Verena Tunnicliffe

A Biogeographical Perspective of the Deep-Sea Hydrothermal Vent Fauna

ABSTRACT Biogeography seeks to distinguish patterns in the distribution of species and to determine causal processes. Hydrothermal vent habitats have several properties that invite biogeographic studies: constrained to active deep-sea ocean ridges, known in most oceans and anticipated in the rest, patchy in distribution, extreme conditions and a limited group of inhabitants. Biologists have studied 30 vent sites mostly in the Pacific and Atlantic. Currently, 443 invertebrate species are known to generic level although many more are under study. Additionally, 32 octopus and fish species are observed in and around vents. The faunas of other sulphide-rich deep-water habitats such as margin cold seeps and organic masses (wood, carcasses) do not show great affinity at the species level to the vent fauna but the higher taxonomic affiliations suggest close evolutionary ties for many groups. Many studies address the formation of regional faunas using the first- known sites on the Galapagos Rift and northern East Pacific Rise as the major sites of comparison. Physical disjunction of ridge crests is a likely factor in promoting the extensive provinciality that currently exists. Nonetheless, faunas on two sides of the Pacific and in the Atlantic have closer relations to each other than to the nearby “normal” deep-sea fauna. At the individual ridge scale, extensive gene flow among separated populations occurs in many species and serves to maintain the regional species pool. However, major discontinuities between major ridges reduce or eliminate gene flow; vicariant processes appear to be important. The role of differing rates of spreading in different provinces and the concomitant effects on vent habitats and faunas need further investigation. Over 75% of vent species occur at only one site and none occur at all sites. Examination of the reproductive characters of some widespread species reveals no special dispersal strategy nor does reproductive strategy predict the extent of distribution. Vestimentiferan tubeworm species are highly endemic and found only at Pacific vents; their limited spread may be a result of recent entry into the habitat. Alvinellid polychaete cladogenetic pattern does not match geographic regions, indicating independent penetration by numerous lineages. Endemicity among vent gastropods is high with over 60% of genera limited to this habitat; many affiliations with other sulphide-rich habitats can be identified. Among the vent gastropods there are some lineages that may have entered the vent habitat in the Mesozoic. Hydrothermal vents provide a good testing ground for processes that control patterns in diversity. Ecological and historical controls at both local and regional scales can be discerned with further study.

Biological colonization of new hydrothermal vents following an eruption on Juan de Fuca Ridge

Abstract A recent eruption on CoAxial Segment of Juan de Fuca Ridge initiated hydrothermal conditions with rapid changes in water chemistry and growth of microbial communities. Vent animals recruited from distal sources within a year. One site with newly erupted lava attracted no animals to high-iron and low-sulphide conditions. However, sustained release of flocculent material at a second site suggests extensive subterranean microbial production; here, the dissolved sulphide/heat ratio peaked during the first year. The first larval recruits included vestimentiferans, alvinellid polychaetes and nemerteans; despite the small areal extent of venting, one-third of the regional vent species pool had arrived by 2 years. Near-optimal growth conditions and recruitment by many species continued in the centre of the system but several habitats went extinct within 2 years. Rapid response and exploitation by vent animals must be an important adaptation to such ephemeral conditions.

Long-term eruptive activity at a submarine arc volcano

Three-quarters of the Earths 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.

Biogeography and evolution of hydrothermal-vent fauna in the eastern Pacific Ocean

The biogeography and evolutionary history of animals that live at hydrothermal vents are connected intimately to the spreading history of mid-ocean ridges. Extensive collections from two active ridge systems in the eastern Pacific Ocean provide an opportunity to examine the regional dispersion of vent-limited organisms. The degrees to which these habitat-limited species from disjunct areas are related gives preliminary information about exchange routes, dispersability, and rates of taxonomic change. Differences between vent faunae from the northern Juan de Fuca and southern East Pacific Rise systems indicate that geographical differentiation has occurred. Geophysical evidence shows that North America interposed as a barrier between the northeast and equatorial Pacific spreading ridges about 35 Ma BP. The vicariating vent fauna of the Juan de Fuca Ridge has since formed an endemic assemblage of generally lower diversity than that found at East Pacific Rise vents. Taxonomic comparisons suggest that rates of speciation have been low. Examination of spreading histories elsewhere should provide predictions of evolutionary patterns in the hydrothermal-vent faunae.

Hydrothermal vents of Explorer Ridge, northeast Pacific

Abstract The first submersible exploration of Explorer Ridge found extensive hydrothermal fields in relatively old pillow basalts. Massive coalescing spires formed the basis for 25 m high mounds atop which chimneys emit grey ‘moke’ and water over 300°C. These sulfides are among the largest such ocean deposits found to date. Three types of vents were found: (1) abiotic iron- and zinc-rich vents; (2) low temperature biotic vents; and (3) high temperature H 2 S-rich vents. Coordinated suites of water, rock and animal samples indicated a basic similarity to vents on Juan de Fuca Ridge while demonstrating a wide range of variation.

Dynamic character of the hydrothermal vent habitat and the nature of sulphide chimney fauna

Abstract A major substratum for vent organisms on Juan de Fuca and Explorer Ridges of the northeast Pacific is the polymetallic sulphide chimney. The deposition processes and subsequent growth of such chimneys provide a dynamic and extreme habitat that changes rapidly. During initial venting stages, colonization must await stabilization of the chimney structure. As the porous anhydrite shell accumulates sulphide minerals, protection from direct hot water contact increases for organisms colonizing the outer walls while sufficient vent water still diffuses for the support of chemosynthesis. Vestimentiferan worms are found on small sulphide mounds but the active growth and collapse of anhydrite spires is a major source of disruption and mortality. High temperature venting and spire growth appear to attract alvinellid polychaetes which may be implicated in the process of strengthening and sealing the anhydrite spires. Fauna on the growing chimney is subject to changes in fluid flow patterns that can make the structure uninhabitable. Large chimneys are inhabited by more species indicating that a diversification of habitat results from variations in mineralization and fluid availability. Chimney fauna has become specialized in exploiting an unpredictable and unstable habitat in an extreme example of the control of biotic development by the physical environment.

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.

Crustal accretion and the hot vent ecosystem

We examine evidence for links between seafloor spreading rate and properties of vent habitat most likely to influence species diversity and other ecosystem properties. Abundance of vent habitat along spreading centres appears positively related to spreading rate while habitat stability shows an opposite relationship. Habitat heterogeneity is lowest at faster spreading ridges. Limited data indicate an increasing species diversity with spreading rate, complicated by historical factors. Ecosystem productivity and efficiency of resource utilisation may also reflect diversity differences.

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.

Geological, chemical, and biological evidence for recent volcanism at 17.5°S: East Pacific Rise

The superfast-spreading portion of the East Pacific Rise at 17.5°S is a magmatically robust section of mid-ocean ridge. Plumes characterized by high volatile/metal ratios, which has been hypothesized to be indicative of recent magmatism, were found between 17°22′S and 17°35′S in November–December 1993. Dives with the French submersible Nautile in December 1993 observed young sheet flows and widespread venting centered on the segments shoalest point at 17°26′S. Eight submersible dives made one year later with the Japanese submersible Shinkai 6500 in September–November 1994 found glassy, unsedimented lavas, a range of diffuse and high-temperature vents, and several types of biologic communities on the ridge crest beneath the volatile-rich 1993 plumes. The diffuse vents range from small areas in the youngest lavas characterized by very low-temperature flow (<10°C) and a relatively low macrofaunal diversity, to larger areas where the (apparent) older surface was covered with a dense and diverse biotope including anemones, tubeworms, mussels and serpulids. Several inactive vents marked by dead mussel/clam beds are present in the southernmost portion of the site in the older lavas. Submersible mapping indicates that the youngest lava (L0 unit) erupted for at least 4 km along the strike of the ridge at the southern site, and for 5–10 km at the northern site. The flow is up to 400 m in width at the southern site and may be as much as 1–2 km in width at the northern site. Comparison of the observed 1993 Fe/S, H2S/heat, and 3He/heat plume values with time series measurements at sites on the northern East Pacific Rise and the Juan de Fuca Ridge, where the onset of the magmatic event is known, implies that the last magmatic event at 17.5′S occurred within several years prior to 1993. Continued rapid cooling of the underlying heat source is implied from the significant diminishment in the light-scattering intensity and rise height of the overlying plumes recorded during 1994 submersible dives. The type and diversity of the vent biota found on the L0 vents also suggests a young system. The spatial and temporal scales of the accretion event at the 17.5°S EPR site are similar in scale to eruptions on the intermediate-rate spreading North Cleft segment (Juan de Fuca Ridge) but the 17.5°S event has more subtle gradients in the effusion rate of the eruptions and thermal and chemical character of the hydrothermal system.