Anastasios Tselepides

Deep-Sea Biodiversity in the Mediterranean Sea: The Known, the Unknown, and the Unknowable

Deep-sea ecosystems represent the largest biome of the global biosphere, but knowledge of their biodiversity is still scant. The Mediterranean basin has been proposed as a hot spot of terrestrial and coastal marine biodiversity but has been supposed to be impoverished of deep-sea species richness. We summarized all available information on benthic biodiversity (Prokaryotes, Foraminifera, Meiofauna, Macrofauna, and Megafauna) in different deep-sea ecosystems of the Mediterranean Sea (200 to more than 4,000 m depth), including open slopes, deep basins, canyons, cold seeps, seamounts, deep-water corals and deep-hypersaline anoxic basins and analyzed overall longitudinal and bathymetric patterns. We show that in contrast to what was expected from the sharp decrease in organic carbon fluxes and reduced faunal abundance, the deep-sea biodiversity of both the eastern and the western basins of the Mediterranean Sea is similarly high. All of the biodiversity components, except Bacteria and Archaea, displayed a decreasing pattern with increasing water depth, but to a different extent for each component. Unlike patterns observed for faunal abundance, highest negative values of the slopes of the biodiversity patterns were observed for Meiofauna, followed by Macrofauna and Megafauna. Comparison of the biodiversity associated with open slopes, deep basins, canyons, and deep-water corals showed that the deep basins were the least diverse. Rarefaction curves allowed us to estimate the expected number of species for each benthic component in different bathymetric ranges. A large fraction of exclusive species was associated with each specific habitat or ecosystem. Thus, each deep-sea ecosystem contributes significantly to overall biodiversity. From theoretical extrapolations we estimate that the overall deep-sea Mediterranean biodiversity (excluding prokaryotes) reaches approximately 2805 species of which about 66% is still undiscovered. Among the biotic components investigated (Prokaryotes excluded), most of the unknown species are within the phylum Nematoda, followed by Foraminifera, but an important fraction of macrofaunal and megafaunal species also remains unknown. Data reported here provide new insights into the patterns of biodiversity in the deep-sea Mediterranean and new clues for future investigations aimed at identifying the factors controlling and threatening deep-sea biodiversity.

Benthic response to particulate fluxes in different trophic environments : a comparison between the Gulf of Lions-Catalan Sea (western-Mediterranean) and the Cretan Sea (eastern-Mediterranean)

Quantitative information on particle fluxes, sedimentary OM composition, microbial and meiofaunal parameters is summarised from various stations in the Gulf of Lions and Catalan Sea (North-Western Mediterranean) and in the Cretan Sea (Eastern Mediterranean), investigated between 1993 and 1996. Benthic responses in relation to the different trophic conditions in the two areas were compared in terms of: (1) temporal and spatial variability of the mass fluxes; (2) pelagic–benthic coupling in organic matter composition (such as proteins, lipids, soluble carbohydrates and CPE); (3) microbial response to changes in organic matter composition and POC fluxes; (4) meiofaunal response to changes in organic matter composition and particle fluxes; (5) relative significance of bacteria and meiofauna. The two areas were also compared to identify ratios between productivity, vertical fluxes and benthic standing stocks. Mass fluxes at equal depths were up to two orders of magnitude higher in the Western than in the Eastern Mediterranean. Clear seasonal changes were reported in both areas, although mass fluxes and variability were consistently higher in the North-Western Mediterranean. From primary production estimates in the Western and Eastern Mediterranean (140–160 vs. ≈19–60 mgC m−2 d−1, respectively) it has been calculated that a carbon export from the euphotic layer to 1000 m depth is equivalent to about 10% in the Gulf of Lions and 2–3% in the Cretan Sea. Chlorophyll-a concentrations, at similar depths, were 2–3 times higher in the Western basin. Carbohydrates were the dominant biochemical component in the Cretan Sea sediments while total amino-acids represented an important fraction of the biodegradable material in the Gulf of Lions–Catalan Sea. In the Western Mediterranean, bacterial densities (annual mean 7.9×108 cells g−1) were about 4 times higher than in the Cretan Sea (annual mean 2.1×108 cells g−1), indicating that, in deep-sea sediments, different trophic conditions are influencing bacterial densities. Meiofaunal abundance and biomass were similar on the continental shelves of both areas (940–2558 ind./10 cm2) but, at bathyal depths, densities in the Cretan Sea (range: 60–120 ind./10 cm2) were 4–25 times lower than those in the NW-Mediterranean (500–1500 ind./10 cm2). In contrast to what was observed in the North-Western Mediterranean, deep-sea meiofaunal assemblages of the Cretan Sea did not react (in terms of density or biomass) to the seasonal variations in food inputs. Here, the bacterial to meiofaunal biomass ratio displayed much higher values (up to >20), possibly causing competition for food sources with small metazoans. The efficiency with which the POC fluxes were being exploited was estimated. In the NW-Mediterranean about 0.14 mgC/d are available to each meiofaunal individual compared to the 0.07 mgC ind.−1 of the Eastern Mediterranean. Similarly, 3.3 mgC were provided daily per 1 mgC of bacterial biomass in the Western Mediterranean, compared to 0.07 in the Eastern Mediterranean. These data indicate that the benthic components in the Cretan Sea, are subject to more limiting trophic conditions, and so might have a higher efficiency in exploiting the particulate organic fluxes.

Particle Size Distribution of Airborne Microorganisms and Pathogens during an Intense African Dust Event in the Eastern Mediterranean

Background The distribution of microorganisms, and especially pathogens, over airborne particles of different sizes has been ignored to a large extent, but it could have significant implications regarding the dispersion of these microorganisms across the planet, thus affecting human health. Objectives We examined the microbial quality of the aerosols over the eastern Mediterranean region during an African storm to determine the size distribution of microorganisms in the air. Methods We used a five-stage cascade impactor for bioaerosol collection in a coastal city on the eastern Mediterranean Sea during a north African dust storm. Bacterial communities associated with aerosol particles of six different size ranges were characterized following molecular culture–independent methods, regardless of the cell culturability (analysis of 16S rRNA genes). Results All 16S rDNA clone libraries were diverse, including sequences commonly found in soil and marine ecosystems. Spore-forming bacteria such as Firmicutes dominated large particle sizes (> 3.3 μm), whereas clones affiliated with Actinobacteria (found commonly in soil) and Bacteroidetes (widely distributed in the environment) gradually increased their abundance in aerosol particles of reduced size (< 3.3 μm). A large portion of the clones detected at respiratory particle sizes (< 3.3 μm) were phylogenetic neighbors to human pathogens that have been linked to several diseases. Conclusions The presence of aerosolized bacteria in small size particles may have significant implications to human health via intercontinental transportation of pathogens.

Deep-sea ecosystem response to climate changes: the eastern Mediterranean case study

Abstract Climate change is significantly modifying ecosystem functioning on a global scale, but little is known about the response of deep-sea ecosystems to such change. In the past decade, extensive climate change has modified the physico–chemical characteristics of deep waters in the eastern Mediterranean. Climate change has caused an immediate accumulation of organic matter on the deep-sea floor, altered the carbon and nitrogen cycles and has had negative effects on deep-sea bacteria and benthic fauna. Evidence from a miniature ocean model provides new ways of interpreting signals from the deep sea and indicates that, contrary to what might have been expected, deep-sea ecosystems do respond quickly to climate change.

Dynamics of meiofaunal assemblages on the continental shelf and deep-sea sediments of the Cretan Sea (NE Mediterranean): relationships with seasonal changes in food supply

Abstract Quantitative information on metazoan meiofaunal abundance and biomass was obtained from three continental shelf (at 40, 100 and 200 m depth) and four deep-sea stations (at 540, 700, 940 and 1540 m depth) in the Cretan Sea (South Aegean Sea, NE Mediterranean). Samples were collected on a seasonal basis (from August 1994 to September 1995) with the use of a multiple corer. Meiofaunal abundance and biomass on the continental shelf of the Cretan Sea were high, in contrast to the extremely low values reported for the bathyal sediments that showed values comparable to those reported for abyssal and hadal environments. In order to explain the spatial and seasonal changes in metazoan meiofauna these data were compared with: (1) the concentrations of ‘food indicators’ (such as proteins, lipids, soluble carbohydrates and CPE) (2) the bacterial biomass (3) the flux of labile organic compounds to the sea floor at a fixed station (D7, 1540 m depth). Highly significant relationships between meiofaunal parameters and CPE, protein and lipid concentrations and bacterial biomass were found. Most of the indicators of food quality and quantity (such as CPE, proteins and carbohydrates) showed a clear seasonality with highest values in February and lowest in September. Such changes were more evident on the continental shelf rather than at deeper depths. On the continental shelf, significant seasonal changes in meiofaunal density were related to changes in the input of labile organic carbon whereas meiofaunal assemblages on the deep-sea stations showed time-lagged changes in response to the food input recorded in February 95. At all deep-sea stations meiofaunal density increased with a time lag of 2 months. Indications for a time-lagged meiofaunal response to the food inputs were also provided by the increase in nauplii densities during May 95 and the increase in individual biomass of nematodes, copepods and polychaetes between February and May 1995. The lack of strong seasonal changes in deep sea meiofaunal density suggests that the supply of organic matter below 500 m is not strong enough to support a significant meiofaunal development. Below 700 m depth >92% of the total biomass in the sediment was represented by bacteria. The ratio of bacterial to meiofaunal biomass increased with increasing water depth indicating that bacteria are probably more effective than meiofauna in exploiting refractory organic compounds. These data lead us to hypothesise that the deep-sea sediments of the Cretan Sea are largely dependent upon a benthic microbial loop.

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).

Meiofauna of the deep Eastern Mediterranean Sea: distribution and abundance in relation to bacterial biomass, organic matter composition and other environmental factors

Abstract Quantitative information on the abundance and biomass of metazoan meiofauna was obtained from samples collected at 15 deep-sea stations in the Eastern Mediterranean Sea (533–2400m). Meiofaunal abundance was compared to bacterial biomass and other environmental factors such as the total sedimentary organic matter content, the concentrations of the main biochemical classes of organic compounds (i.e. proteins, carbohydrates and lipids) and to ATP. To estimate the sedimentation potential of primary organic matter, sediment bound chloroplastic pigment equivalents (CPE) were assayed. Meiofaunal density was very low ranging from 4 ind.10cm−2 (Station A4, 1658m depth) to 290 ind.10cm−2 (Station A12, 636m depth). Nematodes were the numerically dominant taxon (68% of total meiofauna) and were usually confined to the top 6cm of the sediments. Total meiofaunal biomass ranged from 2.78μgC 10cm−2 (Station A4) to 598.34μgC 10cm−2 (Station 15A). There was a significant decrease in the density of metazoan meiofauna with water depth. Bacterial biomass largely dominated the total biomass (as the sum of bacterial and meiofaunal biomass) with an average of 73.2% and accounted for 35.8% of the living biomass (as ATP carbon) whereas meiofaunal biomass accounted only for 6.56%. Bacterial biomass was significantly related to the DNA concentrations of the sediment. A significant correlation between ATP concentration and CPE content was also found. No correlations were found between meiofauna, ATP and CPE, or between meiofauna and bacterial parameters. The significant relationship between meiofaunal density and the ratio of labile organic matter/total organic matter indicates that deep-sea meiofauna inhabiting an extremely oligotrophic environment (such as the Eastern Mediterranean) may be more nutritionally dependent upon the quality than on the quantity of sedimentary organic matter.

Organic matter composition of the continental shelf and bathyal sediments of the Cretan Sea (NE Mediterranean)

Abstract The seasonal, spatial and bathymetric changes in the distribution of chloroplastic pigments (Chl a, phaeopigments and CPE), TOC, TON, ATP, bottom water nutrient content and the main biochemical classes of organic compounds (lipids, proteins and carbohydrates) were recorded from May 1994 to September 1995 over the continental margin of northern Crete. The concentration of chloroplastic pigment equivalents (CPE) was always low, dropping dramatically along the shelf-slope gradient. Microbial activity (ATP) also dropped sharply beyond the continental shelf following a distribution pattern similar to TOC and TON. Lipid, protein and carbohydrate concentrations, as well as biopolymeric carbon were comparable to those reported for other more productive areas, however, the quality of the organic matter itself was rather poor. Thus, carbohydrates, the dominant biochemical class, were characterised by being highly (80–99%) refractory, as soluble carbohydrates represented (on annual average) only 6% of the total carbohydrate pool. Protein and lipid concentrations strongly decreased with depth, indicating depletion of trophic resources in the bathyal zone. Proteins appeared to be the more degradable compounds and indeed the protein to carbohydrate ratios were found to decrease strongly in the deeper stations. Organic matter content and quality decreased both with increasing distance from the coast and within the sediment. All sedimentary organic compounds were found to vary between sampling periods, with the changes being more pronounced over the continental shelf. The different temporal patterns of the various components suggest a different composition and/or origin of the OM inputs during the different sampling periods. The amount of material reaching the sediments below 540 m is extremely low, suggesting that most of the organic material is decomposed and/or utilised before reaching the sea floor. In conclusion, the continental shelf and bathyal sediments of the Cretan Sea can be considered, from a trophic point of view, as two different subsystems.

Macrobenthic community structure over the continental margin of Crete (South Aegean Sea, NE Mediterranean)

Macrobenthic faunal composition, abundance, biomass and diversity together with a suite of sedimentary environmental parameters were investigated on a seasonal basis in order to determine factors regulating faunal distribution over the oligotrophic continental margin of the island of Crete (South Aegean Sea, North Eastern Mediterranean). Macrofaunal species composition was similar to that of the western Mediterranean and the neighboring Atlantic having several common dominant species. Mean benthic biomass, abundance and diversity decreased with depth, with a major transition zone occurring at 540 m, beyond which values declined sharply. At comparable depths biomass and abundance values were considerably lower to those found in the Atlantic, high-lighting the extreme oligotrophy of the area. The continental margin of Crete was characterised by a high diversity upper continental shelf environment (dominated by surface deposit feeding polychaetes) and a very low diversity slope and deep-basin environment (dominated by carnivorous and filter feeding polychaetes). Classification and ordination analyses revealed the existence of four principle clusters divided by a faunal boundary between 200 and 540 m, as well as beyond 940 m depth. Significant correlations between macrofauna and sediment parameters led to the conclusion that besides depth, food availability (as manifested by the concentration of chloroplastic pigments) is the principle regulating factor in the system. Such being the case, the prevailing hydrographic features that structure the pelagic food web and are directly responsible for the propagation of organic matter to the benthos also affect its community structure.

Links between Geographic Location, Environmental Factors, and Microbial Community Composition in Sediments of the Eastern Mediterranean Sea

The bacterial community composition of marine surface sediments originating from various regions of the Eastern Mediterranean Sea (12 sampling sites) was compared by parallel use of three fingerprinting methods: analysis of 16S rRNA gene fragment heterogeneity by denaturing gradient electrophoresis (DGGE), terminal restriction fragment length polymorphism (T-RFLP), and analysis of phospholipid-linked fatty acid composition (PLFA). Sampling sites were located at variable depths (30–2860 m; water column depth above the sediments) and the sediments differed greatly also in their degree of petroleum contamination (0.4–18 μg g−1), organic carbon (0.38–1.5%), and chlorophyll a content (0.01–7.7 μg g−1). Despite a high degree of correlation between the three different community fingerprint methods, some major differences were observed. DGGE banding patterns showed a significant separation of sediment communities from the northern, more productive waters of the Thermaikos Gulf and the oligotrophic waters of the Cretan, S. Ionian, and Levantine Sea. T-RFLP analysis clearly separated the communities of deep sediments (>1494 m depth) from their shallow (<617 m) counterparts. PLFA analysis grouped a shallow station from the productive waters of the north with the deep oligotrophic sediments from the Ionian and Levantine Sea, with low concentrations of PLFAs, and hence low microbial biomass, as the common denominator. The degree of petroleum contamination was not significantly correlated to the apparent composition of the microbial communities for any of the three methods, whereas organic carbon content and sediment chlorophyll a were important in this regard.