Amy R. Baco

Do mussels take wooden steps to deep-sea vents?

Symbiont-containing mussels (Mytilidae) are found at hydrothermal vents and cold seeps on the ocean floor, but it is not known whether these taxa represent an ancient lineage endemic to these surroundings or are more recent invaders. Here we show that several small and poorly known mussels, commonly found on sunken wood and whale bones in the deep sea, are closely related to vent and seep taxa, and that this entire group is divergent from other Mytilidae. Our results indicate that vents and seeps were recently invaded by modern mytilid taxa and suggest that decomposing wood and bone may have served as ‘steps’ for the introduction of mytilid taxa to vents and seeps.

Biotic and Human Vulnerability to Projected Changes in Ocean Biogeochemistry over the 21st Century

Mora and colleagues show that ongoing greenhouse gas emissions are likely to have a considerable effect on several biogeochemical properties of the worlds oceans, with potentially serious consequences for biodiversity and human welfare.

Vestimentiferan on a Whale Fall

Discovery of chemosynthetic communities associated with whale bones led to the hypothesis that whale falls may serve as stepping-stones for faunal dispersal between disjunct hydrothermal vents and cold seeps on the ocean floor (1). The initial observation was followed by a faunal inventory that revealed a diverse assemblage of microbes and invertebrates, supported by chemoautotrophic production, living in close proximity to whale remains (2, 3). To date, the conspicuous absence from whale falls of vestimentiferan tubeworms (a predominant constituent of eastern Pacific vent and seep habitats) has been a major objection to the stepping-stone hypothesis (4-5). We report the first evidence of a vestimentiferan tubeworm associated with a whale fall (Fig. 1). The tubeworm, Escarpia spicata, was identified by morphological criteria and DNA sequence data from a portion of the mitochondrial cytochrome oxidase C subunit I (COI) gene. Additionally, the bacterial endosymbiont in the tubeworm possessed a 16S rRNA gene that was similar to that of endosymbionts from vestimentiferans in sedimented cold-seep environments.

Sediment community structure around a whale skeleton in the deep Northeast Pacific: Macrofaunal, microbial and bioturbation effects

Chemoautotrophic communities on lipid-rich whale skeletons are known from a total of 16 modern and fossil sites in the deep Pacific Ocean. While the attached fauna of modern whale bones has been studied, the impact of whale falls on surrounding sediment assemblages remains largely unevaluated. Using the research submersible Alvin, we sampled the sediment community at distances of 0, 0.5, 1, 2, 4, and ∼100 m from the lipid-rich skeleton of a 21 m balaenopterid on the 1240 m seafloor in Santa Catalina Basin. When sampled in 1988 and 1991, the skeleton had been on the seafloor for >4 yr and supported a large attached chemoautotrophic assemblage. Sedimentary organic content, microbial biomass and bacterial abundance were not significantly different near the skeleton than in background sediments, and pore-water sulfide concentrations were only modestly elevated (to ⩽20 μM) adjacent to the bones. The species composition of infaunal macrobenthos near the skeleton was similar to that in background sediments, providing little evidence of a specialized enrichment and/or sulfophilic assemblage. Nonetheless, macrofaunal abundance within 0.5 m of the skeleton was reduced by >40%, due to a decline in the paraonid polychaete Levinsenia oculata. The reduction in L. oculata (the community dominant) caused a sharp increase in rarefaction diversity near the skeleton. Bioturbation intensities, evaluated from 234Th profiles, were also dramatically reduced in sediments near the skeleton, as were rates of extracellular lipase activity. We postulate that reduced infaunal abundance and bioturbation near the skeleton resulted from the interference effects of vesicomyid clam-shell debris, and that the low bioturbation rates in turn limited extracellular lipase activity. We conclude that whale skeletons, and the remains of their associated chemoautotrophic assemblages, may physically impact nearby sediment communities for years after the organic and sulfide enrichment effects of whale falls have dissipated, yielding changes in infaunal diversity and bioturbation.

Hydrothermal Vents and Methane Seeps: Rethinking the Sphere of Influence

Although initially viewed as oases within a barren deep ocean, hydrothermal vent and methane seep communities are now recognized to interact with surrounding ecosystems on the sea floor and in the water column, and to affect global geochemical cycles. The importance of understanding these interactions is growing as the potential rises for disturbance from oil and gas extraction, seabed mining and bottom trawling. Here we synthesize current knowledge of the nature, extent and time and space scales of vent and seep interactions with background systems. We document an expanded footprint beyond the site of local venting or seepage with respect to elemental cycling and energy flux, habitat use, trophic interactions, and connectivity. Heat and energy are released, global biogeochemical and elemental cycles are modified, and particulates are transported widely in plumes. Hard and biotic substrates produced at vents and seeps are used by “benthic background” fauna for attachment substrata, shelter, and access to food via grazing or through position in the current, while particulates and fluid fluxes modify planktonic microbial communities. Chemosynthetic production provides nutrition to a host of benthic and planktonic heterotrophic background species through multiple horizontal and vertical transfer pathways assisted by flow, gamete release, animal movements, and succession, but these pathways remain poorly known. Shared species, genera and families indicate that ecological and evolutionary connectivity exists among vents, seeps, organic falls and background communities in the deep sea; the genetic linkages with inactive vents and seeps and background assemblages however, are practically unstudied. The waning of venting or seepage activity generates major transitions in space and time that create links to surrounding ecosystems, often with identifiable ecotones or successional stages. The nature of all these interactions is dependent on water depth, as well as regional oceanography and biodiversity. Many ecosystem services are associated with the interactions and transitions between chemosynthetic and background ecosystems, for example carbon cycling and sequestration, fisheries production, and a host of non-market and cultural services. The quantification of the sphere of influence of vents and seeps could be beneficial to better management of deep-sea environments in the face of growing industrialization.

Molecular systematics of the bubblegum coral genera (Paragorgiidae, Octocorallia) and description of a new deep-sea species

Bubblegum octocorals (Paragorgia and Sibogagorgia) play an important ecological role in many deep-sea ecosystems. However, these organisms are currently threatened by destructive fishing methods such as bottom trawling. Taxonomic knowledge of conservation targets is necessary for the creation and implementation of efficient conservation strategies. However, for most deep-sea coral groups this knowledge remains incomplete. For instance, despite its similarities with Paragorgia, Sibogagorgia is particular in lacking polyp sclerites, which are present in groups like Paragorgia and the Coralliidae. Although two kinds of sclerites are very similar between Paragorgia and Sibogagorgia, other characters challenge the monophyly of these genera. Here we help to clarify the taxonomy and evolutionary relationships of the bubblegum octocorals and related taxa by examining molecular data. We employed nucleotide sequences of mitochondrial (ND6, ND6-ND3 intergenic spacer, ND3, ND2, COI, msh1 and 16S) and nuclear (28S and ITS2) genomic regions from several taxa to infer molecular phylogenetics and to examine the correspondence of morphological features with the underlying genetic information. Our data strongly supported the monophyly of the genus Paragorgia, the family Coralliidae (precious corals), and a group of undescribed specimens resembling Sibogagorgia. Further morphological observations were congruent regarding the uniqueness of the undescribed specimens, here defined as a new species, Sibogagorgia cauliflora sp. nov., which occurs in both sides of the North American landmass at depths below 1700 m. This new species resembles S. dennisgordoni with branching in one plane but has fairly different radiate sclerites and significantly divergent DNA sequences. The existence of several diagnostic characters of Sibogagorgia in S. cauliflora indicates that they indeed belong to this genus. It is however remarkable that a small number of medullar canals are also found in this species; medullar canals have been considered as the main diagnostic character of Paragorgia. Thus, the evidence generated here indicates that the presence or absence of these canals per se is not a conclusively diagnostic character for either genus. The lack of internal-node resolution in the inferred phylogenetic hypotheses of these genera does not allow us to propose a clear scenario regarding the evolution of these traits.

Population genetic structure of the Hawaiian precious coral Corallium lauuense (Octocorallia: Coralliidae) using microsatellites

Seamount fauna are threatened by destructive fisheries practices, yet little is known about the physical and biological processes (e.g., dispersal and connectivity) that maintain species on seamounts. Gorgonian octocorals are among the dominant epifaunal taxa of many seamounts and represent a model taxon with which to understand processes of dispersal and gene flow in seamount fauna. One of the more common deep-sea octocorals on the seamounts and islands of the Hawaiian Archipelago is the precious coral Corallium lauuense. Here, we present results of a preliminary study to examine the population genetic structure of widely-distributed populations of C. lauuense within and among eight Hawaiian seamounts using three highly polymorphic microsatellite loci. Genic diversity and population differentiation estimated from the number of alleles, heterozygosity, and a hierarchical analysis of molecular variance revealed relatively high levels of genetic diversity as well as low yet significant levels of population differentiation among several of the seamounts and islands (predominantly among population comparisons with any site and the Kauai and Makapu’u coral beds). Despite these genetic differences between sites, population differentiation based on F ST and R ST for all sites was not significant at any locus. No linkage disequilibrium or pattern of isolation by distance was observed, and heterozygote deficiency was found in every population within at least one locus. The low heterozygosity throughout the Hawaiian Archipelago raises the concern that this species may be suffering from inbreeding depression. Further investigation of precious coral population demographic structure is needed to assess the risk of habitat loss and fisheries activities on these seamounts.

Diversity of Zoanthids (Anthozoa: Hexacorallia) on Hawaiian Seamounts: Description of the Hawaiian Gold Coral and Additional Zoanthids

The Hawaiian gold coral has a history of exploitation from the deep slopes and seamounts of the Hawaiian Islands as one of the precious corals commercialised in the jewellery industry. Due to its peculiar characteristic of building a scleroproteic skeleton, this zoanthid has been referred as Gerardia sp. (a junior synonym of Savalia Nardo, 1844) but never formally described or examined by taxonomists despite its commercial interest. While collection of Hawaiian gold coral is now regulated, globally seamounts habitats are increasingly threatened by a variety of anthropogenic impacts. However, impact assessment studies and conservation measures cannot be taken without consistent knowledge of the biodiversity of such environments. Recently, multiple samples of octocoral-associated zoanthids were collected from the deep slopes of the islands and seamounts of the Hawaiian Archipelago. The molecular and morphological examination of these zoanthids revealed the presence of at least five different species including the gold coral. Among these only the gold coral appeared to create its own skeleton, two other species are simply using the octocoral as substrate, and the situation is not clear for the final two species. Phylogenetically, all these species appear related to zoanthids of the genus Savalia as well as to the octocoral-associated zoanthid Corallizoanthus tsukaharai, suggesting a common ancestor to all octocoral-associated zoanthids. The diversity of zoanthids described or observed during this study is comparable to levels of diversity found in shallow water tropical coral reefs. Such unexpected species diversity is symptomatic of the lack of biological exploration and taxonomic studies of the diversity of seamount hexacorals.

A synthesis of genetic connectivity in deep‐sea fauna and implications for marine reserve design

With anthropogenic impacts rapidly advancing into deeper waters, there is growing interest in establishing deep‐sea marine protected areas (MPAs) or reserves. Reserve design depends on estimates of connectivity and scales of dispersal for the taxa of interest. Deep‐sea taxa are hypothesized to disperse greater distances than shallow‐water taxa, which implies that reserves would need to be larger in size and networks could be more widely spaced; however, this paradigm has not been tested. We compiled population genetic studies of deep‐sea fauna and estimated dispersal distances for 51 studies using a method based on isolation‐by‐distance slopes. Estimates of dispersal distance ranged from 0.24 km to 2028 km with a geometric mean of 33.2 km and differed in relation to taxonomic and life‐history factors as well as several study parameters. Dispersal distances were generally greater for fishes than invertebrates with the Mollusca being the least dispersive sampled phylum. Species that are pelagic as adults were more dispersive than those with sessile or sedentary lifestyles. Benthic species from soft‐substrate habitats were generally less dispersive than species from hard substrate, demersal or pelagic habitats. As expected, species with pelagic and/or feeding (planktotrophic) larvae were more dispersive than other larval types. Many of these comparisons were confounded by taxonomic or other life‐history differences (e.g. fishes being more dispersive than invertebrates) making any simple interpretation difficult. Our results provide the first rough estimate of the range of dispersal distances in the deep sea and allow comparisons to shallow‐water assemblages. Overall, dispersal distances were greater for deeper taxa, although the differences were not large (0.3–0.6 orders of magnitude between means), and imbalanced sampling of shallow and deep taxa complicates any simple interpretation. Our analyses suggest the scales of dispersal and connectivity for reserve design in the deep sea might be comparable to or slightly larger than those in shallow water. Deep‐sea reserve design will need to consider the enormous variety of taxa, life histories, hydrodynamics, spatial configuration of habitats and patterns of species distributions. The many caveats of our analyses provide a strong impetus for substantial future efforts to assess connectivity of deep‐sea species from a variety of habitats, taxonomic groups and depth zones.

Comparing Molecular Variation to Morphological Species Designations in the Deep-Sea Coral Narella Reveals New Insights into Seamount Coral Ranges

Recent studies have countered the paradigm of seamount isolation, confounding conservation efforts at a critical time. Efforts to study deep-sea corals, one of the dominant taxa on seamounts, to understand seamount connectivity, are hampered by a lack of taxonomic keys. A prerequisite for connectivity is species overlap. Attempts to better understand species overlap using DNA barcoding methods suggest coral species are widely distributed on seamounts and nearby features. However, no baseline has been established for variation in these genetic markers relative to morphological species designations for deep-sea octocoral families. Here we assess levels of genetic variation in potential octocoral mitochondrial barcode markers relative to thoroughly examined morphological species in the genus Narella. The combination of six markers used here, approximately 3350 bp of the mitochondrial genome, resolved 83% of the morphological species. Our results show that two of the markers, ND2 and NCR1, are not sufficient to resolve genera within Primnoidae, let alone species. Re-evaluation of previous studies of seamount octocorals based on these results suggest that those studies were looking at distributions at a level higher than species, possibly even genus or subfamily. Results for Narella show that using more markers provides haplotypes with relatively narrow depth ranges on the seamounts studied. Given the lack of 100% resolution of species with such a large portion of the mitochondrial genome, we argue that previous genetic studies have not resolved the degree of species overlap on seamounts and that we may not have the power to even test the hypothesis of seamount isolation using mitochondrial markers, let alone refute it. Thus a precautionary approach is advocated in seamount conservation and management, and the potential for depth structuring should be considered.