Ana Colaço

Temporal change in deep-sea benthic ecosystems: a review of the evidence from recent time-series studies

Societal concerns over the potential impacts of recent global change have prompted renewed interest in the long-term ecological monitoring of large ecosystems. The deep sea is the largest ecosystem on the planet, the least accessible, and perhaps the least understood. Nevertheless, deep-sea data collected over the last few decades are now being synthesised with a view to both measuring global change and predicting the future impacts of further rises in atmospheric carbon dioxide concentrations. For many years, it was assumed by many that the deep sea is a stable habitat, buffered from short-term changes in the atmosphere or upper ocean. However, recent studies suggest that deep-seafloor ecosystems may respond relatively quickly to seasonal, inter-annual and decadal-scale shifts in upper-ocean variables. In this review, we assess the evidence for these long-term (i.e. inter-annual to decadal-scale) changes both in biologically driven, sedimented, deep-sea ecosystems (e.g. abyssal plains) and in chemosynthetic ecosystems that are partially geologically driven, such as hydrothermal vents and cold seeps. We have identified 11 deep-sea sedimented ecosystems for which published analyses of long-term biological data exist. At three of these, we have found evidence for a progressive trend that could be potentially linked to recent climate change, although the evidence is not conclusive. At the other sites, we have concluded that the changes were either not significant, or were stochastically variable without being clearly linked to climate change or climate variability indices. For chemosynthetic ecosystems, we have identified 14 sites for which there are some published long-term data. Data for temporal changes at chemosynthetic ecosystems are scarce, with few sites being subjected to repeated visits. However, the limited evidence from hydrothermal vents suggests that at fast-spreading centres such as the East Pacific Rise, vent communities are impacted on decadal scales by stochastic events such as volcanic eruptions, with associated fauna showing complex patterns of community succession. For the slow-spreading centres such as the Mid-Atlantic Ridge, vent sites appear to be stable over the time periods measured, with no discernable long-term trend. At cold seeps, inferences based on spatial studies in the Gulf of Mexico, and data on organism longevity, suggest that these sites are stable over many hundreds of years. However, at the Haakon Mosby mud volcano, a large, well-studied seep in the Barents Sea, periodic mud slides associated with gas and fluid venting may disrupt benthic communities, leading to successional sequences over time. For chemosynthetic ecosystems of biogenic origin (e.g. whale-falls), it is likely that the longevity of the habitat depends mainly on the size of the carcass and the ecological setting, with large remains persisting as a distinct seafloor habitat for up to 100 years. Studies of shallow-water analogs of deep-sea ecosystems such as marine caves may also yield insights into temporal processes. Although it is obvious from the geological record that past climate change has impacted deep-sea faunas, the evidence that recent climate change or climate variability has altered deep-sea benthic communities is extremely limited. This mainly reflects the lack of remote sensing of this vast seafloor habitat. Current and future advances in deep-ocean benthic science involve new remote observing technologies that combine a high temporal resolution (e.g. cabled observatories) with spatial capabilities (e.g. autonomous vehicles undertaking image surveys of the seabed).

Nutritional relations of deep-sea hydrothermal fields at the Mid-Atlantic Ridge: a stable isotope approach

Nutritional relations among invertebrates from the hydrothermal vent fields at the Mid Atlantic Ridge (MAR) were studied via the carbon and nitrogen stable isotope approach. A large number of specimens of different vent species from different MAR vent fields were analysed, providing a general picture of the community structure. The isotopic composition at each vent field presents the same general trend. There is an obvious dichotomyof the trophic structure, with the mussels being significantlydepleted in 13 C and shrimps being significantlyenriched in 13 C. MAR and Pacific vent fields present the same picture, despite a different species composition. Primaryconsumers are divided into main groups according to their d 13 C signature: >� 15 (shrimps) and o� 20% (mussels). Vent predators are tightlylinked to one or the other group, but a mixed diet cannot be excluded. Bathyal species are top predators, making incursions into the vent fields to profit from the large biomass. Taking into account the above associations, a descriptive trophic model was elaborated. At the base of the food chain the chemolithotrophic bacteria predominate. Four trophic levels were then distinguished: primaryconsumers, feeding onlyon bacteria; mixotrophs feeding on bacteria and small invertebrates; vent predators feeding onlyon small invertebrates; and finallytop predators that are mainlyconstituted bydeep-sea fauna. r 2002 Elsevier Science Ltd. All rights reserved.

Non-indigenous marine species of the Azores

Marine benthic species introduced to the Azores are collated from scientific publications, internal reports and own data. Twelve algae and 21 invertebrates are classified as non-indigenous species, 18 as cryptogenic. Two species of algae and two ascidians are regarded as particularly invasive along the shores of this oceanic archipelago.

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.

Mapping Condor Seamount Seafloor Environment and Associated Biological Assemblages (Azores, NE Atlantic)

Publisher Summary Seamounts are among the most common topographic features in the world ocean. Depending on their particular morphological traits, they can also be referred to as banks, knolls, guyots, mounds, or hills. Condor seamount is a linear volcano located in the Azores (northeast Atlantic), 35 km in length, 2–6 km wide, and of varied seafloor morphology. A scientific observatory devoted to research on seamount ecosystem structure and functioning has been established on Condor, secured by a temporary fishing closure. Multiple projects have contributed to this observatory by targeting the seamount with snapshots and long-term deployments of moored, satellite-based, and shipborne technologies. This chapter presents a brief characterization of the seamounts seafloor environment by focusing on the multibeam bathymetry data and a series of video, oceanographic, and fishery surveys. A classification based upon the bathymetric position index is presented to characterize the landscape composition of the seamount. Habitats of conservation importance, such as coral gardens and deep-sea sponge aggregations, are documented. A qualitative zonation of the benthic assemblages based on the video surveys is presented along with dominant fish and crustacean catch data for comparable depth strata. Understanding how deep-sea habitat-building species like corals and sponges distribute at fine scales over the complex topography of individual seamounts is therefore critical information to design usage zonation schemes.

Spatial variation of metal bioaccumulation in the hydrothermal vent mussel Bathymodiolus azoricus

The variability of the bioaccumulation of metals (Ag, Cd, Cu, Fe, Mn and Zn) was extensively studied in the mussel Bathymodiolus azoricus from five hydrothermal vent sites inside three main vent fields of increasing depth along the Mid-Atlantic Ridge: Menez Gwen, Lucky Strike and Rainbow. Metal bioaccumulation varied greatly between vent fields and even between sites inside a vent field with B. azoricus showing a great capacity to accumulate metals. The bioaccumulation of these metals also varied significantly among tissues. The main target was the gills where metals were mainly associated with soluble compounds whereas in the digestive gland they were mainly associated with insoluble compounds. Storage of metals under insoluble forms in B. azoricus seems to be a major pathway for the detoxification of both essential and non-essential metals. Mussels from the studied fields can be discriminated following their metallic load but the segregation relies partially on the composition of the metal-enriched fluids.

Evidence of seasonal reproduction in the Atlantic vent mussel Bathymodiolus azoricus and an apparent link with the timing of photosynthetic primary production

Here we present evidence of seasonal reproduction in the deep-sea vent mussel Bathymodiolus azoricus, a dominant member of the Mid-Atlantic Ridge (MAR) hydrothermal fauna in the Azores region. This is the first time that seasonal reproduction has been suggested for any deep-sea vent organism. This discovery was made possible by the use of novel, acoustically-retrievable cages, which allowed us to extend the frequency and temporal range of sampling that was previously limited to the summer months. The main spawning peak, at the Menez Gwen vent field (840 m) occurs in late December-January and shows a correlation with a winter-spring bloom in primary production in the euphotic zone. Our results suggest that this surface-derived material may act as both a food source for the dispersing mussel larvae and as a reproductive cue/supplementary nutritional source for the adult mussels. Further evidence of a dependence on photosynthetic inputs comes from the relationship between particulate feeding levels, which themselves correlate with the phytoplankton peak, and the amounts of storage tissue in the mantle, which ultimately gets converted into gonad. Thus, the pattern and energetics of reproduction in the Atlantic vent mussel B. azoricus closely resembles that found in the coastal mussel Mytilus edulis, which has been described as an adaptation for optimizing the timing of reproduction against a background of seasonally-varying food availability. This discovery emphasizes the complexity of the nutritional pathways found in some deep-sea chemosynthetic environments and highlights the need for more time-series studies.

Particle flux in the Rainbow hydrothermal vent field (Mid-Atlantic Ridge) : Dynamics, mineral and biological composition

In order to provide information about the export and the distribution of hydrothermal particulate material to the surrounding deep ocean, four moorings were deployed in the vicinity of the hydrothermal Rainbow vent e eld (Mid-Atlantic Ridge, 36° 14 9N, 2250 m depth). The e rst mooring was a sediment trap with a current meter deployed at 2 m from a chimney of the Rainbow vent e eld and 1.5 m above the bottom (a.b.) for 16 days. It represented the reference for the initial composition of particles produced by the vent. The total mean mass particle e ux (6.9 g m 2 2 d 2 1 ) was distinctly higher than the e ux measured at the shallower hydrothermal vents on the MAR segment. This particulate e ux showed a high temporal variation at the scale of a few days and was characterized by a high concentration of sulphur (17.2%) and copper (3.5%) and a very low concentration of organic carbon (0.14%). Several hundred bivalve larvae belonging to the hydrothermal mytilid Bathymodio- lus azoricus were collected in this trap at the beginning of the experiment. The density of larvae decreased strongly at the end, indicating a patchiness distribution or a discontinuous reproduction of this species. The other three moorings, including sediment traps, current-meters and thermistor chains, were deployed for 304 days at different distances and altitudes from the Rainbow vent e eld. The mean speed of the current in the rift valley was low (6 cm s 2 1 ) and was oriented toward the north. The total mean particle mass e ux measured with the e ve sediment traps varied little, from 10.6 to 25.0 mg m m 2 2 d 2 1 , and displayed temporal variations which are typical of deep-sea environ- ments with seasonal changes in the overlying production. However, in the trap at 500 m from the vents 150 m a.b., the presence of the hydrothermal plume can be observed: the sulphur, iron and copper concentrations of particles were signie cantly higher compared to the particles sampled in the pelagic reference trap. The plume composition was about 50% hydrothermal particles and 50% pelagic particles and its upper limit reached 300 m a.b. at this distance. In the traps at 1000 m from the vents, the elemental composition of particles was similar to the pelagic particles and we assume that these traps were not in the plume during the experiment. The zooplankton obtained in the long-term trap samples revealed high density variations in relation to the distance from the vent site. The nutrient enrichment around the hydrothermal area and the abundance of free living bacteria explain these variations in zooplankton density.

Seasonal variations in lipid composition of the hydrothermal vent mussel Bathymodiolus azoricus from the Menez Gwen vent field

Specimens of the hydrothermal mussel Bathymodiolus azoricus collected in Menez Gwen hydrothermal vent field (NE Atlantic) during 2002-2003 were examined for feeding patterns variations through three seasons. The fatty acid profile and lipid classes of the mussels were studied, together with the MODIS/AQUA-derived near-surface chlorophyll a to test the hypothesis that surface productivity might be related to the feeding patterns of this species. The lipid levels showed pronounced seasonal fluctuations with the highest values occurring in January and August. Seasonal variations in lipid classes and fatty acid composition of neutral and polar lipids in the mussels are presented. Differences in the fatty acid profile of lipid classes in different seasons suggest that the higher energy requirements in summer and winter were supplied by bacterial biomarkers omega7 MUFA (monounsaturated fatty acids), whereas omega6 PUFA (polyunsaturated fatty acids) and NMI (non-methylene-interrupted) fatty acids predominated during the spring. The MODIS/AQUA data show marked seasonal variability and an anomalous peak during January of 2003, although this cannot be directly linked to lipid composition variation.

Changes of gill and hemocyte-related bio-indicators during long term maintenance of the vent mussel Bathymodiolus azoricus held in aquaria at atmospheric pressure

The deep-sea hydrothermal vent mussel Bathymodiolus azoricus has been the subject of several studies aimed at understanding the physiological adaptations that vent animals have developed in order to cope with the particular physical and chemical conditions of hydrothermal environments. In spite of reports describing successful procedures to maintain vent mussels under laboratory conditions at atmospheric pressure, few studies have described the mussels physiological state after a long period in aquaria. In the present study, we investigate changes in mucocytes and hemocytes in B. azoricus over the course of several months after deep-sea retrieval. The visualization of granules of mucopolysaccharide or glycoprotein was made possible through their inherent auto-fluorescent property and the Alcian blue-Periodic Acid Schiff staining method. The density and distribution of droplets of mucus-like granules was observed at the ventral end of lamellae during acclimatization period. The mucus-like granules were greatly reduced after 3 months and nearly absent after 6 months of aquarium conditions. Additionally, we examined the depletion of endosymbiont bacteria from gill tissues, which typically occurs within a few weeks in sea water under laboratory conditions. The physiological state of B. azoricus after 6 months of acclimatization was also examined by means of phagocytosis assays using hemocytes. Hemocytes from mussels held in aquaria up to 6 months were still capable of phagocytosis but to a lesser extent when compared to the number of ingested yeast particles per phagocytic hemocytes from freshly collected vent mussels. We suggest that the changes in gill mucopolysaccharides and hemocyte glycoproteins, the endosymbiont abundance in gill tissues and phagocytosis are useful health criteria to assess long term maintenance of B. azoricus in aquaria. Furthermore, the laboratory set up to which vent mussels were acclimatized is an applicable system to study physiological reactions such as hemocyte immunocompetence even in the absence of the high hydrostatic pressure found at deep-sea vent sites.