Limits of life: Thermal tolerance of deep-sea hydrothermal vent copepods and implications for community succession

Organisms that live in extreme marine environments naturally experience intermittent exposures to the limits of their physiological potential at different time scales and have developed diverse strategies to survive these variations. We tested the tolerance to thermal stress of deep-sea dirivultid copepod communities from focused and diffuse flows at East Pacific Rise 9°50'N hydrothermal vents in relation to habitat type, oxygen concentration and habitat pressure to unravel their physiological limits to extreme temperature. Lethal median time and temperature experiments were performed to derive the respective thermal death time (TDT) curves. Results showed that dirivultid copepods possess high thermal tolerance exclusively for short exposures and that in situ vent fluid flow conditions were an important predictor for maximum tolerated temperatures. Anoxia had a major negative impact on vent copepod survival, whereas atmospheric pressure did not have a significant effect. Results for the upper thermal tolerance of copepods were remarkably similar to macro- and megafauna from the same habitats, while tolerance to hypoxia or anoxia seems to increase with size. Data on relative abundance of dirivultid copepods in their habitats over the past two decades, coupled with data on temperature and anoxia tolerance, suggest that physiological limits strongly impact copepod community composition at focused flow habitats regardless of successional stage. In contrast, complex interplays of interspecific competition, food-source partitioning and experienced small-scale environmental heterogeneity within megafauna aggregations might shape dirivultid community dynamics in diffuse flow habitats.

In the decade following documented volcanic activity on the East Pacific Rise near 9°50′N, we monitored hydrothermal vent fluid temperature variations in conjunction with approximately yearly vent fluid sampling to better understand the processes and physical conditions that govern the evolution of seafloor hydrothermal systems. The temperature of both diffuse flow (low‐temperature) and focused flow (high‐temperature) vent fluids decreased significantly within several years of eruptions in 1991 and 1992. After mid‐1994, focused flow vents generally exhibited periods of relatively stable, slowly varying temperatures, with occasional high‐ and low‐temperature excursions lasting days to weeks. One such positive temperature excursion was associated with a crustal cracking event. Another with both positive and negative excursions demonstrated a subsurface connection between adjacent focused flow and diffuse flow vents. Diffuse flow vents exhibit much greater temperature variability than adjacent higher‐temperature vents. On timescales of a week or less, temperatures at a given position within a diffuse flow field often varied by 5°–10°C, synchronous with near‐bottom currents dominated by tidal and inertial forcing. On timescales of a week and longer, diffuse flow temperatures varied slowly and incoherently among different vent fields. At diffuse flow vent sites, the conceptual model of a thermal boundary layer immediately above the seafloor explains many of the temporal and spatial temperature variations observed within a single vent field. The thermal boundary layer is a lens of warm water injected from beneath the seafloor that is mixed and distended by lateral near‐bottom currents. The volume of the boundary layer is delineated by the position of mature communities of sessile (e.g., tubeworms) and relatively slow‐moving organisms (e.g., mussels). Vertical flow rates of hydrothermal fluids exiting the seafloor at diffuse vents are less than lateral flow rates of near‐bottom currents (5–10 cm/s). The presence of a subsurface, shallow reservoir of warm hydrothermal fluids can explain differing temperature behaviors of adjacent diffuse flow and focused flow vents at 9°50′N. Different average temperatures and daily temperature ranges are explained by variable amounts of mixing of hydrothermal fluids with ambient seawater through subsurface conduits that have varying lateral permeability.

The response of deep-sea vent microorganisms to mercury (Hg) was investigated through measurements of total Hg (THg) concentrations in hydrothermal fluids from diffuse and focused flow vents on the East Pacific Rise at 9uN and the estimations of the proportion of Hg-resistant chemosynthetic thiosulfate-oxidizing microbes in a representative subset of diffuse flow fluids. Fluids were enriched in THg, with concentrations ranging from 15 to 445 pmol L21 and 3.5 6 0.1 to 11.0 6 0.8 nmol L21 in diffuse and focused flow emissions, respectively. In diffuse flow samples, most probable numbers (MPN) indicated that 0.25–24.6% of the total chemosynthetic thiosulfateoxidizing bacteria were resistant to Hg. The highest resistance levels were observed in samples with the highest THg concentrations, indicating that adaptation to life with toxic Hg had occurred in the diffuse flow environment. High THg concentrations in vent emissions and adaptation to Hg among chemosynthetic vent microbes indicate that (1) Hg in vent emissions may contribute to the oceanic Hg mass balance, and (2) activities of chemosynthetic microbes may mobilize solid-phase Hg in metal sulfide and contribute to Hg detoxification in deep-sea diffuse flow vents. Thus, the activities of chemosynthetic microbes may be critical to the mobility, geochemical cycling, and toxicity of Hg in the vent ecosystem.

Temporal and spatial patterns of biological community development at nascent deep-sea hydrothermal vents (9°50′N, East Pacific Rise)

Habitat created or modified by the physical architecture of large or spatially dominant species plays an important role in structuring communities in a variety of terrestrial, aquatic, and marine habitats. At hydrothermal vents, the giant tubeworm Riftia pachyptila forms large and dense aggregations in a spatially and temporally variable environment. The density and diversity of smaller invertebrates is higher in association with aggregations of R. pachyptila than on the surrounding basalt rock seafloor. Artificial substrata designed to mimic R. pachyptila aggregations were deployed along a gradient of productivity to test the hypothesis that high local species diversity is maintained by the provision of complex physical structure in areas of diffuse hydrothermal flow. After 1 year, species assemblages were compared among artificial aggregations in low‐, intermediate‐, and high‐productivity zones and compared to natural aggregations of R. pachyptila from the same site. Hydrothermal vent fauna colonized every artificial aggregation, and both epifaunal density and species richness were highest in areas of high chemosynthetic primary production. The species richness was also similar between natural aggregations of R. pachyptila and artificial aggregations in intermediate‐ and high‐productivity zones, suggesting that complex physical structure alone can support local species diversity in areas of chemosynthetic primary production. Differences in the community composition between natural and artificial aggregations reflect the variability in microhabitat conditions and biological interactions associated with hydrothermal fluid flux at low‐temperature hydrothermal vents. Moreover, these local ecological factors may further contribute to the maintenance of regional species diversity in hydrothermal vent communities on the East Pacific Rise.

Habitat, growth and physiological ecology of a basaltic community of Ridgeia piscesae from the Juan de Fuca Ridge

Meter scale seafloor topography and sidescan backscatter imagery of volcanic terrain along the axis of the fast-spreading northern East Pacific Rise (EPR) near 9° 50'N, coupled with visual and photographic observations provide data that constrain spatial relationships between hydrothermal vents and primary volcanic features and processes along the EPR axis. High-temperature (>350°C) hydrothermal vents are present in several areas within the EPR axial trough where recent eruptions have been focused and where drainback of lava into the primary eruptive fissure occurred. Chaotic collapse crusts and draped sheet lava surfaces along the margin of eruptive fissures typify sites where drainback primarily occurred. These areas are also coincident with ∼10-30 m-wide channels that serve to transport lava across the crestal plateau. Regions of diffuse hydrothermal flow at low temperatures (<35°C) and vent animal communities are concentrated along the primary eruptive fissure that fed the 1991 eruption at the 9° 50'N EPR area. The relationship between seafloor eruption processes and hydrothermal vent locations within the EPR axial trough is linked to the formation of high permeability zones created by: focusing of eruptions along discrete portions of fissures; volcanic episodicity during eruptive phases lasting hours to days; and drainback of lava into the primary fissure at these same locations during waning stages of seafloor eruptions.

Hydrothermal vents differ both in surface input and subsurface geochemistry. The effects of these differences on their microbial communities are not clear. Here, we investigated both alpha and beta diversity of diffuse flow-associated microbial communities emanating from vents at a basalt-based hydrothermal system along the East Pacific Rise (EPR) and a sediment-based hydrothermal system, Guaymas Basin. Both Bacteria and Archaea were targeted using high throughput 16S rRNA gene pyrosequencing analyses. A unique aspect of this study was the use of a universal set of 16S rRNA gene primers to characterize total and diffuse flow-specific microbial communities from varied deep-sea hydrothermal environments. Both surrounding seawater and diffuse flow water samples contained large numbers of Marine Group I (MGI) Thaumarchaea and Gammaproteobacteria taxa previously observed in deep-sea systems. However, these taxa were geographically distinct and segregated according to type of spreading center. Diffuse flow microbial community profiles were highly differentiated. In particular, EPR dominant diffuse flow taxa were most closely associated with chemolithoautotrophs, and off axis water was dominated by heterotrophic-related taxa, whereas the opposite was true for Guaymas Basin. The diversity and richness of diffuse flow-specific microbial communities were strongly correlated to the relative abundance of Epsilonproteobacteria, proximity to macrofauna, and hydrothermal system type. Archaeal diversity was higher than or equivalent to bacterial diversity in about one third of the samples. Most diffuse flow-specific communities were dominated by OTUs associated with Epsilonproteobacteria, but many of the Guaymas Basin diffuse flow samples were dominated by either OTUs within the Planctomycetes or hyperthermophilic Archaea. This study emphasizes the unique microbial communities associated with geochemically and geographically distinct hydrothermal diffuse flow environments.

Recruitment variation during a pilot colonization study of hydrothermal vents (9°50′N, East Pacific Rise)

This is the first study, to my knowledge, quantifying the respiratory pigment haemoglobin discovered in a deep-sea copepod. Haemoglobin in copepods has previously been documented in only one other species from the deep water of an Italian lake. Specimens of the siphonostomatoid Scotoecetes introrsus Humes were collected during submersible dives at 2500 m depth near a hydrothermal vent at the East Pacific Rise (9 degrees N). The haemoglobin content in the copepods' haemolymph was 4.3 +/- 0.6 micrograms per individual female (n = 6) and 1.8 +/- 0.1 micrograms per individual male (n = 6). Weight-specific concentrations of haemoglobin were identical for females and males (0.25 +/- 0.04 and 0.26 +/- 0.02 microgram per microgram dry weight, respectively). These haemoglobin concentrations are higher than those found in other small crustaceans. Activity of the electron transport system indicated that the respiration rates in S. introrsus (13.7 +/- 7.7 microliters O2 per milligram dry weight per hour) were similar to those in the shallow-water copepod Acartia tonsa (9.1 +/- 1.3 microliters O2 per milligram dry weight per hour). It was concluded that the possession of highly concentrated haemoglobin allows S. introrsus to colonize a geologically young, thermally active site such as the vicinity of a hydrothermal vent, despite the prevailing oxygen depletion.

Temporal and spatial changes in the copepod community during the 1974–1998 spring seasons in the Kuroshio region; a time period of profound changes in pelagic fish populations

Hydrothermal vents in the deep sea are harsh, temporally unpredictable habitats with what appears to be a distinct fauna. Decades of subsea research with crewed and remote vehicles have generated a list of known species; is the species list complete? Evidence derived from mollusks sampled at hydrothermal vents on the East Pacific Rise (EPR), and Gorda and Juan de Fuca ridges suggests that the answer is yes. A 2006 compilation of hydrothermal vent species based on decades of research is updated and compared to specimens from these three active ridges in collections of the Field Museum of Natural History (FMNH) that resulted from limited collecting activity. Only three dives at each of the two Gorda Ridge vents collected all named species; 90% of the 20 species known from Juan de Fuca Ridge were collected in nine cruises. At the EPR, only 81% of the 43 known species were collected, but differences among the ridges were not significant. The limited FMNH collections increased the known ranges of six species from Juan de Fuca to Gorda Ridge and of nine species on the EPR. In addition, the EPR appears to host more rare species, potentially due to the frequent temporal changes at these vents. Mollusks currently known from each ridge, with their expanded ranges, are listed; the implications of these results for recent discoveries of slow-spreading vent fields are discussed.

The ecology and biogeography of meiofauna at deep-sea hydrothermal vents have historically received less attention than those of mega- and macrofauna. This study examines the composition of major meiofaunal taxa in beds of the mussel Bathymodiolus thermophilus at hydrothermal vents on the northern and southern East Pacific Rise (EPR) and presents the first comparison of species assemblages of the dominant taxon, the nematodes, among sites spanning 27 degrees of latitude. Meiofaunal samples were collected by submersible from three mussel beds at 9°N on the EPR and four mussel beds between 17 and 18°S in 1999. Estimated ages of the mussel beds at the time of sampling range from 4 to &gt;20 years, enabling investigation of the influence of mussel bed age on meiofaunal assemblages. Overall, the meiofauna of the mussel beds was dominated by nematodes, with copepods constituting the second most abundant meiofaunal group. There was variation in the ratio of nematodes to copepods between sites, however, with copepods more abundant than nematodes in the youngest mussel beds. Apart from polychaete larvae, other meiofaunal groups were generally present at very low abundance (&lt;1%) in the samples and restricted in diversity to gastropod larvae, acari, foraminifera, ostracoda and turbellaria. Seventeen nematode species from 14 genera and 11 families were found in the samples, with no evidence of endemicity to hydrothermal vents at the generic level. Four genera present were not previously recorded at hydrothermal vents. Nematode species richness, species:genus ratios and abundances were low compared with other deep-sea habitats, though the ecological relevance of comparisons with soft-sediment benthos is discussed. Nematode assemblages exhibited high dominance by a few species, with one species of Thalassomonhystera most abundant at five of the seven vent sites. Multivariate analysis of nematode assemblages reveals similarities among sites that do not match geographical proximity. The youngest mussel beds were most similar to each other and exhibited lower species richness than other sites, consistent with colonization of mussel bed habitat by nematodes over time. Similarity in the composition of nematode assemblages among sites separated by ~3000 km indicates that they lie within a single biogeographic province, consistent with that proposed for mussel bed macrofauna. At a generic level, samples exhibited some overlap with nematode assemblages at vents elsewhere on the EPR, on the Mid Atlantic Ridge and in the North Fiji Basin.

Observations from 17 ALVIN dives and 14 ANGUS runs plus laboratory study of basalt samples collected with ALVIN help to constrain the morphologic, volcanic and petrologic evolution of four seamounts near the East Pacific Rise (EPR). Comparison among the four volcanoes provides evidence for a general pattern of near-EPR seamount evolution and shows the importance of sedimentation, mass wasting, hydrothermal activity and other geologic processes that occur on submerged oceanic volcanoes. Seamount 5, closest to the EPR (1.0 Ma) is the youngest seamount and may still be active. Its summit is covered by fresh lavas, recent faults and hydrothermal deposits. Seamount D is on crust 1.55 Ma and is inactive; like seamount 5, it has a breached caldera and is composed exclusively of N-MORB. Seamounts 5 and D represent the last stages of growth of typical N-MORB-only seamounts near the EPR axis. Seamounts 6 and 7 have bumpy, flattish summits composed of transitional and alkalic lavas. These lavas probably represent caldera fillings and caps overlying an edifice composed of N-MORB. Evolution from N-MORB-only cratered edifices to the alkalic stage does not occur on all near-EPR seamounts and may be favored by location on structures with relative-motion-parallel orientation.

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 305:67-77 (2005) - doi:10.3354/meps305067 Epifaunal community structure associated with Riftia pachyptila aggregations in chemically different hydrothermal vent habitats Breea Govenar1,4,*, Nadine Le Bris2, Sabine Gollner3, Joanne Glanville1, Adrienne B. Aperghis1, Stéphane Hourdez1,5, Charles R. Fisher1 1Department of Biology, The Pennsylvania State University, 208 Mueller Laboratory, University Park, Pennsylvania 16802, USA2Département Environnement Profond, Ifremer, Centre de Brest, BP 70, 29280 Plouzané, France3Department of Marine Biology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria4Present address: Biology Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA5Present address: Equipe Ecophysiologie, CNRS-UPMC UMR 7144, Station Biologique, BP 74, 29682 Roscoff, France *Email: bgovenar@whoi.edu ABSTRACT: The vestimentiferan tubeworm Riftia pachyptila (Polychaeta: Sibloglinidae) often dominates early succession stages and high productivity habitats at low-temperature hydrothermal vents on the East Pacific Rise. We collected 8 aggregations of R. pachyptila and the associated epifaunal community at 2 discrete sites of diffuse hydrothermal activity, in December 2001 and December 2002. Because of the high spatial and temporal variability of the biotic and abiotic factors related to hydrothermal vent activity, significant differences in the structure and the composition of the community were expected to occur at the scale of either 1 yr or 500 m distance between very different sites. There was no significant difference in the temperature ranges of the diffuse flow between sites or years, even though the environmental conditions were very different at the 2 sites. At 1 site (Riftia Field), the diffuse hydrothermal fluids had relatively low concentrations of sulfide, low pH, and high concentrations of iron. At the other site (Tica), the diffuse hydrothermal fluids had higher sulfide concentrations, the pH was closer to neutral, and iron was undetectable. The physiological condition of R. pachyptila appeared to reflect the availability of sulfide at each site. However, the structure and the composition of the epifaunal community were remarkably similar between sites and years, with the exception of a few species. Aggregations of R. pachyptila support high local species diversity relative to the surrounding seafloor and high community similarity in different hydrothermal vent habitats. KEY WORDS: Hydrothermal vent · East Pacific Rise · Riftia pachyptila · Community structure · Epifauna · Benthos Full text in pdf format PreviousNextExport citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 305. Online publication date: December 23, 2005 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2005 Inter-Research.