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.

Phylogeny and taxonomy of Haloclavidae (Verrill, 1899) with a redescription of the parasitic, burrowing sea anemone, Peachia chilensis Carlgren, 1931.

Haloclavidae Verrill, 1899 is a family of burrowing sea anemones grouped within the superfamily Actinioidea (Rafinesque, 1815). Currently, it includes 30 species in 10 genera. Characters given for this family in descriptions of its taxa have not been consistent, with numerous exceptions to the expectations of the familial diagnosis. Previous phylogenetic analyses have shown that Haloclavidae is potentially a polyphyletic group, but resolution of relationships of the few representatives of Haloclavidae included in analyses has been problematic. Here we address questions of monophyly and affinity of Haloclavidae using three mitochondrial and two nuclear markers. We assess the monophyly of Haloclavidae in the context of all major lineages of Actiniaria Hertwig, 1882, emphasizing diversity of superfamily Actinioidea. We use parsimony-based character optimization to interpret the distribution of key traits in the superfamily. We find that Haloclavidae is not monophyletic and propose two new families, Peachiidae fam. nov. and Harenactidae fam. nov., while also retaining some species in the family Haloclavidae, so that taxonomy better reflects relationships and diversity of the group. In addition, we redescribe a species within the newly created Peachiidae, Peachia chilensis Carlgren, 1931. We use recent larval samples obtained in Antofagasta, Chile, and the histological slides from the original description to redescribe P. chilensis, to provide a complete account of cnidae, external, and internal morphology. Finally, we compare P. chilensis to other burrowing anemones found in Chile and provide an understanding of the genus Peachia that reflects recent phylogenetic perspective on diversity of anemones previously assigned to family Haloclavidae.

Mixotrophic chemosynthesis in a deep-sea anemone from hydrothermal vents in the Pescadero Basin, Gulf of California.

BACKGROUND: Numerous deep-sea invertebrates, at both hydrothermal vents and methane seeps, have formed symbiotic associations with internal chemosynthetic bacteria in order to harness inorganic energy sources typically unavailable to animals. Despite success in nearly all marine habitats and their well-known associations with photosynthetic symbionts, Cnidaria remain one of the only phyla present in the deep-sea without a clearly documented example of dependence on chemosynthetic symbionts. RESULTS: A new chemosynthetic symbiosis between the sea anemone Ostiactis pearseae and intracellular bacteria was discovered at ~ 3700 m deep hydrothermal vents in the southern Pescadero Basin, Gulf of California. Unlike most sea anemones observed from chemically reduced habitats, this species was observed in and amongst vigorously venting fluids, side-by-side with the chemosynthetic tubeworm Oasisia aff. alvinae. Individuals of O. pearseae displayed carbon, nitrogen, and sulfur tissue isotope values suggestive of a nutritional strategy distinct from the suspension feeding or prey capture conventionally employed by sea anemones. Molecular and microscopic evidence confirmed the presence of intracellular SUP05-related bacteria housed in the tentacle epidermis of O. pearseae specimens collected from 5 hydrothermally active structures within two vent fields ~ 2 km apart. SUP05 bacteria (Thioglobaceae) dominated the O. pearseae bacterial community, but were not recovered from other nearby anemones, and were generally rare in the surrounding water. Further, the specific Ostiactis-associated SUP05 phylotypes were not detected in the environment, indicating a specific association. Two unusual candidate bacterial phyla (the OD1 and BD1-5 groups) appear to associate exclusively with O. pearseae and may play a role in symbiont sulfur cycling. CONCLUSION: The Cnidarian Ostiactis pearseae maintains a physical and nutritional alliance with chemosynthetic bacteria. The mixotrophic nature of this symbiosis is consistent with what is known about other cnidarians and the SUP05 bacterial group, in that they both form dynamic relationships to succeed in nature. The advantages gained by appropriating metabolic and structural resources from each other presumably contribute to their striking abundance in the Pescadero Basin, at the deepest known hydrothermal vents in the Pacific Ocean.

Origin and evolution of the symbiosis between sea anemones (Cnidaria, Anthozoa, Actiniaria) and hermit crabs, with additional notes on anemone-gastropod associations.

The anemone-crab mutualism is ubiquitous in temperate and tropical marine environments. In this symbiosis, one or more anemones live on a shell inhabited by a hermit crab and reciprocal phoretic, trophic, and defensive benefits are exchanged between the partners. Sea anemone-hermit crab symbionts belong to three families: Hormathiidae (Calliactis and Paracalliactis), Sagartiidae (Carcinactis and Verrillactis), and Actiniidae (Stylobates). Hermit crabs establish most partnerships by detaching anemones and placing them on their shell; sea anemones can also mount shells unaided, triggered by a mollusc-derived substance in the periostracum of the shell. At least partial cooperation by the anemones is necessary for successful establishment of the symbiosis. Here, we expand the evolutionary framework for hormathiid symbionts by generating a phylogeny with at least one member of each actiniarian symbiotic genus with hermit crabs using five molecular markers (16S, 12S, 18S, 28S, CO3). We not only corroborated the results from a previous study by finding two origins of hermit crab symbiosis within Hormathiidae, but also found additional origins for hermit crab symbiosis within Actiniaria. We provide for the first time evidence of a close relationship between symbionts Carcinactis dolosa and V. paguri. The ability to secrete chitin by the ectoderm of the column is inferred to be broadly convergent within Actiniaria whereas the secretion of a chitinous carcinoecium by the pedal disc is a distinct but convergent morphological adaptation of several lineages within Actiniaria. Our finding of multiple origins for both the hermit crab and gastropod symbioses suggests that the shell-mounting behavior might only have been the precursor of the hermit crab association among Calliactis spp.

Mitogenomics suggests a sister relationship of Relicanthus daphneae (Cnidaria: Anthozoa: Hexacorallia: incerti ordinis) with Actiniaria.

Relicanthus daphneae (formerly Boloceroides daphneae) was first described in 2006 as a giant sea anemone based on morphology. In 2014, its classification was challenged based on molecular data: using five genes, Relicanthus was resolved sister to zoanthideans, but with mixed support. To better understand the evolutionary relationship of Relicanthus with other early-branching metazoans, we present 15 newly-sequenced sea anemone mitochondrial genomes and a mitogenome-based phylogeny including all major cnidarian groups, sponges, and placozoans. Our phylogenetic reconstruction reveals a moderately supported sister relationship between Relicanthus and the Actiniaria. Morphologically, the cnidae of Relicanthus has apical flaps, the only existing synapomorphy for sea anemones. Based on both molecular and morphological results, we propose a third suborder (Helenmonae) within the Actiniaria to accommodate Relicanthus. Although Relicanthus shares the same gene order and content with other available actiniarian mitogenomes, it is clearly distinct at the nucleotide level from anemones within the existing suborders. The phylogenetic position of Relicanthus could reflect its association with the periphery of isolated hydrothermal vents, which, although patchy and ephemeral, harbor unique chemosynthetic communities that provide a relatively stable food source to higher trophic levels over long evolutionary timescales. The ability to colonize the deep sea and the periphery of new vent systems may be facilitated by Relicanthus' large and extremely yolky eggs.

Phylogenetic relationships among the clownfish-hosting sea anemones.

The clownfish-sea anemone symbiosis has been a model system for understanding fundamental evolutionary and ecological processes. However, our evolutionary understanding of this symbiosis comes entirely from studies of clownfishes. A holistic understanding of a model mutualism requires systematic, biogeographic, and phylogenetic insight into both partners. Here, we conduct the largest phylogenetic analysis of sea anemones (Order Actiniaria) to date, with a focus on expanding the biogeographic and taxonomic sampling of the 10 nominal clownfish-hosting species. Using a combination of mtDNA and nuDNA loci we test (1) the monophyly of each clownfish-hosting family and genus, (2) the current anemone taxonomy that suggests symbioses with clownfishes evolved multiple times within Actiniaria, and (3) whether, like the clownfishes, there is evidence that host anemones have a Coral Triangle biogeographic origin. Our phylogenetic reconstruction demonstrates widespread poly- and para-phyly at the family and genus level, particularly within the family Stichodactylidae and genus Stichodactyla, and suggests that symbioses with clownfishes evolved minimally three times within sea anemones. We further recover evidence for a Tethyan biogeographic origin for some clades. Our data provide the first evidence that clownfish and some sea anemone hosts have different biogeographic origins, and that there may be cryptic species of host anemones. Finally, our findings reflect the need for a major taxonomic revision of the clownfish-hosting sea anemones.

Metapeachia schlenzae sp. nov. (Cnidaria: Actiniaria: Haloclavidae) a new burrowing sea anemone from Brazil, with a discussion of the genus Metapeachia.

The diversity of burrowing sea anemones from Brazil is poorly known with only three species recorded. Metapeachia schlenzae sp. nov. is described from specimens collected in the intertidal zone of São Sebastião and Cabo Frio in the southeastern coast of Brazil. Metapeachia schlenzae sp. nov. is the second species described for the genus and the second haloclavid recorded from Brazil. A comparison between Metapeachia schlenzae sp. nov. and Metapeachia tropica, the type species of the genus, is included. The two valid species of Metapeachia differ in the morphology of the conchula, internal anatomy, cnidae and geographical distribution.

Toward a natural classification: phylogeny of acontiate sea anemones (Cnidaria, Anthozoa, Actiniaria).

Acontia-nematocyst-dense, thread-like extensions of the mesenterial filaments-are the characteristic feature of the actiniarian group Acontiaria. Phylogenetic analyses have shown that acontiate taxa form a clade that also includes some taxa without acontia. We analyse five molecular markers from 85 actiniarians to explore the phylogenetic relationships among families in Acontiaria, including acontiate species assigned to other higher taxa and species without acontia that have been allied to Acontiaria. Based on our results, we redefine the group to accommodate those lineages that have lost acontia, and formalize it as superfamily Metridioidea. Based on stable and well supported clades, we resurrect Phelliidae and Amphianthidae, redefine Kadosactinidae and Actinoscyphiidae, and move two species to new genera: that previously termed Sagartiogeton erythraios belongs in Jasonactis gen. nov.; and that previously termed Anthosactis pearseae belongs in Ostiactis gen. nov., type genus of Ostiactinidae fam. nov. We also synonymized Halcampoididae and Halcampidae (as Halcampidae) and Andvakiidae and Isophelliidae (as Andvakiidae). The results of our phylogenetic analyses indicate that the diagnostic morphological characters used in the family-level taxonomy of acontiate actiniarians such as the nematocysts of the acontia, the marginal sphincter muscle, and mesenteries divisible into macro- and micro-cnemes, have to be revisited, as these features are highly homoplasious.

Evolution of sea anemones (Cnidaria: Actiniaria: Hormathiidae) symbiotic with hermit crabs.

Sea anemones in genera Adamsia, Calliactis and Paracalliactis (family Hormathiidae) engage in a mutualistic symbiosis with hermit crabs in which the anemone gains substrate and food in exchange for defending the crab. Some of the sea anemones also expand the living space of the crab by producing a carcinoecium, a chitinous structure that overlies the initial gastropod shell in which the hermit crab lives. The symbiosis is initiated either by the crab, or by the anemone. Although behavioral and physiological aspects of this symbiosis have been studied, interpretations cannot be generalized without an evolutionary framework. After reconstructing relationships among members of Hormathiidae using DNA sequences, we find that the association has evolved at least twice: Adamsia nests within Calliactis in a single clade, and Paracalliactis belongs to a different clade within the family. The carcinoecium and complex behavioral and anatomical features associated with the symbiosis are interpreted as having evolved at least twice within Hormathiidae and seem to be phylogenetically labile.

Phylogenetic signal in mitochondrial and nuclear markers in sea anemones (Cnidaria, Actiniaria).

The mitochondrial genome of basal animals is generally more slowly evolving than that of bilaterians. This difference in rate complicates the study of relationships among members of these lineages and the discovery of cryptic species or the testing of morphological species concepts within them. We explore the properties of mitochondrial and nuclear ribosomal genes in the cnidarian order Actiniaria, using both an ordinal- and familial-scale sample of taxa. Although the markers do not show significant incongruence, they differ in their phylogenetic informativeness and the kinds of relationships they resolve. Among the markers studied here, the fragments of 12S rDNA and 18S rDNA most effectively recover well-supported nodes; those of 16S rDNA and 28S rDNA are less effective. The general patterns we observed are similar to those in other hexacorallians, although Actiniaria alone show saturation of transitions for ordinal-scale analyses.