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



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Text S1. Taxonomic revision and methodological specifications


Here we provide the detailed information for the taxonomic revision of macrophytes (seaweeds and seagrasses), invertebrates and Ascidiacea (subphylum Tunicata, phylum Chordata) in the Mediterranean Sea. This information is summarized in Table 1 in the main body of the study and Table S1, while checklists and specific figures are included in Tables S7-S29 and Figures S1-S6.

Seaweeds and seagrasses

Here we include a wide array of organisms usually known as seaweeds, and a reduced group of aquatic flowering plants known as seagrasses. They are a phylogenetic heterogeneous group of eukaryotic photosynthetic organisms. The application of molecular tools to the classification of living organisms has led to a better understanding of the phylogenetic relationships between them and has been demonstrated that brown seaweeds are included in the group Chromista while red seaweeds, green seaweeds, and flowering plants belong to Plantae. Here we do not include blue green algae (phylum Cyanobacteria), which, although classically considered in the textbooks of botany, they are prokaryotic. Most of the brown, red and green algae grow usually attached in the sea bottom or the intertidal zone, while blue greens both thrive as a component of the benthos and the plankton. Their taxonomy is being reshaped continuously, and it is hard to know the real diversity of this group at the "species" level.

The Mediterranean Sea was probably the first area in the world where SCUBA diving techniques were used in the study and collection of macroalgae [1], which is the main and best methodology currently in use. However, deep waters below 50 meters depth are still usually sampled by indirect methods such as dredging or bottom trawling. Plants thriving in the mediolittoral and upper infralittoral zone can be easily collected by hand with no special equipment or simply with the provision of a face mask and a snorkel. See Tsuda and Abbott [2] for a more detailed description of collection, handling, preservation and identification of macroalgae.

Athanasiadis [3] provides a thorough revision of the history of Mediterranean phycology (or algae studies), which began long time ago with the descriptions of several algal species by Theophrastus three centuries B.C., increased during the early Linnean period (Gmelin, Lamarck, Lamouroux, Roth, Bory de Saint Vincent and others), was maintained in the 19th century (C. Agardh, J. Agardh, Kützing, Meneghini, Ardissone, Montagne, Schmitz, Berthold, Foslie and others) and continued until the end of the 19th century, when Zanardini published the first Mediterranean illustrated flora, and the start of the 20th century when Preda published a red algal flora of Italy, Sauvageau his monograph on Cystoseira, and De Toni his monumental "Sylloge Algarum". Afterwards, Hamel, Funk, J. Feldmann, Feldmann-Mazoyer, Dangeard, and Ercegovic made important contributions to the phycology in the mid of the 20th century. At present, there are several teams working in the taxonomy of Mediterranean seaweeds, mainly in Italy, France and Spain. Several countries or regions have checklists of marine macroalgae: Morocco, Algeria, Tunis, Libya, Malta, Alexandria (Egypt), Turkey, Aegean Sea, Adriatic Sea, Italy, Sicily, Corsica, eastern Pyrenees (France), and Catalonia and Andalusia (Spain). Moreover, partial checklists of Mediterranean seaweeds have been published since 1992 [4,5,6]. There are also studies focused in introduced species [e.g. 7,8,9,10], a subject that is in constant revision [11].



The total number of taxa currently present in the Mediterranean basin is 1131 (see the annotated checklist of every phyla and for the criteria used in making the lists, Table S7). Phaeophyceae (268 taxa), Pelagophyceae (two species), and Xanthophyceae (seven species) are the three classes within the phylum Heterokontophyta with benthic representatives (this class also hosts the Chrysophyceae, Raphidophyceae, Dictyochophyceae, and others with planktonic representatives). The Mediterranean representatives of the phylum Rhodophyta belong to five classes: Bangiophyceae (eight species), Compsopogonophyceae (17 species), Porphyridiophyceae (1 species), Stylonematophyceae (five species), and Florideophyceae (626 taxa). The highly diverse phylum Chlorophyta hosts five classes with Mediterranean benthic representatives: Chlorophyceae (12 species), Prasinophyceae (six species), Trebouxiophyceae (three species), Ulvophyceae (73 taxa) and Bryopsidophyceae (52 taxa). Some (ten) of the species reported within the Chlorophyceae (Volvocales) and Prasinophyceae (Chlorodendrales, Pyramimonadales) are unicellular and can be considered to be phytoplanktonic, although they thrive in mediolittoral and supralittoral pools and have been classically included in the checklists of marine macroalgae. Thus, strictly benthic chlorophytes number 180 instead of the 190 reported in Table 1. We also include in the list of the flowering plants (phylum Magnoliophyta) those that are usually considered as seagrasses (four autochthonous species and one introduced) as well as two other species typical from brackish waters that they can also be collected in extremely shallow lagoons and sheltered bays (Ruppia spp.).

The percentage of endemic species at a basin level ranges from approximately 10% in the phylum Chlorophyta to 30% in the phylum Heterokontophyta, with an average of 22.3% for all the macrophytobenthos (see Table S8). The higher number of endemics is found within the Rhodophyceae, which hosts a large number of deep water red algae considered to be endemic. However, this number is decreasing as increasing studies of macroalgae are made in Macaronesian islands and warm-temperate eastern Atlantic Ocean (coasts of Portugal and Spain) using SCUBA. They are reporting a high number of Mediterranean supposed endemics [e.g. 12,13,14,15]. Within the red algae the highest numbers of endemics are found in Polysiphonia (12) and Acrochaetium (nine), but both genus need nomenclatural and taxonomical reinvestigations, and these numbers could decrease significantly. Other genera with a high number of endemics include Peyssonnelia (six), Rodriguezella (four), Osmundea (four), and Kallymenia (three). Ptilophora mediterranea is an interesting endemic of the eastern Mediterranean basin with its closest relatives being found in the Indian Ocean, suggesting that it is a paleoendemic that overcame the Messinian salinity crisis. Within the brown algae, the genus Cystoseira alone accounts for 37 endemic taxa (23 species, and 14 infraspecific entities), which makes this genus a landmark in the marine Mediterranean flora. Most Cystoseira endemic species are considered neoendemic as they have probably evolved from Atlantic taxa entering the Mediterranean Sea from the Atlantic Ocean starting after the Messinian salinity crisis [16]. Moreover species of the genus Cystoseira act as ecosystem engineers in sublitoral Mediterranean communities and are of paramount ecological importance, similar to that played by species of the order Laminariales in other temperate seas and oceans. Also a member of the order Fucales, Fucus virsoides, is a neoendemic restricted to the northern Adriatic and the only true Mediterranean representative of this genus. Another important endemic brown alga is Laminaria rodriguezii, known from the Adriatic and the western basin, with apparently no relationships with other European species of this genus, and considered to be a Tethys relic [17]. Stands of Laminaria rodriguezii are restricted to deep waters, usually below 70 meters depth. Other canopy-forming Laminariales and Tilopteridales (e.g. Laminaria ochroleuca, Saccorhiza polyschides) are very uncommon in the Mediterranean and they are only found in the Messinian strait, between Italy and Sicily, and in places subjected to surface water inflow from the Atlantic ocean (southern Spain and Moroccan and Algerian coasts). Amongst the green algae, the highest number of endemics is found in Ulva but, again, this is a genus where nomenclatural and taxonomical reinvestigations are required. Within the flowering plants, Posidonia oceanica is the only endemic, with its closest relatives found again in the Indian Ocean (coasts of southern Australia), suggesting that P. oceanica is a Tethys relic [17]. Moreover, P. oceanica forms extensive meadows in the infralittoral zone, from the surface in sheltered areas to more than 40 m depth in the crystal-clear waters of the eastern Mediterranean, which makes it the most important Mediterranean shallow-water ecosystem. It is only absent in the easternmost area of the Mediterranean, the Moroccan coast and areas of southern Spain situated close to the Strait of Gibraltar.

The Mediterranean Sea is a hot spot for marine introduced species and up to 114 introduced macrophytes have been reported, representing the 10% of the known marine flora. At present, the main vector of introduction of marine macrophytes is aquaculture which surpasses the Suez Canal [7]. The highest number of exotic algae is currently found in coastal lagoons from the Gulf of Lions and northern Adriatic and not in the eastern basin, unlike other groups [18]. According to Boudouresque and Verlaque [8], at least eight introduced species merit the category of invasive as they play a conspicuous role in the recipient ecosystems: Sargassum muticum, Stypopodium schimperi, Acrothamnion preissii, Asparagopsis armata, Lophocladia lallemandii, Womersleyella setacea, Caulerpa racemosa var. cylindracea, Caulerpa taxifolia and Halophila stipulacea. However, sometimes the invasive capacity of these species is not the same in the different sub-basins, geographical areas or environments and we still do not know which are the features of the species and the environment that allow a species to become invasive.

There is a gradient of species richness between the western to the eastern basin as it has been observed in most groups of organisms (Table 2). For example of the total number of 263 species of the order Ceramiales (Rhodophyta) reported in the checklist, 94% appear in the western basin, 80% in the border between eastern and western basins (Sicily, Tunisia, Ionian Sea), 75% in the Adriatic, and 73% in the eastern basin.

Some seagrass meadows, algal stands, and algal-dominated communities and landscapes are known to be threatened in the Mediterranean [19]. Airoldi and Beck [20] reported coastal development and water quality, followed by destructive fishing, and diseases, pests and predators as the main drivers of the loss of seagrass meadows and macroalgal stands along European coasts, including the Mediterranean. Coastal management, and chemical pollution, as well as trawling, invasive species, increased epiphytism and increased herbivory by sea-urchins are amongst the main causes of the decline of Posidonia oceanica meadows [21]. Overgrazing by sea urchins, out-competition by mussels, habitat destruction related to coastal management, chemical pollution, increased water turbidity, human trampling and direct plant destruction attributed to net fishing and even scientific sampling have been blamed for the local extinction of up to 11 taxa belonging to the genera Cystoseira and Sargassum in the eastern Pyrenees (France) [22]. Colonization by turf algae [23] and global change [24] have also been considered as factors explaining the decrease in Fucales (i.e. brown algae). Increasing abundance of turf-forming, filamentous, or ephemeral algae are also reported as the main cause for the decline of macroalgal stands [25,26]. Trawling, alien invasions, waste waters, diving activities and large scale events involving mass-mortalities are reported as the main causes of disturbance affecting deep-water coralline algae-dominated environments (coralligenous and maërl beds) [27]. At present there is no species of macroalgae or seagrass that has became extinct at the basin scale, but there are some reports of extinctions at local scales [e.g. 22], which can result in a total extinction for some endemics with reduced geographical distribution (e.g. some Cystoseira spp.).

The only text regarding habitat and species protection at a regional scale that has been signed by all the Mediterranean countries is the Barcelona Convention. Two Action Plans ("Marine Vegetation" and "Coralligenous and other calcareous bioconcretions") specifically deal with the protection of macrophytobenthos and the habitats they constitute. Another Action Plan ("Introduced and Invasive Species") and the Protocol concerning Specially Protected Areas and Biological Diversity ("SPA Protocol") deal also in part with marine macroalgae and seagrasses. At present, there are 14 species of macrophytes that are listed in the Annex II of the SPA Protocol but in 2009 a list with 44 species was proposed to the National Focal Points for approval. Engineering species, both fleshy (most Cystoseira spp., Sargassum spp., Laminaria spp., Posidonia oceanica, Zostera spp.) and calcareous (Titanoderma ramosissimum, T. trochanter, Tenarea tortuosa, Lithophyllum byssoides) will all be hopefully included in the Annex II in the near future, as well as some rare and highly threatened deep-water endemics.

At a European level there are several EEC Directives that protect marine vegetation: Habitats Directive (92/43/EEC), Water Framework Directive (2000/60/EC) and Marine Strategy Directive (2008/56/EC). Within the Habitats Directive, although no marine macrophytes are listed in the Annex II - species whose conservation requires the designation of special areas of conservation -, Posidonia oceanica meadows are a priority natural habitat type and Member States have designated special areas of conservation to ensure its protection. The Water Framework Directive indirectly protects macroalgae and seagrasses as its purpose is to prevent further deterioration and to protect/enhance the ecological status of aquatic coastal (and freshwater) ecosystems, in a similar way that it is stated in the Marine Strategy Directive for all marine ecosystems. Moreover, a Council Regulation (EC 1967/2006, 21 December 2006) concerning management measures for the sustainable exploitation of fishery resources in the Mediterranean Sea, prohibits fishing with trawl nets, dredges, seines or similar nets above seagrass meadows, coralligenous concretions and maërl beds, which, if correctly implemented in all Member States, should be an important measure for protection of these habitats.

However, even with all these regulations, and as far as the protection of marine macrophytobenthic diversity is concerned, habitat destruction and degradation, changes in water quality and turbidity associated to pollution, habitat modification due to changes in the food web of anthropogenic origin, and invasive species will continue to be the major threats in the short and mid-term. We already know that the impact of increasing temperatures and decreasing pH associated to climate change will enhance the development of warm water species (and doing so the expansion of Lessepsian migrants), will cause the rarefaction or even extinction of some species of cold water affinities, will enhance the production of fleshy algae, and will inhibit the growth of calcareous algae [e.g. 28,29].

Animalia

All animal phyla with marine representatives are present in the Mediterranean Sea, including the puzzling phyla discovered in recent times, Loricifera and Cycliphora, by Reinhardt Kristensen in 1983, and R. Kristensen and Peter Funch in 1995, respectively. Loricifera was first recorded in the Mediterranean Sea by Todaro and Kristensen [30] with the description of the new species Nanoloricus khaitatus. Larvae of two additional undescribed species of this phylum have been mentioned by Hofrichter [31]. On the other hand, Baker et al. [32] and Baker and Giribet [33] pointed out the presence of at least two species of Cycliphora in the Mediterraean, Symbium pandora and a undescribed species found in Croatia.

In this synthesis, we especially focused our efforts on diversity of the phyla a) Porifera, b) Cnidaria, with emphasis on Anthozoa, c) Mollusca, d) Annelida, with emphasis on Polychaeta, e) Arthropoda, with emphasis on Decapoda, Cumacea and Mysidacea, f) Bryozoa, g) Echinodermata, h) Sipuncula, i) other invertebrates such as nematodes, and less conspicuous species of the meiobenthos, j) Tunicata with emphasis on Ascidiacea, and k) the subphylum Vertebrata (including fish, marine mammals, sea turtles and seabirds).

- Porifera

Mediterranean sponges are an important component of the sublittoral and circalittoral hard substrata communities. They thrive in sciaphilic habitats such as the coralligenous environment [34], submerged or semi-submerged caves [35,36], living also in the proximity of hydrothermal vents [37]. This phylum has been a subject of interest for humans in the littoral of the Mediterranean Sea since the time of Aristotle (4th century BC), who reported five different sponge species in his zoological writings [38]. However, systematic investigation of sponge species occurred after the 17th century. Mediterranean sponge faunal list (at least demosponges which contain 85% of all living sponges) has been recently reviewed and updated by Pansini and Longo [39] and Voultsiadou [40]. Here we updated previous efforts using literature references.

The total number of species from the Mediterranean Sea is to date 681, including 629 Demospongiae, 44 Calcarea, and 8 Hexactinellida. Lists of the Porifera species recorded from the Mediterranean are available in the World Porifera Database [41] and the World Register of Marine species [42], and corresponding percentages (calculated according to the Systema Porifera, [43] for each demosponge order separately are illustrated in Figure S1. Due to their sessile habit and their short-lived, current dependant larvae [44], a large number of the Mediterranean demosponges (~48%) are endemic and only 11.5% are cosmopolitan or circumtropical [39]. The strong zoogeographical affinity of the Mediterranean sponge fauna with that of the Atlantic [45] is reflected in species composition, with 37.5% of the Mediterranean sponges being of Atlantic origin, while only few (~3%) are Indo-Pacific [39]. Although several species had been assumed to be Lessepsian migrants [46], recent studies [47] support that their identity with known Red Sea or Indo-Pacific species can be either rejected or remains highly doubtful, and that they are rather thermophilous remnants from an ancient warm period of the Mediterranean. Deep-sea sponges have been studied mostly in the western Mediterranean [48,49]; although bathyal species have been considered as widely distributed [50] and eurybathic [51] recent research revealed several species endemic in the bathyal zone of the eastern Basin [52].

The distribution of demosponge species and genera richness in the different regions of the Mediterranean is also uneven (Figure S2). Four major zoogeographic sub-areas have been identified in the Mediterranean according to the affinities of their sponge fauna: the north-western, north-eastern, the central zone, and the south-eastern areas [40]. A clear prevalence of the north-western basin, which hosts 78% of the total Mediterranean demosponge species and a decline pattern in sponge diversity from the north-western to the south-eastern is observed. The 14 demosponge orders are represented all over the Mediterranean; nevertheless, a gradual decrease in species numbers of Poecillosclerida and an increase of Dictyoceratida, Halichondrida, and Homosclerophorida is observed from the northwest to the southeast Mediterranean [53].

The Mediterranean sponge fauna can be characterized as well studied. However, the knowledge of the distribution of the sponge fauna is far from uniform. While substantial effort has been invested in the study of the northern coastline, investigation in the southern areas and the Levantine has been arguably sporadic and limited [39]. This is especially crucial for environments where sponge diversity is acknowledged to be high, such as sciaphilic habitats, or those which constitute a promising field for discovering new biodiversity, such as deep-sea and extreme environments [37,52,54]. Lately there has been an additional source of new sponge diversity in the form of cryptic species. The difficulties that sponges manifest to the taxonomist are notorious, mostly due to the lack or plasticity of distinguishing morphologic characters that is inherent in several taxa or groups [55]. Molecular data from recent studies have highlighted this concealed biodiversity [56,57,58,59,60].

Sponges demonstrate a wide variety of roles related to the functioning of marine ecosystems, including creation and modification of substrate, benthic-pelagic coupling, as well as a spectrum of interactions and associations with marine organisms [61,62,63]. Although sponges are present in most aquatic environments, the preponderance of their biodiversity occurs in specific habitats, such as coastal hard substrate formations, caves and overhangs, reefs and seamounts, as well as detritic and coralligenous seabeds. These ecosystems are highly vulnerable to degradation both by localized factors such as coastal pollution or industrial fishing [64,65] and global climate change phenomena [66]. The latter can also have a direct effect on sponge diversity, promoting mortality events on several species of the littoral community [67,68]. Thus, the protection of Mediterranean sponge biodiversity is utterly dependant on the protection of those sensitive aquatic environments. Initiations on protection and management plans both in local and global scale will thus have critical effect on the preservation of evidenced or yet unspecified sponge diversity. Sponges also frequently act as ecosystem engineers offering a living substratum to numerous other organisms [69]. Thus, they constitute important biodiversity hotspots in the Mediterranean environment deserving special attention and protection.

Sponges can be commercial products, with a commercial interest that has been traditionally restricted to the common high quality ‘bath sponges’ of the Mediterranean. Five species, Spongia officinalis, S. mollisima, S. zimocca, S. lamella, and Hippospongia communis have been harvested since early historical times and intensively throughout the 20th century, especially at the eastern and southern part of the basin [70]. The economic and social importance of bath sponges has been significant, as they were, and still are, exported and utilized worldwide [71]. Moreover, the Mediterranean is rich in sponge species with potential bioactive components [72] producing secondary metabolites with anticancer, antibiotic, anti-inflammatory, or antifouling activity [73]. Since production requirements can not be sustainably met by harvesting wild populations, in situ sponge culture is being investigated [74]. Mariculture has been investigated for the production of Mediterranean bath sponges [75], especially after the natural populations faced a dramatic decline due to the combined effect of uncontrolled harvesting and several mass mortality events [76], as well as climate warming [68,77].

Progress towards management and protection measures aiming at species is critical, regarding sponges utilized as biological resources. Those include the Mediterranean bath sponges, as well as species with proved or potential value for the pharmaceutical industry. The lack of control characterizing intensive bath sponge harvesting throughout the 20th century in the Mediterranean is acknowledged as an apparent cause for the recent decline of natural populations. Sixteen Mediterranean sponge species have been included in the Barcelona (Annex II and III) the Bern Convention (Appendices II and III) as worthy of protection or exploitation regulation.


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