Here, we utilize information on alien species distribution from EASIN to investigate the distribution patterns of marine alien species in the Mediterranean Sea, in relation to the main pathways of introduction. We investigate how specific human activities opening of the Suez Canal, shipping, aquaculture may shape the patterns of alien species distribution and consequently the overall biodiversity patterns in the Mediterranean Sea. We also compare the distributions of alien species with those of native ones to investigate differences in their patterns, and thus induced changes in pre-existing distribution patterns of native biodiversity.
The link between alien species and pathways was based on Zenetos et al. For each species one of the following uncertainty categories on the pathway s of introduction was adopted:. This is the case e. This applies e. In many cases inference is based on known examples of introductions elsewhere for the same or similar species, the biology and ecology of the species, the habitats it occupies in both the native and introduced range, and its pattern of dispersal if known , e.
Inference is based on the activities in the locality where the species was found and may include evidence on similarly behaving species reported elsewhere. In the present analysis of spatial distribution by pathway only species linked to a single pathway were included i. Species of uncertainty category 3 were excluded from any pathway-specific analysis to avoid the distortion of pathway-related spatial patterns by erroneously including species that might actually have been introduced through another pathway.
In the absence of a permanent monitoring network and of a biased effort favoring specific locations e. All alien species were included in all other analyses non-pathway-specific. Figure 1. In derogation of the random sampling approach, we included the Venice and the Thau lagoons, as these sites have been well-studied and highlighted in the literature as hotspots of alien species Occhipinti Ambrogi, ; Boudouresque et al. Similarity patterns were explored through non-metric multidimensional scaling nMDS; Kruskal, , based on a similarity matrix constructed using the Jaccard coefficient Jaccard, Permutational multivariate analysis of variance Permanova; Anderson, was used to test for differences among ecoregions, using type III sum of squares and random permutations of the appropriate units.
We also included available data regarding the spatial distribution of native fish and invertebrate species described in the Mediterranean Sea Coll et al. We assessed the spatial congruence of native and alien species by calculating the correlation coefficient between the native and alien raster layers, i. Only the cells adjacent to the coastline were included in this analysis, as alien species are generally concentrated in coastal and shelf waters otherwise the overabundance of zero values in the offshore cells would mask any significant correlation.
A total of species of uncertainty levels 1 and 2 have been introduced in the Mediterranean Sea through the Suez Canal. An aggregated map of these Lessepsian species Figure 2 shows a characteristic pattern of high species richness in the south-eastern Levantine Sea, which declines anticlockwise along the coastline of the Levantine Sea and further westwards and northwards along the northern Mediterranean coast, and also westwards along the north-African coastline.
Figure 2. Shipping, through ballast waters and hull-fouling, was the most probable pathway for the introduction of species uncertainty levels 1 and 2. The distribution of these species Figure 3 is strikingly different to the one of Lessepsian species. Figure 3.
Through aquaculture, either as commodities or as contaminants, 64 species have been introduced in the Mediterranean Sea uncertainty levels 1 and 2. Most of species introduced through aquaculture are macrophytes 41 species and invertebrates 14 species that arrived as contaminants of shellfish.
Richness of species introduced by aquaculture is quite low in the Near East and northern African coastlines, with the exception of northern Tunisia Figure 4. Figure 4. There is a difference in the magnitude of species richness among the species introduced through the Suez Canal, shipping, and aquaculture Figures 2 — 4. This indicates the higher contribution of Lessepsian species in the overall spatial pattern of species richness of all alien species.
Besides differences in the spatial patterns of species richness by pathway, varying patterns among the main taxonomic groups are also observed Figure 5. Alien fish richness is the highest in the Levantine and the southeastern part of the Aegean Sea and the lowest in the western and northern regions of the Mediterranean.
For alien invertebrates, the spatial pattern of species richness is similar but there are some additional areas of increased richness such as the French coastline around the Thau lagoon, northern Adriatic, and eastern Sicily. Richness of alien macrophytes has a quite different spatial pattern, with increased richness in the western Mediterranean.
These patterns are linked to the dominant pathways of introduction for each group, i. Figure 5. The pie charts depict the relative importance of the three main pathways for each taxonomic group only uncertainty levels 1 and 2 were included.
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Alien species composition differs among ecoregions Figure 6. With the exception of the Venice lagoon site 18 and the Thau lagoon site 24 that appear more similar to each other than to other sites of the same ecoregions western Mediterranean and Adriatic, respectively , sites from the same ecoregion appear close together in the nMDS plot. Similarity appears well-correlated to geographical distance, with sites of the Levantine being more similar to sites of the Tunisian plateau and Gulf of Sidra and the Aegean Sea than to sites of the Adriatic, western Mediterranean, and Alboran Sea.
Sites of the latter ecoregions are grouped closely in the nMDS plot, while the Ionian Sea is in the middle of all other ecoregions, in conformity to its geographical location. Figure 6. Site Venice lagoon; site Thau lagoon. Bottom panel : nMDS graph of the 37 sites, based on Jaccard similarity. The underlying dataset is available as a Supplementary File. The biodiversity spatial pattern of native species fish and invertebrates differs to that of alien species Figure 7. Native species richness decreases from the north-western to the south-eastern regions of the basin, where a minimum value of 84 species is mapped.
Native species richness is also higher in coastal and shelf areas, and decreases with depth. Figure 7. The data are plotted using a linear scale from minimum to maximum values. The highest estimated values of the ratio of alien to native species richness are observed in the eastern Mediterranean especially in the Levantine and the south-eastern Aegean Sea , with a maximum value of 0. In the central and eastern Mediterranean, the alien to native species ratio is much lower. Figure 8. Alien-to-native ratio of fish and invertebrates richness in the coastal areas of the Mediterranean Sea.
Note: Distributional data were available for a limited number of native invertebrates and thus the absolute values of this indicator appear elevated. However, this is not expected to affect the spatial patterns depicted in this figure. The evidence herein provided demonstrates how human activities and interventions shipping, aquaculture, opening of the Suez Canal modify large-scale biodiversity patterns in the Mediterranean Sea by assisting biological invasions.
In the Mediterranean Sea, a northwestern-to-southeastern gradient of native species richness is observed, although this could be, at least partly, due to gaps in our knowledge of the biota along the southern and eastern rims Figure 7 ; Coll et al. Native biodiversity is generally higher in coastal and shelf waters in most groups of both vertebrates and invertebrates, with some local exceptions.
Similarly, alien species are concentrated in coastal and shelf waters. Very few alien species have been reported in offshore areas, which may be explained by the thriving of shallow-water thermophilic demersal aliens, or because important vectors of alien species ships and aquaculture operate in shallow waters, but also due to the reduced sampling effort off-shore Danovaro et al.
However, the opposite in relation to native biodiversity basin-wide trend of alien species richness is observed, decreasing from southeast to northwest. Biodiversity patterns are substantially modified, and locally the induced change in species composition, abundance and richness can be even more marked. In several hotspot areas, alien species now constitute a substantial part of the communities and have in many cases caused a shift to novel habitats, with an entirely modified ecosystem functioning Katsanevakis et al.
In the eastern Mediterranean Levantine Sea , this high richness of alien species is highly reflected also in terms of total biomass and community structure. Most of the alien species that are established in the Mediterranean Sea were introduced in the last decades. Hence, the observed large-scale change of biodiversity patterns in the Mediterranean is a phenomenon that has been evolving mainly during the last century. This unprecedented change has been greatly driven by the opening of the Suez Canal in and its continuous enlargement, but also by the increasing seaborne trade, responsible for many shipping-mediated introductions, and the intentional introduction of alien commodity species and, unintentionally, of contaminant species for aquaculture Katsanevakis et al.
Herein, we focused on species richness as an indicator of biodiversity, as is common in the ecological literature May, ; Bianchi and Morri, Alien species richness and the ratio between alien and native species Figure 8 were used as indicators of biodiversity change and impact. Another indicator that has been previously used is the change in the intensity of spatial congruence between alien and endemic fauna Ben Rais Lasram and Mouillot, However, in many cases these indicators are not the best to indicate biodiversity change or impact.
Some individual keystone and high-impact alien species can have a much more severe impact than dozens of other non-invasive aliens. For example, the two herbivore rabbitfish Siganus luridus and S. They are able to create and maintain barrens rocky areas almost devoid of erect algae and contribute to the transformation of the ecosystem from one dominated by lush and diverse brown algal forests to a degraded one dominated by bare rock and patches of crustose coralline algae Sala et al. The large-scale and severe impact of these two species in the shallow rocky shores of the eastern Mediterranean is probably greater than that of the other alien fish in the Mediterranean altogether, which is not depicted by a species richness indicator.
Similarly, a few very invasive macroalgae can dominate algal assemblages creating homogenized microhabitats, greatly impacting native communities. This is the case of the invasive green alga Caulerpa cylindracea , which can easily overgrow and eliminate other macroalgal or invertebrate species and may form compact multilayered mats up to 15 cm thick that trap sediment and may create an anoxic layer underneath Klein and Verlaque, ; Katsanevakis et al. Several biotopes, such as Mediterranean communities of sublittoral algae and coralligenous communities, are affected by C.
This species alone can have much greater impact than dozens of other non-invasive alien macrophytes, which again is not evident in an alien species richness indicator. The ecosystems of many regions of the Mediterranean Sea have been substantially modified Boudouresque et al. Especially Lessepsian migration is considered as the most significant biogeographic change currently underway worldwide Bianchi et al. Although so far there are no recorded basin-wide extinctions of native marine species in the Mediterranean, there are many examples of local extirpations and range shifts concurrent with alien invasions Galil, However, there is no evidence so far of extensive basin-wide taxonomic homogenization of the Mediterranean biota due to biological invasions.
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There are marked differences in the introduced biota among ecoregions Figure 6 , which is more intense for Lessepsian and aquaculture-introduced species. Hence, at a Mediterranean scale, communities are continuously changing but there is no sign of a reduced degree of heterogeneity across ecoregions. This may not be the case at smaller scales e. The future of the Mediterranean Sea biota is difficult to predict. During the past two decades, Mediterranean waters have been warming at a rather high rate, especially in the eastern region, and this trend is predicted to continue in the long-term influencing biogeochemical cycles and ecosystem functioning Durrieu de Madron et al.
The sea surface temperature contours are shifted northwards Coll et al. Warming of the Mediterranean Sea favors the establishment and spread of thermophilic species, such as most of the Lessepsian migrants Bianchi, ; Bianchi et al. At least in the Levant Basin, environmental conditions are favorable for communities of Indo-Pacific hermatypic corals, and the arrival and establishment of the first reef builders and a great diversity of associated fish and invertebrates is probably only a matter of time Por, A better understanding of how the human-shaped new biodiversity patterns will affect the Mediterranean food webs, ecosystem functioning, and the provision of ecosystem services for the benefit of humans is challenging Borja, but urgently needed.
A possible way to assess this is through the employment of ecosystem models, which in the last decades have been increasingly used worldwide to evaluate ecosystem structure and functions and the impacts of human activities on marine systems e. Thus, future studies should be set up and carried out to assess and better understand alien species in an ecosystem context. Alien species often benefit some components of native biodiversity and can enhance or provide new ecosystem services Katsanevakis et al.
In marine regions subject to rapid change, such as the Mediterranean Sea, introduced species may even secure ecosystem processes and functioning Walther et al. It is unknown if the future Mediterranean ecosystems will be more resilient, and may continue to provide the same ecosystem services, but it is likely they will be very different than the past ecosystems before the major wave of biological invasions of the last century. Stelios Katsanevakis and Ana Cristina Cardoso conceived the study. Analysis of pathways of introduction was conducted by Argyro Zenetos and Stelios Katsanevakis. The mapping of human activities was provided by Chiara Piroddi.
Mapping of native species distribution, estimation and mapping of alien-to-native ratios, and related spatial analyses were conducted by Marta Coll, Jeroen Steenbeek, and Frida Ben Rais Lasram. Stelios Katsanevakis prepared a first draft of the manuscript and all coauthors contributed to the final version. The Associate Editor Christos Dimitrios Arvanitidis declares that, despite being affiliated to the same institution as author Argyro Zenetos, the review process was handled objectively and no conflict of interest exists.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Anderson, M. A new method for non-parametric multivariate analysis of variance. CrossRef Full Text. Ben Rais Lasram, F. Increasing southern invasion enhances congruence between endemic and exotic Mediterranean fish fauna.
Invasions 11, — Bianchi, C. Biodiversity issues for the forthcoming tropical Mediterranean Sea. Hydrobiologia , 7— The changing biogeography of the Mediterranean Sea: from the old frontiers to the new gradients. Genova 75, 81— Marine biodiversity of the Mediterranean Sea: situation, problems and prospects for future research. Biogeographia 24, — Borja, A. Grand challenges in marine ecosystems ecology. Boudouresque, C. Ceccaldi, I. Dekeyser, M. DAISIE aims to integrate information on current invasions across Europe through the development of an online, peer-reviewed database of alien species.
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Linking information on the species' status at both country- and Europe-wide levels should improve understanding and prediction of invasion dynamics [ 8 ] and help prevent their spread into new areas. We included all papers that dealt with aliens in any European country. While other journals include papers on alien species especially aquatic species , this figure shows an increase in interest in the area based on the ecological and conservation journals examined. Representing many of the leading scientists in the field of biological invasions, the group brings together a variety of expertise from academia, government, non-governmental organizations, and private enterprises.
In bi-annual workshops, participants address a range of challenging issues. An efficient policy dealing with invasive species should raise awareness of the range of impacts caused by different aliens across ecosystems. For this purpose, DAISIE is developing a European invasive alien species information system to provide information on species traits, distribution, and management.
These lists have been successful at focusing attention on the problem of invasive species, and are widely cited. Following the most recent workshop after much discussion , DAISIE members drew up a list of species encompassing the breadth of alien taxa, European ecosystems, impacts on biodiversity, ecosystems, human health, and economy. There was limited correspondence with the global IUCN list, highlighting the importance of regional initiatives. The process raised several key questions: Can we directly compare impacts on biodiversity with those on human health?
Does the greater visibility of a few vertebrate impacts outweigh less well-understood effects of numerous alien invertebrates? Should we prioritise species that are already a problem or those with large potential to become problematic? Even within taxonomic groups, issues arise around criteria for selecting the worst aliens. For some species, a consensus among experts is easily reached; however, in other cases the criteria for selection may yield different lists. For example, the alien Canada goose Branta canadensis is widely distributed across Europe with documented negative effects on agriculture [ 10 ], and is often considered one of the worst avian invaders.
Di Castri, Francesco
In contrast, there is less agreement on the impacts of the common myna Acridotheres tristis in Europe Figure 2. Although currently present in only a few countries in Europe, it is on the IUCN worst-invaders list, being known to rapidly spread in newly invaded areas [ 11 ], and to seriously affect breeding success of native birds [ 12 ].
The lively discussion generated by these issues highlights a need for robust, clear, and replicable criteria for scientific or policy-making purposes, especially for lists covering wide geographic areas. As DAISIE finishes its first year, the alien species database is starting to take form: some of the first results will be reported at the Neobiota conference in September Ultimately, a European invasive alien species gateway will link the European-wide alien database with the expertise registry and the information system. Already, updates submitted by experts across Europe track new alien species, such as a first record in Italy, in March , for the raccoon dog Nyctereutes procyonoides , a potentially high-impact invader.
Together, these databases will provide a powerful online tool to assess impacts of existing biological invasions, and to predict and control future spread. They will be freely available to scientists, decision makers, and the public. This integrated European effort is among the first to address biological invasions at a continental scale, but undoubtedly other large-scale efforts will benefit from this collaboration.
A long-term commitment to the maintenance and expansion of this program will be an important challenge to undertake, ensuring the future benefits of information sharing for the preservation of native biodiversity and for society. National Center for Biotechnology Information , U. PLoS Biol. Published online Aug Author information Copyright and License information Disclaimer.
Di Castri, Francesco [WorldCat Identities]
E-mail: li. Susan M. 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 properly credited.
This article has been corrected. See PLoS Biol. This article has been cited by other articles in PMC.