Roberto Danovaro

The biodiversity of the Mediterranean Sea: estimates, patterns, and threats.

The Mediterranean Sea is a marine biodiversity hot spot. Here we combined an extensive literature analysis with expert opinions to update publicly available estimates of major taxa in this marine ecosystem and to revise and update several species lists. We also assessed overall spatial and temporal patterns of species diversity and identified major changes and threats. Our results listed approximately 17,000 marine species occurring in the Mediterranean Sea. However, our estimates of marine diversity are still incomplete as yet—undescribed species will be added in the future. Diversity for microbes is substantially underestimated, and the deep-sea areas and portions of the southern and eastern region are still poorly known. In addition, the invasion of alien species is a crucial factor that will continue to change the biodiversity of the Mediterranean, mainly in its eastern basin that can spread rapidly northwards and westwards due to the warming of the Mediterranean Sea. Spatial patterns showed a general decrease in biodiversity from northwestern to southeastern regions following a gradient of production, with some exceptions and caution due to gaps in our knowledge of the biota along the southern and eastern rims. Biodiversity was also generally higher in coastal areas and continental shelves, and decreases with depth. Temporal trends indicated that overexploitation and habitat loss have been the main human drivers of historical changes in biodiversity. At present, habitat loss and degradation, followed by fishing impacts, pollution, climate change, eutrophication, and the establishment of alien species are the most important threats and affect the greatest number of taxonomic groups. All these impacts are expected to grow in importance in the future, especially climate change and habitat degradation. The spatial identification of hot spots highlighted the ecological importance of most of the western Mediterranean shelves (and in particular, the Strait of Gibraltar and the adjacent Alboran Sea), western African coast, the Adriatic, and the Aegean Sea, which show high concentrations of endangered, threatened, or vulnerable species. The Levantine Basin, severely impacted by the invasion of species, is endangered as well. This abstract has been translated to other languages (File S1).

A Census of Marine Biodiversity Knowledge, Resources, and Future Challenges

The resources available for research are always limited. When setting priorities for research funding, governments, industry, and funding agencies must balance the demands of human health, food supply, and standards of living, against the less-tangible benefits of discovering more about the planets biodiversity. Scientists have discovered almost 2 million species indicating that we have made great gains in our knowledge of biodiversity. However, this knowledge may distract attention from the estimated four-fifths of species on Earth that remain unknown to science, many of them inhabiting our oceans [1], [2]. The worlds media still find it newsworthy when new species are discovered [1]. However, the extent of this taxonomic challenge no longer appears to be a priority in many funding agencies, perhaps because society and many scientists believe we have discovered most species, or that doing so is out of fashion except when new technologies are employed. Another symptom of this trend may be that the increased attention to novel methods available in molecular sciences is resulting in a loss of expertise and know-how in the traditional descriptive taxonomy of species [3]. The use of molecular techniques complements traditional methods of describing species but has not significantly increased the rate of discovery of new species (at least of fish), although it may help classify them [4]. At least in Europe, there was a mismatch between the number of species in a taxon and the number of people with expertise in it [5]. Unfortunately, because most species remain to be discovered in the most species-rich taxa [2], [5], [6], [7], there are then few experts to appreciate that this work needs to be done. Evidently, a global review of gaps in marine biodiversity knowledge and resources is overdue. History of discovering marine biodiversity Although the economic exploitation of marine resources dates back to prehistoric times, and historical documentation has existed since the third century B.C. with Aristotles contributions in the Mediterranean Sea (e.g. [8]), the establishment of systematic collections of marine organisms began only during the seventeenth and eighteenth centuries. Global marine biodiversity investigations at these times depended not only on the availability of expertise, but also on foreign policies of the colonial powers of the time. For those reasons, the specimens collected from several regions (e.g., Caribbean, Japan, South America, Africa) were mostly brought to Europe, where they were described, deposited in museum collections, and used for the production of marine biological monographs. These early publications contained descriptions and checklists of many marine species, such as molluscs, crustaceans, fishes, turtles, birds, and mammals (e.g. [9], [10], [11]). The history of research on marine biodiversity can generally be divided into three periods: early exploratory studies, local coastal “descriptive” studies, and large-scale multidisciplinary investigations and syntheses. These periods vary in timing by different seas and countries. The first exploratory studies in several regions (e.g., South America, Caribbean, South Africa, Pacific Ocean) took place from the mid-1700s until the late-1800s, in association with mainly European, North American, and Russian exploration expeditions, such as the Kamchatka Expedition in the 1740s, James Cooks voyages in the 1770s, the cruise of HMS Beagle in the 1830s, the voyage of HMS Challenger in the 1870s, and the first deep-sea investigations in the Mediterranean Sea [8], [9], [12], [13]. Pioneer investigations on deep-sea organisms were conducted in the Aegean Sea, where Forbes [14] noticed that sediments became progressively more impoverished in terms of biodiversity with increasing sampling depth. The azoic hypothesis proposed by Forbes suggested that life would be extinguished beyond 500 m depth, although a work published 68 years earlier provided indisputable evidence of the presence of life in the Gulf of Genoa at depths down to 1,000 m [15]. The taxonomists who described marine species at these times seldom collected specimens themselves in the field and, therefore, had only second-hand information about the distribution and ecology of the samples they received [4], [8]. Some of the early descriptions of tropical species thus do not even have the locality where the holotype or voucher material was collected (some examples in Chenu 1842–1853). The second period of regional studies was initiated by enhanced availability of research resources (experts, institutes, and vessels) in developing countries around the mid-1900s. The earliest institutions and research stations, many of which continue to operate, were founded in some areas as early as the late 1800s and early 1900s (e.g. [11], [16], [17]). Wide-scale establishment of laboratories in several continents (Europe, New Zealand, North and South America) have only been operational since the 1950s–1960s. The third stage, large-scale multidisciplinary investigations, has evolved since the 1990s, and is related to development and application of modern technologies and implementation of large, multinational research projects. Perhaps the largest of such investigations was the Census of Marine Life (Census).

Major viral impact on the functioning of benthic deep-sea ecosystems

Viruses are the most abundant biological organisms of the world’s oceans. Viral infections are a substantial source of mortality in a range of organisms—including autotrophic and heterotrophic plankton—but their impact on the deep ocean and benthic biosphere is completely unknown. Here we report that viral production in deep-sea benthic ecosystems worldwide is extremely high, and that viral infections are responsible for the abatement of 80% of prokaryotic heterotrophic production. Virus-induced prokaryotic mortality increases with increasing water depth, and beneath a depth of 1,000 m nearly all of the prokaryotic heterotrophic production is transformed into organic detritus. The viral shunt, releasing on a global scale ∼0.37–0.63 gigatonnes of carbon per year, is an essential source of labile organic detritus in the deep-sea ecosystems. This process sustains a high prokaryotic biomass and provides an important contribution to prokaryotic metabolism, allowing the system to cope with the severe organic resource limitation of deep-sea ecosystems. Our results indicate that viruses have an important role in global biogeochemical cycles, in deep-sea metabolism and the overall functioning of the largest ecosystem of our biosphere.

Global Patterns and Predictions of Seafloor Biomass Using Random Forests

A comprehensive seafloor biomass and abundance database has been constructed from 24 oceanographic institutions worldwide within the Census of Marine Life (CoML) field projects. The machine-learning algorithm, Random Forests, was employed to model and predict seafloor standing stocks from surface primary production, water-column integrated and export particulate organic matter (POM), seafloor relief, and bottom water properties. The predictive models explain 63% to 88% of stock variance among the major size groups. Individual and composite maps of predicted global seafloor biomass and abundance are generated for bacteria, meiofauna, macrofauna, and megafauna (invertebrates and fishes). Patterns of benthic standing stocks were positive functions of surface primary production and delivery of the particulate organic carbon (POC) flux to the seafloor. At a regional scale, the census maps illustrate that integrated biomass is highest at the poles, on continental margins associated with coastal upwelling and with broad zones associated with equatorial divergence. Lowest values are consistently encountered on the central abyssal plains of major ocean basins The shift of biomass dominance groups with depth is shown to be affected by the decrease in average body size rather than abundance, presumably due to decrease in quantity and quality of food supply. This biomass census and associated maps are vital components of mechanistic deep-sea food web models and global carbon cycling, and as such provide fundamental information that can be incorporated into evidence-based management.

A three-year time series of elemental and biochemical composition of organic matter in subtidal sandy sediments of the Ligurian Sea (northwestern Mediterranean)

Abstract Variations in organic matter composition and microphytobenthic biomass were examined in the surface sandy sediments at a water depth of 10 m in the Gulf of Marconi (NW Mediterranean Sea) over a three year period. Seasonal changes in elemental (organic C and total N) and biochemical (lipids, proteins, carbohydrates) composition of sediment organic matter as well as Chla were assessed in order to provide information about the origin and fate of sedimentary organic matter, the contribution of microphytobenthic biomass, seasonal and interannual variations of food quantity and quality, and factors related to food availability. Data obtained in this three-year study revealed that organic matter determined with a muffle furnace is clearly an overestimate of the organic content of the sediment and is thus of little significance for benthic ecologists studying community dynamics in relation to food availability. Labile organic matter, utilized to estimate the food potentially available for benthic consumers, accounted for only a small percentage (on average less than 10%) of total organic C. The highest labile fraction was observed in spring, whereas minima were recorded in winter. Analysis of elemental and biochemical composition of organic matter showed an inverse relationship between amount of organic matter and its potential availability to consumers; small quantities of high-quality organic matter were replaced by large quantities of refractory material. The labile portion was mostly microphytobenthic (65% of the labile carbon). Protein: carbohydrate ratios were low and confirmed the role of proteins as a potentially limiting factor for consumers. Significant differences in nutritional quality of the sediment organic matter were observed from year to year, changes due to the increase in specific labile compound content.

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.

Sunscreens Cause Coral Bleaching by Promoting Viral Infections

Background Coral bleaching (i.e., the release of coral symbiotic zooxanthellae) has negative impacts on biodiversity and functioning of reef ecosystems and their production of goods and services. This increasing world-wide phenomenon is associated with temperature anomalies, high irradiance, pollution, and bacterial diseases. Recently, it has been demonstrated that personal care products, including sunscreens, have an impact on aquatic organisms similar to that of other contaminants. Objectives Our goal was to evaluate the potential impact of sunscreen ingredients on hard corals and their symbiotic algae. Methods In situ and laboratory experiments were conducted in several tropical regions (the Atlantic, Indian, and Pacific Oceans, and the Red Sea) by supplementing coral branches with aliquots of sunscreens and common ultraviolet filters contained in sunscreen formula. Zooxanthellae were checked for viral infection by epifluorescence and transmission electron microscopy analyses. Results Sunscreens cause the rapid and complete bleaching of hard corals, even at extremely low concentrations. The effect of sunscreens is due to organic ultraviolet filters, which are able to induce the lytic viral cycle in symbiotic zooxanthellae with latent infections. Conclusions We conclude that sunscreens, by promoting viral infection, potentially play an important role in coral bleaching in areas prone to high levels of recreational use by humans.

Detritus-Bacteria-Meiofauna interactions in a seagrass bed (Posidonia oceanica) of the NW Mediterranean

The biochemical composition of the sediment organic matter, and bacterial and meiofaunal dynamics, were monitored over an annual cycle in aPosidonia oceanica bed of the NW Mediterranean to test the response of the meiofauna assemblage to fluctuations in food availability. Primary production cycles of the seagrass and its epiphytes were responsible for relatively high (compared to other Mediterranean systems) standing stocks of organic carbon in sediments (from 1.98 to 6.16 mg Cg−1 sediment dry weight). The biopolymeric fraction of the organic matter (measured as lipids, carbohydrates, and proteins) accounted for only a small fraction (18%) of the total sedimentary organic carbon. About 25% of the biopolymeric fraction was of microphytobenthic origin. Sedimentary organic carbon was mostly refractory (56 to 84%) and probably largely not utilizable for benthic consumers. The biopolymeric fraction of the organic matter was characterized by high carbohydrate concentrations (from 0.27 to 5.31 mg g−1 sediment dry weight in the top 2 cm) and a very low protein content (from 0.07 to 0.80 mg g−1 sediment dry weight), which may be a limiting factor for heterotrophic metabolism in seagrass sediments. RNA and DNA concentrations of the Sediments varied significantly during the year. High RNA and DNA values occurred during the microphytobenthic bloom and in correspondence with peaks of bacterial abundance. Bacteria accounted for a small fraction of the total organic carbon (0.65%) and of the biopolymeric organic carbon (4.64%), whilst microphytobenthos accounted for 3.79% of total organic carbon and for 25.08% of the biopolymeric carbon. Bacterial abundance (from 0.8 to 5.8 × 108 g−1 sediment dry weight) responded significantly to seasonal changes of organic matter content and composition and was significantly correlated with carbohydrate concentrations. Bacteria might be, in the seagrass system, an important N storage for higher trophic levels as il accounted for 25% of the easily soluble protein. pool and contributed significantly to the total DNA pool (on average 12%). Total meiofaunal density ranged from 236 to 1858 ind. 10 cm−2 and was significantly related, with a time lag, to changes in bacterial standing stocks indicating that microbes might represent an important resource. Bacterial abundance and biomass were also significantly related to nematode abundance. These results indicate that bacteria may play a key role in the benthic trophic

Composition of organic matter in sediments facing a river estuary (Tyrrhenian Sea): relationships with bacteria and microphytobenthic biomass

The relationships between the biochemical composition of sediment organic matter and bacteria and microphytobenthic biomass distribution, were investigated along the coast of Northern Tuscany (Tyrrhenian Sea). Organic matter appeared to be of highly refractory composition. Among the three main biochemical classes, proteins were the major component (0.96 mg g-1 sediment d.w.) followed by total carbohydrates (0.81 mg g-1 sediment d.w.) and lipids (8.1 µg g-1 sediment d.w.). Bacterial number in surface sediments (0–2 cm) ranged from 1.7 to 24.5 × 108 cells g-1 of sediment dry weight showing a strong decrease with sediment depth. In surface sediments, significant correlations were found between bacterial biomass and protein concentration. Bacterial activity (measured by the frequency of dividing cells) was significantly related to lipid concentration. Bacterial and microphytobenthic biomass accounted for 3.1 and 18.1% respectively of the sediment organic carbon. In surface sediments bacterial lipids accounted, on average, for 27 % of total lipids, whereas bacterial proteins and carbohydrates accounted for 2.5 and 0.5% of total proteins and carbohydrates, respectively.The benthic degradation process indicated that lipids were a highly degradable compound (about 35% in the top 10 cm). Carbohydrate decreased for 25.6% in the top 10 cm, whereas proteins increased with depth, thus indicating that this compound may resist to diagenetic decomposition.These data suggest that specific organic compounds need to be measured rather than bulk carbon and nitrogen measurements in order to relate microbial biomass to the quality of organic matter.

Differential responses of bacteria, meiofauna and macrofauna in a shelf area (Ligurian Sea, NW Mediterranean): role of food availability

Abstract Density and biomass of bacteria, meio- and macrofauna were examined along a transect of eight stations (5–135 m depth) facing the estuary of the river Entella (Ligurian Sea) during summer 1990. Sediment samples were collected to determine organic detritus composition (total organic matter, lipid, protein and carbohydrate concentrations) and microphytobenthic biomass (as chlorophyll-a). Synoptic water samples were collected to determine the quantity and the quality of suspended matter (total suspended matter, particulate lipids, proteins, carbohydrates and chloroplastic pigments). Particulate organic matter in the surface water decreased from the coast towards the open sea both in quality and quantity. By contrast, the organic-matter concentration in the sediment increased with water depth. Quantity and biochemical composition of suspended and sedimentary organic matter affected the distribution of all the benthic assemblages. Bacteria appeared to be controlled by different parameters at different depths: generally they appeared to depend upon sediment particle surface and the quantity of organic matter, but when metazoan (particularly meiofauna) densities were high, grazing pressure might also exert a control on their abundance. The distribution of meio- and macrofauna along the continental shelf of the oligotrophic Ligurian Sea appears to depend more upon the quality of organic matter than on its quantity.