Hydrothermal vent fauna of the Galápagos Rift: updated species list with new records.

The sighting of giant bivalves and tubeworms at the Rose Garden vent field on the Galápagos Rift in 1977 marked the discovery of hydrothermal vents, a turning point for modern biology. The following decade saw a flurry of taxonomic descriptions of vent endemic species from the first vents. With the finding of high-temperature "black smokers" on the East Pacific Rise, exploration shifted away from Galápagos. A faunal list of Galápagos vents with 65 species was published in 1991, then updated to 74 species in 2006. Since then, few expeditions returned to the Galápagos Rift. Here, we revisited several Galápagos vents including recently confirmed high-temperature sites and inactive sulfide mounds. From our collecting efforts and observations, as well as revisions from the literature, we update the faunal list to 92 species including 15 new records, restricted to obvious vent associates. Accurate regional faunal lists are important for understanding the biogeography of vent fauna, and our list will also be valuable for setting management strategies.

Differential patterns of connectivity in Western Pacific hydrothermal vent metapopulations: A comparison of biophysical and genetic models.

Hydrothermal ecosystems face threats from planned deep-seabed mining activities, despite the fact that patterns of realized connectivity among vent-associated populations and communities are still poorly understood. Since populations of vent endemic species depend on larval dispersal to maintain connectivity and resilience to habitat changes, effective conservation strategies for hydrothermal ecosystems should include assessments of metapopulation dynamics. In this study, we combined population genetic methods with biophysical models to assess strength and direction of gene flow within four species of the genus Alviniconcha (A. boucheti, A. kojimai, A. strummeri and A. hessleri) that are ecologically dominant taxa at Western Pacific hydrothermal vents. In contrast to predictions from dispersal models, among-basin migration in A. boucheti occurred predominantly in an eastward direction, while populations within the North Fiji Basin were clearly structured despite the absence of oceanographic barriers. Dispersal models and genetic data were largely in agreement for the other Alviniconcha species, suggesting limited between-basin migration for A. kojimai, lack of genetic structure in A. strummeri within the Lau Basin and restricted gene flow between northern and southern A. hessleri populations in the Mariana back-arc as a result of oceanic current conditions. Our findings show that gene flow patterns in ecologically similar congeneric species can be remarkably different and surprisingly limited depending on environmental and evolutionary contexts. These results are relevant to regional conservation planning and to considerations of similar integrated analyses for any vent metapopulations under threat from seabed mining.

Species assemblage networks identify regional connectivity pathways among hydrothermal vents in the Northwest Pacific.

The distribution of species among spatially isolated habitat patches supports regional biodiversity and stability, so understanding the underlying processes and structure is a key target of conservation. Although multivariate statistics can infer the connectivity processes driving species distribution, such as dispersal and habitat suitability, they rarely explore the structure. Methods from graph theory, applied to distribution data, give insights into both connectivity pathways and processes by intuitively formatting the data as a network of habitat patches. We apply these methods to empirical data from the hydrothermal vent habitats of the Northwest Pacific. Hydrothermal vents are "oases" of biological productivity and endemicity on the seafloor that are imminently threatened by anthropogenic disturbances with unknown consequences to biodiversity. Here, we describe the structure of species assemblage networks at hydrothermal vents, how local and regional parameters affect their structure, and the implications for conservation. Two complementary networks were formed from an extensive species assemblage dataset: a similarity network of vent site nodes linked by weighted edges based on their pairwise assemblage similarity and a bipartite network of species nodes linked to vent site nodes at which they are present. Using these networks, we assessed the role of individual vent sites in maintaining network connectivity and identified biogeographic sub-regions. The three sub-regions and two outlying sites are separated by their spatial arrangement and local environmental filters. Both networks detected vent sites that play a disproportionately important role in regional pathways, while the bipartite network also identified key vent sites maintaining the distinct species assemblages of their sub-regions. These regional connectivity pathways provide insights into historical colonization routes, while sub-regional connectivity pathways are of value when selecting sites for conservation and/or estimating the multivent impacts from proposed deep-sea mining.

Redescription of Bathymodiolus septemdierum Hashimoto and Okutani, 1994 (Bivalvia, Mytilida, Mytilidae), a mussel broadly distributed across hydrothermal vent locations in the western Pacific and Indian Oceans.

Mussels of the genus Bathymodiolus Kenk & Wilson belong to the foundation fauna at hydrothermal vents in the global deep sea. In the western Pacific and Indian oceans, the three nominal taxa B. septemdierum Hashimoto and Okutani, B. brevior Cosel, Métivier & Okutani and B. marisindicus Hashimoto are currently recognized as separate species despite morphological and genetic evidence for their conspecificity. All three are listed with the International Union for Conservation of Nature Red List based on highly restricted ranges. We compile and supplement existing morphometric and molecular data to revise the Bathymodiolus septemdierum species group. We redescribe B. septemdierum as a single species with B. brevior and B. marisindicus recognized as junior synonyms. Given the exceptionally broad range of B. septemdierum, we propose removal of these three taxa from the IUCN Red List.

Beta diversity differs among hydrothermal vent systems: Implications for conservation.

Deep-sea hydrothermal vent habitats are small, rare and support unique species through chemosynthesis. As this vulnerable ecosystem is increasingly threatened by human activities, management approaches should address biodiversity conservation. Diversity distribution data provide a useful basis for management approaches as patterns of ß-diversity (the change in diversity from site to site) can guide conservation decisions. Our question is whether such patterns are similar enough across vent systems to support a conservation strategy that can be deployed regardless of location. We compile macrofaunal species occurrence data for vent systems in three geological settings in the North Pacific: volcanic arc, back-arc and mid-ocean ridge. Recent discoveries in the Mariana region provide the opportunity to characterize diversity at many vent sites. We examine the extent to which diversity distribution patterns differ among the systems by comparing pairwise ß-diversity, nestedness and their additive components. A null model approach that tests whether species compositions of each site pair are more or less similar than random provides insight into community assembly processes. We resolve several taxonomic uncertainties and find that the Mariana arc and back-arc share only 8% of species despite their proximity. Species overlap, species replacement and richness differences create different diversity distributions within the three vent systems; the arc system exhibits much greater ß-diversity than both the back-arc and mid-ocean ridge systems which, instead, show greater nestedness. The influence of nestedness on ß-diversity also increased from the arc to back-arc to ridge. Community assembly processes appear more deterministic in the arc and ridge systems while back-arc site pairs deviate little from the null expectation. These analyses reflect the need for a variety of management strategies that consider the character of diversity distribution to protect hydrothermal vents, especially in the context of mining hydrothermal deposits.

Deep-Sea Misconceptions Cause Underestimation of Seabed-Mining Impacts.

Scientific misconceptions are likely leading to miscalculations of the environmental impacts of deep-seabed mining. These result from underestimating mining footprints relative to habitats targeted and poor understanding of the sensitivity, biodiversity, and dynamics of deep-sea ecosystems. Addressing these misconceptions and knowledge gaps is needed for effective management of deep-seabed mining.

Allopatric and Sympatric Drivers of Speciation in Alviniconcha Hydrothermal Vent Snails.

Despite significant advances in our understanding of speciation in the marine environment, the mechanisms underlying evolutionary diversification in deep-sea habitats remain poorly investigated. Here, we used multigene molecular clocks and population genetic inferences to examine processes that led to the emergence of the six extant lineages of Alviniconcha snails, a key taxon inhabiting deep-sea hydrothermal vents in the Indo-Pacific Ocean. We show that both allopatric divergence through historical vicariance and ecological isolation due to niche segregation contributed to speciation in this genus. The split between the two major Alviniconcha clades (separating A. boucheti and A. marisindica from A. kojimai, A. hessleri, and A. strummeri) probably resulted from tectonic processes leading to geographic separation, whereas the splits between co-occurring species might have been influenced by ecological factors, such as the availability of specific chemosynthetic symbionts. Phylogenetic origin of the sixth species, Alviniconcha adamantis, remains uncertain, although its sister position to other extant Alviniconcha lineages indicates a possible ancestral relationship. This study lays a foundation for future genomic studies aimed at deciphering the roles of local adaptation, reproductive biology, and host-symbiont compatibility in speciation of these vent-restricted snails.

Unique Solid Phase Microextraction Sampler Reveals Distinctive Biogeochemical Profiles among Various Deep-Sea Hydrothermal Vents.

Current methods for biochemical and biogeochemical analysis of the deep-sea hydrothermal vent ecosystems rely on water sample recovery, or in situ analysis using underwater instruments with limited range of analyte detection and limited sensitivity. Even in cases where large quantities of sample are recovered, labile dissolved organic compounds may not be detected due to time delays between sampling and preservation. Here, we present a novel approach for in situ extraction of organic compounds from hydrothermal vent fluids through a unique solid phase microextraction (SPME) sampler. These samplers were deployed to sample effluent of vents on sulphide chimneys, located on Axial Seamount in the North-East Pacific, in the Urashima field on the southern Mariana back-arc, and at the Hafa Adai site in the central Mariana back-arc. Among the compounds that were extracted, a wide range of unique organic compounds, including labile dissolved organic sulfur compounds, were detected through high-resolution LC-MS/MS, among which were biomarkers of anammox bacteria, fungi, and lower animals. This report is the first to show that SPME can contribute to a broader understanding of deep sea ecology and biogeochemical cycles in hydrothermal vent ecosystems.

An hypoxia-tolerant flatfish: consequences of sustained stress on the slender sole Lyopsetta exilis (Pleuronectidae) in the context of a changing ocean.

Slender sole Lyopsetta exilis is an abundant groundfish on the continental shelf and inner waters of British Columbia, Canada, where it reaches a maximum standard length of 44 cm. Benthic image surveys coupled with oxygen measurements in Saanich Inlet document a dense population in bottom conditions near anoxia (0.03 ml l-1 oxygen) where diel migrating zooplankton intersect the bottom; we confirm this species is a planktivore, which limits its depth range to the base of the migration layer. In a comparison with slender sole from a nearby well-oxygenated habitat, several probable effects of living in severe hypoxia emerge: both sexes are significantly smaller in Saanich and the sex ratio is male-skewed. Otoliths from the Saanich fish were difficult to read due to many checks, but both sexes were smaller at age with the largest female (20 cm) from the hypoxia zone registering 17 years. Hypoxia appears to have a direct consequence on growth despite good food supply in this productive basin. Hyperventilation, a low metabolic rate and a very low critical oxygen tension help this fish regulate oxygen uptake in severely hypoxic conditions; it will be particularly resilient as the incidence of hypoxia increases on the continental shelf. Data from small-mesh bottom-trawl surveys over four decades reveal an increase in mean annual catch per unit effort in southern regions of the province, including the outer shelf and the Strait of Georgia. The California Cooperative Oceanic Fisheries Investigations (CalCOFI) ichthyoplankton database records a general decline in fish larvae on the Oregon-California shelf since 1990, but slender sole larvae are increasing there, as they are in the Strait of Georgia. We project that the slender sole will gain relative benefits in the future warming, deoxygenated northeast Pacific Ocean.

Drivers of temporal beta diversity of a benthic community in a seasonally hypoxic fjord.

Global expansion of oxygen-deficient (hypoxic) waters will have detrimental effects on marine life in the Northeast Pacific Ocean (NEP) where some of the largest proportional losses in aerobic habitat are predicted to occur. However, few in situ studies have accounted for the high environmental variability in this region while including natural community-assembly dynamics. Here, we present results from a 14-month deployment of a benthic camera platform tethered to the VENUS cabled observatory in the seasonally hypoxic Saanich Inlet. Our time series continuously recorded natural cycles of deoxygenation and reoxygenation that allowed us to test whether a community from the NEP showed hysteresis in its recovery compared to hypoxia-induced decline, and to address the processes driving temporal beta diversity under variable states of hypoxia. Using high-frequency ecological time series, we reveal (i) differences in the response and recovery of the epibenthic community are rate-limited by recovery of the sessile species assemblage; (ii) both environmental and biological processes influence community assembly patterns at multiple timescales; and (iii) interspecific processes can drive temporal beta diversity in seasonal hypoxia. Ultimately, our results illustrate how different timescale-dependent drivers can influence the response and recovery of a marine habitat under increasing stress from environmental change.

Hydrothermal vent fields discovered in the southern Gulf of California clarify role of habitat in augmenting regional diversity.

Hydrothermal vent communities are distributed along mid-ocean spreading ridges as isolated patches. While distance is a key factor influencing connectivity among sites, habitat characteristics are also critical. The Pescadero Basin (PB) and Alarcón Rise (AR) vent fields, recently discovered in the southern Gulf of California, are bounded by previously known vent localities (e.g. Guaymas Basin and 21° N East Pacific Rise); yet, the newly discovered vents differ markedly in substrata and vent fluid attributes. Out of 116 macrofaunal species observed or collected, only three species are shared among all four vent fields, while 73 occur at only one locality. Foundation species at basalt-hosted sulfide chimneys on the AR differ from the functional equivalents inhabiting sediment-hosted carbonate chimneys in the PB, only 75 km away. The dominant species of symbiont-hosting tubeworms and clams, and peripheral suspension-feeding taxa, differ between the sites. Notably, the PB vents host a limited and specialized fauna in which 17 of 26 species are unknown at other regional vents and many are new species. Rare sightings and captured larvae of the 'missing' species revealed that dispersal limitation is not responsible for differences in community composition at the neighbouring vent localities. Instead, larval recruitment-limiting habitat suitability probably favours species differentially. As scenarios develop to design conservation strategies around mining of seafloor sulfide deposits, these results illustrate that models encompassing habitat characteristics are needed to predict metacommunity structure.

Oxygen limitations on marine animal distributions and the collapse of epibenthic community structure during shoaling hypoxia.

Deoxygenation in the global ocean is predicted to induce ecosystem-wide changes. Analysis of multidecadal oxygen time-series projects the northeast Pacific to be a current and future hot spot of oxygen loss. However, the response of marine communities to deoxygenation is unresolved due to the lack of applicable data on component species. We repeated the same benthic transect (n = 10, between 45 and 190 m depths) over 8 years in a seasonally hypoxic fjord using remotely operated vehicles equipped with oxygen sensors to establish the lower oxygen levels at which 26 common epibenthic species can occur in the wild. By timing our surveys to shoaling hypoxia events, we show that fish and crustacean populations persist even in severe hypoxia (<0.5 mL L(-1) ) with no mortality effects but that migration of mobile species occurs. Consequently, the immediate response to hypoxia expansion is the collapse of community structure; normally partitioned distributions of resident species coalesced and localized densities increased. After oxygen renewal and formation of steep oxygen gradients, former ranges re-established. High frequency data from the nearby VENUS subsea observatory show the average oxygen level at our site declined by ~0.05 mL L(-1) year(-1) over the period of our study. The increased annual duration of the hypoxic (<1.4 mL L(-1) ) and severely hypoxic periods appears to reflect the oxygen dynamics demonstrated in offshore source waters and the adjacent Strait of Georgia. Should the current trajectory of oxygen loss continue, community homogenization and reduced suitable habitat may become the dominant state of epibenthic systems in the northeast Pacific. In situ oxygen occurrences were not congruent with lethal and sublethal hypoxia thresholds calculated across the literature for major taxonomic groups indicating that research biases toward laboratory studies on Atlantic species are not globally applicable. Region-specific hypoxia thresholds are necessary to predict future impacts of deoxygenation on marine biodiversity.

Phenotypic variation and fitness in a metapopulation of tubeworms (Ridgeia piscesae Jones) at hydrothermal vents.

We examine the nature of variation in a hot vent tubeworm, Ridgeia piscesae, to determine how phenotypes are maintained and how reproductive potential is dictated by habitat. This foundation species at northeast Pacific hydrothermal sites occupies a wide habitat range in a highly heterogeneous environment. Where fluids supply high levels of dissolved sulphide for symbionts, the worm grows rapidly in a "short-fat" phenotype characterized by lush gill plumes; when plumes are healthy, sperm package capture is higher. This form can mature within months and has a high fecundity with continuous gamete output and a lifespan of about three years in unstable conditions. Other phenotypes occupy low fluid flux habitats that are more stable and individuals grow very slowly; however, they have low reproductive readiness that is hampered further by small, predator cropped branchiae, thus reducing fertilization and metabolite uptake. Although only the largest worms were measured, only 17% of low flux worms were reproductively competent compared to 91% of high flux worms. A model of reproductive readiness illustrates that tube diameter is a good predictor of reproductive output and that few low flux worms reached critical reproductive size. We postulate that most of the propagules for the vent fields originate from the larger tubeworms that live in small, unstable habitat patches. The large expanses of worms in more stable low flux habitat sustain a small, but long-term, reproductive output. Phenotypic variation is an adaptation that fosters both morphological and physiological responses to differences in chemical milieu and predator pressure. This foundation species forms a metapopulation with variable growth characteristics in a heterogeneous environment where a strategy of phenotypic variation bestows an advantage over specialization.

A year in hypoxia: epibenthic community responses to severe oxygen deficit at a subsea observatory in a coastal inlet.

Changes in ocean ventilation driven by climate change result in loss of oxygen in the open ocean that, in turn, affects coastal areas in upwelling zones such as the northeast Pacific. Saanich Inlet, on the west coast of Canada, is a natural seasonally hypoxic fjord where certain continental shelf species occur in extreme hypoxia. One study site on the VENUS cabled subsea network is located in the hypoxic zone at 104 m depth. Photographs of the same 5 m(2) area were taken with a remotely-controlled still camera every 2/3 days between October 6(th) 2009 and October 18(th) 2010 and examined for community composition, species behaviour and microbial mat features. Instruments located on a near-by platform provided high-resolution measurements of environmental variables. We applied multivariate ordination methods and a principal coordinate analysis of neighbour matrices to determine temporal structures in our dataset. Responses to seasonal hypoxia (0.1-1.27 ml/l) and its high variability on short time-scale (hours) varied among species, and their life stages. During extreme hypoxia, microbial mats developed then disappeared as a hippolytid shrimp, Spirontocaris sica, appeared in high densities (200 m(-2)) despite oxygen below 0.2 ml/l. The slender sole Lyopsetta exilis was abundant in severe hypoxia and diminished as oxygen increased in the summer. This planktivore may be responding to changes in the depth of the diurnal migration of zooplankton. While the squat lobster Munida quadrispina was common at all times, juveniles disappeared in fluctuating conditions. Despite low oxygen conditions, animal densities were high indicating that the risk from hypoxia is balanced by factors such as food availability and escape from less tolerant predators. As hypoxia increases on the continental shelf, we expect benthic communities to become dominated by low diversity, hypoxia-tolerant species of low commercial significance.

The sponge pump: the role of current induced flow in the design of the sponge body plan.

Sponges are suspension feeders that use flagellated collar-cells (choanocytes) to actively filter a volume of water equivalent to many times their body volume each hour. Flow through sponges is thought to be enhanced by ambient current, which induces a pressure gradient across the sponge wall, but the underlying mechanism is still unknown. Studies of sponge filtration have estimated the energetic cost of pumping to be <1% of its total metabolism implying there is little adaptive value to reducing the cost of pumping by using "passive" flow induced by the ambient current. We quantified the pumping activity and respiration of the glass sponge Aphrocallistes vastus at a 150 m deep reef in situ and in a flow flume; we also modeled the glass sponge filtration system from measurements of the aquiferous system. Excurrent flow from the sponge osculum measured in situ and in the flume were positively correlated (r>0.75) with the ambient current velocity. During short bursts of high ambient current the sponges filtered two-thirds of the total volume of water they processed daily. Our model indicates that the head loss across the sponge collar filter is 10 times higher than previously estimated. The difference is due to the resistance created by a fine protein mesh that lines the collar, which demosponges also have, but was so far overlooked. Applying our model to the in situ measurements indicates that even modest pumping rates require an energetic expenditure of at least 28% of the total in situ respiration. We suggest that due to the high cost of pumping, current-induced flow is highly beneficial but may occur only in thin walled sponges living in high flow environments. Our results call for a new look at the mechanisms underlying current-induced flow and for reevaluation of the cost of biological pumping and its evolutionary role, especially in sponges.

Deep-sea hydrothermal vent animals seek cool fluids in a highly variable thermal environment.

The thermal characteristics of an organism's environment affect a multitude of parameters, from biochemical to evolutionary processes. Hydrothermal vents on mid-ocean ridges are created when warm hydrothermal fluids are ejected from the seafloor and mixed with cold bottom seawater; many animals thrive along these steep temperature and chemical gradients. Two-dimensional temperature maps at vent sites have demonstrated order of magnitude thermal changes over centimetre distances and at time intervals from minutes to hours. To investigate whether animals adapt to this extreme level of environmental variability, we examined differences in the thermal behaviour of mobile invertebrates from aquatic habitats that vary in thermal regime. Vent animals were highly responsive to heat and preferred much cooler fluids than their upper thermal limits, whereas invertebrates from other aquatic environments risked exposure to warmer temperatures. Avoidance of temperatures well within their tolerated range may allow vent animals to maintain a safety margin against rapid temperature fluctuations and concomitant toxicity of hydrothermal fluids.

Long-term eruptive activity at a submarine arc volcano.

Three-quarters of the Earth's volcanic activity is submarine, located mostly along the mid-ocean ridges, with the remainder along intraoceanic arcs and hotspots at depths varying from greater than 4,000 m to near the sea surface. Most observations and sampling of submarine eruptions have been indirect, made from surface vessels or made after the fact. We describe here direct observations and sampling of an eruption at a submarine arc volcano named NW Rota-1, located 60 km northwest of the island of Rota (Commonwealth of the Northern Mariana Islands). We observed a pulsating plume permeated with droplets of molten sulphur disgorging volcanic ash and lapilli from a 15-m diameter pit in March 2004 and again in October 2005 near the summit of the volcano at a water depth of 555 m (depth in 2004). A turbid layer found on the flanks of the volcano (in 2004) at depths from 700 m to more than 1,400 m was probably formed by mass-wasting events related to the eruption. Long-term eruptive activity has produced an unusual chemical environment and a very unstable benthic habitat exploited by only a few mobile decapod species. Such conditions are perhaps distinctive of active arc and hotspot volcanoes.