Lauren S. Mullineaux

Larval dispersal potential of the tubeworm Riftia pachyptila at deep-sea hydrothermal vents

Hydrothermal vents are ephemeral because of frequent volcanic and tectonic activities associated with crust formation. Although the larvae of hydrothermal vent fauna can rapidly colonize new vent sites separated by tens to hundreds of kilometres, the mechanisms by which these larvae disperse and recruit are not understood. Here we integrate physiological, developmental and hydrodynamic data to estimate the dispersal potential of larvae of the giant tubeworm Riftia pachyptila. At in situ temperatures and pressures (2 °C and 250 atm), we estimate that the metabolic lifespan for a larva of R. pachyptila averages 38 days. In the measured flow regime at a fast-spreading ridge axis (9° 50′ N; East Pacific Rise), this lifespan results in potential along-ridge dispersal distances that rarely exceed 100 km. This limited dispersal results not from the physiological performance of the embryos and larvae, but instead from transport limitations imposed by periodic reversals in along-ridge flows and sustained episodes of across-ridge flow. The lifespan presented for these larvae can now be used to predict dispersal under current regimes at other hydrothermal vent sites.

Initial contact, exploration and attachment of barnacle (Balanus amphitrite) cyprids settling in flow

Settlement responses of barnacle (Balanus amphitrite) cyprids to boundary-layer flows were examined in laboratory flume-experiments. The leading-edge configuration of flat plates was altered in order to manipulate flows without changing surface topography or freestream velocity. Settlement along the plates correlated strongly with downstream gradients in shear stress. Analyses of video images taken during the experiments indicate that cyprids first contact plates in regions where plate-ward advection is high, and subsequent exploratory movement along the plate is oriented with flow direction at the plate surface. After exploration, cyprids reject a surface more frequently in a fast flow (10 cm s−1 freestream velocity) than in a slow flow (5 cm s−1), but rejection occurs in shear stresses well below the threshold that would prevent attachment and exploration. A higher rejection rate does not result in lower settlement, however, since contact rate is higher in fast than slow flows. The movement of cyprids in flow thus appears to be a passive transport process during the initial contact stage of settlement, but an active behavioral response to flow direction and shear stress during later stages of exploration and attachment.

PREDATION STRUCTURES COMMUNITIES AT DEEP-SEA HYDROTHERMAL VENTS

The structure and dynamics of natural communities result from the interplay of abiotic and biotic factors. We used manipulative field experiments to determine the relative roles of abiotic conditions and biotic interactions in structuring deep-sea (2500 m depth) communities along environmental gradients around hydrothermal vents of the eastern tropical Pacific Ocean (East Pacific Rise, at 9 50 N). We tested (1) whether predation by crabs and fishes affects the recruitment of benthic species and subsequent community structure and (2) whether the effects of predation vary along the steep gradients of tem- perature, oxygen, sulfide, and metal concentrations near vents. Recruitment substrates (ba- salt cubic blocks, roughly 10 cm on a side), both uncaged and caged to exclude predators (crabs, fishes, whelks, and octopi), were deployed along a decreasing vent fluid-flux gra- dient. The exclusion of predators for 8 mo increased the abundance of small mobile gas- tropods and amphipod crustaceans but decreased the abundance of sessile invertebrates, including juvenile vestimentiferan worms, tubiculous polychaetes, and mussels. Effects of predation were strongest nearest to hydrothermal vents, where abiotic environmental con- ditions were most extreme but productivity and the overall abundances of benthic inver- tebrates and mobile predators were the greatest. Additional 5-mo experiments conducted at three different locations showed similar trends at all sites, indicating that these effects of predation on benthic community structure are repeatable. Stomach-content analyses of the most abundant predators found at vents indicated that the zoarcid fish ( Thermarces cerberus) primarily feeds on the vent snail Cyathermia naticoides, the limpet Lepetodrilus elevatus, and the amphipod crustacean Ventiella sulfuris, the very species that showed the greatest increase following predator exclusion. In contrast, brachyuran ( Bythograea ther- mydron) and galatheid (Munidopsis subsquamosa ) crab stomachs did not contain small mobile grazers, and crabs presented with arrays of the most common vent invertebrate species preferred mussels and vestimentiferans over limpets. Our results indicate that pre- dation by large mobile predators influences the structure of hydrothermal vent communities, directly by reducing the abundance of gastropod prey species, and indirectly by reducing

SUCCESSIONAL MECHANISM VARIES ALONG A GRADIENT IN HYDROTHERMAL FLUID FLUX AT DEEP‐SEA VENTS

Invertebrate communities inhabiting deep-sea hydrothermal vents undergo substantial succession on time scales of months. Manipulative field experiments assessed the relative roles of environmental state and biotic interactions in determining temporal succession along a spatial gradient in vent fluid flux at three vent sites near 9 8509 N on the East Pacific Rise (2500 m water depth). Species colonization patterns on cubic basalt blocks (10 cm on a side) deployed by the submersible Alvin revealed both positive (facilitation) and negative (inhibition) biological interactions, in the context of established succession theory. Over a series of four cruises from 1994 to 1998, blocks were exposed to colonists for consecutive and continuous intervals in short-term (5 1 8 5 13 mo) and longer-term (8 1 29 5 37 mo) experiments. Colonists grouped into a mobile functional group were less abundant in the continuous interval (13 mo) than in the synchronous pooled-consecutive intervals (5 1 8 mo) of the short-term experiment, indicating that early colonists inhibited subsequent recruitment. Colonists grouped into a sessile functional group exhibited the opposite pattern, indicating facilitation. Similar trends, though not statistically significant, were observed in the longer-term experiment. The character of species interactions varied along a gradient in hydrothermal fluid flux (and inferred productivity), with inhibitory interactions more prominent in zones with high temperatures, productivity, and faunal densities, and facilitative interactions appearing where temperatures, productivity, and den- sities were low. Analyses of primary succession on introduced basalt blocks suggest that biological interactions during early vent community development strongly modify initial patterns of settlement, even in the absence of sustained temporal change in the vent fluid flux.

Pelagic and benthic ecology of the lower interface of the Eastern Tropical Pacific oxygen minimum zone

The distributions of pelagic and benthic fauna were examined in relation to the lower boundary of the oxygen minimum zone (OMZ) on and near Volcano 7, a seamount that penetrates this feature in the Eastern Tropical Pacific. Although the broad, pronounced OMZ in this region is an effective barrier for most zooplankton, zooplankton abundances, zooplankton feeding rates, and ambient suspended particulate organic carbon (POC) peaked sharply in the lower OMZ (about 740–800 m), in association with the minimum oxygen concentration and the increasing oxygen levels just below it. Zooplankton in the lower OMZ were also larger in size, and the pelagic community included some very abundant, possibly opportunistic, species. Elevated POC and scatter in the light transmission data suggested the existence of a thin, particle-rich, and carbon-rich pelagic layer at the base of the OMZ. Gut contents of planktonic detrifvores implied opportunistic ingestion of bacterial aggregates, possibly from this layer. Benthic megafaunal abundances on the seamount, which extended up to 730 m, peaked at about 800 m. There was a consistent vertical progression in the depth of first occurrence of different megafaunal taxa in this depth range, similar to intertidal zonation. Although the vertical gradients of temperature, salinity, and oxygen were gradual at the lower OMZ interface (in contrast to the upper OMZ interface at the thermocline), temporal variability in oxygen levels due to internal wave-induced vertical excursions of the OMZ may produce the distinct zonation in the benthic fauna. The characteristics of the lower OMZ interface result from biological interactions with the chemical and organic matter gradients of the OMZ. Most zooplankton are probably excluded physiologically from pronounced OMZs. The zooplankton abundance peak at the lower interface of the OMZ occurs where oxygen becomes sufficiently high to permit the zooplankton to utilize the high concentrations of organic particles that have descended through the OMZ relatively unaltered because of low metazoan abundance. A similar scenario applies to megabenthic distributions. Plankton layers and a potential short food chain (bacteria to zooplankton) at OMZ interfaces suggest intense utilization and modification of organic material, localized within a thin midwater depth zone. This could be a potentially significant filter for organic material sinking to the deep-sea floor.

Larval recruitment in response to manipulated field flows

Settlement responses to boundary-layer flow of several invertebrate taxa, including the hydroid Tubularia crocea, the bryozoans Bugula turrita and Schizoporella unicornis, and the tube-building polychaete Hydroides dianthus were studied in manipulated field flows in Great Harbor, Massachusetts, USA. During three experiments in 1989 and two in 1990, densities of newly-recruited larvae were measured on flat plates, whose flow regimes had been manipulated by altering the leading-edge configurations. Settlement responses to flow were strongly species-specific, with T. crocea preferring regions of both high turbulence and strong shear stress, and S. unicornis settling a most exclusively in regions of high shear stress. B. turrita settled most prominently in regions of reduced shear stress, exhibiting settlement patterns that closely approximated predictions from a model of passive particle contact. H. dianthus showed a moderate avoidance of regions with high shear stress. These results indicate that boundary-layer flows affect settlement of several common encrusting species, a probable consequence of larval behaviors such as substrate rejection or exploration in response to flow. These responses are likely to generate patchiness during initial colonization of natural habitats, and certainly affect colonization of settlement panels commonly used in marine ecological studies.

Tubeworm succession at hydrothermal vents: use of biogenic cues to reduce habitat selection error?

Abstract Species colonizing new deep-sea hydrothermal vents along the East Pacific Rise show a distinct successional sequence: pioneer assemblages dominated by the vestimentiferan tubeworm Tevnia jerichonana being subsequently invaded by another vestimentiferan Riftia pachyptila, and eventually the mussel Bathymodiolus thermophilus. Using a manipulative approach modified from shallow-water ecological studies, we test three alternative hypotheses to explain the initial colonization by T. jerichonana and its subsequent replacement by R. pachyptila. We show that R. pachyptila and another vestimentiferan, Oasisia alvinae, colonized new surfaces only if the surfaces also were colonized by T. jerichonana. This pattern does not appear to be due to restricted habitat tolerances or inferior dispersal capabilities of R. pachyptila and O. alvinae, and we argue the alternative explanation that T. jerichonana facilitates the settlement of the other two species and is eventually outcompeted by R. pachyptila. Unlike the classic model of community succession, in which facilitating species promote their own demise by modifying the environment to make it more hospitable for competitors, we suggest that T. jerichonana may produce a chemical substance that induces settlement of these competitors. This process of selecting habitat based on biogenic cues may be especially adaptive and widespread among later-successional species that occupy a physically variable and unpredictable environment. In these cases, the presence of weedy species implies some integrated period of environmental suitability, whereas an instantaneous assessment of physical habitat conditions, such as water temperature for vent tubeworms, provides a poorer predictor of long-term habitat suitability.

Surface-Generated Mesoscale Eddies Transport Deep-Sea Products from Hydrothermal Vents

Deep-reaching eddies transport heat and material hundreds of kilometers from the northern East Pacific Rise. Atmospheric forcing, which is known to have a strong influence on surface ocean dynamics and production, is typically not considered in studies of the deep sea. Our observations and models demonstrate an unexpected influence of surface-generated mesoscale eddies in the transport of hydrothermal vent efflux and of vent larvae away from the northern East Pacific Rise. Transport by these deep-reaching eddies provides a mechanism for spreading the hydrothermal chemical and heat flux into the deep-ocean interior and for dispersing propagules hundreds of kilometers between isolated and ephemeral communities. Because the eddies interacting with the East Pacific Rise are formed seasonally and are sensitive to phenomena such as El Niño, they have the potential to introduce seasonal to interannual atmospheric variations into the deep sea.

Larvae of benthic invertebrates in hydrothermal vent plumes over Juan de Fuca Ridge

Larvae of benthic invertebrates collected in the water column above Juan de Fuca Ridge show distinct variations in abundance and composition in, and away from, the neutrally-buoyant hydrothermal plume emanating from underlying vents. Larvae of vent gastropods (Lepetodrilus sp. and two peltospirid species) occur in significantly higher abundances in the plume than away from it (mean abundance=21.0 individuals 1000 m−3 vs 1.4 individuals 1000 m−3), and larvae of vent bivalves (Calyptogena? sp.) occur exclusively in the plume (mean abundance=0.5 individuals 1000 m−3). Larvae from other benthic taxa known not to be endemic to Juan de Fuca vent communities, such as anthozoans, pholad clams, bryozoans and echinoderms, are less abundant in the plume than away (mean abundance=47.5 vs 16.9 individuals 1000 m−3) at comparable depths and heights above the bottom. These results support the hypothesis that larvae of vent species are entrained into buoyant hydrothermal plumes and transported at the level of lateral spreading several hundred meters above the seafloor. The discovery of vent-associated larvae in the plume suggests that models used to predict hydrodynamic processes in the plume will also be useful for modeling larval dispersal. Advanced imaging and new molecular-based approaches will be required to resolve taxonomic uncertainties in some larval groups (e.g. certain polychaete families) in order to distinguish vent species and make comprehensive flux estimates of all vent larvae in the neutrally-buoyant plume.

Larvae from afar colonize deep-sea hydrothermal vents after a catastrophic eruption

The planktonic larval stage is a critical component of life history in marine benthic species because it confers the ability to disperse, potentially connecting remote populations and leading to colonization of new sites. Larval-mediated connectivity is particularly intriguing in deep-sea hydrothermal vent communities, where the habitat is patchy, transient, and often separated by tens or hundreds of kilometers. A recent catastrophic eruption at vents near 9°50′N on the East Pacific Rise created a natural clearance experiment and provided an opportunity to study larval supply in the absence of local source populations. Previous field observations have suggested that established vent populations may retain larvae and be largely self-sustaining. If this hypothesis is correct, the removal of local populations should result in a dramatic change in the flux, and possibly species composition, of settling larvae. Fortuitously, monitoring of larval supply and colonization at the site had been established before the eruption and resumed shortly afterward. We detected a striking change in species composition of larvae and colonists after the eruption, most notably the appearance of the gastropod Ctenopelta porifera, an immigrant from possibly more than 300 km away, and the disappearance of a suite of species that formerly had been prominent. This switch demonstrates that larval supply can change markedly after removal of local source populations, enabling recolonization via immigrants from distant sites with different species composition. Population connectivity at this site appears to be temporally variable, depending not only on stochasticity in larval supply, but also on the presence of resident populations.