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STEP 1. ACTIVATE YOUR PRIOR KNOWLEDGE - assess the problem

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STEP 1. ACTIVATE YOUR PRIOR KNOWLEDGE - assess the problem

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When Yellowstone National Park was created in 1872 in the USA (Arkansas), Grey Wolf (Canis lupus) populations were already in decline in the area. The creation of the National Park did not provide protection for wolves or other predators, and government predator control programs in the first decades of the 1900s essentially assisted in the elimination of the Grey Wolf from the Park. The last wolves were killed in 1926. After that time, sporadic reports of wolves still occurred, but scientists confirmed that sustainable wolf populations had been extirpated and were absent from that area during the mid-1900s.

Starting in the 1940s, park managers, biologists, conservationists and environmentalists began what would ultimately turn into a campaign to reintroduce the Grey Wolf into the Yellowstone National Park. When the Endangered Species Act of 1973 was passed, the road to legal reintroduction was clear. In 1995, Grey Wolves were first reintroduced in the area. The history of wolves in Yellowstone National Park chronicles the extirpation, absence and reintroduction of Grey Wolves, and how the reintroduction was not without controversy or surprises for scientists, governments and park managers.
The wolves were brought in because the increased elk population was overgrazing the deciduous, woody species such as aspen and cottonwood.

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STEP 3. CREATEFurther enrich your BioArea!

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STEP 3. CREATEFurther enrich your BioArea!

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●      two examples of animals with a predator-prey relation;

The Wolf on Greek mountains eats wild rabbits, while shark species in the Aegean see eat smaller species of fish

●      two parasitic organisms;

Scabies, also known as the seven-year itch, is a contagious skin infestation by the mite Sarcoptes scabiei.
Inonotus obliquus, commonly known as chaga mushroom is a fungus in the family Hymenochaetaceae. It is parasitic on birch and other trees.

●      the ecological niche of two characteristic animals;

The position of a species in an ecosystem in terms of the physical characteristics of the are where the species lives and the function of the species in the biological community.
The gray wolf's niche in their ecosystem is: Hunt in packs, Have a small amount of cubs - mostly two offspring Has no natural predators - top predator in its niche, Feed on any animals to survive. This includes animals both smaller or larger than them / alive or dead. May clash with other predators like the puma or bear. Gray wolves help even out the population by eating other animals both large and small. Apex Predator - They are the cornerstone of their ecosystem. They "filter" their ecosystem by getting rid of old injured animals. This also then provides food for scavengers. Gray wolves play a critical role in their ecosystem since there are predators for them.
On the Other hand, deer live in mixed forests habitats, on wooded farmlands and even in suburban areas of established cities. In winter they take to coniferous forests for shelter. Deer are a prey species, providing food for coyotes, bobcats, cougars, wolves and occasionally humans. In turn, the species helps keep vegetation in check.

●      two organisms that share the same food (niche partitioning) and the way that they manage it;

An good example is the Galapagos Islands.

The Darwin Finches & Marine Iguanas on the islands are adapted to their desired food source.

On each island a Darwin Finch is slightly different from one on another island.

The Marine Iguanas eat sea weed in & around the coast, then go back to the island to lounge upon.

The Finches eat whatever the food source on the island they are adapted to.

This is an example of where two niches do not collide, the Finches can't eat the sea weed (not to mention, I don't know many birds which do eat sea weed as a 'first' choice) & the Marine Iguana like most Iguanas are mainly herbivores, but the 1,000s of years of evolution has made both species depending if a variation of the Darwin Finch is on an island the Iguanas live on, has made no competition between them.

●      based on the simplified trophic pyramid found in slide 6 of the resource topic 2.1 'Relationship of organisms in ecosystems', make an analogous one with plants and animals from your own BioArea.

As we see in the picture, herbivores eat plants, and carnivores eat herbivores. As a result, this pyramid is created. In my BioArea we can see most of the species depected in the pictures, such as plants, insects, worms, frogs and amphibians in general, as well as wolves.

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The Mediterranean Hotspot: from knowledge to action to preserve its biodiversity

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The Mediterranean Hotspot: from knowledge to action to preserve its biodiversity

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Infographic video about the current conservation actions and knowledge on the conservation status of more than 3,000 species at the Mediterranean level, with key figures for all the taxonomic groups assessed in the last 10 years, as well as the Key Biodiversity Areas identified by the IUCN Centre for Mediterranean Cooperation.

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IUCN, International Union for Conservation of Nature

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The Mediterranean Hotspot: from knowledge to action to preserve its biodiversity

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Volcanoes in Greece: Famous and active - Greeka.com

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Discover the most famous Greece volcanoes in the mainland and the Greek islands: In Santorini, Nisyros, Methana, Milos and others.

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The palaeogeography of Greece from Miocene to present

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The palaeogeography of Greece from Miocene to present

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a publication of the plants of Greece in the late 18th century, resulting from a survey by John Sibthorp and Ferdinand Bauer.

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radcliffe science library; rsl; science libraries

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The Radcliffe Science Library provides services to support the teaching and learning needs of the science community at Oxford University.

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Natura 2000 is a network of nature protection areas in the territory of the European Union. It is made up of Special Areas of Conservation (SACs) and Special Protection Areas (SPAs) designated respectively under the Habitats Directive and Birds Directive. The network includes both terrestrial and marine sites (Marine Protected Areas (MPAs)).

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Greece’s biodiversity at riskA call for action

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Greece’s biodiversity at riskA call for action

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Greece hosts a large proportion of the species that are threatened at the European level, and has the important responsibility for protecting these species within its territory. Species in Greece require greater action to improve their status.

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The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats

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The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats

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Marta Coll,

Chiara Piroddi,

Jeroen Steenbeek,

Kristin Kaschner,

Frida Ben Rais Lasram,

Jacopo Aguzzi,

Enric Ballesteros,

Carlo Nike Bianchi,

Jordi Corbera,

Thanos Dailianis

Abstract

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).

Citation: Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F, Aguzzi J, et al. (2010) The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PLoS ONE 5(8): e11842. https://doi.org/10.1371/journal.pone.0011842

Editor: Steven J. Bograd, NOAA/NMFS/SWFSC, United States of America

Received: February 24, 2010; Accepted: June 10, 2010; Published: August 2, 2010

Copyright: © 2010 Coll et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: The authors gratefully acknowledge the support given by the European Census of Marine Life, the Total Foundation and the Alfred P. Sloan Foundation. MC was supported financially by the European Commission Marie Curie Postdoctoral Fellowship through the International Outgoing Fellowships (Call FP7-PEOPLE-2007-4-1-IOF) for the ECOFUN project and by Dalhousie University (Halifax, Canada). EB acknowledges financial support from GRACCIE project C5D2007-00067 funded by the Spanish Ministry of Science and Innovation. BG thanks the support of SESAME funded by the European Commission's Sixth Framework Program on Sustainable Development, Global Change and Ecosystems. JISS acknowledges ECOLIFE (CGL2008-05407-C03-03) funds of the Ministry of Science and Innovation of Spain. The present paper is a contribution of JG, DM and XT to the projects 2009SRG665 and 2009SGR484 of the "Generalitat de Catalunya", and of DM and XT to project CTM2007-66635 funded by the Ministry of Science and Innovation of Spain. Research by C. N. Bianchi on Mediterranean Sea biodiversity is partly supported by the project "The impacts of biological invasions and climate change on the biodiversity of the Mediterranean Sea" (Italy-Israel co-operation) funded by the Italian Ministry of the Environment. The funders had no role in study design, data collection and analysis, decision to published, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

The Mare medi terraneum (in Latin) describes the Mediterranean as a "sea in the middle of the land." This basin is the largest (2,969,000 km ²) and deepest (average 1,460 m, maximum 5,267 m) enclosed sea on Earth ( Figure 1a).

(A) Main biogeographic regions, basins, and administrative divisions of the Mediterranean Sea, (B) Annual mean sea surface temperature (°C) (2003, NOAA), (C) Annual mean relative primary production (2002, Inland and Marine Waters Unit, Institute for Environment and Sustainability, EU Joint Research Centre, Ispra, Italy), and (D) maximum average depth (m) (NOAA).

Situated at the crossroads of Africa, Europe, and Asia, the Mediterranean coasts have witnessed the flourishing and decline of many civilizations. The region was an important route for merchants and travelers of ancient times, allowing for trade and cultural exchange, and today it is notable for contributions to global economy and trade. Its coasts support a high density of inhabitants, distributed in 21 modern states, and it is one of the top tourist destinations in the world, with 200 million tourists per year [1].

The Mediterranean Sea connects through the Strait of Gibraltar to the Atlantic Ocean in the west and through the Dardanelles to the Sea of Marmara and the Black Sea in the northeast. In the southeast, the Suez Canal links the Mediterranean to the Red Sea and the Indian Ocean ( Figure 1a). In the Strait of Sicily, a shallow ridge at 400 m depth separates the island of Sicily from the coast of Tunisia and divides the sea into two main subregions: the western (area  = 0.85 million km ²) and the eastern (area = 1.65 million km ²).

General oceanographic conditions in the Mediterranean have been previously described in detail [e.g., [2]-[5]]. It is a concentration basin: evaporation is higher in its eastern half, causing the water level to decrease and salinity to increase from west to east. The resulting pressure gradient pushes relatively cool, low-salinity water from the Atlantic across the Mediterranean basin. This water warms up to the east, where it becomes saltier and then sinks in the Levantine Sea before circulating west and exiting through the Strait of Gibraltar. The climate in the region is characterized by hot, dry summers and cool, humid winters. The annual mean sea surface temperature shows a high seasonality and important gradients from west to east and north to south ( Figure 1b) [3]. The basin is generally oligotrophic, but regional features enrich coastal areas through changing wind conditions, temporal thermoclines, currents and river discharges, and municipal sewage [6], [7], [8] ( Figure 1c). The basin is characterized by strong environmental gradients [9], in which the eastern end is more oligotrophic than the western. The biological production decreases from north to south and west to east and is inversely related to the increase in temperature and salinity.

The Mediterranean has narrow continental shelves and a large area of open sea. Therefore, a large part of the Mediterranean basin can be classified as deep sea ( Figure 1d) and includes some unusual features: (1) high homothermy from 300-500 m to the bottom, where temperatures vary from 12.8°C-13.5°C in the western basin to 13.5°C-15.5°C in the eastern, and (2) high salinity of 37.5-39.5 psu. Unlike in the Atlantic Ocean, where temperature decreases with depth, there are no thermal boundaries in the deep sea of the Mediterranean [10]. Shelf waters represent 20% of the total Mediterranean waters, compared with the 7.6% of the world oceans, and therefore play a proportionally greater role here than in the world's oceans [4]. Shelves in the south are mainly narrow and steep (e.g., Moroccan, Algerian, and Libyan coasts, with the exception of the Gulf of Gabés), while those in the north are wider (e.g., the north and central Adriatic Sea, the Aegean Sea, and the Gulf of Lions) [4] ( Figure 1d). These features influence the morphology and constrain the connections to the Atlantic, the Red Sea, and the Indian Ocean [3], [11].

The enclosed Mediterranean had a varied geological history, including isolation from the world ocean, that led to its near drying out during the Messinian crisis (5.96 million years ago) and to drastic changes in climate, sea level, and salinity [12], [13]. The geological history, biogeography, ecology, and human history have contributed to the Mediterranean's high cultural and biological diversity [14]-[17].

The recent marine biota in the Mediterranean Sea is primarily derived from the Atlantic Ocean, but the wide range of climate and hydrology have contributed to the co-occurrence and survival of both temperate and subtropical organisms [18], [19]. High percentages of Mediterranean marine species are endemic [16], [20]. This sea has as well its own set of emblematic species of conservation concern, such as sea turtles, several cetaceans, and the critically endangered Mediterranean monk seal (Monachus monachus). It is the main spawning grounds of the eastern Atlantic bluefin tuna (Thunnus thynnus) [e.g., [21]-[25]]. There are several unique and endangered habitats, including the seagrass meadows of the endemic Posidonia oceanica, vermetid reefs built by the endemic gastropod Dendropoma petraeum, coralligenous assemblages [e.g., [26]-[29]], and deep-sea and pelagic habitats that support unique species and ecosystems [e.g., [30]-[32]]. Many sensitive habitats exist within the coastal ecosystems. There are 150 wetlands of international importance for marine and migrating birds, and some 5,000 islands and islets [33]-[35].

The region has numerous laboratories, universities, and research institutes dedicated to exploring the sea around them [e.g., [36]]. In addition to the unique geologic, biogeographic, physical, and ecological features, our current understanding of the high biodiversity of the Mediterranean Sea is built on the long tradition of study dating from the times of the Greeks and Romans. Historical documentation began with Aristotle, who contributed to the classification and description of marine biodiversity, and was followed by the work of Plinius (Historia naturalis, liber IX) in the first century B.C., Carl von Linné in the eighteenth century, and many others to the middle of the nineteenth century [e.g., [37]-[40]]. The first deep-sea investigations began at the end of the nineteenth century [e.g., [41]-[43]]. The expeditions of the R.V. "Calypso" by Jacques-Yves Cousteau in the Mediterranean during the 1950s and 1960s provided as well valuable material that supported many important publications on the Mediterranean diversity. The history of ecological research and species discovery in the region has been thoroughly reviewed by Riedl [44], Margalef [45], and Hofrichter [46], though mostly confined to the western Mediterranean.

Numerous detailed taxonomic inventories now exist, most of which are specific to sub-regions or to a range of organisms [e.g., [47]-[56], among many others]. Efforts continue to provide complete datasets of taxonomic groups for the entire basin [e.g., [57]-[67]], although they need periodic updates. Freely available databases for macroorganism inventory include the Medifaune database [68], the Food and Agriculture Organization Species Identification Field Guide for Fishery Purposes [69], the FNAM (Fishes of the North-Eastern Atlantic and the Mediterranean) atlas [70], and the ICTIMED database [71].

However, Web-based datasets often lack updates because of limitations in funding or expertise, and in general, the marine biodiversity of the Mediterranean is less known than its terrestrial counterpart [33], [72]. There are still important gaps at population, community, habitat, and sub-region levels, as well as in basic information about taxonomy distribution, abundance, and temporal trends of several groups [72], [73]. In some areas biodiversity data exist, but it is not easily accessible, because the inventories are not publicly available [74]. Data are also lacking to evaluate the conservation status of many species [34].

The Mediterranean region has been inhabited for millennia, and ecosystems have been altered in many ways [e.g., [5],[16],[45],[75]]. Therefore, impacts of human activities are proportionally stronger in the Mediterranean than in any other sea of the world [33].

Therefore, combined natural and anthropogenic events shaped the biodiversity of the Mediterranean Sea in the past and are likely to continue to do so. Within this complex framework, our aims were threefold:

1. Review available estimates of Mediterranean marine biodiversity, including new estimates of less conspicuous organisms, updating previous checklists, and incorporating living organisms from microbes to top predators.

2. Describe the main spatial and temporal patterns of biodiversity, including innovative ways of describing these patterns.

3. Summarize the main drivers of change and threats to marine biodiversity.

We have collated available information, generated coherent patterns, and identified the current state of knowledge and information gaps, challenges, and prospects for future research. We embrace the concept of biodiversity in its broader definition as the variation of life at all levels of biological organization, but we have focused our efforts on documenting species-level diversity.

Methods

Diversity estimates

Depiction of patterns

Threats to biodiversity

Changes in diversity are partially driven by anthropogenic factors, in addition to natural forces. Therefore, our last aim was to identify and quantify the importance of historical and current human-induced drivers and threats to marine biodiversity.

We used the aggregated results presented by Lotze et al. [113] and explicitly separated the data available for the north Adriatic Sea as an example to explore historical threats in the Mediterranean. Those authors evaluated human impacts that caused or contributed to the depletion or extirpation of species in the north Adriatic Sea over historical time scales.

We also identified current human threats to diversity using published data on specific taxa and areas of the Mediterranean ( File S2) and the opinion of experts. Each expert was asked to (1) list main threats to diversity for their taxonomic expertise group using data available and experience, and (2) rank those threats from 1 to 5, taking into account the relative importance of each threat to the biodiversity (0: no importance, 1: lowest in importance, 5: highest in importance). The experts repeated the ranking exercise considering data available and projecting their results 10 years into the future ( File S2).

In addition and to visualize the impacts of climate warming on species diversity, we documented the mean location of February (the coldest month of the year in the Mediterranean) sea surface isotherms (°C) for the period 1985 to 2006, integrating several data sources. We also generated current and projected future temperature maps, which we compared with sea surface temperature (SST) data from the 1980s. First, we compiled weekly SST data from the National Climatic Data Center (National Operational Model Archive and Distribution System Meteorological Data Server, NOMADS, NOAA Satellite and Information Service), and interpolated maps at 0.1° resolution. Next, we averaged weekly SST values from 1981 to 1984 for each 0.1° grid cell. Last, we used the Mediterranean model OPAMED8 based on the A2 IPCC scenario [120] to visualize the future climate. This model considers main forcing parameters (river runoffs, exchanges with connected seas, and wind regimes) and was used to generate climate data for the middle (2041-2060) and the end of the twenty-first century (2070-2099).

Results

Diversity estimates in the Mediterranean

Within the Animalia, the greater proportion of species records were from subphylum Crustacea (13.2%) and phyla Mollusca (12.4%), Annelida (6.6%), Platyhelminthes (5.9%), Cnidaria (4.5%), the subphylum Vertebrata (4.1%), Porifera (4.0%), Bryozoa (2.3%), the subphylum Tunicata (1.3%), and Echinodermata (0.9%). Other invertebrate groups encompassed 14% of the species, and Plantae included 5%. Detailed biodiversity estimates of main taxonomic groups of benthic macroscopic primary producers and invertebrates are summarized in Table 1 and documented in File S2 in detail.

Available information showed that the highest percentage of endemic species was in Porifera (48%), followed by Mysidacea (36%), Ascidiacea (35%), Cumacea (32%), Echinodermata (24%), Bryozoa (23%), seaweeds and seagrasses (22%), Aves (20%), Polychaeta (19%), Pisces (12%), Cephalopoda (10%), and Decapoda (10%) ( File S2). The average of the total endemics was 20.2%. In some groups the percentage of endemics was now lower than in the past, partly due to new finding of Mediterranean species in adjacent Atlantic waters ( File S2).

The biodiversity of the "smallest"

An important bulk of species diversity was attributed to the prokaryotic (Bacteria and Archaea) and eukaryotic (Protists) marine microbes. However, the differences in the methodologies and types of studies and the continuously changing state of our knowledge of marine microbial diversity make it difficult to provide species estimates for the Mediterranean (or from anywhere else) and establish comparisons.

However, researchers have made efforts to obtain estimates of the dominant microbial species in Mediterranean waters. The expansion of electron microscopy in the last decades of the twentieth century helped to untangle inconsistencies in the distribution of some described species and to consolidate the establishment of a biogeography of many protist taxa. More recently, molecular techniques (metagenomics) have been used to enumerate the microorganisms present in a given sample and have completely transformed the field by changing ideas and concepts. These advances have highlighted the problems with the species concept when applied to microbial communities, which may be based on morphology, biology, or phylogeny [125]. Furthermore, different methodologies have biases that give different views of microbial diversity [e.g., [126],[127]], and now we know that microdiversity is a general characteristic of microbial communities [128], making the delimitation of "diversity" units difficult. To avoid some of the problems with the "species" delimitation, some authors prefer to use "functional diversity": the amount and types of microbial proteins (e.g., functions) in the sample [e.g., [129]], rather than "species" diversity.

According to the compilation published in Hofrichter [87], the number of described protist species in the Mediterranean is approximately 4,400 ( Table 1). However, this estimate requires cautious interpretation and it is likely that many morphospecies, more or less well described, will include a number of cryptic or pseudocryptic variants [e.g., [125]]. Molecular methods have recently uncovered new sequences that are being associated with the organisms they represent [130]. Fingerprinting techniques [131] have been used to compare microbial communities and establish the scale of variability of these communities. For example, Schauer et al. [132] determined that, along the coastal northwestern Mediterranean, the time of the year was more important than exact location in determining bacterial community structure. Acinas et al. [133] and Ghiglione et al. [134] showed that microbial communities tend to be similar in the horizontal scale and much more variable on the vertical scale, but these techniques are not appropriate to determine the number of species present and usually refer only to the dominant organisms. Recent application of new methodologies (such as metagenomics and 454-tag sequencing) will in the near future provide more accurate estimates.

All studies to date concur in identifying members of the SAR11 group as some of the most abundant Mediterranean bacteria, comprising 25-45% of the reported sequences [e.g., [126],[127]]. These are followed by other Alphaproteobacteria, which tend to be more common in coastal regions and during algal blooms (such as Roseobacter-like). Cyanobacteria (Prochlorococcus and Synechococcus), diverse culturable ( Alteromonadales) and unculturable Gammaproteobacteria and Bacteroidetes form the rest of the diversity with some differences with depth and with distance from land. Several studies have concentrated in the diversity of subgroups of these abundant bacteria in the Mediterranean [e.g., [135],[136]].

A similar situation to that with prokaryotes occurs with small eukaryotes, which are photosynthetic, heterotrophic, or mixotrophic organisms. These small eukaryotes are found in abundances of 10 ³-10 ⁴ ml −1 and have low morphological variability [147]. Thus we must rely on molecular techniques to grasp their diversity. Molecular work has allowed the discovery of new groups of eukaryotes present in this smallest size class [148], [149].

The study of Mediterranean protists has benefited from the early establishment of marine laboratories and a number of illustrated books and checklists [e.g., [150]-[155]]. More recent inventories can be found in Velasquez and Cruzado [156] and Velasquez [157] for diatoms, Gómez [158] for dinoflagellates and Cros [159] for coccolithophorids. The compilation of northwestern Mediterranean diatom taxa of Velasquez [157] records 736 species and 96 genera. The checklist of Gómez [158] contains 673 dinoflagellate species in 104 genera.

Most of the biodiversity work on ciliates has focused on tintinnids or loricate ciliates, while studies involving naked ciliates tend to use groupings based on ecological morphotypes and only rarely include detailed taxonomical work [e.g., [155],[166]-[168]]. Numbers of species ranging from 40 to 68 were recorded in one to several-year surveys of various Mediterranean sites [among others 154]. Other groups, such as the Foraminifera, which have calcium carbonate tests, and the Radiolaria, which produce siliceous or strontium sulfate skeletons, have been the subject of many stratigraphical and paleoceanographical studies. However, biodiversity work on living Foraminifera and Radiolaria in the Mediterranean is scarce [e.g., [155],[169],[170]]. Hofrichter [87] provided a systematic summary of the main groups and species of both autotrophic and heterotrophic protists found in the Mediterranean.

The biodiversity at high trophic levels

Species that occupy the upper trophic levels, normally beyond the level of secondary consumers, are classified as predators. They have lower diversity than other taxonomic groups, but information available is usually more detailed ( Table 1 and File S2). We reviewed data available for fish, seabirds, marine mammals, and turtles in the Mediterranean Sea.

Ground-breeding species such as seabirds (gulls and terns) are counted using census bands [171] and monitored by satellite tracking. However, procellariiforms reproduce in caves and burrows in cliffs on remote, inaccessible islets, and census methods to estimate population densities are not totally reliable. Population models, based on demographic parameters, allow researchers to estimate extinction probabilities [172]. A census of marine mammals or turtles normally uses transect data collected from aerial or boat-based sighting surveys developed to assess abundance, while movement patterns are tracked with transmitters and monitored by satellite tracking as well. Fish species are mainly studied using scuba diving or fishing techniques.

There is still some discussion about diversity estimates for these taxonomic groups. For fish species, for example, several estimates of Mediterranean diversity exist: Quignard [173] lists a total of 562 fish species occurring in the Mediterranean Sea; Whitehead et al. [70] mention 589; Fredj and Maurin [68] list a total of 612 species (and identified 30 species as uncertain); and Quignard and Tomasini [90] register 664 species. Hofrichter [87] summarizes 648 species, and Golani et al. [89] report a total of 650 fishes ( File S2). Fish diversity estimates also change as new species are described or reclassified. The updated list of exotic fish species [88] reveals that the Mediterranean currently contains 116 exotic species, although more species are likely to be cited. There is also a long-standing controversy regarding genetic differentiation among a few fish populations and sub-basins, especially of commercial species due to management implications (for example for the European anchovy Engraulis encrasicolus), although results are still under debate [e.g., [174]].

Approximately 80 fish species are elasmobranchs, although the status of some is uncertain because of infrequency or uncertain reporting [e.g., [123],[175],[176]]. According to Cavanagh and Gibson [123], nine of these elasmobranch species may not breed in the Mediterranean, while some are rare because the Mediterranean represents the edge of their distribution ranges. Only four batoid species are Mediterranean endemics: the Maltese skate (Leucoraja melitensis), the speckled skate (Raja polystigma), the rough ray (R. radula), and the giant devilray (Mobula mobular) [175].

Nine species of marine mammals are encountered regularly in the Mediterranean ( File S2) [92], [93], [94], [97]. Of these species, five belong to the Delphinidae, and one each to the Ziphiidae, Physeteridae, Balaenopteridae, and Phocidae. Other 14 species are sporadically sighted throughout the basin and are considered "visitors" or "non-residents."

Of the seven living species of sea turtles, two (the green and the loggerhead Chelonia mydas and Caretta caretta - Cheloniidae) commonly occur and nest in the Mediterranean, and one (leatherback turtle Dermochelys coriacea - Dermochelyidae) is regularly sighted but there is no evidence of nesting sites. The other two (hawksbill and Kemp's riddle turtles Eretmochelys imbricata and Lepidochelys kempi - Cheloniidae) are extremely rare and considered to be vagrants in the Mediterranean ( File S2) [22], [95], [96], [98], [99].

What is hidden in the deep?

Because of the large size of the Mediterranean deep-sea ecosystems ( Figure 1d), our knowledge of the benthic deep-sea diversity is incomplete [177]. In the past 20 years, several studies on deep-sea sediment diversity have been undertaken in various oceans [e.g., [178],[179]] but have been limited to a few taxonomic groups. However, due to technological improvements that render the deep waters more accessible, the deep-sea benthos of the Mediterranean has received increased attention and there is progress toward a more comprehensive view of the levels, patterns, and drivers of deep-sea biodiversity in this semienclosed basin [180].

However, the populations of the most common benthic mollusks in depths greater than 1,000 m off the Israeli coast are composed of both adult and juvenile specimens, and one species, Yoldia micrometrica, the most common and abundant species in the eastern Mediterranean, is unrecorded from the westernmost part of the sea. In addition, and though much reduced in diversity and richness compared with the deep-sea fauna of the western and central basins of the Mediterranean, the Levantine bathybenthos is composed of autochthonous, self-sustaining populations of opportunistic, eurybathic species that have settled there following the last sapropelic event [189]-[191].

Macpherson [192] and Briggs [193] have suggested that within the Atlantic-Mediterranean region, the fauna (including invertebrates and fishes) of the Mediterranean is more diverse than that of the Atlantic and displays considerable endemism. For strictly deep-dwelling species (e.g., the deep-water decapod crustacean family Polychelidae), the Gibraltar sill is not an impenetrable barrier for some deep-waters macrobenthic species [194]. Moreover, available hypotheses did not consider meiofauna diversity, which is characterized by direct development [188] but also by a small size, which allows organisms' resuspension and drifting over wide regions. This is consistent with information on the most abundant deep-sea phylum, the Nematoda, which often accounts for more than 90% of total meiofauna abundance [9], [195]. Nematode diversity has been investigated only in a few areas of the deep sea in the Mediterranean: slopes of the Gulf of Lions, Catalan margin and Corsica, Tyrrhenian basin, and Eastern Mediterranean [e.g., [196]-[198]]. Recent collections from a limited number of sites throughout the Mediterranean basin (at approximately 1,000 m, 3,000 m, and 4,000 m depth), suggest that, conversely to what was expected, the deep-sea nematode fauna of the Mediterranean basin is rather diverse.

At bathyal and abyssal depths, levels of nematode genera and species richness are similar to those reported from other deep-sea areas of the world oceans [198]. In the deep sea of the Mediterranean, small-bodied taxa (e.g., meiofauna) can reach a high diversity, and with the presence of a high prokaryotic diversity in the sediments of the deep-sea Mediterranean [199], this may change the view that the Mediterranean deep-sea biota is impoverished in comparison with its Atlantic counterpart. Endemic macrobenthic species account for approximately 13-15% of total species number at depths from 200 m to 1,000 m, and approximately 20% at 2,000 m [200]. These estimates are similar for each taxon ( Table 1) and are further supported by the continuous discovery of new species (both within the highly diverse Nematoda and in rare phyla such as the Loricifera) in different sectors of the deep Mediterranean [180]. Therefore, the general conclusion that the biodiversity is high in coastal systems and low in the deep sea of the Mediterranean might not hold true. Detailed references about the deep Mediterranean can be found in [180].

New biodiversity

The biodiversity of the Mediterranean is definitively influenced by the introduction of new species [e.g., [88],[201]-[208]]. Since the first review of exotic species in the Mediterranean [209], the studies in this topic have intensified. Now more than 600 metazoan species have been recorded as alien, these representing 3.3% of the total estimates ( Table 1, and File S2 for detailed information by taxonomic group). However, this estimate is continuously increasing and may be as high as 1,000 species if unicellular aliens and foraminiferans are included [e.g., [206],[207],[208]].

Most of these introductions are littoral and sublittoral benthic or demersal species (or their symbionts). Because the shallow coastal zone, and especially the benthos, has been extensively studied and is more accessible than deeper waters, new arrivals probably will be encountered and identified in shallow waters. The species most likely to be introduced by the predominant pathways (the Suez Canal, vessels, and mariculture) are shallow-water species.

As far as can be deduced, the majority of aliens in the Mediterranean entered through the Suez Canal (Erythrean aliens) (53%), and an additional 11% were introduced primarily through the Canal and then dispersed by vessels. Introductions from vessels from other parts of the world account for 22% of introduced species, and aquaculture accounts for 10%. A further 2% arrived with the introduction of aquaculture and were secondarily spread by vessels. The means of introduction differ greatly among the phyla: whereas of the alien macrophytes, 41% and 25% were introduced through mariculture and vessels, respectively, the majority of alien crustaceans, mollusks, and fish are Erythrean aliens (59%, 64%, and 86%, respectively), and mariculture introductions are few (4%, 5%, and 4%, respectively) [[216], B.S. Galil, personal observation].

The numbers of alien species that have been recorded over the past century have increased in recent decades. The increasing role of the Mediterranean as a hub of international commercial shipping, a surge in the development of marine shellfish farming over the last 25 years, and the continued enlargement of the Suez Canal have contributed to the resurgence of introductions since the 1950s. Many introduced species have established permanent populations and extended their range: 214 alien species have been recorded from three or more peri-Mediterranean countries, and 132 have been recorded from four or more countries [[216], B.S. Galil, personal observation].

Spatial patterns of Mediterranean biodiversity

Temporal trends

In this section, however, we summarized main changes since the end of the last ice age (approximately 12,000 years ago). During this time there were notable climate-driven fluctuations but also human-induced changes due to the long periods of exploration and exploitation, and more recently the reopening to the Red Sea through the Suez Canal, the globalization of commerce and trade, increasing pollution and eutrophication of coastal areas, habitat modification and loss, and finally the looming climate change.

Early evidence of human interaction with marine fauna in the Mediterranean Sea comes from the Paleolithic period and continues through the Mesolithic and Neolithic periods (approximately 20,000-4000 B.C.). Zooarchaeological remains are found in Franchthi Cave in the southern Argolid, Greece [238], Las Cuevas de Nerja in southern Spain [239], Athlit Yam, a submerged site south of Haifa Bay in Israel [240], Cape Andreas Kastros in Cyprus [241], and the Strait of Gibraltar [242]. In Greece, fish bones of large tuna, Sparidae and Mugillidae, were found. Zooarchaeological remains in Spain include 20 taxa and show changes in mean fish size and range over time that have been considered as indication of overfishing. At Cape Andreas Kastros in Cyprus and in Athilit Yam, 90% of the remains are grey trigger fish (Balistes capriscus), which points to intensive fishing regardless of size. In Gibraltar, remains of Mediterranean monk seals and mollusks consumed by humans were found. However, stable isotope analyses of human bones show that between 10,000 and 8000 B.C., the main Mediterranean coastal populations did not rely significantly on marine food [243], [244].

Since the fifth century B.C., humans have exploited marine resources. Aristotle, in his zoological works dating to the fourth century B.C., focuses his scientific interest on fish and invertebrates exploited by humans in various ways [245]. Fisheries in the Aegean communities by that period are characterized by variability both in the nature and abundance of the exploited fish and in the manner of their exploitation [246]. Mollusks and other invertebrates are part of the diet of ancient Greeks, and their consumption is connected with the treatment or prevention of various health problems and diseases [247]. Bath sponges of the genera Spongia and Hippospongia, collected by skillful divers, are widely exploited for household and personal hygiene purposes, and play a principal role in medical practice [248].

Commercial fishing and fish processing activities play an important role in the Pontic economy. The export of fish and fish products, including salt-fish ( tarichos) and fish sauce ( garum) mainly from European anchovy to the Aegean Sea, continue into the Roman period [249]. These products are exported from the western Mediterranean, but g arum is forgotten in the west by the tenth century, although it is still prepared in Constantinople in the fifteenth and sixteenth centuries [250]. Naval trade traffic becomes intense, and invasions of islands from the mainland are already common, and they result in the beginning of the introduction of alien species in those ecosystems. Some of these introductions (rats, carnivores) trigger the extirpation of many seabird colonies, and they have shaped the current distribution of several seabird species [251], [252].

Seafood becomes increasingly popular toward the end of Roman domination, probably because of the proximity of, and access to, marine resources. There is historical evidence of overfishing in some parts of the Western Mediterranean in the early Imperial period [253]. Even then, certain fishing techniques are prohibited to manage or counteract the decline in fish stocks (such as fishing by torch lights at night), and efforts are made to boost natural availability with introduced fish and shellfish stocks. For example, the parrot fish (Sparisoma cretense) is captured in the Aegean Sea and released in the Tyrrhenian Sea [253], [254]. There are also pictorial remains that show fishing gear and a large variety of targeted species during Roman times. Gastropods [255], the red coral Corallium rubrum [256], and several species of sponges [257] were exploited on an industrial scale.

Fishing, fish processing, industrial exploitation of several marine species, and development of improved fishing gear continue during the Byzantine period [253]. Various literary sources point out that targeted species, among them the currently overfished tuna, are conspicuous. There is a 200-year gap between the Moslem conquest of the Near East and northern Africa and the appearance in the ninth century of the first Arabic written sources [250]. In northern Africa, the first written evidence dates from the tenth century and refers to fishing gear used to catch mullets, Atlantic bluefin tuna (with large spears), and fish in shallow waters [258]. Zooarchaeological material from the Israeli coastline dating from the Byzantine through the Moslem Crusader and Mamluk periods (fourteenth century) points to a high consumption of marine and freshwater fish that are still fished in Israel today, such as the thin-lipped grey mullet (Liza ramada), Sparidae, and the parrot fish [250]. There is noticeable fishing activity dating from the Byzantine, Moslem (tenth century), and later Norman periods (eleventh to thirteenth centuries) in southern Italy and in Sicily, where Atlantic bluefin tuna is the main target species exploited by traps ( tonnara) [259].

Harvesting of the gastropods Hexaplex trunculus and Bolinus brandaris is an example of the successive exploitation of marine resources from the Iron Age until the thirteenth century in the Eastern Mediterranean. These species are specifically harvested for the purple pigments extracted from their shells and used to dye clothes. This harvest disappear from the Levantine area in the late twelfth century, and from Greece a century later, although both species are still abundant to this day [250]. Another example of human exploitation of marine resources from historical times is the hunting of seabirds on islands, particularly of shearwaters, which probably constituted the only source of protein in periods of scarcity especially on small islands. In places such as Formentera (Balearic Islands), humans contribute to the depletion, and partial extinction, of Balearic shearwaters (Puffinus mauretanicus), with consequences at the level of the marine trophic web [260].

Human impacts on marine biodiversity grow increasingly stronger as the Mediterranean cities and ports continue to grow and more recent centuries witnessed substantial advances in technology. It is assumed that since the fourteenth century, the adoption of new fishing methods (such as the tonnara, a sort of drift net mainly used for tuna fishing) in the Western Mediterranean, their spread to southern Italy [261], [262], and their introduction to the Adriatic in the seventeenth century [261], [263] increase fishing catches. Fishing catches increase to an extent that even the early fishermen organizations (sixteenth century), such as Cofradias in Catalonia [262] and the Prud' homies in Provence [264], are concerned about possible negative effects on exploited stocks. Such effects are further intensified by the increasing industrialization in the nineteenth century, with an increase in the efficiency of existing fishing gear (e.g., otter trawl) and the introduction of new ones (such as midwater pelagic trawls, hydraulic dredges, and iron-toothed dredges). Industrialized fishing had severe impacts on species, habitats, and ecosystems [265]. Several studies also show historical changes in fish communities of different regions of the basin [e.g., [25],[123],[266]-[268]]. These findings point to a general severe depletion of top predators in the basin, including Atlantic bluefin tuna, which is considered critically endangered according to the declining trend observed in the Atlantic and the Mediterranean in the last 50 years. Historical fluctuations in the abundance of this species have been described on the basis of a centuries-long time-series of tuna trap catches, starting in the seventeenth century, and suggested to be linked to climate fluctuations [269].

Despite this comparative wealth of historic information about temporal trends mainly linked to the history of human exploitation of Mediterranean marine biodiversity, many unknowns remain in spatial and chronological gaps from prehistoric periods to the present. Ancient, medieval, and early modern records contain qualitative rather than quantitative data, and it is difficult to depict general diversity trends at either a species or ecosystem level at the scale of the whole Mediterranean.

Interesting results do emerge from analyses of specific regions. The overall trends reported by Lotze et al. [113] for the north Adriatic Sea indicated that prehistoric people had no measurable effect on marine resources around this basin ( Figure 8a, see File S2 for species included in the analysis). This changed during the Classical period (500 B.C. to A.D. 600) [270], and especially during Roman times, when reports of species depletion and overexploitation in coastal waters increased. It is possible that marine species recovered from heavy exploitation after the collapse of the Roman Empire, as has been documented for terrestrial resources [33]. However, human population increased during the Medieval period (approximately A.D. 600 to 1500), increasing the pressure on marine resources. With the onset of the industrialization in Europe in the nineteenth century, signs of species depletions and rareness increased and accelerated throughout the twentieth century, when the first extirpations of species were also recorded. Biodiversity did not decrease, however, because some species were newly introduced into the Adriatic Sea [271]. No temporal trend is known for alien species in the Adriatic Sea, so we showed ( Figure 8a) a timeline of mollusk invasions in the Mediterranean as a whole [272], which started in the late nineteenth century and accelerated during the twentieth century. The depletion of formerly abundant species and the invasion of new species caused a shift in species composition and diversity in the north Adriatic Sea [113]. Local species depletions and extirpations mostly occurred among large species, including marine mammals, birds, reptiles, and commercial fish and invertebrates, while species invasions were mainly by smaller species at lower trophic levels, such as invertebrates and algae ( Figure 8b). Such fundamental changes in species composition had effects on the structure and functioning of food webs and ecosystems [113], [273].

Population declines have also been noted among marine mammals throughout the Mediterranean. These species include sperm whales, which have been declining since the end of the 1980s [274]; short-beaked common dolphins, which began to decline around the 1970s [93], [275]; common bottlenose dolphins, which have decreased by at least 30% over the past 60 years [97], [276]; and striped dolphins, which have been in decline since the early 1990s [277]. The Mediterranean monk seal, in particular, was deliberately hunted during the Roman period [278], and it disappeared in the greatest part of the Mediterranean basin during the early 1900s [279], [280]. Currently, it mainly occurs in small, isolated areas of the Greek and Turkish coasts, and northwest African coastal waters ( Figure 9), but the presence of Mediterranean monk seal in some of these areas is uncertain. There are fewer loggerhead and green turtles throughout the Mediterranean, although historical records were available to determine the severity of their population decline [22], [95]. Known nesting sites especially for the loggerhead turtle disappeared in several areas of the basin [22] ( Figure 9).

Although the population trends for most seabird species are not well known, all reliable long-term information suggests that most seabird species have recovered on the European coasts during the last three decades. This recovery is due to more restrictive conservation policies at national and international levels. With the exception of shearwaters, seabird species show relatively stable population trends. Gulls and terns, after two decades (1980s and 1990s) of sharp increase in their densities (up to an average 13% annual growth rate in Audouin's gull) [171], are now in dynamic equilibrium [281]. Sparse data on shags suggest a slow recovery in the last two decades. Storm petrel populations are stable at the few long-term monitored sites [282], but many suitable breeding sites have been destroyed since historical times along coastlines. Paleontological records confirm that the distribution of many species was much larger, even occupying habitats in the interior of large islands relatively far from the sea, where recolonization is now impossible [283]. Population recoveries of Mediterranean seabirds must be considered only partial, and only occurring where protection is effective [284].

Threats to diversity and hot spots

As shown above, anthropogenic factors have influenced the general patterns and temporal trends of Mediterranean marine diversity with varying degrees of intensity. Quantifying the importance of each threat is essential for future analysis.

Lotze et al. [113] provided data to evaluate the human impacts that caused or contributed to the depletion or extirpation of species in the north Adriatic Sea over historical time scales. Exploitation stood out as the most important factor causing or contributing to 93% of depletions and 100% of local extinctions or extirpations ( Figure 8c). Habitat loss or destruction was the second-most-important human impact, followed by eutrophication, introduced predators, disease, and general disturbance. While 64% of depletions and 88% of local extinctions were caused by a single human impact, in all other cases the combination of two or several human causes was responsible for the decline or loss. This highlights the importance of cumulative human impacts, especially in coastal ecosystems, with emphasis on species with commercial interest.

Figure 11 shows past changes and projected future increases in sea surface temperature (SST) in the Mediterranean Sea. The 15°C isotherm, whose one-century climatological mean crosses the Straits of Sicily, may have moved northward in recent times ( Figure 11a). This can imply that a number of tropical Atlantic species that entered the Mediterranean during the last interglacial (125,000 to 110,000 years ago) will reenter the Western Mediterranean in the near future [286]-[288]. In the meantime, in the Western Mediterranean, the "14°C divide" [289], the one-century climatological mean of the surface isotherm for February that coincides with a frontal system created by mesoscale eddies in the Algerian Basin [290] and that may act as a barrier to dispersal, has apparently moved northward in recent times ( Figure 11a). The southern sectors of the Mediterranean harbor many native warm-water species that do not occur or get much rarer in the northern sectors. These "southerners" are apparently confined by the 14°C divide. Perhaps not coincidentally, many of these native but "meridional" warm-water species have colonized the northern sectors, which are thus facing a process of "meridionalization" [e.g., [286],[291],[292]]. In addition, the mean SST made in early 1980s ( Figure 11b) revealed that the warmest area of the Mediterranean was the Levantine Basin, with a mean SST of 21.8°C, and the coolest areas were the Gulf of Lions and the Ligurian Sea, with a mean SST of 16.9°C. Climate models predicted that by 2041-2060, the major part of the Mediterranean will become warmer except the northern Adriatic, which is expected to become cooler (OPAMED8 model based on the A2 IPCC scenario, Figure 11c). By 2070-2099, the Mediterranean is projected to warm by 3.1°C ( Figure 11d), the last cool enclaves being the Gulf of Lions and the northern Adriatic, with a mean SST of 18°C.

Taking into account data regarding marine biodiversity and threats, we mapped vertebrate endangered species and have tried to locate potential hot spot areas of special concern for conservation in the Mediterranean ( Figure 12). The first attempt included fish, marine mammals, and sea turtles, which are considered important sentinels for ocean health. The identified hot spots highlighted the ecological importance of most of the western Mediterranean shelves. The Strait of Gibraltar and adjacent Alboran Sea and African coast were identified as representing important habitat for many threatened or endangered vertebrate species. The most threatened invertebrate species in the Mediterranean, the limpet Patella ferruginea, is also distributed along this area [293]. Both the northern Adriatic and Aegean seas also showed concentrations of endangered, threatened, or vulnerable species. Other equally species-rich waters along the northeast African coast, and the southern Adriatic Sea, were of lesser concern for the protection of endangered species.

Discussion

Estimates and patterns of marine diversity in the Mediterranean Sea

Our estimate of 17,000 species for marine biodiversity in the Mediterranean updated and exceeded previous values, which were on the order of 8,000-12,000 species ( Table 3). In comparison with the 1992 estimate [15], the total number of recorded species has increased substantially. As a result of recent efforts and improvements in analytical methods and instruments, our estimates of invertebrates and protists, in particular, have undergone an upward revision in recent years. Current estimates of sponges, cnidarians, polychaetes, mollusks, arthropods, echinoderms, ascidians, and other invertebrates all exceed those dating back to the early 1990s. However, since most microbial diversity is basically unknown, global numbers and their evolution are uncertain.

Estimates from global databases that include Mediterranean information up to September 2009 range from 4% and 25% of the total species diversity estimated in our study ( Table 3). They covered vertebrate taxa fairly comprehensively, but other taxonomic groups were underrepresented. WoRMS included 8,562 records of Mediterranean marine species, which represented 50% of species registered in this study. Mediterranean databases such as ICTIMED (specialized in fish diversity) included about 70% of fish diversity reported in our study.

In addition, the data used to draw spatial patterns were collected from the 1980s to 2000s, so results may differ from the current situation and may represent potential ranges and values rather than current ones. However, similarities exist between results achieved with distribution maps drawn with expert data and predicted results using AquaMaps models. These similarities indicated that the species richness maps resulting from this study are a useful first attempt to represent comprehensive species richness patterns at the Mediterranean scale. Differences encountered using both methods may be due to limitations of the data. By their nature, expert-drawn maps or sightings often represent underestimates of total species distributions because of the absence or lack of effort in certain areas (in our case the southern shorelines of Mediterranean along the coasts of northern Africa and the eastern sites) and the inability to detect rarer species without sufficient efforts. On the other side, AquaMaps model predictions do not currently factor human impacts or ecological interactions and may be closer to fundamental or historical niche rather than realized niche. Therefore some AquaMaps predictions may represent overestimates (a good example is the Mediterranean monk seal; see www.aquamaps.org). Besides, the relative probability of occurrence calculated from AquaMaps does not distinguish between a rare species that might only have been sighted once in a given cell, and a more abundant species that might be sighted every day. AquaMaps rely exclusively on data accessible through OBIS/GBIF, which currently contains few Mediterranean records. Therefore, for many species, occurrence was inferred from habitat use outside of the Mediterranean. Because the Mediterranean environment represents some environmental extremes (such as salinity and temperature records), occurrences in the eastern part may not have been captured adequately by AquaMaps, and this could partially explain the low values in this region. These limitations are extended to our first attempt to depict hot spot areas in the Mediterranean. The eastern region hosts important populations of elasmobranchs and marine mammals that are currently threatened, but their probability of occurrence estimated by AquaMaps model is lower than 0.4. Further studies should be able to reconcile both mapping sources and confirm or correct patterns.

Explanations for the observed heterogeneity of species richness in the Mediterranean Sea include the threshold of the Siculo-Tunisian Strait that divides the Mediterranean into two basins, and the paleo-biogeographical history of the Mediterranean Sea. The western basin shows more biological similarity with the Atlantic Ocean, hosting a higher number of cold-temperate species, while the eastern basin shows more biological similarities with the Indo-Pacific, and hosts a larger number of subtropical species. The Siculo-Tunisian Strait still partially acts as a barrier to the dispersal of many species between the two basins and constitutes their meeting point.

Diversity differences between areas may also reflect changes in water masses and circulation [305], [306] as well as changes in temperature and salinity [307]. The diversity of some groups is definitively influenced by this temperature gradient. For the sipunculans, richness may be linked to the temperature of the water masses during the year [289], which reflects a physiological barrier between cold and warm water for cold- and warm-water species. For example, Golfingia margaritacea is mainly a temperate and boreal species [229], and its presence in the Mediterranean may indicate the prevalence of colder water masses. In contrast, other thermophilic species, such as Phascolion convestitum and Aspidosiphon elegans, have been proposed as Lessepsian migrants [229], [308].

Diversity distribution in the Mediterranean is also associated with a productivity gradient. Higher productivity areas show higher diversity partially because they are important feeding and reproductive sites for several taxa. Most of these areas occur in the Western Mediterranean and the northern Adriatic that, for example, host many species of fish, seabirds, marine mammals, and turtles [e.g., [91],[110],[309]]. Their distribution is associated with feeding habits [e.g., [92],[93],[97],[276],[280]]. Moreover, some fish, seabirds, sea turtles, and mammals show opportunistic feeding behavior, exploiting discards from trawling and purse seines, and to a lesser extent from artisanal long-lining [e.g., [310]-[312]]. In developed Mediterranean countries, discards from trawl fishing can be up to 400% of the commercially valuable catches, and such amounts of food, which may be predictable in space and time, are scavenged by many species. Most Mediterranean marine mammals are predominantly offshore and prefer deep-water habitats, but a few species can venture to inshore waters and scavenge fishery discards [97], [309], [313].

The three main categories explaining the drivers of biodiversity in the deep Mediterranean are (i) bathymetric gradients, which are associated with increasing pressure and decreasing food availability in deeper sediments; (ii) geographical and physicochemical features, which are responsible for the north-northwest-south-southeast gradient in trophic conditions; and (iii) environmental heterogeneity (e.g., grain size distribution, habitat complexity, distribution of food inputs) [179], [180]. Our understanding of the mechanisms driving deep-sea biodiversity patterns is still limited, but some of the factors frequently invoked are (a) sediment grain size and substrate heterogeneity [231]; (b) productivity, organic content, or microbial activity [314]; (c) food resources [233]; (d) oxygen availability [315]; (e) water currents [185]; and (f) occasional catastrophic disturbances [219]. Thus, the spatial distribution of available energy may influence the distribution of benthic abundance, biomass, and biodiversity [9], [184], [196], [219], [316]-[318]. Food availability depends almost entirely on the supply of energy from the water column and decreases with depth, which may explain most of the variability between the observed spatial patterns of the benthic biodiversity in the deep Mediterranean Sea.

Threats to diversity

In the past, geological and physical changes lie at the root of the most dramatic changes in biodiversity in the Mediterranean Sea. Today, human activities are essential elements to consider as well, and several of them threaten marine diversity. The most important threats in this region are habitat loss, degradation and pollution, overexploitation of marine resources, invasion of species, and climate change.

The unknowns and limitations

The study of Mediterranean marine diversity over many years has produced a significant amount of information. Yet this information remains incomplete with the discovery and description of new species, especially of smaller, less conspicuous and cryptic biota ( Table 1 and File S2). The biodiversity in the Mediterranean Sea may be in fact much higher than is currently known.

We do not have credible measures of microbial richness, but development of new technologies will allow us to decide whether this is knowable or not. The description of microbial diversity is probably better approached through the continued study at selected sites, such as the Microbial Observatories, for which data exist on both identification methodologies and the functioning of the ecosystem. Current Mediterranean observatories are at Blanes Bay, Gulf of Naples, Villefranche's Point B, Dyfamed station, and the Mola and SOLA stations in Banyuls. Sites in the southern and eastern Mediterranean are still to be added.

Further exploration and taxonomic work on seaweeds and seagrasses is needed in all the African countries (mainly in Libya and Egypt), the Levantine Sea (Israel, Lebanon, Cyprus, Syria), and the Aegean Sea (Greece and Turkey). Phycological surveys are also required in Croatia, because several species (and even genera) described from the Adriatic have never been found again and require taxonomic reevaluation. We do not expect a significant increase in the rate of description of new species, but the description of new macroalgal species continues [e.g., [415],[416]]. A large number of species are poorly known, and our checklist includes several taxa inquirenda (see File S2). Accurate morphological studies, and new molecular tools, are required to decipher the taxonomy of several genera, including Ectocarpus, Cystoseira, Acrochaetium, Polysiphonia, and Ulva.

Sampling biases are another source of uncertainty in the estimation of marine biodiversity. In particular, the three-dimensional character of marine ecosystems requires much more study at depths where light penetration is perceived as important but is poorly understood. Light intensity decreases with increasing depth and species perform extensive migrations within the water column or along the seabed. Endobenthic species display rhythms of emergence, including burying or burrowing within the substrate and sheltering in natural holes [425]. Marine species react to light intensity cycles, which may include movements in and out of our sampling windows [426]. Information gathered without attention to such rhythmicity will affect perceived population distribution, biomass, and estimated biodiversity [425]. These issues have been integral to land ecology since the early twentieth century [427] but have been rarely considered in the marine environment. In the Mediterranean, Sardà et al. [428] considered this problem during day-night sampling at and below the end of the twilight zone (1,000 m depth) and observed day-night fluctuations in their catches. Midday and midnight trawl catches at different depths during October showed great differences in fish, cephalopod, and crustacean species composition and relative abundance in the deeper areas (see Figure 14a). Waveform analysis of crustacean catches showed behavioral rhythms that affected presence or absence from catches made at different times during a 24-hour cycle ( Figure 14b). Because trawl surveying is one of the commonest methods of sampling in marine waters [429], and is one of the most used in the Mediterranean Sea, future biodiversity studies should correct for the practice of sampling only during daytime. In addition, observations of important diel variation in the fauna associated with seagrasses include a notable increase of species richness and abundance in nighttime samples [430], [431]. This issue brings together the problem of biodiversity and climate change due to expected changes in species migrations and rhythmicity.

While Mediterranean vertebrate species are better known than the invertebrates, our understanding is still incomplete and often outdated. The FNAM atlas [70], which contains data collected and edited during the 1980s and 1990s, is based on regional data and expert knowledge and is the only record of geographic ranges for all Mediterranean fish species. Several areas of the southern Mediterranean have never been surveyed scientifically. Long-term monitoring programs are absent or unavailable for many countries. Since vertebrate species may be useful indicators of changes in ocean food webs [432], a major challenge that remains is to achieve time-series sampling of species diversity, abundance, and habitat data. These time series should have large spatial and temporal scales to develop useful indicators of changes in Mediterranean marine ecosystems and provide measures of ecological connections and ecosystem services.

A clearer identification of hot spot areas will require the inclusion of new data on macroalgae and seagrasses, invertebrates, and seabirds. Most of the Mediterranean seabird species (with the exception of some large gulls) are protected by European laws because of their small or declining populations or the small number of breeding sites. Nine species are included in Annex II of the EU list of endangered or threatened species. The Balearic shearwater is critically endangered [172], and the monitored colonies of Cory's and Mediterranean shearwaters are slowly declining [433]. Although information is incomplete for macroalgae and invertebrates [293], [434], a total of 11 species of macroalgae, 3 of flowering plants, 9 of sponges, 3 of cnidarians, 17 of mollusks, 2 of crustacean decapods, and 3 of echinoderms are now listed as endangered or threatened in the Annex II of the Barcelona Convention for the Protection of the Marine Environment and the Coastal Region of the Mediterranean (1995). A recent proposal (2009) for amendments in the annex II increased to four the number of flowering plants and to 16 plus all the species of the genus Cystoseira (with the exception of C. compressa) the number of endangered species of macroalgae.

Conclusions

The Mediterranean Sea is a region of high biodiversity that ranks among the best known in the world, although much work remains to be done. The description of new species, especially of invertebrates and protists, undergoes upward revision, and new discoveries continually modify previous estimates. Increased efforts are required in taxonomy and sampling of poorly known ecosystems and on long-term monitoring programs of species and habitats. The invasion of alien species will continue to change the biodiversity of the Mediterranean Sea and requires continuous monitoring.

The first attempt to integrate the spatial data and temporal trends presented here enables one to visualize macroecological patterns at the Mediterranean scale. These results depict a region of high diversity and heterogeneity, but they also evidence the need for further study of geographical areas that are largely unexplored, mainly the African coasts and certain zones of the southeastern basin and the deep sea.

Our study illustrates that the Mediterranean is a complex region where ecological and human influences meet and strongly interact, posing a large and growing potential impact to marine biodiversity. Although much is known about individual threats, knowledge is very limited about how multiple impacts will interact. Therefore, there is the need to develop comprehensive analysis of conservation and management initiatives to preserve Mediterranean biodiversity. Owing to the Mediterranean physically, ecologically, and socioeconomically steep gradients, this region may be seen as a model of the world's oceans and a suitable laboratory to study marine ecosystems and decipher future trends.

In addition to further sampling and taxonomic efforts, much of what remains to be done requires free distribution of publicly available data from national and regional research initiatives. This will facilitate database updates and enable scientific discussion. Marine surveys are not always accessible at the regional level and, when available, data coverage is often incomplete. Regional initiatives (such as MedObis) provide promising platforms for the integration of efforts devoted to marine biodiversity within the Mediterranean region, but they must be kept up to date. Individual and collaborative research efforts must continue to advance our knowledge of marine biodiversity in the Mediterranean Sea and narrow down the unknowns.

Acknowledgments

The authors gratefully acknowledge the support given by the European Census of Marine Life, the Census of Marine Life, and the Fisheries Centre (University of British Columbia, Canada). They thank Charles Griffiths, Michele DuRand, Dale Langford, and Iain Taylor for edition and correction of the paper.

References

1. 34. IUCN-MED (2009) Centre for Mediterranean Cooperation: http://www.uicnmed.org/web2007/en/ and http://www.iucn.org/about/union/secretariat/offices/iucnmed/. Accessed December, 2009.

2. 98. NOAA (2007) Hawksbill Sea Turtle (Eretmochelys imbricata). Five year Review: Summary and Evaluation: NOAA and U.S. Fish and Wildlife Service. 90 p.

3. 101. Johnson WM, Karamanlidis AA, Dendrinos P, Fernández de Larrinoa P, Gazo M, et al. (2009) Mediterranean Monk Seal (Monachus monachus). http://www.monachus-guardian.org. Accessed December, 2009.

4. 111. Oro D, Baccetti N, Boukhalfa D, Eken G, El Hili A, et al. (2000) Current breeding distribution and status of Audouin's gulls Larus audouinii in the Mediterranean. In: Sultana JYP, editor. Monitoring and conservation of birds, mammals and sea turtles of the Mediterranean and Black seas: BirdLife Malta, Malta. pp. 69-80.

5. 117. Avella FJ, Gonzalez LM (1984) Monk seal (Monachus monachus) - A survey along the Mediterranean coast of Morocco;. In: Ronald K, Duguy R, editors. pp. 60-78. Second International Conference on the Monk Seals, La Rochelle, France, 5-6 October 1984. Annales de la Societé des Sciences Naturelles de la Charente-Maritime. Supplement, Decembre 1984.

6. 194. Abelló P, Cartes JE (1992) Population characteristics of the deep-sea lobsters Polycheles typhlops and Stereomastis sculpta (Decapoda: Polychelidae) in a bathyal mud community of the Mediterranean Sea. Marine Biology 114: 109-117.

7. 212. Hassan M, Harmelin-Vivien M, Bonhomme F (2003) Lessepsian invasion without bottleneck: Example of two rabbitfish species (Siganus rivulatus and Siganus luridus). Journal of Experimental Marine Biology and Ecology 291: 219-232.

8. 254. Bullock A (2008) Lo Scarus degli antichi: La storia dello Sparisoma cretense nel secolo I;. In: Gertwagen R, Raicevich S, Fortibuoni T, Giovanardi O, editors. pp. 94-105. Chioggia (Italy).

9. 336. Thibaut T, Pinedo S, Torras X, Ballesteros E (2005) Long-term decline of the populations of Fucales (Cystoseira spp. and Sargassum spp.) in the Albères coast (France, North-western Mediterranean). Marine Pollution Bulletin 50: 1472-1489.

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The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats

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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.

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The Karpathos frog (Pelophylax cerigensis) 

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The Karpathos frog (Pelophylax cerigensis) 

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This is a species of frog in the family Ranidae. It is endemic to Greece.

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Mastic (Greek: Μαστίχα) is a resin obtained from the mastic tree (Pistacia lentiscus). In Greece, it is known as the "tears of Chios," being traditionally produced on that Greek island, and, like other natural resins, is produced in "tears" or droplets.

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Προϊόντα Μαστίχας | mastihashop ΚΟΡΥΦΑΙΑ ΕΛΛΗΝΙΚΑ ΠΡΟΪΟΝΤΑ

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Απολαύστε ένα γλυκό ταξίδι μέσα από το mastihashop

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Biodiversity of marine sessile epifauna at an Aegean island subjectto hydrothermal activity: Milos, eastern Mediterranean Sea

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Biodiversity of marine sessile epifauna at an Aegean island subjectto hydrothermal activity: Milos, eastern Mediterranean Sea