Molecular taxonomy and phylogeny of the Geodiidae (Porifera, Demospongiae, Astrophorida) – combining phylogenetic and Linnaean classification

Cárdenas, P., Rapp, H. T., Schander, C. & Tendal, O. S. (2009). Molecular taxonomy and phylogeny of the Geodiidae (Porifera, Demospongiae, Astrophorida) – combining phylogenetic and Linnaean classification.—Zoologica Scripta, 39, 89–106. According to the fossil records, the Geodiidae represents one of the oldest families of demosponges (Phylum Porifera). There are approximately 220 described extant species, geographically and bathymetrically widely distributed around the world. Species of this family all share a two-layered cortex with ball-shaped spicules called ‘sterrasters’ in the endocortex. However, molecular studies have questioned the monophyly of the group. Moreover, the evolutionary history and the intrafamily relationships of the Geodiidae are not fully resolved. Using a partial sequence of the cytochrome c oxidase subunit 1 (COI) gene and a partial sequence of the 28S rDNA gene (D1–D2 domains), we present the first molecular phylogeny focusing on this group. The congruent results from the two gene fragments suggest that (i) the Geodiidae is monophyletic, (ii) the Erylinae/Geodinae subdivision sensu Sollas, 1888 is valid and that (iii) Isops and Sidonops are junior synonyms of Geodia. The synonymization of Isops and Sidonops implies that the oscule/pore morphology as a diagnostic character should be abandoned. Geodia hentscheli nom. nov. has been given for Geodia mesotriaena ( Hentschel, 1929 ). This study served as the basis for a revised phylogenetic classification of the Geodiidae. Well-supported clades led to the establishment of clade names following the PhyloCode. The Geodinae clade is strongly supported and notably composed of Depressiogeodia, Cydonium and Geodia. A morphological synapomorphy of Geodinae is the presence of euasters in the ectocortex. The Erylinae (Erylus, Penares, Caminus and Pachymatisma) form a strongly supported monophyletic group with three morphological synapomorphies: (i) loss of anatriaenes and protriaenes, (ii) microrhabds (or spherules) in the ectocortex and (iii) short-shafted triaenes. The Erylus monophyly is ambiguous. Erylus species are distributed in three well-supported clades. Finally, spicule homology in the cortex of the Geodiidae is discussed.     

Taxonomic review of Bourguyiinae,cladistic analysis,and a new hypothesis of biogeographic relationships of the Brazilian Atlantic Rainforest (Arachnida: Opiliones,Gonyleptidae)

The subfamily Bourguyiinae Mello‐Leitão, 1923 (Gonyleptidae) is revised, and both phylogenetic and biogeographic hypotheses are proposed. Bourguyiinae is monophyletic, and is the sister group of the remainder of the Gonyleptidae species used for analysis, except for the Metasarcinae, which collectively is the sister group of Metavononoides orientalis Mello‐Leitão, 1923 (Cosmetidae). Bourguyiinae is divided into two genera: Bourguyia (six species) and Asarcus (four species). The genus‐level synonyms proposed here are as follows: Caldasius, Styloleptes, and Stylopisthos are junior synonyms of Bourguyia; Bogdana, Cnemoleptes, and Opisthoplites are junior synonyms of Asarcus. The species synonyms proposed here are as follows: Afranius amarali Mello‐Leitão, 1934 is a junior synonym of Bourguyia albiornata Mello‐Leitão, 1923 ; Drastus hamatus Roewer, 1943 and Styloleptes conspersus Piza, 1943 are junior synonyms of Bourguyia trochanteralis Roewer, 1930 ; Asarcus corallipes Simon, 1879 , Asarcus lutescens Sørensen, 1884 , Asarcus pallidus Mello‐Leitão, 1923 , and Opisthoplites ypsilon Sørensen, 1884 are junior synonyms of Asarcus longipes Kollar in Koch, 1839 ; Asarcus nigriconspersus Soares & Soares, 1945 is a junior synonym of Asarcus ingenuus Melo‐Leitão, 1940. New species described are: Bourguyia bocaina sp. nov. (Serra da Bocaina, São José do Barreiro, São Paulo), Bourguyia vinosa sp. nov. (E.B. Boracéia, Salesópolis, São Paulo), and Asarcus putunaberaba sp. nov. (Parque Nacional do Caparaó, Alto Caparaó, Minas Gerais). Bourguyiinae is endemic to the Atlantic Rainforest in the Brazilian states of Minas Gerais, Rio de Janeiro, São Paulo, and Paraná. Based on the modified data matrix of Pinto‐da‐Rocha et al., we propose a new biogeographical hypothesis for the Atlantic Rainforest. We suggest that Bourguyiinae species were originally distributed from the coastal region of Paraná to the north of Rio de Janeiro and south‐east of Minas Gerais, with subsequent dispersals both to northern and southern areas. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156 , 319–362.     

Monitoring Microbial Community Composition by Fluorescence In Situ Hybridization During Cultivation of the Marine Cold-Water Sponge Geodia barretti

To determine the stability and specificity of microbes associated with the marine cold-water sponge Geodia barretti during cultivation, we compared the microbial community of freshly retrieved specimens to that of cultivated explants by fluorescence in situ hybridization (FISH). G. barretti hosts a specific homogeneous microbial community in its mesohyl, which is maintained during a cultivation period of 8 months. In 10-day-old explants, bright colonies of unusually large bacterial cells, located predominantly at canal walls, were observed in addition to the common bacteria. Bacteria of the aberrant type included both lineages present in whole sponges and foreign ones, notably numerous genera of sulfate-reducing bacteria. We assume that these represent infectious bacteria that eluded the innate immune system of the sponge. Explants that resist these microbial attacks during the critical phase of cultivation eliminate infectious bacteria. The intrinsic microbial community of G. barretti is not affected by these infections and remains persistent over a cultivation period of at least several months.     

On the Brazilian species of halipegine genera (Trematoda: Derogenidae) from fishes,with new morphological data,hosts and synonyms

The genus Genarchella Travassos, Artigas & Pereira, 1928 is reinstated for some species from South American fishes previously attributed to Halipegus Looss, 1899. Aspects of the morphology of G. genarchella Travassos, Artigas & Pereira, 1928 and G. parva Travassos, Artigas & Pereira, 1928 are redescribed. Astyanax bimaculatus, Moenkhausia doceana, Oligosarcus robustus and Salminus maxillosus are recorded as new hosts of G. parva, and H. cryptorchis Mané-Garzon & Gascón, 1973 and H. szidati Yamaguti, 1971 [= G. tropica of Szidat (1954)] are listed amongst new synonyms of this species. Aspects of the morphology of Thometrema magnifica (Szidat, 1954) and T. overstreeti (Brooks, Mayes & Thorson, 1979) are redescribed. T. rioplatense Lunaschi, 1989 is considered a synonym of T. overstreeti. New host-records of T. overstreeti are Pimelodus maculatus and Rhamdia sp. G. genarchella of Hamann (1986) is considered as synonym of T. overstreeti. Paravitellotrema Watson, 1976, Caballeroiella Lamothe-Argumedo, 1977 and Quadripaludus Jimenez, Guajardo & Briseno, 1981 are considered synonyms of Genarchella. The features distinguishing Halipegus, Genarchella and Thometrema Amato, 1968 are discussed.     

Recruitment in the field of balanus improvisus and mytilus edulis in response to the antifouling cyclopeptides barettin and 8,9-dihydrobarettin from the marine sponge geodia barretti

In this field investigation the two cyclopeptides, isolated from the marine sponge Geodia barretti Bowerbank (Geodiidae, Astrophorida), are shown to be very efficient in preventing recruitment of the barnacle Balanus improvisus (Cirripedia, Crustacea) and the blue mussel Mytilis edulis (Protobranchia, Lamellibranchia) when included in different marine paints. These brominated cyclopeptides, named barettin and 8,9-dihydrobarettin were incorporated in different non-toxic coatings. The substances were used in the concentrations 0.1 and 0.01% in all treatments. The most efficient paint was a SPC polymer. This paint, in combination with barettin and 8,9-dihydrobarettin, reduced the recruitment of B. improvisus by 89% (barettin, 0.1%) and by 67% (8,9-dihydrobarettin, 0.1%) as compared to control panels. For M. edulis, the reduction of recruitment was 81% with barettin (0.1%) and 72% with 8,9-dihydrobarettin (0.1%) included in the SPC paint. This indicates that the two compounds from G. barretti could provide non-toxic alternatives as additives in antifouling paints, since the heavy metal-based marine paints are to be replaced.     

SYSTEMATICS OF GRATELOUPIA FILICINA (HALYMENIACEAE,RHODOPHYTA), BASED ON rbcL SEQUENCE ANALYSES AND MORPHOLOGICAL EVIDENCE,INCLUDING THE REINSTATEMENT OF G. MINIMA AND THE DESCRIPTION OF G. CAPENSIS SP. NOV.1

Grateloupia filicina (C. Agardh) Lamouroux, originally described from the Mediterranean Sea, has long been considered a textbook example of a marine red alga with a cosmopolitan distribution. An rbcL‐based molecular phylogeny, encompassing samples covering the entire geographic distribution of the species, revealed a plethora of “cryptic” species, whereby the presence of genuine G. filicina is limited to the Mediterranean basin. The phylogeny revealed a strong biogeographic imprint, with specimens from temperate regions resolved in clades composed of species inhabiting the same geographic region. Presence of widely divergent morphologies in the temperate clades indicated that several lineages have converged independently to a G. filicina‐type morphology. Tropical representatives are resolved in a single clade with very uniform G. filicina‐type morphology and pairwise sequence divergences that are lower than the average divergence observed in temperate lineages. This, combined with a lack of clear geographic structure among the tropical lineages, may indicate a more recent divergence with long‐range dispersal capacities. Violations to the biogeographic signal in temperate lineages seemed to be due to either inadequate taxonomy or recent introductions. Grateloupia minima P. & H. Crouan, a taxon placed in synonymy under G. filicina, is reinstated as a separate species distributed in the northeast Atlantic Ocean. Grateloupia capensis sp. nov. is described to accommodate specimens from South Africa with a G. filicina‐type morphology, and G. filicina var. luxurians is elevated to species status. Morphological and anatomical characters were put forward that support the distinctiveness of these three distinct species.     

Strong population structure but no equilibrium yet: Genetic connectivity and phylogeography in the kelp Saccharina latissima (Laminariales,Phaeophyta)

Kelp aquaculture is globally developing steadily as human food source, along with other applications. One of the newer crop species is Saccharina latissima, a northern hemisphere kelp inhabiting temperate to arctic rocky shores. To protect and document its natural genetic variation at the onset of this novel aquaculture, as well as increase knowledge on its taxonomy and phylogeography, we collected new genetic data, both nuclear and mitochondrial, and combined it with previous knowledge to estimate genetic connectivity and infer colonization history. Isolation‐with‐migration coalescent analyses demonstrate that gene flow among the sampled locations is virtually nonexistent. An updated scenario for the origin and colonization history of S. latissima is developed as follows: We propose that the species (or species complex) originated in the northwest Pacific, crossed to the northeast Pacific in the Miocene, and then crossed the Bering Strait after its opening ~5.5 Ma into the Arctic and northeast Atlantic. It subsequently crossed the Atlantic from east to west. During the Pleistocene, it was compressed in the south with evidence for northern refugia in Europe. Postglacial recolonization led to secondary contact in the Canadian Arctic. Saccharina cichorioides is shown to probably belong to the S. latissima species complex and to derive from ancestral populations in the Asian North Pacific. Our novel approach of comparing inferred gene flow based on coalescent analysis versus Wright's island model suggests that equilibrium levels of differentiation have not yet been reached in Europe and, hence, that genetic differentiation is expected to increase further if populations are left undisturbed.     

Epiphytic lichen synusiae and functional trait groups in boreo‐nemoral deciduous forests are influenced by host tree and environmental factors

Deciduous forests with temperate broad‐leaved tree species are particularily important in terms of biodiversity and its protection, but are threatened habitats in northern Europe. Using multivariate analyses we studied the effect of forest site type, environmental variables and host tree properties on epiphytic lichen synusiae as well as on the composition of species‐specific functional traits. Epiphytic lichens were examined on Acer platanoides, Fraxinus excelsior, Quercus robur, Tilia cordata, Ulmus glabra and U. laevis in two types of forests: Humulus‐type floodplain forests and Lunaria‐type boreo‐nemoral forests on the talus slopes of limestone escarpment (klint forests). Klint forests located near the seashore were under greater maritime influence compared to floodplain forests located in inland Estonia which experience stronger air temperature contrasts. In addition to stand level and climatic variables, tree level factors (bark pH, trunk circumference and cover of bryophytes) considerably affected the species composition of the lichen synusiae. Overall, 137 lichen species were recorded, including 14 red‐listed species characteristic of deciduous trees. We defined 13 lichen societies and showed their preference to forests of a specific site type and/or host tree properties. In forests of both types, most of the epiphytic lichens were crustose, and had apothecia as the fruit bodies and chlorococcoid algae as the photobiont. However, the proportion of lichens with a foliose or fruticose growth form, as well as the proportion of lichens with vegatative diaspores, were higher in floodplain forests. In klint forests with a stronger influence from the wind, crustose species completely dominated, while species with vegetative diaspores were rare and most species dispersed sexually. Lichens with Trentepohlia as the photobiont were characteristic of these forests, and lichens with lirellate ascomata were prevailing, indicating the great uniqueness of the kint forests for epiphytic lichens in the boreo‐nemoral region.     

Synchroneity of Pliocene planktonic foraminiferal datums in the North Atlantic

Leg 94 of the Deep Sea Drilling Project has provided a unique set of paleomagnetically dated cores, taken along a N-S transect in the North Atlantic. High deposition rates in the sediments, combined with the palaeomagnetic ages, have enabled existing planktonic foraminiferal zonations to be tested and a new zonation for the mid- to high latitudes to be erected. The PL zonation of Berggren (1973, 1977) is shown to be adequate as far north as 41°N, although both the LAD's ofGlobigerina nepenthes andGloborotalia margaritae occur earlier than in tropical regions. North of 41°N these two species have very diachronous LAD's, even though they are common during their range in the northern sites. The new zonation for the mid to high latitude North Atlantic is based on the FAD ofG. margaritae, FAD ofG. puncticulata, LAD ofG. cf. crassula, LAD ofN. atlantica, FAD ofG. inflata and FAD of sinistrally coiled encrustedN. pachyderma.     

Recent drastic changes in the gammarid fauna (Crustacea, Amphipoda) of the Vistula River deltaic system in Poland caused by alien invaders

During the last decade of 20th century, the nonindigenous gammarid species Gammarus tigrinus, Dikerogammarus haemobaphes, Pontogammarus robustoides and Obesogammarus crassus invaded the lower Vistula River and its deltaic, partly brackish regions. G. tigrinus, an oligohaline North‐American species, was introduced to western Europe in the 1950s; the remaining three species are oligohaline/freshwater Ponto‐Caspian species. All these species are now invading central and western Europe using the network of man‐made canals connecting different European river systems. In the Vistula River, the native European freshwater gammarid species Gammarus pulex and G. varsoviensis were replaced in the 1920s by the Ponto‐Caspian Chaetogammarus ischnus (syn. Echinogammarus ischnus), which in turn has been outnumbered by the more recent invasions of D. haemobaphes and P. robustoides. In brackish waters, the native Atlantic‐boreal species Gammarus zaddachi and Gammarus duebeni are replaced or at least outnumbered by G. tigrinus, P. robustoides and O. crassus. Possible invasion routes are discussed.     

PHYLOGEOGRAPHY OF GRACILARIA TIKVAHIAE (GRACILARIACEAE,RHODOPHYTA): A STUDY OF GENETIC DISCONTINUITY IN A CONTINUOUSLY DISTRIBUTED SPECIES BASED ON MOLECULAR EVIDENCE1

Gracilaria tikvahiae, a highly morphologically variable red alga, is one of the most common species of Gracilariaceae inhabiting Atlantic estuarine environments and the Intracoastal Waterway of eastern North America. Populations of G. tikvahiae at the extremes of their geographic range (Canada and southern Mexico) are subjected to very different environmental regimes. In this study, we used two types of genetic markers, the chloroplast‐encoded rbcL and the nuclear internal transcribed spacer (ITS) region, to examine the genetic variability within G. tikvahiae, for inferring the taxonomic and phylogenetic relationships between geographically isolated populations, and to discuss its distributional information in a phylogeographic framework. Based on rbcL and ITS phylogenies, specimens from populations collected at the extreme distributional ranges reported for G. tikvahiae are indeed part of the same species; however, rbcL‐ but not ITS‐based phylogenies detected phylogenetic structure among the ten G. tikvahiae different haplotypes found in this study. The four distinct rbcL lineages were identified as 1) a Canadian–northeast U.S. lineage, 2) a southeast Florida lineage, 3) an eastern Gulf of Mexico lineage, and 4) a western Gulf of Mexico lineage. We found no evidence for the occurrence of G. tikvahiae in the Caribbean Sea. Observed phylogeographic patterns match patterns of genetic structures reported for marine animal taxa with continuous and quasicontinuous geographic distribution along the same geographic ranges.     

Introductory comments

Abstract

Associated microorganisms have been described in numerous marine sponges. Their metabolic activity, however, has not yet been investigated in situ. We quantified for the first time microbial processes in a living sponge. Sulfate reduction rates of up to 1200 nmol cm^?3d^?1 were measured in the cold-water bacteriosponge Geodia barretti . Oxygen profiles and chemical analysis of sponge tissue and canal water revealed steep oxygen gradients and a rapid turnover of oxygen and sulfide, dependent on the pumping activity of the sponge. Identification of the microbial community with fluorescently labelled oligonucleotide probes (FISH) indicates the presence of sulfate-reducing bacteria belonging to the Desulfoarculus/Desulfomonile/Syntrophus -cluster in the choanosome of this sponge. Analysis of lipid biomarkers indicates biomass transfer from associated sulfate-reducing bacteria or other anaerobic microbes to sponge cells. These results show the presence of an anoxic micro-ecosystem in the sponge G. barretti, and imply mutualistic interactions between sponge cells and anaerobic microbes. Understanding the importance of anaerobic processes within the sponge/microbe system may help to answer unsolved questions in sponge ecology and biotechnology.     

Morphological Differentiation Between Geographically Separated Populations of <Emphasis Type="Italic">Neomysis integer</Emphasis> and <Emphasis Type="Italic">Mesopodopsis slabberi</Emphasis> (Crustacea,Mysida)

Morphological variation was examined in Neomysis integer and Mesopodopsis slabberi, two abundant, low dispersal mysid species (Crustacea, Mysida) along the European coasts. Both species dominate the hyperbenthic communities in the northeast Atlantic, and M. slabberi is also widely distributed in the Mediterranean and Black Sea. Three populations of these species were sampled throughout their distribution range; samples of N. integer were collected in the northeast Atlantic Eems-Dollard, Gironde and Guadalquivir estuaries; in the case of M. slabberi, mysids were sampled in two northeast Atlantic estuaries (Eems-Dollard and Guadalquivir) and one Mediterranean site (Ebro Delta). A total of 12 morphometric and 2 meristic characters were measured from 30–64 mysids per sample. Multivariate analysis showed clear morphometric differences between populations of both species. The morphological differentiation within M. slabberi was highly concordant with the available genetic data from mitochondrial loci, pointing to a large divergence between the Atlantic and Mediterranean populations. However, due to some overlap of individuals between the different populations, the present morphometric analysis does not suffice to assign the different populations to a separate (sub)species status. In the case of N. integer, the morphometric patterns showed a divergence of the Gironde population. Differentiation of populations within this mysid, as in M. slabberi, were mainly related to eye and telson morphology. Potential interactions of the mysid morphology and environmental conditions are discussed.     

<Emphasis Type="Italic">Adelobotrys atlantica</Emphasis> (<Emphasis Type="Italic">Melastomataceae: Merianieae</Emphasis>): the first species of <Emphasis Type="Italic">Adelobotrys</Emphasis> from Brazil’s Mata Atlântica

Summary  A new species of Adelobotrys DC., A. atlantica Schulman, is described and illustrated. This is the first record of the genus in the Atlantic rainforests of Brazil. The only known specimen of the new species was collected in 1943 close to the sizeable city of Ilhéus in an area that has probably now been converted to managed land. It is therefore possible that A. atlantica is already extinct.     

Incongruent phylogeographies in spite of similar morphology, ecology, and distribution:Phippsia algida andP. concinna (Poaceae) in the North Atlantic region

Phylogeographic and taxonomic relationships among 54 North Atlantic populations of the snowbed grass genusPhippsia were investigated based on isozymes and genetically based morphological variation. The results support recognition of two distinct species,P. algida andP. concinna, the latter with at least two subspecies. Both of these self-fertilizing arctic pioneer species were genetic allotetraploids almost without intrapopulational variation. The two species showed strikingly different phylogeographies in the North Atlantic region in spite of their similarity in morphology, habitat ecology, mating system, and dispersal ecology, and in spite of their present cooccurrence in many geographic areas, sometimes even in the same snowbeds. The same electrophoretic multilocus phenotype was observed in all populations ofP. algida, and although this species showed considerable morphological variation, the variation was unstructured geographically. Thus,P. algida showed a pattern similar to other arctic species investigated in the North Atlantic region; it has probably dispersed postglacially across the sea barriers among Greenland, Svalbard, Iceland, and Scandinavia. In contrast,P. concinna was virtually fixed for different multilocus phenotypes in the three main geographic areas analyzed (S Norway, Svalbard, Greenland), corresponding to fairly distinct divergence in morphology. This pattern suggests absence of postglacial among-area dispersal ofP. concinna in spite of all of its similarities with its congener; it may have immigrated to the North Atlantic from different source areas and/or survived the last glaciationin situ.     

Scleractinia (Cnidaria: Anthozoa) from INDEMARES 2010–2012 expeditions to the Avilés Canyon System (Bay of Biscay,Spain, northeast Atlantic)

Twenty-eight species of scleractinian corals were collected between 55 and 2,291 m depth during INDEMARES 2010–2012 expeditions to the Avilés Canyon System and the near continental shelf (Bay of Biscay). Most interesting species are described and all depicted. All species were already known from the northeast Atlantic, although some are seldom reported. Deltocyathus eccentricus and Flabellum chunii are northernmost records in the eastern Atlantic, and species first collected from the Bay of Biscay. From a literature review and new records given herein, 31 species of Scleractinia are known from the Avilés Canyon System. Live specimens of six species were recorded outside their previously known bathymetric ranges in the Bay of Biscay and nearby areas, either at shallower depths (Caryophyllia sarsiae, Monomyces pygmaea, Stephanocyathus nobilis), or deeper depths (C. atlantica, C. sarsiae, Enallopsammia rostrata, Solenosmilia variabilis). Desmophyllum cristagalli has the widest bathymetric range (551–2,291 m), and Lophelia pertusa is the most widely distributed species (24 stations). Tabulating the number of live species occurring in each 100-m depth interval of the canyon system, highest species richness occurs in the 700–800-, 800–900-, and 1,400–1,500-m depth intervals (11 species). The habitat-forming species L. pertusa and Madrepora oculata were abundant in some stations building well-developed coral banks. Live colonies of the big-sized species S. variabilis and E. rostrata co-occurred at the deepest station sampled that yielded scleractinia (2,291 m).