed the diversity and structure of the sessile community across treatments after eight months. Seeding the substrate with S. rubra resulted in no difference to unseeded communities, which were dominated by the exotic bryozoan Schizoporella errata (>66% of the substrate) and supported on average 16.9 ± 1.3 and 14.2 ± 2.0 morphospecies, respectively. However, seeding the substrate with M. angulosa resulted in a distinct community dominated by the seeded sponge (>97% of the substrate) and supporting only 3.2 ± 0.5 morphospecies. Besides, all 13 registered exotic species were reported from communities seeded with S. rubra, 11 from the unseeded communities, but only three were observed in those seeded with M. angulosa. While the consequences of the low diversity of the community seeded with M. angulosa must be addressed since poor communities are usually associated with low biotic resistance to invasion, seeding resulted in a high dominance of the native sponge, reducing the monopolization of resources by exotic species. These results suggest that seeding the substrate with native species should be implemented along with other interventions for managing artificial habitats in the coastal zone.

Predator control of marine communities increases with temperature across 115 degrees of latitude.

Early naturalists suggested that predation intensity increases toward the tropics, affecting fundamental ecological and evolutionary processes by latitude, but empirical support is still limited. Several studies have measured consumption rates across latitude at large scales, with variable results. Moreover, how predation affects prey community composition at such geographic scales remains unknown. Using standardized experiments that spanned 115° of latitude, at 36 nearshore sites along both coasts of the Americas, we found that marine predators have both higher consumption rates and consistently stronger impacts on biomass and species composition of marine invertebrate communities in warmer tropical waters, likely owing to fish predators. Our results provide robust support for a temperature-dependent gradient in interaction strength and have potential implications for how marine ecosystems will respond to ocean warming.

Enduring regardless the conditions: Plasticity in modular growth as a strategy to cope with hydrodynamic variation by the invasive sun-coral (Tubastraea spp.).

The susceptibility of a community to invasions is not the only factor influencing the success of the introduction of non-indigenous species (NIS). Because the conditions of the invaded environment tend to be unpredictable, plastic responses should increase the success of NIS in a new environment. Sun-corals are invaders in the Atlantic Ocean that present a range of strategies and plastic responses to deal with stress and distinct environmental conditions. We experimentally tested the plastic responses of sun-corals when exposed to different predation pressures and hydrodynamics in a recreational marina where sun-corals abundance varies spatially along with the environmental conditions. We separated young sun-coral colonies in two experiments: one controlling the presence of predators and the other manipulating water motion. While predation had no effect, revealing that even small young colonies are somehow protected against predators, corals increased colony area under reduced water motion but grew more polyps under greater water motion. These results highlight that plasticity in modular growth may be important for sun-corals to successfully invade distinct regions despite the hydrodynamic conditions. Increasing the colony area implicate in monopolization of space in calmer waters whilst growing more polyps allows it to have more mouths for feeding in turbulent food-poor waters. This response is particularly interesting as it is similar to the response of another NIS in the same site-the bryozoan Schizoporella errata. Phenotypic plasticity of reproductive strategies, including asexual propagation as observed here, appears to be relevant for modular NIS by facilitating the success on the invasion process in variable habitats.

Colonization history meets further niche processes: how the identity of founders modulates the way predation structure fouling communities.

Community assembly relies on deterministic niche-based processes (e.g., biotic interactions), and stochastic sources of unpredictable variation (e.g., colonization history), that combined will influence late-stage community structure. When community founders present distinct functional traits and a colonization-competition trade-off is not operating, initial colonization can result in late-stage assemblages of variable diversity and composed by different species sets, depending if early colonizers facilitate or inhibit subsequent colonization and survival. By experimentally manipulating the functional identity of founders and predators access during the development of fouling communities, we tested how founder traits constrain colonization history, species interactions and thereby regulate community diversity. We used as founders functionally different fouling organisms (colonial and solitary ascidians, and arborescent and flat-encrusting bryozoans) to build experimental communities that were exposed or protected against predation using a caging approach. Ascidians and bryozoans are pioneer colonizers in benthic communities and also good competitors, but the soft-body of ascidians makes them more susceptible to predators than mineralized bryozoans. When ascidians were founders, their dominance (but not richness) was reduced by predation, resulting in no effects of predators on overall diversity. Conversely, when bryozoans were founders, both space limitation and predator effects resulted in species-poor communities, with reduced number and cover of ascidian species and high overall dominance at the end of the experiment. We, thus, highlight that current species interactions and colonization contingencies related to founder identity should not be viewed as isolated drivers of community organization, but rather as strongly interacting processes underlying species distribution patterns and diversity.

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.

Evaluation of antileishmanial activity of harzialactone a isolated from the marine-derived fungus Paecilomyces sp.

Fractionation of extracts from the culture broth of the marine-derived fungus, Paecilomyces sp. 7A22, resulted in the isolation of the harzialactone A (HA), a known compound previously isolated from fungi of marine environments. The chemical structure of HA was determined by spectroscopic analyses. Upon evaluation of HA on antileishmanial assays against Leishmania amazonensis, HA exhibited significant activity against promastigotes forms with IC50 of 5.25 µg mL-1 and moderate activity against intracellular amastigotes with IC50 of 18.18 µg mL-1. This is the first report on the antileishmanial activity of HA, and the effects of HA presented in this work suggest that this class of compounds are suitable for future biological in vitro and in vivo studies for the search of natural products with activity against Leishmania spp. Furthermore, the present results corroborate marine-derived fungi as a promising source of natural products with antiparasitic activity.

Bioactive Aliphatic Sulfates from Marine Invertebrates.

The occurrence of sulfated steroids and phenolics in marine organisms is quite widespread, being typically reported from Echinoderms. In contrast, alkane and alkene aliphatic sulfates are considerably rarer with examples being reported from a diverse array of organisms including echinoderms, sponges and ascidians. While no ecological roles for these metabolites have been proposed, they do exhibit a diverse array of biological activities including thrombin inhibition; the ability to induce metamorphosis in larvae; antiproliferative, antibacterial and antifungal properties; and metalloproteinase inhibition. Of particular interest and an avenue for future development is the finding of antifouling properties with low or nontoxic effects to the environment. This review focuses on alkyl sulfates and related sulfamates, their structures and biological activities. Spectroscopic and spectrometric techniques that can be used to recognize the presence of sulfate groups are also discussed, data for which will enhance the ability of researchers to recognize this class of chemically- and biologically-interesting marine natural products.

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.

Colonial ascidians strongly preyed upon, yet dominate the substrate in a subtropical fouling community.

Higher diversity and dominance at lower latitudes has been suggested for colonial species. We verified this pattern in species richness of ascidians, finding that higher colonial-to-solitary species ratios occur in the tropics and subtropics. At the latitudinal region with the highest ratio, in southeastern Brazil, we confirmed that colonial species dominate space on artificial plates in two independent studies of five fouling communities. We manipulated settlement plates to measure effects of predation and competition on growth and survivorship of colonial versus solitary ascidians. Eight species were subjected to a predation treatment, i.e. caged versus exposed to predators, and a competition treatment, i.e. leaving versus removing competitors, to assess main and interactive effects. Predation had a greater effect on growth and survivorship of colonial compared to solitary species, whereas competition did not show consistent patterns. We hypothesize that colonial ascidians dominate at this subtropical site despite being highly preyed upon because they regrow when partially consumed and can adjust in shape and space to grow into refuges. We contend that these means of avoiding mortality from predation can have large influences on diversification patterns of colonial species at low latitudes, where predation intensity is greater.

Persistence and space preemption explain species-specific founder effects on the organization of marine sessile communities.

Community assembly may not follow predictable successional stages, with a large fraction of the species pool constituted by potential pioneering species and successful founders defined through lottery. In such systems, priority effects may be relevant in the determination of trajectories of developing communities and hence diversity and assemblage structure at later advanced states. In order to assess how different founder species may trigger variable community trajectories and structures, we conducted an experimental study using subtidal sessile assemblages as model. We manipulated the identity of functionally different founders and initial colony size (a proxy of the time lag before the arrival of later species), and followed trajectories. We did not observe any effects of colony size on response variables, suggesting that priority effects take place even when the time lag between the establishment of pioneering species and late colonizers is very short. Late community structure at experimental panels that started either with the colonial ascidian Botrylloides nigrum, or the arborescent bryozoan Bugula neritina, was similar to control panels allowed natural assembling. In spite of high potential for fast space domination, and hence negative priority effects, B. nigrum suffered high mortality and did not persist throughout succession. Bugula neritina provided complex physical microhabitats through conspecific clustering that have enhanced larval settlement of late species arrivals, but no apparent facilitation was observed. Differently, panels founded by the encrusting bryozoan Schizoporella errata led to different and less diverse communities compared to naturally assembled panels, evidencing strong negative priority effects through higher persistence and space preemption. Schizoporella errata founder colonies inhibited further conspecific settlement, which may greatly relax intraspecific competition, allowing resource allocation to colony growth and space domination, thus reducing the chances for the establishment of other species.

Current conditions and colonization history asymmetrically shape the organization of shallow sessile communities after simulated state shifts.

Historical processes affecting biological organization are rarely considered when predicting the effects of disturbance on community structure. In order to assess the relative importance of historical and post-disturbance conditions as determinants of community structure, we undertook reciprocal transplants, at different successional stages, of sessile communities developing at recreational piers that were previously observed to show contrasting fish predation pressure and settlement rate in the São Sebastião Channel, Brazil. Regardless the direction of state shift, after 15 weeks communities converged to the destination site structure, substantially drifting away from the path observed at origin, therefore revealing high susceptibility to environmental change. Although converging, transplanted communities never matched the destination standard in both transplant directions, suggesting that history still mattered, as providing some legacy that lasted, at least, for 15 weeks. The taxonomic groups resisting community drift were hard-bodied invertebrates, which could eventually provide some resilience to these communities through ecosystem engineering.

Distinct community dynamics at two artificial habitats in a recreational marina.

Man-made facilities along coastlines modify water circulation and sedimentation dynamics which can affect the structure of marine benthic and pelagic communities. To test how environmental heterogeneity associated with a recreational marina affects the structure of the fouling community and the benthic-pelagic link, we conducted an experiment in which predation effects on recruitment and community structure were assessed in two artificial habitats: inside the marina, an area of calm waters and often disturbed by boating activity, and the breakwater, a more hydrodynamic area. Using visual censuses and video footages we also described the predation pressure and the identity of predators on the two areas. Inside the marina, the recruitment of ascidians and serpulids, but not of bryozoans, was restricted in some occasions, possibly due to reduced water circulation. Predation, mainly by the silver porgy fish Diplodus argenteus, reduced the survivor of didemnid ascidians on both areas, but predation intensity was 40 times higher in the breakwater than inside the marina. While the two artificial habitats did not necessarily support distinct communities, low recruitment coupled to weak predation inside the marina, a less dynamic environment, likely imply lower resilience and more susceptibility to disturbance.