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.

First occurrence of Beroe forskalii (Ctenophora) in South American Atlantic coastal waters, with notes on the use of macrociliary patterns for beroid identification.

Beroe forskalii Milne Edwards, 1841 is an oceanic ctenophore with a global distribution. The present study provides the first record of Beroe forskalii for the South American Atlantic coast, including a redescription of the species and a discussion on the utility of macrociliary patterns for the correct identification of at least some beroid species, exemplified by a comparison of the macrociliary patterns of Beroe forskalii and Beroe ovata (Chamisso & Eysenhardt, 1821).

Saturated Iso-Type Fatty Acids from the Marine Bacterium Mesoflavibacter zeaxanthinifaciens with Anti-Trypanosomal Potential.

Chagas disease is a Neglected Tropical Disease with limited and ineffective therapy. In a search for new anti-trypanosomal compounds, we investigated the potential of the metabolites from the bacteria living in the corals and sediments of the southeastern Brazilian coast. Three corals, Tubastraea coccinea, Mussismilia hispida, Madracis decactis, and sediments yielded 11 bacterial strains that were fully identified by MALDI-ToF/MS or gene sequencing, resulting in six genera-Vibrio, Shewanella, Mesoflavibacter, Halomonas, Bacillus, and Alteromonas. To conduct this study, EtOAc extracts were prepared and tested against Trypanosoma cruzi. The crude extracts showed IC50 values ranging from 15 to 51 µg/mL against the trypomastigotes. The bacterium Mesoflavibacter zeaxanthinifaciens was selected for fractionation, resulting in an active fraction (FII) with IC50 values of 17.7 µg/mL and 23.8 µg/mL against the trypomastigotes and amastigotes, respectively, with neither mammalian cytotoxicity nor hemolytic activity. Using an NMR and ESI-HRMS analysis, the FII revealed the presence of unsaturated iso-type fatty acids. Its lethal action was investigated, leading to a protein spectral profile of the parasite altered after treatment. The FII also induced a rapid permeabilization of the plasma membrane of the parasite, leading to cell death. These findings demonstrate that these unsaturated iso-type fatty acids are possible new hits against T. cruzi.

Ontogenetic transitions, biomechanical trade-offs and macroevolution of scyphozoan medusae swimming patterns.

Ephyrae, the early stages of scyphozoan jellyfish, possess a conserved morphology among species. However, ontogenetic transitions lead to morphologically different shapes among scyphozoan lineages, with important consequences for swimming biomechanics, bioenergetics and ecology. We used high-speed imaging to analyse biomechanical and kinematic variables of swimming in 17 species of Scyphozoa (1 Coronatae, 8 "Semaeostomeae" and 8 Rhizostomeae) at different developmental stages. Swimming kinematics of early ephyrae were similar, in general, but differences related to major lineages emerged through development. Rhizostomeae medusae have more prolate bells, shorter pulse cycles and higher swimming performances. Medusae of "Semaeostomeae", in turn, have more variable bell shapes and most species had lower swimming performances. Despite these differences, both groups travelled the same distance per pulse suggesting that each pulse is hydrodynamically similar. Therefore, higher swimming velocities are achieved in species with higher pulsation frequencies. Our results suggest that medusae of Rhizostomeae and "Semaeostomeae" have evolved bell kinematics with different optimized traits, rhizostomes optimize rapid fluid processing, through faster pulsations, while "semaeostomes" optimize swimming efficiency, through longer interpulse intervals that enhance mechanisms of passive energy recapture.

Mitochondrial Imbalance of Trypanosoma cruzi Induced by the Marine Alkaloid 6-Bromo-2'-de-N-Methylaplysinopsin.

Chagas disease, caused by Trypanosoma cruzi, affects seven million people worldwide and lacks effective treatments. Using bioactivity-guided fractionation, NMR, and electrospray ionization-high resolution mass spectrometry (ESI-HRMS) spectral analysis, the indole alkaloid 6-bromo-2'-de-N-methylaplysinopsin (BMA) was isolated and chemically characterized from the marine coral Tubastraea tagusensis. BMA was tested against trypomastigotes and intracellular amastigotes of T. cruzi, resulting in IC50 values of 62 and 5.7 µM, respectively, with no mammalian cytotoxicity. The mechanism of action studies showed that BMA induced no alterations in the plasma membrane permeability but caused depolarization of the mitochondrial membrane potential, reducing ATP levels. Intracellular calcium levels were also reduced after the treatment, which was associated with pH alteration of acidocalcisomes. Using matrix-assisted laser desorption/ionization-time of flight (MALDI-TOF)/MS analysis, alterations of mass spectral signals were observed after treatment with BMA, suggesting a different mechanism from benznidazole. In silico pharmacokinetic-pharmacodynamic (PKPD) parameters suggested a drug-likeness property, supporting the promising usefulness of this compound as a new hit for optimizations.

Life-history traits of Tubastraea coccinea: Reproduction, development, and larval competence.

The sun coral Tubastraea coccinea Lesson, 1829 (Dendrophylliidae) is a widely distributed shallow-water scleractinian that has extended its range to non-native habitats in recent decades. With its rapid spread, this coral is now one of the main invasive species in Brazil. Its high invasive capability is related to opportunistic characteristics, including several reproductive strategies that have allowed it to disperse rapidly and widely. To better understand the reproductive biology of T. coccinea and aid in developing management strategies for invaded areas, we investigated aspects of its reproductive performance and life cycle, including the effects of colony size, seawater temperature and salinity, and lunar periodicity on offspring production and larval metamorphosis competence. A total of 18,139 offspring were released in different developmental stages, mainly from the larger colonies, which also produced larvae with longer competence periods. The main reproductive peak occurred during the First Quarter and New Moon phases and was highest in water temperatures around 26°C. Together, these results help to explain the rapid expansion of T. coccinea into non-native habitats such as the Caribbean and southwestern Atlantic, and will inform actions of the recent Brazilian National Plan for the prevention, eradication, control, and monitoring of sun corals.

Chaetopterus variopedatus Bioluminescence: A Review of Light Emission within a Species Complex.

Chaetopterus variopedatus has been studied for over a century in terms of its physiology, ecology and life history. One focus of research is on its intrinsic bioluminescent emissions, which can be observed as a blue light emitted from the extremities of individual body segments, or as a secreted mucus. Even though research shows that C. variopedatus is a species complex miscategorized as a single species, all of the variants of this polychaete produce light, which has been investigated in terms of both physiology and biochemistry. Despite decades of study, there are still many questions about the luminescence reaction, and, as of yet, no clear function for light emission exists. This review summarizes the current knowledge on C. variopedatus luminescence in addition to briefly describing its morphology, life cycle and ecology. Possible functions for luminescence were discussed using observations of specimens found in Brazil, along with a comparison of previous studies of other luminescent organisms. Further study will provide a better understanding of how and why C. variopedatus produces luminescence, and purifying the protein and luciferin involved could lead to new bioanalytical applications, as this reaction is unique among all known luminescent systems.

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.

Marine and coastal biodiversity studies, 60 years of research funding from FAPESP, what we have learned and future challenges / Estudos de biodiversidade marinha e costeira, 60 anos de financiamento à pesquisa da FAPESP, o que aprendemos e desafios futuros

Abstract In this study we survey and analyze 300 projects related to marine biodiversity funded by FAPESP from 1972 to 2021, of which 46 were nested in the BIOTA Program. From a unique project in the 1970's, the number gradually increased until 2009, when BIOTA promoted a call on marine biodiversity, which led to a boost in the number of funded projects in the subsequent years. The geographical range of the projects expanded over the years and, from studies based on the coast of São Paulo State, the focus gradually shifted to broader areas of the Brazilian coast, then to other areas of the Atlantic, and eventually became global. The majority of projects focused on coastal benthic organisms living on hard-bottom. In terms of taxa, six groups accounted for about 60% of the projects (viz. Crustacea, Actinopterygii, Mollusca, Chondrichthyes, Cnidaria, and Rhodophyta), but it is observed an increase in the number of groups studied over the decades. The 300 projects refer to a set of 82 different topics, of which the top five are taxonomy, phylogeny, community, "omics", and pollution. The analyses show a long-standing effort in marine biodiversity surveys, with ongoing updated approaches regarding scope and methods. Research on strategic areas is discussed, including deep-sea and marine microbiota. Climate change and the increasing pressure of human activity on the ocean, including pollution, acidification and invasive species, are among the main challenges for the future. Projects producing and using basic research data in an integrative and transdisciplinary way offer multiple perspectives in understanding changes in ecosystem functioning and, consequently, are essential to support public policies for the conservation and sustainable use of marine biodiversity at different scales. UNESCO's Decade of Ocean (starting 2021) is a window of opportunity to strengthen marine research, to promote national and international collaboration, to build up networks involving the public and private sector, but particularly to draw society's attention to the importance of knowing marine environments and using ocean resources in a sustainable way. The advancement of ocean literacy is one of the main legacies for future generations promoted by integrated research programs such as BIOTA-FAPESP.

Resumo Neste estudo levantamos e analisamos 300 projetos relacionados à biodiversidade marinha financiados pela FAPESP entre 1972 a 2021, dos quais 46 foram realizados no Programa BIOTA. De um projeto único na década de 1970, o número foi aumentando gradativamente até 2009, quando o BIOTA promoveu uma chamada sobre biodiversidade marinha, o que impulsionou o número de projetos financiados nos anos seguintes. A abrangência geográfica dos projetos se expandiu ao longo dos anos e, a partir de estudos baseados no litoral do Estado de São Paulo, o foco gradualmente se deslocou para áreas mais amplas da costa brasileira, depois para outras áreas do Atlântico, e acabou se tornando global. A maioria dos projetos se concentrou em organismos costeiros, bentônicos, em substrato consolidado. Em termos de táxons, seis grupos responderam por cerca de 60% dos projetos (Crustacea, Actinopterygii, Mollusca, Chondrichthyes, Cnidaria e Rhodophyta), mas observa-se um aumento no número de grupos estudados ao longo das décadas. Os 300 projetos referem-se a um conjunto de 82 temas diferentes, dos quais os cinco principais são taxonomia, filogenia, comunidade, "ômicas" e poluição. As análises mostram um esforço de longa data em pesquisas de biodiversidade marinha, com abordagens atualizadas em relação ao escopo e métodos. A pesquisa em áreas estratégicas é discutida, incluindo os estudos sobre a microbiota marinha e em águas profundas. As mudanças climáticas e a crescente pressão da atividade humana sobre o oceano, incluindo poluição, acidificação e espécies invasoras, estão entre os principais desafios para o futuro. Projetos de produção e uso de dados de pesquisa básica de forma integrada e transdisciplinar oferecem múltiplas perspectivas de compreensão das mudanças no funcionamento dos ecossistemas e, consequentemente, são essenciais para subsidiar políticas públicas de conservação e uso sustentável da biodiversidade marinha em diferentes escalas. A Década do Oceano da UNESCO (a partir de 2021) é uma janela de oportunidade para fortalecer a pesquisa marinha, promover a colaboração nacional e internacional, construir redes envolvendo os setores público e privado, mas principalmente para chamar a atenção da sociedade para a importância de conhecer os ambientes marinhos e utilizar os recursos oceânicos de forma sustentável. O avanço da "alfabetização" oceânica é um dos principais legados para as gerações futuras promovidos por programas integrados de pesquisa como o BIOTA-FAPESP.

Census of Cnidaria (Medusozoa) and Ctenophora from South American marine waters.

We have compiled available records in the literature for medusozoan cnidarians and ctenophores of South America. New records of species are also included. Each entry (i.e., identified species or still as yet not determined species referred to as "sp." in the literature) includes a synonymy list for South America, taxonomical remarks, notes on habit, and information on geographical occurrence. We have listed 800 unique determined species, in 958 morphotype entries: 5 cubozoans, 905 hydrozoans, 25 scyphozoans, 3 staurozoans, and 20 ctenophores. Concerning nomenclatural and taxonomical decisions, two authors of this census (Miranda, T.P. & Marques, A.C.) propose Podocoryna quitus as a nomen novum for the junior homonym Hydractinia reticulata (Fraser, 1938a); Euphysa monotentaculata Zamponi, 1983b as a new junior synonym of Euphysa aurata Forbes, 1848; and Plumularia spiralis Milstein, 1976 as a new junior synonym of Plumularia setacea (Linnaeus, 1758). Finally, we also reassign Plumularia oligopyxis Kirchenpauer, 1876 as Kirchenpaueria oligopyxis (Kirchenpauer, 1876) and Sertularella margaritacea Allman, 1885 as Symplectoscyphus margaritaceus (Allman, 1885).

Ctenostomatous Bryozoa from São Paulo, Brazil, with descriptions of twelve new species.

This paper describes 21 ctenostomatous bryozoans from the state of São Paulo, Brazil, based on specimens observed in vivo. A new family, Jebramellidae n. fam., is erected for a newly described genus and species, Jebramella angusta n. gen. et sp. Eleven other species are described as new: Alcyonidium exiguum n. sp., Alcyonidium pulvinatum n. sp., Alcyonidium torquatum n. sp., Alcyonidium vitreum n. sp., Bowerbankia ernsti n. sp., Bowerbankia evelinae n. sp., Bowerbankia mobilis n. sp., Nolella elizae n. sp., Panolicella brasiliensis n. sp., Sundanella rosea n. sp., Victorella araceae n. sp. Taxonomic and ecological notes are also included for nine previously described species: Aeverrillia setigera (Hincks, 1887), Alcyonidium hauffi Marcus, 1939, Alcyonidium polypylum Marcus, 1941, Anguinella palmata van Beneden, 1845, Arachnoidella evelinae (Marcus, 1937), Bantariella firmata (Marcus, 1938) n. comb., Nolella sawayai Marcus, 1938, Nolella stipata Gosse, 1855 and Zoobotryon verticillatum (delle Chiaje, 1822).

Evidence for polyphyly of the genus Scrupocellaria (Bryozoa: Candidae) based on a phylogenetic analysis of morphological characters.

The bryozoan genus Scrupocellaria comprises about 80 species in the family Candidae. We propose a hypothesis for the phylogenetic relationships among species assigned to Scrupocellaria to serve as framework for a phylogenetic classification using 35 morphological characters. Our results suggest that the genus Scrupocellaria is polyphyletic. Scrupocellaria s. str. is redefined according to four morphological features: vibracular chamber with a curved setal groove, ooecium with a single ectooecial fenestra, two axillary vibracula, and a membranous operculum with a distinct distal rim. Thus, the genus includes only 11 species: Scrupocellaria aegeensis, Scrupocellaria delilii, Scrupocellaria harmeri, Scrupocellaria incurvata, Scrupocellaria inermis, Scrupocellaria intermedia, Scrupocellaria jullieni, Scrupocellaria minuta, Scrupocellaria puelcha, Scrupocellaria scrupea, and Scrupocellaria scruposa. The monophyly of Cradoscrupocellaria is supported and five new genera are erected: Aquiloniella n. gen., Aspiscellaria n. gen., Paralicornia n. gen., Pomocellaria n. gen. and Scrupocaberea n. gen. Two other new genera, Bathycellaria n. gen. and Sinocellaria n. gen., are erected to accommodate two poorly known species, Scrupocellaria profundis Osburn and Scrupocellaria uniseriata Liu, respectively. Scrupocellaria congesta is tentatively assigned to Tricellaria. Fifteen species are reassigned to Licornia: Licornia cookie n. comb., Licornia micheli n. comb., Licornia milneri n. comb., Licornia curvata n. comb., Licornia diegensis n. comb., Licornia drachi n. comb., Licornia mexicana n. comb., Licornia pugnax n. comb., Licornia raigadensis n. comb., Licornia regularis n. comb., Licornia resseri n. comb., Licornia securifera n. comb., Licornia spinigera n. comb., Licornia tridentata n. comb., and Licornia wasinensis n. comb. Notoplites americanus n. name is proposed as a replacement name for Scrupocellaria clausa Canu & Bassler. Three fossil species are reassigned to Canda: Canda rathbuni n. comb., Canda triangulata n. comb. and Canda williardi n. comb. A species is reassigned to Notoplites, Notoplites elegantissima n. comb. The generic assignment of eleven species of Scrupocellaria, including Scrupocellaria macandrei, remains uncertain.

Embryonic, larval, and juvenile development of the sea biscuit Clypeaster subdepressus (Echinodermata: Clypeasteroida).

Sea biscuits and sand dollars diverged from other irregular echinoids approximately 55 million years ago and rapidly dispersed to oceans worldwide. A series of morphological changes were associated with the occupation of sand beds such as flattening of the body, shortening of primary spines, multiplication of podia, and retention of the lantern of Aristotle into adulthood. To investigate the developmental basis of such morphological changes we documented the ontogeny of Clypeaster subdepressus. We obtained gametes from adult specimens by KCl injection and raised the embryos at 26 degrees C. Ciliated blastulae hatched 7.5 h after sperm entry. During gastrulation the archenteron elongated continuously while ectodermal red-pigmented cells migrated synchronously to the apical plate. Pluteus larvae began to feed in 3 d and were 20 d old at metamorphosis; starved larvae died 17 d after fertilization. Postlarval juveniles had neither mouth nor anus nor plates on the aboral side, except for the remnants of larval spicules, but their bilateral symmetry became evident after the resorption of larval tissues. Ossicles of the lantern were present and organized in 5 groups. Each group had 1 tooth, 2 demipyramids, and 2 epiphyses with a rotula in between. Early appendages consisted of 15 spines, 15 podia (2 types), and 5 sphaeridia. Podial types were distributed in accordance to Lovén's rule and the first podium of each ambulacrum was not encircled by the skeleton. Seven days after metamorphosis juveniles began to feed by rasping sand grains with the lantern. Juveniles survived in laboratory cultures for 9 months and died with wide, a single open sphaeridium per ambulacrum, aboral anus, and no differentiated food grooves or petaloids. Tracking the morphogenesis of early juveniles is a necessary step to elucidate the developmental mechanisms of echinoid growth and important groundwork to clarify homologies between irregular urchins.

Fauna de hidrozoários atecados (Hydrozoa, Anthoathecata) da costa do Estado do Ceará, Brasil / The anthoathecate hydroid fauna (Hydrozoa, Anthoathecata) of the coast of Ceará State, Brazil

Espécies de hidrozoários atecados coletadas em praias da costa do estado do Ceará foram estudadas. No total foram encontradas nove espécies: Bimeria vestita, Pennaria disticha, Eudendrium caraiuru, Eudendrium carneum, Eudendrium pocaruquarum, Eudendrium sp., Sphaerocoryne sp., Porpita porpita e Coryne sp., todas registradas pela primeira vez para a região.

Species of athecate hydroids collected on beaches of the coast of Ceará State were studied. Nine species were found: Bimeria vestita, Pennaria disticha, Eudendrium caraiuru, Eudendrium carneum, Eudendrium pocaruquarum, Eudendrium sp., Sphaerocoryne sp., Porpita porpita and Coryne sp., all recorded for the first time in the region.