Mediterranean demersal resources and ecosystems:
25 years of MEDITS trawl surveys
M.T. Spedicato, G. Tserpes, B. Mérigot and E. Massutí (eds)

INTRODUCTIONTop

The distribution of living species and communities is determined by a combination of large-scale biogeographic history, migration patterns and environmental conditions (Wiens and Donoghue 2004Wiens J.J., Donoghue M.J. 2004. Historical biogeography, ecology and species richness. Trends Ecol. Evol. 19: 639-644.). The biodiversity of the Mediterranean Sea is therefore primarily shaped by its geographical position and the main connections with surrounding oceans, its geological history and the prevailing oceanographic conditions. The Mediterranean is the largest of the seas peripheral to the main oceans, being located between three continents and occupying an elongated basin of 4000 km length (Tyler 2003Tyler P.A. 2003. The peripheral deep seas. In: Tyler P.A. (ed), Ecosystems of the deep oceans. Elsevier Science, Amsterdam, The Netherlands, pp. 261-293.). It is naturally connected to the Atlantic Ocean through the Strait of Gibraltar (320 m depth) and to the Black Sea through the Dardanelles Strait (103 m depth). Since 1869, it has also been artificially connected to the Red Sea by the Suez Canal. Between six and five million years ago, the connection between the Atlantic and the Mediterranean Sea through the Strait of Gibraltar was closed, giving rise to the Messinian Salinity Crisis (Manzi et al. 2013Manzi V., Gennari R., Hilgen F., et al. 2013. Age refinement of the Messinian salinity crisis onset in the Mediterranean. Terra Nova 25: 315-322., Vasiliev et al. 2017Vasiliev I., Mezger E.M., Lugli S., et al. 2017. How dry was the Mediterranean during the Messinian salinity crisis? Palaeogeogr. Palaeoclimatol. Palaeoecol. 471: 120-133.). This salinity crisis involved the complete disappearance of former deep benthic fauna, which means that the present deep Mediterranean organisms have originated from Atlantic migrations since 5.5 million years ago (Lugli et al. 2015Lugli S., Manzi V., Roveri M., et al. 2015. The deep record of the Messinian salinity crisis: Evidence of a non-desiccated Mediterranean Sea. Palaeogeogr. Palaeoclimatol. Palaeoecol., 433: 201-218.).

The Mediterranean Sea is considered a biodiversity hotspot, with an estimate of about 17000 marine species (Coll et al. 2010Coll M., Piroddi C., Steenbeek J., et al. 2010. The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PloS ONE 5: e11842.). Most organisms presently living in the Mediterranean have an Atlantic origin, but tropical species have entered the basin for decades, either actively through the Suez Canal (Lessepsian migration) or the Strait of Gibraltar, or passively mainly through ship transport (Coll et al. 2010Coll M., Piroddi C., Steenbeek J., et al. 2010. The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PloS ONE 5: e11842.). During the last few decades, climate change has also affected the distribution and relative abundances of Mediterranean marine species (Bianchi and Morri 2004Bianchi C.N., Morri C. 2004. Climate change and biological response in Mediterranean Sea ecosystems: a need for broad-scale and long-term research. Ocean Challenge 13: 32-36., Lejeusne et al. 2010Lejeusne C., Chevaldonné P., Pergent-Martini C., et al. 2010. Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends Ecol. Evol. 25: 250-260., Lasram et al. 2010Lasram F.B., Guilhaumon F., Albouy C., et al. 2010. The Mediterranean Sea as a ‘cul-de-sac’ for endemic fishes facing climate change. Global Change Biol. 16: 3233-3245.).

A gradient of species richness from the northwestern to the southeastern Mediterranean is driven by different oceanographic conditions between the two basins (Coll et al. 2010Coll M., Piroddi C., Steenbeek J., et al. 2010. The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PloS ONE 5: e11842.). The main differences are related to a decrease in productivity, as well as an increase in temperature and salinity, from the western to the eastern basin (Danovaro et al. 1999Danovaro R., Dinet A., Duineveld G., et al. 1999. Benthic response to particulate fluxes in different trophic environments: a comparison between the Gulf of Lions-Catalan Sea (western-Mediterranean) and the Cretan Sea (eastern-Mediterranean). Prog. Oceanogr. 44: 287-312., Turley et al. 2000Turley C.M., Bianchi M., Christaki U., et al. 2000. Relationship between primary producers and bacteria in an oligotrophic sea - the Mediterranean and biogeochemical implications. Mar. Ecol. Progr. Ser. 193: 11-18.). As a result of such contrasting conditions, the western and eastern basins display biological similarities to the Atlantic ecosystem (higher number of cold-temperate species) and the Indo-Pacific ecosystem (higher number of subtropical species), respectively (Coll et al. 2010Coll M., Piroddi C., Steenbeek J., et al. 2010. The Biodiversity of the Mediterranean Sea: Estimates, Patterns, and Threats. PloS ONE 5: e11842.).

In this paper we investigate whether the different environmental conditions between the western and eastern basins are reflected in the cephalopod assemblages found throughout the Mediterranean. Cephalopods represent excellent case studies for analysing species-environment interactions owing to their high sensitivity to environmental conditions (Pierce et al. 2008Pierce G.J., Valavanis V.D., Guerra A., et al. 2008. A review of cephalopod-environment interactions in European Seas. Hydrobiologia 612: 49-70., Rodhouse et al. 2014Rodhouse P.G.K., Pierce G.J., Nichols O.C., et al. 2014. Environmental effects on cephalopod population dynamics: implications for management of fisheries. Adv. Mar. Biol. 67: 99-233.). They have short life spans (1.5–2 years at most) and a high population turn-over, so they show rapid responses to changes in external conditions. Although there are several studies on cephalopod assemblages relative to Mediterranean areas in both the western (e.g. Quetglas et al. 2000Quetglas A., Carbonell A., Sanchez P. 2000. Demersal continental shelf and upper slope cephalopod assemblages from the Balearic Sea (north-western Mediterranean). Biological aspects of some deep-sea species. Est. Coast. Shelf Sci. 50: 739-749., González and Sánchez 2002González M., Sánchez P. 2002. Cephalopod assemblages caught by trawling along the Iberian Peninsula Mediterranean coast. Sci. Mar. 66: 199-208., Fanelli et al. 2012Fanelli E., Cartes J.E., Papiol V. 2012. Assemblage structure and trophic ecology of deep-sea demersal cephalopods in the Balearic basin (NW Mediterranean). Mar. Freshwater. Res. 63: 264-274.) and eastern (e.g. Lefkaditou et al. 2003Lefkaditou E., Mytilineou Ch., Maiorano P., et al. 2003. Cephalopod species captured by deep-water exploratory trawling in the Eastern Ionian Sea. J. Northw. Atl. Fish. Sci. 31: 431-440., Krstulović Šifner et al. 2005Krstulović Šifner S., Lefkaditou E., Ungro N., et al. 2005. Composition and distribution of the cephalopod fauna in the eastern Adriatic and eastern Ionian Sea. Israel J. Zool. 51: 315-330., 2011Krstulović Šifner S., Peharda M., Vrgoc N., et al. 2011. Biodiversity and distribution of cephalopods caught by trawling along the Northern and Central Adriatic Sea. Cah. Biol. Mar. 52: 291-302.) basins, all of them are restricted to local scales and differences in sampling and data analysis prevent the comparison of results in most cases (Gaertner et al. 2013Gaertner J.C., Maiorano P., Merigot B., et al. 2013. Large-scale diversity of slope fishes: pattern inconsistency between multiple diversity indices. PloS ONE 8: e66753.).

Like all other faunal components, the bulk of the current Mediterranean teuthofauna comes from the Atlantic Ocean (Bello 2003Bello G. 2003. The biogeography of Mediterranean cephalopods. Biogeographia 33: 209-226.). Up to now, a total of 70 cephalopod species have been reported in the Mediterranean (Bello 2008Bello G. 2008. Cephalopoda. Biol. Mar. Medit. 15: 318-322., 2016Bello G. 2016. Cephalopoda (update December 2016). Biol. Mar. Medit. 15: 318-322.) but only 53 of them are represented by well-established populations (Bello 2003Bello G. 2003. The biogeography of Mediterranean cephalopods. Biogeographia 33: 209-226.). Ten cephalopods are endemic or quasi-endemic in the Mediterranean (Bello 2003Bello G. 2003. The biogeography of Mediterranean cephalopods. Biogeographia 33: 209-226., and pers. comm.), accounting for 14.3% of its teuthofauna.

In this work, data from standardized bottom trawl surveys carried out during the last 22 years by EU Mediterranean countries were used. The wide spatiotemporal scale of these scientific surveys and the data standardization used during the sampling and data processing allow a reliable comparative analysis of the cephalopod assemblages inhabiting the whole Mediterranean basin. In addition to investigating spatial differences in cephalopod assemblages, the available database will also be used to analyse temporal changes in species composition during the last two decades.

MATERIALS AND METHODSTop

Main oceanographic conditions of the Mediterranean

The Mediterranean is a semi-enclosed sea characterized by high salinities, temperatures and densities. The net evaporation exceeds the precipitation, driving an anti-estuarine circulation through the Strait of Gibraltar and contributing to very low nutrient concentrations (Tanhua et al. 2013Tanhua T., Hainbucher D., Schroeder K., et al. 2013. The Mediterranean Sea system: a review and an introduction to the special issue. Ocean Sci. 9: 789-803.). The Mediterranean has a basin-scale east-west gradient in the chlorophyll (Chl a) distribution, with an extremely oligotrophic eastern basin and a more productive western basin (D’Ortenzio and D’Alcala 2009D’Ortenzio F., D’Alcala M.R. 2009. On the trophic regimes of the Mediterranean Sea: a satellite analysis. Biogeosciences 6: 139-148.). Two main types of dynamics coexist (Lavigne et al. 2015Lavigne H., D’Ortenzio F., D’Alcala M.R., et al. 2015. On the vertical distribution of the chlorophyll a concentration in the Mediterranean Sea: a basin-scale and seasonal approach. Biogeosciences 12: 5021-5039.): i) a mid-latitude dynamics associated with bloom conditions in the northwestern basin, showing high occurrence of high surface Chl a profiles in March-April; and ii) a subtropical dynamics encompassing most of the remaining basin, characterized by an omnipresent deep Chl a maximum from spring to autumn and a large variety of Chl a vertical shapes during winter.

The mid-latitude behaviour is also observed for sea surface temperature (SST), with the lowest values found in February and the highest ones in summer, between July and August (Pastor et al. 2017Pastor F., Valiente J.A., Palau J.L. 2017. Sea surface temperature in the Mediterranean: trends and spatial patterns (1982-2016). Pure Appl. Geophys. 175: 4017-4029. ). Although SST shows great spatial variability, and hence clustered areas do not always have the same size or shape or are centred on the same SST values, a set of common shapes are found for every season/month. The winter regime is characterized by a north-to-south increasing temperature gradient organized in latitudinal bands, while summer shows a highly complex structure with a set of distinct well-defined areas not following any simple gradient structure, although in general SST is higher in the southeastern Mediterranean basin. Both spring and autumn show transitional regimes between the two main modes.

A consistent warming trend has been found for Mediterranean SST in the 1982–2016 period (Pastor et al. 2017Pastor F., Valiente J.A., Palau J.L. 2017. Sea surface temperature in the Mediterranean: trends and spatial patterns (1982-2016). Pure Appl. Geophys. 175: 4017-4029. ). This warming rate is not constant throughout the whole time series but shows differences, with a much steeper trend for the last two decades. Analysis of decadal trends has shown a clear increase of the warming trend from 1993 to the present. Three “almost decadal” periods were identified for the last 35 years, with the following mean values (expressed as ×10^–4 °C day^–1): i) 1982-1992 (1.67±0.53); ii) 1993-2004 (2.82±0.47); and iii) 2005-2016 (3.08±0.47).

The salinity of the Mediterranean has also increased during the last 40 years (Borghini et al. 2014Borghini M., Bryden H., Schroeder K., et al. 2014. The Mediterranean is becoming saltier. Ocean Sci. 10: 693-700.). Apart from the SST and salinity increases, other available information indicates that the Mediterranean is clearly not in a steady state. River run-off has been reduced as rivers are dammed and used for irrigation, and models suggest that evaporation is increasing due to the warming climate (Borghini et al. 2014Borghini M., Bryden H., Schroeder K., et al. 2014. The Mediterranean is becoming saltier. Ocean Sci. 10: 693-700.).

Data sampling and analysis

Data were obtained from the international Mediterranean bottom trawl surveys (MEDITS), which have been conducted annually between May and August since 1994, covering depths from 10 down to 866 m. The surveys are performed annually by all riparian EU countries plus Montenegro and Albania. The sampling methodology is standardized among all the countries (for details see Bertrand et al. 2002Bertrand J.A., de Sola L.G., Papaconstantinou C., et al. 2002. The general specifications of the MEDITS surveys. Sci. Mar. 66: 9-17.). A stratified random sampling design is used in the surveys, with the following bathymetric strata: 10-50, 51-100, 101-200, 201-500 and 501-800 m. The standardized gear used is a GOC 73 trawl with a cod-end mesh size of 20 mm and a vertical and horizontal opening of the net of about 2 and 18 m, respectively. The net opening is measured by an attached underwater Scanmar system to calculate the swept area. Trawling is conducted in daylight, with a towing speed of 2-3 knots and haul duration of 30 and 60 minutes over shelf and slope grounds, respectively.

To analyse spatiotemporal differences in cephalopod assemblages over the whole Mediterranean, the basin was divided into six biogeographical zones or bioregions (Fig. 1) in accordance with previous studies (Gaertner et al. 2007Gaertner J.C., Bertrand J.A., Relini G., et al. 2007. Spatial pattern in species richness of demersal fish assemblages on the continental shelf of the northern Mediterranean Sea: a multiscale analysis. Mar. Ecol. Progr. Ser. 341: 191-203., 2013Gaertner J.C., Maiorano P., Merigot B., et al. 2013. Large-scale diversity of slope fishes: pattern inconsistency between multiple diversity indices. PloS ONE 8: e66753., Keller et al. 2016Keller S., Bartolino V., Hidalgo M., et al. 2016. Large-Scale Spatio-Temporal Patterns of Mediterranean Cephalopod Diversity. PloS ONE 11: e0146469.): Iberian-Lions (B1); Tyrrhenian (B2); Ionian (B3); Adriatic (B4); Aegean (B5); and Strait of Sicily (B6). A total of 23749 stations sampled during the last 22 years (1994-2015) were analysed (Table S1 in Supplementary material). Data used in the analyses included the standardized density of cephalopod species in number of individuals (N km^–2) taken at all individual sampling stations.

To identify the main cephalopod assemblages of each bioregion, cluster analyses were applied to the mean cephalopod abundances obtained from the whole time series (1994-2015). Owing to the low frequency of occurrence of most species, samples were pooled within 25-m depth intervals. The resemblance matrix was calculated on the basis of Bray-Curtis similarities between hauls, with a fourth-root transformation of the densities in order to down-weight the effect of the most abundant species (Clarke and Warwick 2001Clarke K.R., Warwick R.M. 2001. Change in marine communities: An approach to statistical analysis and interpretation. PRIMER-E: Plymouth, 176 pp.). The cluster analysis was carried out with the similarity profile (SIMPROF) routine, which defines statistically significant groups among samples (Clarke and Gorley 2006Clarke K.R., Gorley R.N. 2006. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, 190 pp.). Subsequently, the similarity percentage analysis (SIMPER) was used to determine the species characterizing the bathymetric assemblages obtained.

To analyse temporal differences in assemblages, the available dataset was split into two time series of 11 years each (1994-2004 and 2005-2015), corresponding to the last two periods of the aforementioned three warming decadal trends identified in the Mediterranean (Pastor et al. 2017Pastor F., Valiente J.A., Palau J.L. 2017. Sea surface temperature in the Mediterranean: trends and spatial patterns (1982-2016). Pure Appl. Geophys. 175: 4017-4029.). These two time periods are hereafter referred to as the old and the recent time series. Spatial (6 bioregions) and temporal (old vs. recent time series) differences in cephalopod assemblages were tested using the permutational multivariate analysis of variance (PERMANOVA), based on Bray-Curtis similarity matrices after square root transformation (Anderson et al. 2008Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, 214 pp.). Spatial and temporal comparisons were exclusively done for equivalent bathymetric assemblages coming from the cluster analysis. The analyses were obtained after 9999 permutations of raw data. When the number of unique permutations was lower than 100, the Monte Carlo p-value was used instead of the permutation p-value (Anderson et al. 2008Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, 214 pp.). Prior to the PERMANOVA, the homogeneity of multivariate dispersions was tested for all factors using the permutational analysis of multivariate dispersions (PERMDISP). When the PERMANOVA revealed spatial differences in assemblages, pairwise comparisons were carried out to determine which pairs of bioregions differed. The species composition of these differing pairs of assemblages was then used to explain the spatial differences found. Finally, when temporal differences in assemblages were detected, SIMPER analyses comparing the dissimilarity between the old and the recent time series were used to determine the species contributing to those differences.

RESULTSTop

Cephalopod assemblages

Altogether, 47 cephalopod species were taken during the sampling (although shells of Argonauta argo females were noticed in most bioregions, the species was not considered because no live individuals were captured). The highest species richness (S) was found in bioregions B1 (S=42) and B2 and B3 (both with S=41), whereas bioregions B4, B5 and B6 had 35, 36 and 34 species, respectively (Table S2 in Supplementary material). Considering the three main Mediterranean biogeographical provinces that have traditionally been used (Lejeusne et al. 2010Lejeusne C., Chevaldonné P., Pergent-Martini C., et al. 2010. Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends Ecol. Evol. 25: 250-260.), the western (including B1 and B2) and eastern (including B3, B5 and B6) basins had the same number of species (S=43) and the Adriatic (B4) had 35 species.

Cluster analysis revealed four different bathymetric assemblages in all bioregions (Fig. 2). Although the depth ranges of these assemblages varied with the bioregions, they are hereafter referred to as: i) continental shelf (<200 m); ii) upper slope (200-400 m); iii) middle slope (400-650 m); and iv) lower slope (>650 m). In all cases (except between groups A and B from B6), the average similarity between assemblages obtained with the SIMPER analysis decreased with increasing depth (Table S3 in Supplementary material). In most bioregions (B1-B4) the species richness decreased slightly with depth from the shelf to the middle slope and then dropped to the lowest values on the lower slope (Fig. 3). This was not the case, however, for bioregions B5 and B6, which did not show such a decreasing trend and had richness values much higher than the other bioregions in the deepest stratum.

Except on the lower slope of B2 and B4, there were no clear dominant species in any stratum, but a rather homogeneous blend of different species. The lower slopes of B2 and B4, by contrast, were characterized by two dominant species contributing 66% (Histioteuthis reversa and Todarodes sagittatus) and 75% (Todaropsis eblanae and H. reversa), respectively, to the cephalopod assemblage. In all bioregions, a number of generalist species appear in most strata (e.g. Abralia veranyi, Sepietta oweniana, Illex coindetii) and some specialized species characterizing specific strata appear in shallow (e.g. Eledone moschata, Sepia officinalis) and deep (e.g. Bathypolypus sponsalis, Histioteuthis spp.) waters.

Spatial differences

The PERMDISP test revealed homogeneous within-group multivariate dispersions for all four bathymetric assemblages (shelf, p=0.318; upper slope, p=0.287; middle slope, p=0.582; lower slope, p=0.046). The PERMANOVA showed significant spatial differences on the continental shelf (pseudo-F=33.19; p<0.0001), upper slope (pseudo-F=79.86; p<0.0001), middle slope (pseudo-F=54.39; p<0.0001) and lower slope (pseudo-F=3.83; p<0.0001). Pairwise comparisons between bioregions showed significant differences in all cases for the upper slope and middle slope (Table 1). Regarding the continental shelf, significant differences were found for all pairs except for B1-B2 and B3-B6. The lower slope was the most homogeneous stratum since it had the highest number of non-significant pairwise comparisons: B1-B2, B1-B3, B1-B4, B2-B3, B2-B4 and B2-B6.

The SIMPER (Table S3 in Supplementary material) showed that there are no significant changes in the species composition when the same bathymetric stratum is compared among bioregions, but only a change in the contribution of the relative abundance of the different species to the cephalopod assemblages.

The species reported in the following paragraphs refer to those included in the SIMPER results when considering the 80% cut-off value, not the whole list of species found in each bioregion. A number of species appearing in all bioregions characterize the continental shelf, such as Alloteuthis spp., Illex coindetii, Loligo vulgaris and Sepia elegans. Some species were absent in various bioregions (e.g. Loligo forbesii in B3, B4, B6; Octopus vulgaris in B2, B3, B6; Eledone moschata in B2, B3), whereas some species only appeared in a single bioregion (e.g. Octopus salutii in B4; Sepia officinalis in B2).

Similarly, the upper slope was characterized by sepiolids (Sepietta oweniana, Sepiolidae, Rondeletiola minor), Alloteuthis spp., Illex coindetii and Sepia orbignyana. Some species were also absent in various bioregions (e.g. Octopus salutii in B2, B5, B6; Loligo vulgaris in B1, B3, B5, B6; Neorosia caroli in B1, B3, B4, B6) and some species were only present in one bioregion (e.g. Bathypolypus sponsalis and Pteroctopus tetracirrhus in B1).

On the middle slope, the list of cephalopods appearing in all bioregions included species such as Abralia veranyi, Illex coindetii, Rossia macrosoma and Todaropsis eblanae. A single taxon appeared in only one bioregion (Alloteuthis spp. in B5), whereas the number of species absent in different bioregions was larger than that in the rest of the assemblages (a total of 12 cephalopods, including Todarodes sagittatus, Sepietta oweniana and Eledone cirrhosa).

Finally, the SIMPER results from the lower slope differed from the results obtained in the remaining assemblages because there was no common list of species characterizing this assemblage; in fact, only a single species was present in all bioregions (Histioteuthis reversa). Two cephalopods were found only in one bioregion (B. sponsalis and R. minor), whereas the rest of species appeared in various bioregions (e.g. A. veranyi, T. sagittatus, A. lichtensteinii, T. eblanae).

Temporal differences

The PERMDISP test showed homogeneous within-group multivariate dispersions in all cases (Table 2). The PERMANOVA only revealed temporal differences between the old (1994-2004) and the recent (2005-2015) time series for three bioregions (B1, B3 and B6). The Strait of Sicily (B6) was the only bioregion showing significant differences in all four bathymetric assemblages. The Iberian-Lions bioregion (B1) showed differences in all assemblages except on the lower slope, whereas the Ionian bioregion (B3) only displayed differences in two assemblages (upper and lower slope).

As in the case of the spatial analysis, the SIMPER (Table S4 in Supplementary material) showed that there were no significant changes in the species composition within equivalent bathymetric strata when the two time periods are compared, but only changes in the relative species abundances.

DISCUSSIONTop

A total of 47 different cephalopod species have been taken from the Mediterranean Sea during the last 22 years, accounting for 67.1% of the cephalopods recorded in the basin up to now. This percentage highlights the high number of cephalopods that have not been captured by bottom trawl gears during the study period—one third of recorded species—despite the large spatiotemporal sampling (23749 sampling stations). Although the westernmost bioregion (Iberian-Lions; B1) held a higher number of cephalopod species (S=42 vs 36) than the easternmost bioregion (Aegean Sea; B5), there was no clear trend in species richness throughout the Mediterranean, as has already been reported in a recent study (Keller et al. 2016Keller S., Bartolino V., Hidalgo M., et al. 2016. Large-Scale Spatio-Temporal Patterns of Mediterranean Cephalopod Diversity. PloS ONE 11: e0146469.). Whereas Mangold and Boletzky (1988)Mangold K., Boletzky S.v. 1988. Mediterranean cephalopod fauna. In: Clarke M.R., Trueman E.R. (eds), The Mollusca, vol.12, Paleontology and Neontology of Cephalopods. Academic Press, London, pp. 315-330. suggested a general decrease in the species richness from west to east, Bello (2003)Bello G. 2003. The biogeography of Mediterranean cephalopods. Biogeographia 33: 209-226. noted that this theory should be revised according to available updated information. Even for the three main biogeographical provinces traditionally used to divide the Mediterranean (the western and eastern basins and the Adriatic Sea; Mangold and Boletzky 1988Mangold K., Boletzky S.v. 1988. Mediterranean cephalopod fauna. In: Clarke M.R., Trueman E.R. (eds), The Mollusca, vol.12, Paleontology and Neontology of Cephalopods. Academic Press, London, pp. 315-330., Lejeusne et al. 2010Lejeusne C., Chevaldonné P., Pergent-Martini C., et al. 2010. Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends Ecol. Evol. 25: 250-260.), the species richness obtained with our data was the same in both the western and eastern basins (S=43), but was lower in the Adriatic (S=35). As already reported for fish (Gaertner et al. 2007Gaertner J.C., Bertrand J.A., Relini G., et al. 2007. Spatial pattern in species richness of demersal fish assemblages on the continental shelf of the northern Mediterranean Sea: a multiscale analysis. Mar. Ecol. Progr. Ser. 341: 191-203., Granger et al. 2015Granger V., Fromentin J.M., Bez N., et al. 2015. Large-scale spatio-temporal monitoring highlights hotspots of demersal fish diversity in the Mediterranean Sea. Prog. Oceanogr. 130: 65-74.), the absence of a west-east decreasing trend suggests that primary production (i.e. food availability) is possibly not the major factor explaining large-scale patterns of species richness of demersal cephalopods. At a global scale it was found that although net primary productivity at the ocean surface seems to drive diversity patterns of pelagic cephalopods, coastal species diversity can be predicted by climate (SST) and non-climate (spatial area) variables (Rosa et al. 2008Rosa R., Dierssen H.M., Gonzalez L., et al. 2008. Large-scale diversity patterns of cephalopods in the Atlantic open ocean and deep sea. Ecology 89: 3449-3461.).

Given that cephalopods are highly sensitive to changing environmental conditions (Pierce et al. 2008Pierce G.J., Valavanis V.D., Guerra A., et al. 2008. A review of cephalopod-environment interactions in European Seas. Hydrobiologia 612: 49-70., Rodhouse et al. 2014Rodhouse P.G.K., Pierce G.J., Nichols O.C., et al. 2014. Environmental effects on cephalopod population dynamics: implications for management of fisheries. Adv. Mar. Biol. 67: 99-233.), it was expected to find spatial differences in the species composition over the Mediterranean. However, our results revealed no differences in species composition among bioregions, but only changes in the species’ relative abundances, which led to significant differences between all pairs of bioregions in intermediate waters (upper and middle slope assemblages). Assemblages from the upper and middle slope, for instance, are dominated by the squid lllex coindetii in the easternmost bioregions (B3, B4, B5), whereas sepiolids predominate in the remaining bioregions. Assemblages from the shelf were also significantly different between all pairs of bioregions except in two cases, the Iberian-Lions (B1) vs Tyrrhenian Sea (B2) and the Ionian Sea (B3) vs Strait of Sicily (B6). The homogeneity of shelf assemblages in the B1-B2 bioregions might be related to the counter-clockwise circulation of Atlantic waters in the western basin, which produces a basin-wide cyclonic gyre through the Tyrrhenian vein (Millot and Taupier-Letage 2005Millot C., Taupier-Letage T. 2005. Circulation in the Mediterranean Sea. In: Saliot A. (ed.), The Mediterranean Sea. The Handbook of Environmental Chemistry, Vol. 5, Part K. Springer-Verlag, Berlin Heidelberg, pp. 29-66.) that might hinder exchanges of low-moving life stages such as cephalopod paralarvae. The strategic situation of the Strait of Sicily might explain the differences found between the B1-B2 and the B3-B6 assemblages: the surface isotherm of 15°C for February (the coldest month in the year) follows quite closely the biogeographic boundaries of the Strait of Sicily, and biotic differences between the two basins are probably due to differences in temperature regime, i.e. a physiological barrier separating the western and eastern Mediterranean (Bianchi 2007Bianchi C. 2007. Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia 580: 7-21.). In addition, the Strait of Sicily is also characterized by high mesoscale activity (Nieblas et al. 2014Nieblas A.E., Drushka K., Reygondeau G., et al. 2014. Defining Mediterranean and Black Sea Biogeochemical Subprovinces and Synthetic Ocean Indicators Using Mesoscale Oceanographic Features. PloS ONE 9: e111251.) and high fishing rates (Colloca et al. 2017Colloca F., Scarcella G., Libralato S. 2017. Recent trends and impacts of fisheries exploitation on Mediterranean stocks and ecosystems. Front. Mar. Sci. 4: 244.). The lower slope was the most homogeneous stratum since it had the highest number of non-significant pairwise comparisons. This faunal homogeneity is a general feature of deep-sea waters (McClain and Hardy 2010McClain C.R., Hardy S.M. 2010. The dynamics of biogeographic ranges in the deep sea. Proc. Biol. Sci. 277: 3533-3546., Rex and Etter 2010Rex M.A., Etter R.J. 2010. Deep-sea biodiversity. Pattern and Scale. Harvard University Press, London, 356 pp.) and is proably related to the homogeneous conditions and the circulation pattern at such great depths (Millot and Taupier-Letage 2005Millot C., Taupier-Letage T. 2005. Circulation in the Mediterranean Sea. In: Saliot A. (ed.), The Mediterranean Sea. The Handbook of Environmental Chemistry, Vol. 5, Part K. Springer-Verlag, Berlin Heidelberg, pp. 29-66.). Results also revealed that the Aegean bioregion (B5) was significantly different from all other bioregions, a finding which might be related to its high spatial bathymetric variability (Millot and Taupier-Letage 2005Millot C., Taupier-Letage T. 2005. Circulation in the Mediterranean Sea. In: Saliot A. (ed.), The Mediterranean Sea. The Handbook of Environmental Chemistry, Vol. 5, Part K. Springer-Verlag, Berlin Heidelberg, pp. 29-66., Nieblas et al. 2014Nieblas A.E., Drushka K., Reygondeau G., et al. 2014. Defining Mediterranean and Black Sea Biogeochemical Subprovinces and Synthetic Ocean Indicators Using Mesoscale Oceanographic Features. PloS ONE 9: e111251.) and low fishing exploitation rate (Colloca et al. 2017Colloca F., Scarcella G., Libralato S. 2017. Recent trends and impacts of fisheries exploitation on Mediterranean stocks and ecosystems. Front. Mar. Sci. 4: 244.). Compared with the rest of bioregions, for instance, the broader upper slope of the Aegean Sea was characterized by higher abundances of the cuttlefishes Sepia elegans and S. orbignyana, which is in accordance with the sustainable exploitation exerted in the area with a high prevalence of small-scale fisheries (Colloca et al. 2017Colloca F., Scarcella G., Libralato S. 2017. Recent trends and impacts of fisheries exploitation on Mediterranean stocks and ecosystems. Front. Mar. Sci. 4: 244.).

In most bioregions (Iberian-Lions, Tyrrhenian, Ionian and Adriatic) the species richness showed a slight decrease with depth from the shelf to the middle slope before plummeting to the lowest values on the lower slope. The Aegean Sea and the Strait of Sicily, however, did not show that decreasing trend and their richness values at the deepest stratum were much higher than those of the remaining bioregions. Such high values might be due to the fact that the lower slope stratum obtained from our cluster analysis for these two bioregions encompassed a much wider depth range than the rest of the bioregions. Our results did not show the hump-shaped trend of species richness with depth reported in previous cephalopod studies carried out in the Mediterranean (González and Sánchez 2002González M., Sánchez P. 2002. Cephalopod assemblages caught by trawling along the Iberian Peninsula Mediterranean coast. Sci. Mar. 66: 199-208., Krstulović Šifner et al. 2011Krstulović Šifner S., Peharda M., Vrgoc N., et al. 2011. Biodiversity and distribution of cephalopods caught by trawling along the Northern and Central Adriatic Sea. Cah. Biol. Mar. 52: 291-302., Keller et al. 2016Keller S., Bartolino V., Hidalgo M., et al. 2016. Large-Scale Spatio-Temporal Patterns of Mediterranean Cephalopod Diversity. PloS ONE 11: e0146469.).

Except in the deepest stratum of the Adriatic Sea (B4), there were no clear dominant species in any cephalopod assemblage, but a rather homogeneous mix of different species. This indicates a continuous substitution of species with depth rather than discrete assemblages separated by distinct boundaries. In all bioregions, a number of eurytopic (generalist) species appeared in most strata (e.g. A. veranyi, S. oweniana, I. coindetii) and some specialized species characterizing specific strata appeared in shallow (e.g. E. moschata, S. officinalis) and deep (e.g. B. sponsalis, Histioteuthis spp.) waters. On the lower slope of the Adriatic Sea, two deep-sea squid species (T. eblanae and H. reversa) accounted for up to 75% of the cephalopod assemblage. This finding agrees with the well-known comparatively poor deep-sea teuthofauna of the Adriatic, despite the fact that it reaches 1200 m depth in the southern basin and has a relatively wide connection with the Ionian Sea (Mangold and Boletzky 1988Mangold K., Boletzky S.v. 1988. Mediterranean cephalopod fauna. In: Clarke M.R., Trueman E.R. (eds), The Mollusca, vol.12, Paleontology and Neontology of Cephalopods. Academic Press, London, pp. 315-330., Bello 2003Bello G. 2003. The biogeography of Mediterranean cephalopods. Biogeographia 33: 209-226., Keller et al. 2016Keller S., Bartolino V., Hidalgo M., et al. 2016. Large-Scale Spatio-Temporal Patterns of Mediterranean Cephalopod Diversity. PloS ONE 11: e0146469.).

As stated above, the bulk of the current Mediterranean teuthofauna comes from the Atlantic Ocean (Bello 2003Bello G. 2003. The biogeography of Mediterranean cephalopods. Biogeographia 33: 209-226.). However, a comparison of the cephalopod assemblages from the westernmost bioregion (Iberian-Lions; B1) with those from the Gulf of Cadiz (Silva et al. 2011Silva L., Vila Y., Torres M.A., et al. 2011. Cephalopod assemblages, abundance and species distribution in the Gulf of Cadiz (SW Spain). Aquat. Living Resour. 24: 13-26.), an Atlantic area adjacent to the Strait of Gibraltar, revealed great differences in species contribution. Such differences in species relative abundance might be related to the contrasting oceanographic conditions in these two areas (Millot and Taupier-Letage 2005Millot C., Taupier-Letage T. 2005. Circulation in the Mediterranean Sea. In: Saliot A. (ed.), The Mediterranean Sea. The Handbook of Environmental Chemistry, Vol. 5, Part K. Springer-Verlag, Berlin Heidelberg, pp. 29-66., Tanhua et al. 2013Tanhua T., Hainbucher D., Schroeder K., et al. 2013. The Mediterranean Sea system: a review and an introduction to the special issue. Ocean Sci. 9: 789-803.).

Despite claims of biodiversity loss as a result of high anthropogenic impacts in the Mediterranean (Danovaro 2003Danovaro R. 2003. Pollution threats in the Mediterranean Sea: An overview. Chem. Ecol. 19: 15-32., Calvo et al. 2011Calvo E., Simó R., Coma R., et al. 2011. Effects of climate change on Mediterranean marine ecosystems: the case of the Catalan Sea. Climate Res. 50: 1-29., Vasilakopoulos et al. 2014Vasilakopoulos P., Maravelias C.D., Tserpes G. 2014. The Alarming Decline of Mediterranean Fish Stocks. Curr. Biol. 24: 1643-1648.), the species composition of the cephalopod assemblages has not changed during the last 22 years. As in the case of the spatial analysis, temporal differences were only found in the species’ relative abundance of three bioregions: Iberian-Lions, Ionian and Strait of Sicily. The Strait of Sicily was the only bioregion showing significant differences in all four bathymetric assemblages, whereas the Iberian-Lions and the Ionian bioregions displayed differences in three and two assemblages, respectively. As stated above, both natural factors (15°C isotherm boundary, complex topography, high mesoscale variability) and anthropogenic factors (high exploitation rates) might explain the existence of differences at all depths in the Strait of Sicily. The remaining bioregions (Tyrrhenian, Adriatic and Aegean Seas) showed no long-term temporal differences in species’ relative abundance, a finding which might be related, at least in the Tyrrhenian and Aegean Seas, to reduced interchanges of water masses owing to the main topographic characteristics (Millot and Taupier-Letage 2005Millot C., Taupier-Letage T. 2005. Circulation in the Mediterranean Sea. In: Saliot A. (ed.), The Mediterranean Sea. The Handbook of Environmental Chemistry, Vol. 5, Part K. Springer-Verlag, Berlin Heidelberg, pp. 29-66.).

Previous studies of cephalopod assemblages in the Mediterranean confirm our results. A long-term study carried out in the western basin (Fanelli et al. 2012Fanelli E., Cartes J.E., Papiol V. 2012. Assemblage structure and trophic ecology of deep-sea demersal cephalopods in the Balearic basin (NW Mediterranean). Mar. Freshwater. Res. 63: 264-274.) found no significant differences in the bathyal cephalopod assemblages or in the species abundances between the two time periods analysed (1985-92 vs. 2007-10). In a shorter-term study (2000-2007) from the Gulf of Cadiz, the species composition also remained unchanged and only the relative abundance of different groups varied (Silva et al. 2011Silva L., Vila Y., Torres M.A., et al. 2011. Cephalopod assemblages, abundance and species distribution in the Gulf of Cadiz (SW Spain). Aquat. Living Resour. 24: 13-26.). The lack of changes in species composition during the last two decades also applies to fish (Granger et al. 2015Granger V., Fromentin J.M., Bez N., et al. 2015. Large-scale spatio-temporal monitoring highlights hotspots of demersal fish diversity in the Mediterranean Sea. Prog. Oceanogr. 130: 65-74.), which might indicate that the demersal ecosystem was already altered before the beginning of our time series or that noticeable changes will only be revealed at longer temporal scales (Granger et al. 2015Granger V., Fromentin J.M., Bez N., et al. 2015. Large-scale spatio-temporal monitoring highlights hotspots of demersal fish diversity in the Mediterranean Sea. Prog. Oceanogr. 130: 65-74., Keller et al. 2016Keller S., Bartolino V., Hidalgo M., et al. 2016. Large-Scale Spatio-Temporal Patterns of Mediterranean Cephalopod Diversity. PloS ONE 11: e0146469.).

Given that temperature is a key driver of the biogeographic distribution (Puerta et al. 2014Puerta P., Hidalgo M., Gonzalez M., et al. 2014. Role of hydro-climatic and demographic processes on the spatio-temporal distribution of cephalopods in the western Mediterranean. Mar. Ecol. Progr. Ser. 514: 105-118.) and habitat selection (Lauria et al. 2016Lauria V., Garofalo G., Gristina M., et al. 2016. Contrasting habitat selection amongst cephalopods in the Mediterranean Sea: When the environment makes the difference. Mar. Environ. Res. 119: 252-266.) of cephalopods, it is expected that climate change will have significant effects on many temperate species (Hastie et al. 2009Hastie L.C., Pierce G.J., Wang J., et al. 2009. Cephalopods in the North-Eastern Atlantic: Species, biogeography, ecology, exploitation and conservation. Oceanogr. Mar. Biol. 47: 111-190.). Climate change projections for the Mediterranean indicate that it might be an especially vulnerable region (Giorgi and Lionello 2008Giorgi F., Lionello P. 2008. Climate change projections for the Mediterranean region. Global Planet. Change 63: 90-104., Albouy et al. 2013Albouy C., Guilhaumon F., Leprieur F., et al. 2013. Projected climate change and the changing biogeography of coastal Mediterranean fishes. J. Biogeogr. 40: 534-547.). In fact, a consistent warming trend has already been reported in the 1982-2016 period (Pastor et al. 2017Pastor F., Valiente J.A., Palau J.L. 2017. Sea surface temperature in the Mediterranean: trends and spatial patterns (1982-2016). Pure Appl. Geophys. 175: 4017-4029.). As a whole, 25% of the Mediterranean Sea continental shelf was predicted to experience a total modification of endemic species assemblages by the end of the 21st century (Lasram et al. 2010Lasram F.B., Guilhaumon F., Albouy C., et al. 2010. The Mediterranean Sea as a ‘cul-de-sac’ for endemic fishes facing climate change. Global Change Biol. 16: 3233-3245.). Some cephalopod populations from the Mediterranean show an increasing trend in abundance that might be related to the global change (Doubleday et al. 2016Doubleday Z., Prowse T.A.A., Arkhipkin A., et al. 2016. Global proliferation of cephalopods. Curr. Biol. 26: R406-R407., Keller et al. 2017Keller S., Keller A., Puerta P., et al. 2017. Environmentally driven synchronies of Mediterranean cephalopod populations. Prog. Oceanogr. 152: 1-14.). Currently, however, none of the Lessepsian species (Octopus aegina, O. cyanea, Sepioteuthis lessoniana and Tremoctopus gracilis) reported in the Mediterranean up to now (Bello 2016Bello G. 2016. Cephalopoda (update December 2016). Biol. Mar. Medit. 15: 318-322.) were found in our samples. As most Lessepsian species inhabit depths shallower than those prospected during the MEDITS and/or non-trawlable grounds, they in principle are not prone to being captured by trawling gears. A few Lessepsian fish species have been recorded in the MEDITS surveys in the south Aegean and Cretan Seas (Peristeraki et al. 2017Peristeraki P., Tserpes G., Lampadariou N., et al. 2017. Comparing demersal megafaunal species diversity along the depth gradient within the South Aegean and Cretan Seas (Eastern Mediterranean). PloS ONE 12: e0184241.), but no Lessepsian cephalopod species have been recorded so far, although some of them have well-established populations in the eastern Mediterranean (Zenetos et al. 2011Zenetos A., Katsanevakis S., Poursanidis D., et al. 2011. Marine alien species in Greek Seas: Additions and amendments by 2010. Medit. Mar. Sci. 12: 95-120.; Lefkaditou, unpublished data). It is therefore expected that these Lessepsian migrants will spread westwards, as some fish species have already done (Bianchi 2007Bianchi C. 2007. Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia 580: 7-21., Calvo et al. 2011Calvo E., Simó R., Coma R., et al. 2011. Effects of climate change on Mediterranean marine ecosystems: the case of the Catalan Sea. Climate Res. 50: 1-29.), probably leading to spatiotemporal differences in cephalopod assemblages through the Mediterranean, at least during the westward spreading phase. Our study has shown, however, that spatiotemporal differences during the last two decades only affected some specific bioregions and were restricted to variations in the relative species abundance from a common pool of species inhabiting the whole Mediterranean.

ACKNOWLEDGEMENTSTop

This study was performed under the Data Collection Framework (EU Reg. 199/2008) of the European Union (http://datacollection.jrc.ec.europa.eu/), cofunded by the EU and the national governments involved in the study. We would like to thank all the colleagues who participated in the MEDITS surveys during the spatiotemporal window encompassed in this work.

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SUPPLEMENTARY MATERIAL

The following supplementary material is available through the online version of this article and at the following link:
http://scimar.icm.csic.es/scimar/supplm/sm04841esm.pdf

Table S1. – Number of sampling stations by bioregion (Bioreg) sampled during the Mediterranean trawl surveys (MEDITS) carried out in the region between 1994 and 2015. B1, Iberian-Lions; B2, Tyrrhenian; B3, Ionian; B4, Adriatic; B5, Aegean; B6, Strait of Sicily.

Table S2. – Total number of taxa caught in the different bioregions and for the whole Mediterranean (all bioregions combined). Taxa are ordered according to their decreasing values of mean abundance (N km^–2). Tick marks show the taxa not taken into account when calculating the species richness. B1, Iberian-Lions; B2, Tyrrhenian; B3, Ionian; B4, Adriatic; B5, Aegean; B6, Strait of Sicily. (Next pages).

Table S3. – Results of similarity percentage analysis (SIMPER) for the bathymetric cephalopod assemblages obtained by the cluster analysis shown in Figure 2 for the six Mediterranean bioregions analysed (B1-B6). Abu (average abundance); AvSim (average similarity); Con (percentage contribution); Cum (cumulative percentages).

Table S4. – SIMPER analyses of the dissimilarity between the old (1994-2004) and recent (2005-2015) time series by bathymetric strata and bio-region for those stratum-bioregion settings showing significant differences from a previous PERMANOVA (see Table 2). Av.Abu (average abundance); Contrib% (percentage contribution); Cum% (cumulative percentages).