Marta Coll

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).

Management effectiveness of the world's marine fisheries.

A global analysis shows that fishery management worldwide is lagging far behind international standards, and that the conversion of scientific advice into policy, through a participatory and transparent process, holds promise for achieving sustainable fisheries.

Recovery of marine animal populations and ecosystems

Many marine populations and ecosystems have experienced strong historical depletions, yet reports of recoveries are increasing. Here, we review the growing research on marine recoveries to reveal how common recovery is, its magnitude, timescale and major drivers. Overall, 10-50% of depleted populations and ecosystems show some recovery, but rarely to former levels of abundance. In addition, recovery can take many decades for long-lived species and complex ecosystems. Major drivers of recovery include the reduction of human impacts, especially exploitation, habitat loss and pollution, combined with favorable life-history and environmental conditions. Awareness, legal protection and enforcement of management plans are also crucial. Learning from historical recovery successes and failures is essential for implementing realistic conservation goals and promising management strategies.

Ecosystem Overfishing in the Ocean

Fisheries catches represent a net export of mass and energy that can no longer be used by trophic levels higher than those fished. Thus, exploitation implies a depletion of secondary production of higher trophic levels (here the production of mass and energy by herbivores and carnivores in the ecosystem) due to the removal of prey. The depletion of secondary production due to the export of biomass and energy through catches was recently formulated as a proxy for evaluating the ecosystem impacts of fishing–i.e., the level of ecosystem overfishing. Here we evaluate the historical and current risk of ecosystem overfishing at a global scale by quantifying the depletion of secondary production using the best available fisheries and ecological data (i.e., catch and primary production). Our results highlight an increasing trend in the number of unsustainable fisheries (i.e., an increase in the risk of ecosystem overfishing) from the 1950s to the 2000s, and illustrate the worldwide geographic expansion of overfishing. These results enable to assess when and where fishing became unsustainable at the ecosystem level. At present, total catch per capita from Large Marine Ecosystems is at least twice the value estimated to ensure fishing at moderate sustainable levels.

Protected and Threatened Components of Fish Biodiversity in the Mediterranean Sea

The Mediterranean Sea (0.82% of the global oceanic surface) holds 4%-18% of all known marine species (~17,000), with a high proportion of endemism [1, 2]. This exceptional biodiversity is under severe threats [1] but benefits from a system of 100 marine protected areas (MPAs). Surprisingly, the spatial congruence of fish biodiversity hot spots with this MPA system and the areas of high fishing pressure has not been assessed. Moreover, evolutionary and functional breadth of species assemblages [3] has been largely overlooked in marine systems. Here we adopted a multifaceted approach to biodiversity by considering the species richness of total, endemic, and threatened coastal fish assemblages as well as their functional and phylogenetic diversity. We show that these fish biodiversity components are spatially mismatched. The MPA system covers a small surface of the Mediterranean (0.4%) and is spatially congruent with the hot spots of all taxonomic components of fish diversity. However, it misses hot spots of functional and phylogenetic diversity. In addition, hot spots of endemic species richness and phylogenetic diversity are spatially congruent with hot spots of fishery impact. Our results highlight that future conservation strategies and assessment efficiency of current reserve systems will need to be revisited after deconstructing the different components of biodiversity.

Global Patterns in Ecological Indicators of Marine Food Webs: A Modelling Approach

Background Ecological attributes estimated from food web models have the potential to be indicators of good environmental status given their capabilities to describe redundancy, food web changes, and sensitivity to fishing. They can be used as a baseline to show how they might be modified in the future with human impacts such as climate change, acidification, eutrophication, or overfishing. Methodology In this study ecological network analysis indicators of 105 marine food web models were tested for variation with traits such as ecosystem type, latitude, ocean basin, depth, size, time period, and exploitation state, whilst also considering structural properties of the models such as number of linkages, number of living functional groups or total number of functional groups as covariate factors. Principal findings Eight indicators were robust to model construction: relative ascendency; relative overhead; redundancy; total systems throughput (TST); primary production/TST; consumption/TST; export/TST; and total biomass of the community. Large-scale differences were seen in the ecosystems of the Atlantic and Pacific Oceans, with the Western Atlantic being more complex with an increased ability to mitigate impacts, while the Eastern Atlantic showed lower internal complexity. In addition, the Eastern Pacific was less organised than the Eastern Atlantic although both of these systems had increased primary production as eastern boundary current systems. Differences by ecosystem type highlighted coral reefs as having the largest energy flow and total biomass per unit of surface, while lagoons, estuaries, and bays had lower transfer efficiencies and higher recycling. These differences prevailed over time, although some traits changed with fishing intensity. Keystone groups were mainly higher trophic level species with mostly top-down effects, while structural/dominant groups were mainly lower trophic level groups (benthic primary producers such as seagrass and macroalgae, and invertebrates). Keystone groups were prevalent in estuarine or small/shallow systems, and in systems with reduced fishing pressure. Changes to the abundance of key functional groups might have significant implications for the functioning of ecosystems and should be avoided through management. Conclusion/significance Our results provide additional understanding of patterns of structural and functional indicators in different ecosystems. Ecosystem traits such as type, size, depth, and location need to be accounted for when setting reference levels as these affect absolute values of ecological indicators. Therefore, establishing absolute reference values for ecosystem indicators may not be suitable to the ecosystem-based, precautionary approach. Reference levels for ecosystem indicators should be developed for individual ecosystems or ecosystems with the same typologies (similar location, ecosystem type, etc.) and not benchmarked against all other ecosystems.

Structural Degradation in Mediterranean Sea Food Webs: Testing Ecological Hypotheses Using Stochastic and Mass-Balance Modelling

Human-mediated disturbances such as fishing, habitat modification, and pollution have resulted in significant shifts in species composition and abundance in marine ecosystems which translate into degradation of food-web structure. Here, we used a comparative ecological modelling approach and data from two food webs (North-Central Adriatic and South Catalan Sea) and two time periods (mid-late 1970s and 1990s) in the Mediterranean Sea to evaluate how changes in species composition and biomass have affected food-web properties and the extent of ecosystem degradation. We assembled species lists and ecological information for both regions and time periods into stochastic structural and mass-balance food-web models, and compared the outcomes of 22 food-web properties. Our results show strong similarities in structural food-web properties between the North-Central Adriatic and South Catalan Seas indicating similar ecosystem structure and levels of ecological degradation between regions and time periods. In contrast, a comparison with other published marine food webs (Caribbean, Benguela, and US continental shelf) suggested that Mediterranean webs are in an advanced state of ecological degradation. This was reflected by lower trophic height, linkage density, connectance, omnivory, species involved in looping, trophic chain length and fraction of biomass at higher trophic levels, as well as higher generality and fraction of biomass at lower trophic levels. An analysis of robustness to simulated species extinction revealed lower robustness to species removals in Mediterranean webs and corroborated their advanced state of degradation. Importantly, the two modelling approaches used delivered comparable results suggesting that they both capture fundamental information about how food webs are structured.

Setting Priorities for Regional Conservation Planning in the Mediterranean Sea

Spatial prioritization in conservation is required to direct limited resources to where actions are most urgently needed and most likely to produce effective conservation outcomes. In an effort to advance the protection of a highly threatened hotspot of marine biodiversity, the Mediterranean Sea, multiple spatial conservation plans have been developed in recent years. Here, we review and integrate these different plans with the goal of identifying priority conservation areas that represent the current consensus among the different initiatives. A review of six existing and twelve proposed conservation initiatives highlights gaps in conservation and management planning, particularly within the southern and eastern regions of the Mediterranean and for offshore and deep sea habitats. The eighteen initiatives vary substantially in their extent (covering 0.1–58.5% of the Mediterranean Sea) and in the location of additional proposed conservation and management areas. Differences in the criteria, approaches and data used explain such variation. Despite the diversity among proposals, our analyses identified ten areas, encompassing 10% of the Mediterranean Sea, that are consistently identified among the existing proposals, with an additional 10% selected by at least five proposals. These areas represent top priorities for immediate conservation action. Despite the plethora of initiatives, major challenges face Mediterranean biodiversity and conservation. These include the need for spatial prioritization within a comprehensive framework for regional conservation planning, the acquisition of additional information from data-poor areas, species or habitats, and addressing the challenges of establishing transboundary governance and collaboration in socially, culturally and politically complex conditions. Collective prioritised action, not new conservation plans, is needed for the north, western, and high seas of the Mediterranean, while developing initial information-based plans for the south and eastern Mediterranean is an urgent requirement for true regional conservation planning.

Contrasting trait syndromes in angiosperms and conifers are associated with different responses of tree growth to temperature on a large scale

Recent large-scale studies of tree growth in the Iberian Peninsula reported contrasting positive and negative effects of temperature in Mediterranean angiosperms and conifers. Here we review the different hypotheses that may explain these trends and propose that the observed contrasting responses of tree growth to temperature in this region could be associated with a continuum of trait differences between angiosperms and conifers. Angiosperm and conifer trees differ in the effects of phenology in their productivity, in their growth allometry, and in their sensitivity to competition. Moreover, angiosperms and conifers significantly differ in hydraulic safety margins, sensitivity of stomatal conductance to vapor-pressure deficit (VPD), xylem recovery capacity or the rate of carbon transfer. These differences could be explained by key features of the xylem such as non-structural carbohydrate content (NSC), wood parenchymal fraction or wood capacitance. We suggest that the reviewed trait differences define two contrasting ecophysiological strategies that may determine qualitatively different growth responses to increased temperature and drought. Improved reciprocal common garden experiments along altitudinal or latitudinal gradients would be key to quantify the relative importance of the different hypotheses reviewed. Finally, we show that warming impacts in this area occur in an ecological context characterized by the advance of forest succession and increased dominance of angiosperm trees over extensive areas. In this context, we examined the empirical relationships between the responses of tree growth to temperature and hydraulic safety margins in angiosperm and coniferous trees. Our findings suggest a future scenario in Mediterranean forests characterized by contrasting demographic responses in conifer and angiosperm trees to both temperature and forest succession, with increased dominance of angiosperm trees, and particularly negative impacts in pines.