The cladorhizid fauna (Porifera, Poecilosclerida) of the Caribbean and adjacent waters

The carnivorous sponge family Cladorhizidae has been subject to several recent studies, yet the cladorhizid fauna of the Caribbean and adjacent areas remain comparatively poorly known. In this article we provide a description of the novel species Abyssocladia polycephalus sp. nov. from the Muir Seamount NE of Bermuda, belonging to the mainly Pacific genus Abyssocladia, and Asbestopluma (Asbestopluma) caribica sp. nov. from the Beata Ridge. Additionally, we provide a re-description of the poorly known species Chondrocladia (Chondrocladia) verticillata Topsent, 1920, and compare this species with the closely related species C. (C.) concrescens Schmidt, 1880. Finally, we provide a brief overview of the carnivorous sponges known from the Gulf of Mexico, Caribbean Sea and adjacent Atlantic Ocean.publishedVersio

Oceanographic setting and short-timescale environmental variability at an Arctic seamount sponge ground

Mass occurrences of large sponges, or ‘sponge grounds’, are found globally in a range of oceanographic settings. Interest in these grounds is growing because of their ecological importance as hotspots of biodiversity, their role in biogeochemical cycling and bentho-pelagic coupling, the biotechnological potential of their constituent sponges, and their perceived vulnerability to physical disturbance and environmental change. Little is known about the environmental conditions required for sponges to persist and for grounds to form, and very few studies have explicitly characterised and interpreted the importance of oceanographic conditions. Here, results are presented of the first observational oceanographic campaign at a known sponge ground on the Schultz Massif Seamount (SMS; Arctic Mid-Ocean Ridge, Greenland / Norwegian Seas). The campaign consisted of water column profiling and short-term deployment of a benthic lander. It was supported by multibeam echosounder bathymetry and remotely operated vehicle video surveys. The seamount summit hosted several environmental factors potentially beneficial to sponges. It occurred within relatively nutrient-rich waters and was regularly flushed from above with slightly warmer, oxygen-enriched Norwegian Arctic Intermediate Water. It was exposed to elevated suspended particulate matter levels and oscillating currents (with diurnal tidal frequency) likely to enhance food supply and prevent smothering of the sponges by sedimentation. Elevated chlorophyll a concentration was observed in lenses above the summit, which may indicate particle retention by seamount-scale circulation patterns. High sponge density and diversity observed on the summit is likely explained by the combination of several beneficial factors, the coincidence of which at the summit arises from interaction between seamount geomorphology, hydrodynamic regime, and water column structure. Neighbouring seamounts along the mid-ocean ridge are likely to present similarly complex oceanographic settings and, as with the SMS, associated sponge ground ecosystems may therefore be sensitive to changes over a particularly broad range of abiotic factor

Molecular Phylogeny of the Astrophorida (Porifera, Demospongiaep) Reveals an Unexpected High Level of Spicule Homoplasy

Background: The Astrophorida (Porifera, Demospongiaep) is geographically and bathymetrically widely distributed. Systema Porifera currently includes five families in this order: Ancorinidae, Calthropellidae, Geodiidae, Pachastrellidae and Thrombidae. To date, molecular phylogenetic studies including Astrophorida species are scarce and offer limited sampling. Phylogenetic relationships within this order are therefore for the most part unknown and hypotheses based on morphology largely untested. Astrophorida taxa have very diverse spicule sets that make them a model of choice to investigate spicule evolution. Methodology/Principal Findings: With a sampling of 153 specimens (9 families, 29 genera, 89 species) covering the deepand shallow-waters worldwide, this work presents the first comprehensive molecular phylogeny of the Astrophorida, using a cytochrome c oxidase subunit I (COI) gene partial sequence and the 59 end terminal part of the 28S rDNA gene (C1-D2 domains). The resulting tree suggested that i) the Astrophorida included some lithistid families and some Alectonidae species, ii) the sub-orders Euastrophorida and Streptosclerophorida were both polyphyletic, iii) the Geodiidae, the Ancorinidae and the Pachastrellidae were not monophyletic, iv) the Calthropellidae was part of the Geodiidae clade (Calthropella at least), and finally that v) many genera were polyphyletic (Ecionemia, Erylus, Poecillastra, Penares, Rhabdastrella, Stelletta and Vulcanella). Conclusion: The Astrophorida is a larger order than previously considered, comprising ca. 820 species. Based on these results, we propose new classifications for the Astrophorida using both the classical rank-based nomenclature (i.e., Linnaean classification) and the phylogenetic nomenclature following the PhyloCode, independent of taxonomic rank. A key to the Astrophorida families, sub-families and genera incertae sedis is also included. Incongruences between our molecular tree and the current classification can be explained by the banality of convergent evolution and secondary loss in spicule evolution. These processes have taken place many times, in all the major clades, for megascleres and microscleres

The Hexactinellid Deep-Water Sponge Vazella pourtalesii (Schmidt, 1870) (Rossellidae) Copes With Temporarily Elevated Concentrations of Suspended Natural Sediment

Plumes of re-suspended sediment potentially smother and clog the aquiferous system of filter-feeding sponges with unknown implications for their health. For the first time, we examined the physiological responses of repeated exposure to natural sediment in the glass sponge Vazella pourtalesii, which forms dense sponge grounds in Emerald Basin off Nova Scotia, Canada. Ex situ chamber-based measurements of bacterial clearance and oxygen consumption (respiration) rates indicated that individuals subjected to elevated concentrations of suspended sediment expressed normal clearance and respiration rates over 7 days of sediment exposure, indicating an ability to cope with elevated concentrations of indigestible sediment particles. However, clearance rates significantly declined after 14 days of sediment exposure, suggesting an inability to cope with long-term exposure to increased sediment load. Therefore, long-term exposure to elevated concentrations of suspended sediment should be avoided in order to minimize adverse effects on the abundant Vazella sponge grounds.publishedVersio

Seasonal Variability in Near-bed Environmental Conditions in the Vazella pourtalesii Glass Sponge Grounds of the Scotian Shelf

The Scotian Shelf harbors unique aggregations of the glass sponge Vazella pourtalesii that provides an important habitat for benthic and pelagic fauna. Recent studies have shown that these sponge grounds have persisted in the face of strong inter-annual and multi-decadal variability in temperature and salinity. However, little is known of these environmental characteristics on hourly-seasonal time scales. This study presents the first hydrodynamic observations and associated (food) particle supply mechanisms for the Vazella sponge grounds, highlighting the influence of natural variability in environmental conditions on sponge growth and resilience. Near-bottom environmental conditions were characterized by high temporal resolution data collected with a benthic lander, deployed during a period of 10 months in the Sambro Bank Sponge Conservation Area. The lander was equipped with temperature and oxygen sensors, a current meter, a sediment trap and a video camera. In addition, water column profiles of temperature and salinity were collected in an array across the sponge grounds from high to lower sponge presence probability. Over the course of the lander deployment, temperature fluctuated between 8.8–12°C with an average of 10.6 ± 0.4°C. Dissolved oxygen concentration was on average 6.3 mg l–1, and near-bottom current speed was on average 0.12 m s–1, with peaks up to 0.47 m s–1. Semi-diurnal tidal currents promoted constant resuspension of particulate matter in the benthic boundary layer. Surface storm events episodically caused extremely turbid conditions on the seafloor that persisted for several days, with particles being resuspended to more than 13 m above the seabed. The carbon flux in the near-bottom sediment trap peaked during storm events and also after a spring bloom in April, when fresh phytodetritus was observed in the bottom boundary layer. While resuspension events can represent a major stressor for sponges, limiting their filtration capability and remobilizing them, episodes of strong currents and lateral particle transport likely play an important role in food supply and the replenishment of nutrients and oxygen. Our results contextualize human-induced threats such as bottom fishing and climate change by providing more knowledge of the natural environmental conditions under which sponge grounds persist.publishedVersio

The Microbiome and Occurrence of Methanotrophy in Carnivorous Sponges

As shown by recent studies, filter-feeding sponges are known to host a wide variety of microorganisms. However, the microbial community of the non-filtering carnivorous sponges (Porifera, Cladorhizidae) has been the subject of less scrutiny. Here, we present the results from a comparative study of the methanotrophic carnivorous sponge Cladorhiza methanophila from a mud volcano-rich area at the Barbados Accretionary Prism, and five carnivorous species from the Jan Mayen Vent Field (JMVF) at the Arctic Mid-Ocean Ridge. Results from 16S rRNA microbiome data indicate the presence of a diverse assemblage of associated microorganisms in carnivorous sponges mainly from the Gamma- and Alphaproteobacteria, Flavobacteriaceae, and Thaumarchaeota. While the abundance of particular groups varied throughout the dataset, we found interesting similarities to previous microbiome results from non-carnivorous deep sea sponges, suggesting that the carnivorous sponges share characteristics of a previously hypothesized putative deep-sea sponge microbial community. Chemolithoautotrophic symbiosis was confirmed for C. methanophila through a microbial community with a high abundance of Methylococcales and very light isotopic δ13C and δ15N ratios (-60 to -66‰/3.5 to 5.2‰) compared to the other cladorhizid species (-22 to -24‰/8.5 to 10.5‰). We provide evidence for the presence of putative sulfur-oxidizing Gammaproteobacteria in the arctic cladorhizids; however, δ13C and δ15N signatures did not provide evidence for significant chemoautotrophic symbiosis in this case, and the slightly higher abundance of cladorhizids at the JMVF site compared to the nearby deep sea likely stem from an increased abundance of prey rather than a more direct vent association. The phylogenetic position of C. methanophila in relation to other carnivorous sponges was established using a three-gene phylogenetic analysis, and it was found to be closely related to other non-methanotrophic Cladorhiza species with a similar morphology included in the dataset, suggesting a recent origin for methanotrophy in this species. C. methanophila remains the only known carnivorous sponge with a strong, chemolithoautotrophic symbiont association, and methanotrophic symbiosis does not seem to be a widespread property within the Cladorhizidae.publishedVersio

Taxonomy, biogeography and DNA barcodes of Geodiaspecies (Porifera, Demospongiae, Tetractinellida) in the Atlantic boreo-arctic region

Geodia species north of 60°N in the Atlantic appeared in the literature for the first time when Bowerbank described Geodia barretti and G. macandrewii in 1858 from western Norway. Since then, a number of species have been based on material from various parts of the region: G. simplex, Isops phlegraei, I. pallida, I. sphaeroides, Synops pyriformis, G. parva, G. normani, G. atlantica, Sidonops mesotriaena (now called G. hentscheli), and G. simplicissima. In addition to these 12 nominal species, four species described from elsewhere are claimed to have been identified in material from the northeast Atlantic, namely G. nodastrella and G. cydonium (and its synonyms Cydonium muelleri and Geodia gigas ). In this paper, we revise the boreo-arctic Geodia species using morphological, molecular, and biogeographical data. We notably compare northwest and northeast Atlantic specimens. Biological data (reproduction, biochemistry, microbiology, epibionts) for each species are also reviewed. Our results show that there are six valid species of boreo-arctic Atlantic Geodia while other names are synonyms or mis-identifications. Geodia barretti, G. atlantica, G. macandrewii, and G. hentscheli are well established and widely distributed. The same goes for Geodia phlegraei, but this species shows a striking geographical and bathymetric variation, which led us to recognize two species, G. phlegraei and G. parva(here resurrected). Some Geodia are arctic species (G. hentscheli, G. parva), while others are typically boreal (G. atlantica, G. barretti, G. phlegraei , G. macandrewii). No morphological differences were found between specimens from the northeast and northwest Atlantic, except for G. parva . The Folmer cytochrome oxidase subunit I (COI) fragment is unique for every species and invariable over their whole distribution range, except for G. barretti which had two haplotypes. 18S is unique for four species but cannot discriminate G. phlegraei and G. parva. Two keys to the boreo-arctic Geodia are included, one based on external morphology, the other based on spicule morphology

Glass sponge grounds on the Scotian Shelf and their associated biodiversity

Emerald Basin on the Scotian Shelf off Nova Scotia, Canada, is home to a globally unique population of the glass sponge Vazella pourtalesi. Through the analysis of both in situ photographs and trawl catch data from annual multispecies bottom-trawl surveys, we examined community composition, species density, and abundance of epibenthos and fish associated with V. pourtalesi compared to locations without this sponge. Using generalized linear models and analysis of similarities, the importance of V. pourtalesi in enhancing species density and abundance of the associated epibenthic community was assessed against that of the hard substrate on which it settles. Our results indicated that the megafaunal assemblage associated with V. pourtalesi was significantly different in composition and higher in species density and abundance compared to locations without V. pourtalesi. Analysis of similarity of trawl catch data indicated that fish communities associated with the sponge grounds are significantly different from those without V. pourtalesi, although no species were found exclusively on the sponge grounds. Our study provides further evidence of the role played by sponge grounds in shaping community structure and biodiversity of associated deep-sea epibenthic and fish communities. The mechanism for biodiversity enhancement within the sponge grounds formed by V. pourtalesi is likely the combined effect of both the sponge itself and its attachment substrate, which together comprise the habitat of the sponge grounds. We also discuss the role of habitat provision between the mixed-species tetractinellid sponges of the Flemish Cap and the monospecific glass sponge grounds of Emerald Basin.publishedVersio

A Deep-Sea Sponge Loop? Sponges Transfer Dissolved and Particulate Organic Carbon and Nitrogen to Associated Fauna

Cold-water coral reefs and sponge grounds are deep-sea biological hotspots, equivalent to shallow-water tropical coral reefs. In tropical ecosystems, biodiversity and productivity are maintained through efficient recycling pathways, such as the sponge loop. In this pathway, encrusting sponges recycle dissolved organic matter (DOM) into particulate detritus. Subsequently, the sponge-produced detritus serves as a food source for other organisms on the reef. Alternatively, the DOM stored in massive sponges was recently hypothesized to be transferred to higher trophic levels through predation of these sponges, instead of detritus production. However, for deep-sea sponges, the existence of all prerequisite, consecutive steps of the sponge loop have not yet been established. Here, we tested whether cold-water deep-sea sponges, similar to their tropical shallow-water counterparts, take up DOM and transfer assimilated DOM to associated fauna via either detritus production or predation. We traced the fate of 13carbon (C)- and 15nitrogen (N)-enriched DOM and particulate organic matter (POM) in time using a pulse-chase approach. During the 24-h pulse, the uptake of 13C/15N-enriched DOM and POM by two deep-sea sponge species, the massive species Geodia barretti and the encrusting species Hymedesmia sp., was assessed. During the subsequent 9-day chase in label-free seawater, we investigated the transfer of the consumed food by sponges into brittle stars via two possible scenarios: (1) the production and subsequent consumption of detrital waste or (2) direct feeding on sponge tissue. We found that particulate detritus released by both sponge species contained C from the previously consumed tracer DOM and POM, and, after 9-day exposure to the labeled sponges and detritus, enrichment of 13C and 15N was also detected in the tissue of the brittle stars. These results therefore provide the first evidence of all consecutive steps of a sponge loop pathway via deep-sea sponges. We cannot distinguish at present whether the deep-sea sponge loop is acting through a detrital or predatory pathway, but conclude that both scenarios are feasible. We conclude that sponges could play an important role in the recycling of DOM in the many deep-sea ecosystems where they are abundant, although in situ measurements are needed to confirm this hypothesis.publishedVersio

The First Cut Is the Deepest: Trawl Effects on a Deep-Sea Sponge Ground Are Pronounced Four Years on

Few studies have described the effects of physical disturbance and post-recovery of deep-sea benthic communities. Here, we explore the status of deep-sea sponge ground communities four years after being impacted by an experimental bottom trawl. The diversity and abundance of epibenthic megafauna of two distinct benthic communities in disturbed versus control areas were surveyed using a remotely operated vehicle on the Schulz Bank, Arctic Ocean. Four years after disturbance, megafaunal densities of the shallow (∼600 m depth) and deep (∼1,400 m depth) sites were significantly lower on the disturbed patches compared to the control areas. Multivariate analyses revealed a distinct separation between disturbed and control communities for both sites, with trawling causing 29–58% of the variation. Many epibenthic morphotypes were significantly impacted by the trawl, including ascidians, Geodia parva, Hexactinellida spp., Craniella infrequens, Lissodendoryx complicata, Haliclonia sp. Stylocordyla borealis, Gersemia rubiformis and Actiniaria sp. However, we found some smaller morphospecies to be equally abundant with control transects, including Polymastia thielei, Geodia hentscheli, and Stelletta rhaphidiophora, reflecting lower trawl impact for these morphotypes. Overall, our results suggest that these are fragile ecosystems that require much more time than four years to recover from physical disturbance typical of trawling activities.publishedVersio