The systematics of carnivorous sponges.

Carnivorous sponges are characterized by their unique method of capturing mesoplanktonic prey coupled with the complete or partial reduction of the aquiferous system characteristic of the phylum Porifera. Current systematics place the vast majority of carnivorous sponges within Cladorhizidae, with certain species assigned to Guitarridae and Esperiopsidae. Morphological characters have not been able to show whether this classification is evolutionary accurate, and whether carnivory has evolved once or in several lineages. In the present paper we present the first comprehensive molecular phylogeny of the carnivorous sponges, interpret these results in conjunction with morphological characters, and propose a revised classification of the group. Molecular phylogenies were inferred using 18S rDNA and a combined dataset of partial 28S rDNA, COI and ALG11 sequences. The results recovered carnivorous sponges as a clade closely related to the families Mycalidae and Guitarridae, showing family Cladorhizidae to be monophyletic and also including carnivorous species currently placed in other families. The genus Lycopodina is resurrected for species currently placed in the paraphyletic subgenus Asbestopluma (Asbestopluma) featuring forceps spicules and lacking sigmas or sigmancistras. The genera Chondrocladia and Cladorhiza are found to be monophyletic. However, results indicate that the subgenus Chondrocladia is polyphyletic with respect to the subgenera Meliiderma and Symmetrocladia. Euchelipluma, formerly Guitarridae, is retained, but transferred to Cladorhizidae. The four known carnivorous species currently in Esperiopsis are transferred to Abyssocladia. Neocladia is a junior homonym and is here renamed Koltunicladia. Our results provide strong evidence in support of the hypothesis that carnivory in sponges has evolved only once. While spicule characters mostly reflect monophyletic groups at the generic level, differences between genera represent evolution within family Cladorhizidae rather than evolution of carnivory in separate lineages. Conflicting spicule characters can be reinterpreted to support the inclusion of all carnivorous sponges within Cladorhizidae, and a carnivorous habit should thus be considered the main diagnostic character in systematic classification.

The Station Marine d'Endoume, Marseille: 150 years of natural history.

When marine natural sciences began to be the concern of most European scientists, in the middle of the 19th century, Marseille, in southern France, was no exception. The creation, ca. 150 years ago, of the first Zoology Laboratory of the Faculty of Sciences of Marseille took place in 1868. Under the leadership of Antoine-Fortuné Marion, it soon led to the creation of the Station Marine d'Endoume (SME) in 1889. Marion's pioneering work survived both world wars and was then taken to another dimension by Jean-Marie Pérès, head of the marine station from 1948 to 1983. This institution is still alive to date. We here inventoried all the taxa described by SME scientists (1870 to 2021) and arranged them in a public database. Three main periods of activity at the SME are described, as well as the focus made through time to different groups of taxa, selected ecosystems, or biogeographic areas. Through many examples, it was possible to document how these naturalistic, taxonomic descriptions contributed to a broader scientific knowledge within this period. Finally, we discussed trends in taxonomic and naturalistic research, based on the SME experience.

Polyphyly of the genus Axinella and of the family Axinellidae (Porifera: Demospongiaep).

The genus Axinella is difficult to define on the basis of morphological characters and includes a heterogeneous assemblage of species. Several previous authors have suspected the polyphyly of both this genus and the family Axinellidae. To clarify the phylogeny of Axinellidae and Axinella, we propose a new hypothesis based on two molecular markers. In our analyses, Axinellidae and Axinella are polyphyletic assemblages. The 15 species of Axinellidae in our dataset belong to five clades and the nine species of Axinella to three clades. One Axinella clade, named Axinella(p), contains the type-species of the genus: A. polypoides (plus A. aruensis, A. dissimilis, A. infundibuliformis and A. vaceleti). A new clade, Cymbaxinella(p), is proposed, following the PhyloCode, it includes C. damicornis, C. verrucosa, C. corrugata and C. cantharella. The species Axinella cannabina is reallocated to a clade named Acanthella(p). The clades Agelas(p) and Cymbaxinella(p) constitute a new clade: Agelasida(p). Few morphological, biochemical and secondary structures characters support these groupings, highlighting the need for new characters for such problematic sponge groups. This work is an attempt to build a framework for the phylogeny of taxa allocated to Axinella and Axinellidae in the traditional classification.

Axiphenylalaninium and axityrosinium, modified amino acids from the Mediterranean marine sponge Axinella polypoides.

Two new modified amino acids, axiphenylalaninium (1) and axityrosinium (2), along with four known metabolites, C2-alpha-D-mannosylpyranosyl-L-tryptophan (3), N3,5'-cycloxanthosine (4), palythine (5), and taurine, were isolated from the marine sponge Axinella polypoides collected in the Mediterranean Sea. The structures were determined by spectroscopic studies and confirmed by X-ray analysis and chemical modifications.

Agelasines J, K, and L from the Solomon Islands Marine Sponge Agelas cf. mauritiana.

Three new diterpene alkaloids, agelasine J (3), agelasine K (4), and agelasine L (5), were isolated from the marine sponge Agelas cf. mauritiana collected in the Solomon Islands. The structures of these compounds were elucidated by physical data analyses. They displayed in vitro antimalarial activity against Plasmodium falciparum.

Preface.

A volume on Atlantic-Mediterranean deep-sea and cave sponges dedicated to Klaus Rützler and Jean Vacelet to celebrate the publication, sixty years ago, of the first works on the biodiversity of marine caves (Laborel Vacelet 1958; Russ Rützler 1959).

Systematic account of new Porifera (Demospongiae) records from the oceanic Island of Madeira (NE Atlantic).

Few surveys on benthic fauna have been performed on the island of Madeira (Alves et al. 2003 and references therein), and the first sponge specimens were collected opportunistically (Johnson 1863, 1899; Topsent 1904, 1928). Porifera can be considered one of the least studied phyla in the Madeira archipelago, within the Lusitanian province. This is not the case for other regions as the Mediterranean (Boury-Esnault 1971 and references therein), Alboran Sea (Carballo 1994), Canary Islands (Cruz 2002), and the Azores (Topsent 1904; Boury-Esnault Lopes 1985; Xavier 2009), where sponges have been more thoroughly studied.

Sponge inventory of the French Mediterranean waters, with an emphasis on cave-dwelling species.

Mediterranean sponges represent about 10 % of the world sponge biodiversity, with these sessile organisms dominating in terms of diversity and biomass in most of the rocky bottoms shaded from light. After 60 years of intensive study of the sponge diversity along the French coast, we present the first comprehensive reference-list for this biogeographic area. A total of 389 sponge species was recorded, of which 222 known in the Marseille region. In this area, special attention was paid to species from underwater caves. Although this particular habitat appeared as one of the richest, a wealth of hidden diversity still requires description. About 37 % of the sponge diversity can be found in underwater caves, most of these species being also distributed in other habitats. However, 23 % of this sponge diversity is cave-exclusive. An easy and rapid assessment method was developed with a selection of 65 representative sponge species, for the monitoring of semi-dark cave communities. This method, based on data acquisition with photoquadrats and their processing using a DataBase built with ACCESS, was deployed in 13 studied sites. Altogether, this study represents a useful contribution for marine environment managers who might refer to this French reference list and apply the rapid and easy assessment method in the framework of several European Directives and international Conventions.

Metamorphosis of cinctoblastula larvae (Homoscleromorpha, porifera).

The metamorphosis of the cinctoblastula of Homoscleromorpha is studied in five species belonging to three genera. The different steps of metamorphosis are similar in all species. The metamorphosis occurs by the invagination and involution of either the anterior epithelium or the posterior epithelium of the larva. During metamorphosis, morphogenetic polymorphism was observed, which has an individual character and does not depend on either external or species specific factors. In the rhagon, the development of the aquiferous system occurs only by epithelial morphogenesis and subsequent differentiation of cells. Mesohylar cells derive from flagellated cells after ingression. The formation of pinacoderm and choanoderm occurs by the differentiation of the larval flagellated epithelium. This is possibly due to the conservation of cell junctions in the external surface of the larval flagellated cells and of the basement membrane in their internal surface. The main difference in homoscleromorph metamorphosis compared with Demospongiae is the persistence of the flagellated epithelium throughout this process and even in the adult since exo- and endopinacoderm remain flagellated. The antero-posterior axis of the larva corresponds to the baso-apical axis of the adult in Homoscleromorpha.

New hexactinellid sponges from deep Mediterranean canyons.

During the exploration of the NW Mediterranean deep-sea canyons (MedSeaCan and CorSeaCan cruises), several hexactinellid sponges were observed and collected by ROV and manned submersible. Two of them appeared to be new species of Farrea and Tretodictyum. The genus Farrea had so far been reported with doubt from the Mediterranean and was listed as "taxa inquirenda" for two undescribed species. We here provide a proper description for the specimens encountered and sampled. The genus Tretodictyum had been recorded several times in the Mediterranean and in the near Atlantic as T. tubulosum Schulze, 1866, again with doubt, since the type locality is the Japan Sea. We here confirm that the Mediterranean specimens are a distinct new species which we describe. We also provide18S rDNA sequences of the two new species and include them in a phylogenetic tree of related hexactinellids.

How a collaborative integrated taxonomic effort has trained new spongiologists and improved knowledge of Martinique Island (French Antilles, eastern Caribbean Sea) marine biodiversity.

Although sponges are important components of benthic ecosystems of the Caribbean Sea, their diversity remained poorly investigated in the Lesser Antilles. By organizing a training course in Martinique, we wanted both to promote taxonomy and to provide a first inventory of the sponge diversity on this island. The course was like a naturalist expedition, with a field laboratory and a classroom nearby. Early-career scientists and environmental managers were trained in sponge taxonomy. We gathered unpublished data and conducted an inventory at 13 coastal sites. We explored only shallow water habitats (0-30 m), such as mangroves, reefs or rocky bottoms and underwater caves. According to this study, the sponge fauna of Martinique is currently represented by a minimum of 191 species, 134 of which we could assign species names. One third of the remaining non-identified sponge species we consider to be new to science. Martinique appears very remarkable because of its littoral marine fauna harboring sponge aggregations with high biomass and species diversity dominating over coral species. In mangroves, sponges cover about 10% of the surface of subtidal roots. Several submarine caves are true reservoirs of hidden and insufficiently described sponge diversity. Thanks to this new collaborative effort, the Eastern Caribbean has gained a significant increase of knowledge, with sponge diversity of this area potentially representing 40% of the total in the Caribbean Sea. We thus demonstrated the importance of developing exploratory and educational research in areas historically devoid of biodiversity inventories and systematics studies. Finally, we believe in the necessity to consider not only the number of species but their distribution in space to evaluate their putative contribution to ecosystem services and our willingness to preserve them.

Verpacamides A-D, a sequence of C11N5 diketopiperazines relating cyclo(Pro-Pro) to cyclo(Pro-Arg), from the marine sponge Axinella vaceleti: possible biogenetic precursors of pyrrole-2-aminoimidazole alkaloids.

[reaction: see text] Four C(11)N(5) diketopiperazine metabolites named verpacamides A (6), B (7), C (8), and D (9) consisting of a proline-arginine dipeptide skeleton have been isolated from the marine sponge Axinella vaceleti. Verpacamides A-D are a sequence of metabolites showing the transformation of proline and arginine into the oxidized guanidinyl-cyclo(Pro-Pro) 8 and 9. Compounds 6-9 are structurally and chemically related to C(11)N(5) pyrrole-2-aminoimidazole metabolites also isolated from the Axinellidae and Agelasidae families of sponges and exemplified by dispacamide A (4) and dibromophakellin (10).

The integrative taxonomic approach applied to porifera: a case study of the homoscleromorpha.

The two main scientific tasks of taxonomy are species' delineation and classification. These two tasks are often treated differently, with classification accomplished by newly-developed phylogenetic methods, often based on molecular sequences, while delimitation of species is conducted by what is often considered to be an "old-fashioned" typological approach based on morphological description. A new "integrative taxonomy" has been proposed which maintains that species delimitation should be a multidisciplinary undertaking combining several independent datasets. Here we argue that the same principle is relevant to the classification of species. In the past 20 years, we assembled various datasets based on the external morphology, anatomy, cytology, spicule shapes, geography, reproduction, genetic sequences, and metabolomics of homoscleromorph sponges. We show how we used these datasets to describe new species of homoscleromorph sponges and to elucidate their phylogenetic relationships and their phylogenetic position within the phylum Porifera.

Reconstruction of family-level phylogenetic relationships within Demospongiae (Porifera) using nuclear encoded housekeeping genes.

BACKGROUND: Demosponges are challenging for phylogenetic systematics because of their plastic and relatively simple morphologies and many deep divergences between major clades. To improve understanding of the phylogenetic relationships within Demospongiae, we sequenced and analyzed seven nuclear housekeeping genes involved in a variety of cellular functions from a diverse group of sponges. METHODOLOGY/PRINCIPAL FINDINGS: We generated data from each of the four sponge classes (i.e., Calcarea, Demospongiae, Hexactinellida, and Homoscleromorpha), but focused on family-level relationships within demosponges. With data for 21 newly sampled families, our Maximum Likelihood and Bayesian-based approaches recovered previously phylogenetically defined taxa: Keratosa(p), Myxospongiae(p), Spongillida(p), Haploscleromorpha(p) (the marine haplosclerids) and Democlavia(p). We found conflicting results concerning the relationships of Keratosa(p) and Myxospongiae(p) to the remaining demosponges, but our results strongly supported a clade of Haploscleromorpha(p)+Spongillida(p)+Democlavia(p). In contrast to hypotheses based on mitochondrial genome and ribosomal data, nuclear housekeeping gene data suggested that freshwater sponges (Spongillida(p)) are sister to Haploscleromorpha(p) rather than part of Democlavia(p). Within Keratosa(p), we found equivocal results as to the monophyly of Dictyoceratida. Within Myxospongiae(p), Chondrosida and Verongida were monophyletic. A well-supported clade within Democlavia(p), Tetractinellida(p), composed of all sampled members of Astrophorina and Spirophorina (including the only lithistid in our analysis), was consistently revealed as the sister group to all other members of Democlavia(p). Within Tetractinellida(p), we did not recover monophyletic Astrophorina or Spirophorina. Our results also reaffirmed the monophyly of order Poecilosclerida (excluding Desmacellidae and Raspailiidae), and polyphyly of Hadromerida and Halichondrida. CONCLUSIONS/SIGNIFICANCE: These results, using an independent nuclear gene set, confirmed many hypotheses based on ribosomal and/or mitochondrial genes, and they also identified clades with low statistical support or clades that conflicted with traditional morphological classification. Our results will serve as a basis for future exploration of these outstanding questions using more taxon- and gene-rich datasets.

Global diversity of sponges (Porifera).

With the completion of a single unified classification, the Systema Porifera (SP) and subsequent development of an online species database, the World Porifera Database (WPD), we are now equipped to provide a first comprehensive picture of the global biodiversity of the Porifera. An introductory overview of the four classes of the Porifera is followed by a description of the structure of our main source of data for this paper, the WPD. From this we extracted numbers of all 'known' sponges to date: the number of valid Recent sponges is established at 8,553, with the vast majority, 83%, belonging to the class Demospongiae. We also mapped for the first time the species richness of a comprehensive set of marine ecoregions of the world, data also extracted from the WPD. Perhaps not surprisingly, these distributions appear to show a strong bias towards collection and taxonomy efforts. Only when species richness is accumulated into large marine realms does a pattern emerge that is also recognized in many other marine animal groups: high numbers in tropical regions, lesser numbers in the colder parts of the world oceans. Preliminary similarity analysis of a matrix of species and marine ecoregions extracted from the WPD failed to yield a consistent hierarchical pattern of ecoregions into marine provinces. Global sponge diversity information is mostly generated in regional projects and resources: results obtained demonstrate that regional approaches to analytical biogeography are at present more likely to achieve insights into the biogeographic history of sponges than a global perspective, which appears currently too ambitious. We also review information on invasive sponges that might well have some influence on distribution patterns of the future.

New 17-methyl-13-octadecenoic and 3,16-docosadienoic acids from the sponge Polymastia penicillus.

The phospholipid fatty acid composition of the North-East Atlantic sponge Polymastia penicillus (South Brittany, France) was investigated. Sixty fatty acids (FA) were identified as methyl esters (FAME) and N-acyl pyrrolidides (NAP) by gas chromatography-mass spectrometry (GC/MS), including eight Delta5,9 unsaturated FA and three long-chain 2-hydroxylated FA. The major phospholipid FA were palmitic (14.3% of the total FA mixture), vaccenic (12.7%), 15(Z)-docosenoic (13.4%) and 5(Z),9(Z)-hexacosadienoic (13.3%) acids. In addition to the iso- and anteiso-branched saturated FA, several unusual short-chain branched saturated FA were identified. In addition to the known Delta5,9 FA, and interestingly regarding their identification by GC-MS as N-acyl pyrrolidides, was the co-occurrence of unusual FA possessing a Delta3, Delta4 and Delta5 double bond such as iso-4-pentadecenoic, iso-5-heptadecenoic, anteiso-5-heptadecenoic and two new compounds, not hitherto found in nature, namely 17-methyl-13-octadecenoic (0.8%) and 3,16-docosadienoic (1.1%) acids.

Phylogenomics revives traditional views on deep animal relationships.

The origin of many of the defining features of animal body plans, such as symmetry, nervous system, and the mesoderm, remains shrouded in mystery because of major uncertainty regarding the emergence order of the early branching taxa: the sponge groups, ctenophores, placozoans, cnidarians, and bilaterians. The "phylogenomic" approach [1] has recently provided a robust picture for intrabilaterian relationships [2, 3] but not yet for more early branching metazoan clades. We have assembled a comprehensive 128 gene data set including newly generated sequence data from ctenophores, cnidarians, and all four main sponge groups. The resulting phylogeny yields two significant conclusions reviving old views that have been challenged in the molecular era: (1) that the sponges (Porifera) are monophyletic and not paraphyletic as repeatedly proposed [4-9], thus undermining the idea that ancestral metazoans had a sponge-like body plan; (2) that the most likely position for the ctenophores is together with the cnidarians in a "coelenterate" clade. The Porifera and the Placozoa branch basally with respect to a moderately supported "eumetazoan" clade containing the three taxa with nervous system and muscle cells (Cnidaria, Ctenophora, and Bilateria). This new phylogeny provides a stimulating framework for exploring the important changes that shaped the body plans of the early diverging phyla.

NK homeobox genes with choanocyte-specific expression in homoscleromorph sponges.

Data on nonbilaterian animals (sponges, cnidarians, and ctenophores) have suggested that Antennapedia (ANTP) class homeobox genes played a crucial role in the early diversification of animal body plans. Estimates of ancestral gene diversity within this important class of developmental regulators have been mostly based on recent analyses of the complete genome of a demosponge species, leading to the proposal that all ANTP families found in nonsponges animals (eumetazoans) derived from an ancestral "proto-NK" six-gene cluster. However, a single sponge species cannot reveal ancestral metazoan traits, in particular because lineage-specific gene duplications or losses are likely to have occurred during the long history of the Porifera. We thus looked for ANTP genes by degenerate polymerase chain reaction search in five species belonging to the Homoscleromorpha, a sponge lineage recently phylogenetically classified outside demosponges and characterized by unique histological features. We identified new genes of the ANTP class called HomoNK. Our phylogenetic analyses placed HomoNK (without significant support) close to the NK6 and NK7 families of cnidarian and bilaterian ANTP genes and did not recover the monophyly of the proposed "proto-NK" cluster. Our expression analyses of the HomoNK gene OlobNK in adult Oscarella lobularis showed that this gene is a strict marker of choanocytes, the most typical sponge cell type characterized by an apical flagellum surrounded by a collar of microvilli. These results are discussed in the light of the predominant neurosensory expression of NK6 and NK7 genes in bilaterians and of the recent proposal that choanocytes could be the sponge homologs of sensory cells.

Conservation and phylogeny of a novel family of non-Hox genes of the Antp class in Demospongiae (porifera).

A survey across the most basal animal phylum, the Porifera, for the presence of homeobox-containing genes led to the isolation of 24 partial or complete homeobox sequences from 21 sponge species distributed in 15 families and 6 orders of Demospongiae. All the new sequences shared a high identity/similarity with EmH-3 (Ephydatia muelleri), a non-Hox gene from the Antp class. The Demox sequences, EmH-3, and related homeodomains formed a well-supported clade with no true affinity with any known bilaterian family, including the Tlx/Hox11 family, suggesting that the EmH-3 family of genes, comprising 31 members, represents a novel family of non-Hox genes, called the Demox family, widespread among Demospongiae. The presence of the Tlx/Hox11 specific signature in the Demox family and common regulatory elements suggested that the Demox and Tlx/Hox11 families are closely related. In the phylogenetic analyses, freshwater Haplosclerida appeared as monophyletic, and Haplosclerida and Halichondrida as polyphyletic, with a clade comprising Agelas species and Axinella corrugata. As for their expression, high levels of Demox transcripts were found in adult tissues. Our data add to the number of published poriferan homeobox sequences and provide independent confirmation of the current Demospongiae phylogenies.

Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution.

An analysis of the phylogenetic relationships of the 13 orders of Demospongiae, based on 18S and C1, D1 and C2 domains of 28S rRNA (for, respectively, 26 and 32 taxa) has been performed. The class Demospongiae as traditionally defined is not found to be monophyletic. Instead, a clade comprising all demosponges except Homoscleromorpha is well-supported, and we define phylogenetically the name Demospongiae in this more restricted sense to preclude the possibility of drastic alterations of the meaning of Demospongiae in the future, depending on the position of Homoscleromorpha. Within this clade Demospongiae s.s., ceractinomorphs and tetractinomorphs are polyphyletic, implying homoplastic evolution of characters such as reproductive strategies (viviparity vs. oviparity) and skeleton architecture (reticulate vs. radiate). The topology derived from our molecular data provides a basis for proposing a new classification of Demospongiae s.s., and suggests a reverse polarity of some characters, with respect to traditional conceptions: viviparity, presence of monaxon spicules and of spongin appear to be ancestral, whereas oviparity, and presence of tetraxon spicules appear as derived characters.