Javier Cristobo

Deep-sea sponge grounds of the Flemish Cap, Flemish Pass and the Grand Banks of Newfoundland (Northwest Atlantic Ocean): Distribution and species composition

Abstract Distribution and species composition of deep-sea sponge grounds of the Flemish Cap, Flemish Pass and the Grand Banks of Newfoundland are described based on Spanish/EU bottom trawl groundfish surveys between 40 and 1500 m depth. Four areas with large catches of sponges and at least 30 different species have been identified in the study area. Geodia barretti, Geodia macandrewii, Geodia phlegraei, Stryphnus ponderosus and Stelletta normani are the main structural sponges and constitute more than 94% of the total invertebrate biomass of these grounds. The temperature and salinity observed over these bottoms ranged between 3.38 and 3.84°C and between 34.85 and 34.90‰, respectively. The biomass of deep-water sponges per swept area was significantly higher on lightly or untrawled bottoms than in the grounds that are regularly fished. Data from trawl groundfish surveys cannot map the deep-sea sponge grounds to a precision less than the trawl distance of 1.5 nm. Nevertheless it has been used by the Northwest Atlantic Fisheries Organization (NAFO), along with additional Canadian data, to implement the 61/105 United Nations General Assembly Resolution in closing six areas to bottom fishing activities to protect the sponge grounds of the NAFO Regulatory Area.

Bone-eating worms from the Antarctic: the contrasting fate of whale and wood remains on the Southern Ocean seafloor.

We report the results from the first experimental study of the fate of whale and wood remains on the Antarctic seafloor. Using a baited free-vehicle lander design, we show that whale-falls in the Antarctic are heavily infested by at least two new species of bone-eating worm, Osedax antarcticus sp. nov. and Osedax deceptionensis sp. nov. In stark contrast, wood remains are remarkably well preserved with the absence of typical wood-eating fauna such as the xylophagainid bivalves. The combined whale-fall and wood-fall experiment provides support to the hypothesis that the Antarctic circumpolar current is a barrier to the larvae of deep-water species that are broadly distributed in other ocean basins. Since humans first started exploring the Antarctic, wood has been deposited on the seafloor in the form of shipwrecks and waste; our data suggest that this anthropogenic wood may be exceptionally well preserved. Alongside the new species descriptions, we conducted a comprehensive phylogenetic analyses of Osedax, suggesting the clade is most closely related to the frenulate tubeworms, not the vestimentiferans as previous reported.

Chemo-ecological studies on hexactinellid sponges from the Southern Ocean

Hexactinellids (glass sponges) are an understudied class with syncytial organization and poor procariotic associations, thought to lack defensive secondary metabolites. Poriferans, though, are outstanding sources of bioactive compounds; nonetheless, a growing suspicion suggests that many of these chemicals could be symbiont-derived. In Polar latitudes, sponges are readily invaded by diatoms, which could provide natural products. Hexactinellids are typical of deep waters; but in Antarctica, they dominate the upper shelf providing shelter and food supply to many opportunistic mesograzers and macroinvertebrates, which exert strong ecological pressures on them. Aiming to examine the incidence of defensive activities of hexactinellids against consumption, feeding experiments were conducted using their lipophilic fractions. Antarctic hexactinellid and demosponge extracts were tested against the asteroid Odontaster validus and the amphipod Cheirimedon femoratus as putative sympatric, omnivorous consumers. Hexactinellids yielded greater unpalatable activities towards the amphipod, while no apparent allocation of lipophilic defenses was noted. After chemical analyses on the lipophilic fractions from these Antarctic glass sponges, quite similar profiles were revealed, and no peculiar secondary metabolites, comparable to those characterizing other poriferans, were found. Instead, the lipidic compounds 5α(H)-cholestan-3-one and two glycoceramides were isolated for their particular outspread presence in our samples. The isolated compounds were further assessed in asteroid feeding assays, and their occurrence was evaluated for chemotaxonomical purposes in all the Antarctic samples as well as in glass sponges from other latitudes by NMR and MS. Characteristic sphingolipids are proposed as chemical markers in Hexactinellida, with possible contributions to the classification of this unsettled class.

Two new Antarctic Ophryotrocha (Annelida : Dorvilleidae) described from shallow-water whale bones

Marine invertebrate fauna associated with whale remains has lately attracted a great deal of interest. However, very little is known about this fauna in the Southern Ocean, an area with high abundances of cetaceans. To investigate the Antarctic organisms associated with these substrates, we conducted a study using whale bones in the shallow-waters of Deception Island (South Shetland Islands). In this paper, we describe two new species of Ophryotrocha (O. orensanzi sp. nov. and O. clava sp. nov.) from a minke whale (Balaenoptera acutorostrata) fresh caudal vertebra experimentally deployed for about a year and from an unknown whale vertebra presumably dating back to the early twentieth century whaling operations. Ophryotrocha clava sp. nov., found in relative high abundance in the fresh bone, is hypothesized to be an opportunistic species in the context of Antarctic shallow-water organically enriched environments. Ophryotrocha orensanzi sp. nov. appears to be the same species as the unnamed Palpiphitime sp., near lobifera, formerly reported from a nearby area. Phylogenetic analyses based on the nuclear gene H3 and the mitochondrial genes COI and 16S, using MrBayes and Maximum Likelihood analyses, show that O. clava sp. nov. is close to Iphitime hartmanae and is included in the ‘hartmanni’ clade, while O. orensanzi sp. nov. falls in the ‘lobifera’ clade. Remarks about their feeding preferences and ecology are also given. Our findings seem to suggest that members of the genus Ophryotrocha are important components of organically enriched Southern Ocean environments, as has been reported for this clade in other geographic areas.

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.

Bone-Eating Worms Spread: Insights into Shallow-Water Osedax (Annelida, Siboglinidae) from Antarctic, Subantarctic, and Mediterranean Waters

Osedax, commonly known as bone-eating worms, are unusual marine annelids belonging to Siboglinidae and represent a remarkable example of evolutionary adaptation to a specialized habitat, namely sunken vertebrate bones. Usually, females of these animals live anchored inside bone owing to a ramified root system from an ovisac, and obtain nutrition via symbiosis with Oceanospirillales gamma-proteobacteria. Since their discovery, 26 Osedax operational taxonomic units (OTUs) have been reported from a wide bathymetric range in the Pacific, the North Atlantic, and the Southern Ocean. Using experimentally deployed and naturally occurring bones we report here the presence of Osedax deceptionensis at very shallow-waters in Deception Island (type locality; Antarctica) and at moderate depths near South Georgia Island (Subantarctic). We present molecular evidence in a new phylogenetic analysis based on five concatenated genes (28S rDNA, Histone H3, 18S rDNA, 16S rDNA, and cytochrome c oxidase I–COI–), using Maximum Likelihood and Bayesian inference, supporting the placement of O. deceptionensis as a separate lineage (Clade VI) although its position still remains uncertain. This phylogenetic analysis includes a new unnamed species (O. ‘mediterranea’) recently discovered in the shallow-water Mediterranean Sea belonging to Osedax Clade I. A timeframe of the diversification of Osedax inferred using a Bayesian framework further suggests that Osedax diverged from other siboglinids during the Middle Cretaceous (ca. 108 Ma) and also indicates that the most recent common ancestor of Osedax extant lineages dates to the Late Cretaceous (ca. 74.8 Ma) concomitantly with large marine reptiles and teleost fishes. We also provide a phylogenetic framework that assigns newly-sequenced Osedax endosymbionts of O. deceptionensis and O. ‘mediterranea’ to ribospecies Rs1. Molecular analysis for O. deceptionensis also includes a COI-based haplotype network indicating that individuals from Deception Island and the South Georgia Island (ca. 1,600 km apart) are clearly the same species, confirming the well-developed dispersal capabilities reported in other congeneric taxa. In addition, we include a complete description of living features and morphological characters (including scanning and transmission electron microscopy) of O. deceptionensis, a species originally described from a single mature female, and compare it to information available for other congeneric OTUs.

On the identity of two Antarctic brooding nemerteans: redescription of Antarctonemertes valida (Burger, 1893) and description of a new species in the genus Antarctonemertes Friedrich, 1955 (Nemertea, Hoplonemertea)

Nemerteans (ribbon worms) constitute an abundant and occasionally conspicuous group of benthic invertebrates in the Southern Ocean. Although recent work has confirmed that this group is far more diverse than previously recognized, the Antarctic nemertean fauna remains poorly understood when compared to other geographic regions. In most cases, the taxonomic information on the known nemertean fauna is incomplete for this region and/or has been inappropriately documented. As a consequence, many of the species described are considered species inquirendae. Among the nearly 50 species described so far for the Southern Ocean, two hoplonemerteans are known to brood eggs in cocoons: Amphiporus incubator Joubin, 1914 and Amphiporus michaelseni Bürger, 1895a. Here, we redescribe Antarctonemertes valida (Bürger, 1893), a senior synonym of A. michaelseni, and describe a new congeneric species, Antarctonemertes riesgoae sp. nov. Both species show a similar reproductive strategy by brooding their cocoons, and similar external appearance, but clearly differ in other aspects of their morphology, such as the cephalic coloration pattern and the number of proboscidial nerves. We provide novel information about their life habitus, reproductive behaviour, internal anatomy, and their phylogenetic placement within hoplonemerteans using one nuclear (28S rRNA) and two mitochondrial [cytochrome c oxidase subunit I (COI) and 16S rRNA] markers. We also provide a parsimony haplotype network using 16S rRNA, COI, and the internal transcribed spacer region 2 (ITS-2) showing a clear distinction between individuals of both species. Our results stress the need of combining molecular and morphological information when dealing with closely related species of nemerteans.

Management Strategies to Limit the Impact of Bottom Trawling on VMEs in the High Seas of the SW Atlantic

For the past nine years, the issue of protecting biodiversity in the deep sea in areas beyond national jurisdiction – the high seas (HS) – has been widely debated by the United Nations General Assembly (UNGA) and in other international fora. The UNGA adopted a series of resolutions, beginning with Resolution 59/25 in 2004, which called on high seas fishing nations and regional fisheries management organisations (RFMOs) to take urgent action to protect vulnerable marine ecosystems (VMEs) from destructive fishing practices in areas beyond national jurisdiction (Rogers & Gianni, 2010; UNGA, 2004). In December 2006 the UNGA adopted resolution 61/105 on Sustainable Fisheries, calling on flag states, RFMOs and arrangements to immediately act for the sustainable management of fish stocks and to protect VMEs from destructive fishing practices (Portela et al., 2010; UNGA, 2007). In 2009, the UNGA adopted Resolution 64/72 reaffirming the 2006 resolution and made it clear that the measures called for in Resolution 61/105 should be implemented, consistent with the 2009 FAO International Guidelines for the Management of Deep-Sea Fisheries in the High Seas (FAO Deepwater Guidelines), by flag states and RFMOs. Resolution 64/72 placed particular emphasis on conducting impact assessments of bottom fisheries on the high seas (UNGA, 2009: Paras 119–120).

Chemical Interactions in Antarctic Marine Benthic Ecosystems

Antarctic marine ecosystems are immersed in an isolated, relatively constant environment where the organisms inhabiting their benthos are mainly sessile suspension feeders. For these reasons, physical and chemical biotic interactions play an essential role in structuring these marine benthic communities (Dayton et al., 1974; Orejas et al., 2000). These interactions may include diverse strategies to avoid predation (e.g. Iken et al., 2002), competition for space or food (e.g. Bowden et al., 2006) and avoiding fouling (e.g. Rittschof, 2001; Peters et al., 2010). For instance, in the marine benthos, one of the most extended effective strategies among sessile soft-bodied organisms is chemical defense, mediated by several bioactive natural products mostly considered secondary metabolites (e.g. Paul et al., 2011). The study of the “chemical network” (chemical ecology interactions) structuring the communities provides information about the ecology and biology of the involved species, the function and the structure of the community and, simultaneously, it may lead to the discovery of new compounds useful to humans for their pharmacological potential (e.g. Avila, 1995; Bhakuni, 1998; Munro et al., 1999; Faulkner, 2000; Lebar et al., 2007; Avila et al., 2008). In the last three decades, the study of marine chemical ecology has experienced great progress, thanks to the new technological advances for collecting and studying marine samples, and the possibility of identification of molecules with smaller amounts of compounds (e.g. Paul et al., 2006, 2011; Blunt et al., 2011).

A new species of Phorbas (Porifera: Poecilosclerida) from the Bellingshausen Sea, Antarctica

Phorbas is a common genus with cosmopolitan distribution. A new species of sponge, Phorbas megasigma sp. nov. (Porifera: Poecilosclerida: Hymedesmiidae) is described from material collected during the third Spanish expedition on the study of the Antarctic benthos, ‘Bentart 03’. Phorbas megasigma is closely related to P. nexus but differs in the possession of arcuate chelae and very big sigmata as microscleres.