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Keywords:

  • Biological invasions;
  • climate change;
  • coastal;
  • human impacts;
  • invasive fish;
  • Lessepsian;
  • Mediterranean

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

Aim

We examine fish invasions in the south-eastern Mediterranean as a model system for the invasibility of open coasts and provide perspectives through a review of global marine fish invasions.

Location

South-eastern Mediterranean (Levant Sea).

Methods

We compare historical (1990–1994) and modern (2008–2011) trawl surveys from the Mediterranean continental shelf and upper slope of Israel to evaluate the relative abundance and biomass of Indo-Pacific fishes and their impact on diversity and trophic level (TrL). We examine resultant changes in community composition by both univariate and multivariate analyses, and compliment this study with a critical global review of open coast marine fish invasions.

Results

A staggering 55 Indo-Pacific fish species have established permanent populations in the Mediterranean in the last 142 years, more than any other marine ecosystem. This process is accelerating with 13 of 27 new arrivals having established in the 21st century alone. Invasive fish biomass and abundance proportions in the shallow open coast have doubled in just two decades and today the Levantine ecosystem is dominated by non-native species. This proliferation has resulted in significant declines of some indigenous species, some to near extirpation levels.

Main conclusions

Here, we show that non-estuarine ecosystems are much more susceptible to large-scale invasion pressures than previously thought. Our results place invasion in the same category with overexploitation, habitat destruction and pollution, processes normally considered as much more critical perturbations to coastal fish communities. We propose that despite these irreversible alterations, invasions have masked overall TrL changes and diversity declines by replacing native fish with invasives of similar ecological position. As species extirpations increase, we anticipate further declines in indigenous biomass, abundance and diversity in the Mediterranean Sea.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

Invasions of non-native species in the ocean can profoundly reshape indigenous communities, impact conservation strategies and affect human health and the economy (Cohen & Carlton, 1998; Byrnes et al., 2007; Rilov & Crooks, 2009; Golani, 2010). These impacts are believed to largely centre on estuaries and other lower-energy or lower-salinity embayments (Cohen & Carlton, 1998; Wasson et al., 2005; Byrnes et al., 2007; Preisler et al., 2009) owing to a combination of factors, including the concentration of vectors (such as aquaculture and shipping activities) that transport species between estuaries and bays, the presumed lower competition in these environments from native species, and the severe anthropogenic stresses in estuarine systems subject to intensive industrialization and urbanization. While certain high-energy open intertidal shores have been invaded (Preisler et al., 2009), open subtidal coastal systems – and especially fish communities – are generally regarded as under pressures other than invasions that are perceived as greater threats, such as overexploitation, habitat loss (due in part to fisheries activities) and pollution (Reynolds et al., 2005). The perception that non-native species are of lower concern for most open-sea ecosystems may arise from the converse of factors proposed for the susceptibility of estuarine ecosystems to invasions: the higher species diversity and thus presumptive greater competition in the ocean (Stachowicz et al., 1999; Preisler et al., 2009), higher salinities precluding the establishment of fish transported by aquaculture, and that other major vectors, such as ballast water, are regarded as transporting species not only largely between harbours and bays, but also act primarily as a dispersal agent more for invertebrates and phytoplankton than for fish (Whitfield et al., 2002; Carlton & Eldredge, 2009; Rilov & Crooks, 2009; but see Wonham et al., 2000).

Among marine ecosystems altered by invasion, the easternmost Mediterranean Sea stands out as undergoing exceptionally rapid and intense changes (Rilov & Galil, 2009; Golani, 2010) owing to the opening of the Suez Canal in 1869. One of only two inter-oceanic canals in the world (the other being the Panama Canal), and the only one with no freshwater disrupting oceanic connectivity, the Canal has enabled passage of hundreds of taxa, among them 84 fish species (updated here from Golani, 2010) whose frequency of invasion has increased in modern times (Ben Rais Lasram et al., 2008; Rilov & Galil, 2009). The main catalysts of this accelerated fish invasion include continuous removal of high and low-salinity barriers, thus permitting the invasion of species that were not tolerant of either formerly higher and lower mid-canal salinities, or lower canal mouth salinities (Ben Rais Lasram et al., 2008; Rilov & Galil, 2009; Golani, 2010), overexploitation of indigenous fish, thus reducing competition (Ben Yami & Glaser, 1974; Edelist et al., 2011), invasion by organisms of lower trophic levels (TrL) increasing the food supply for new fish invaders (Rilov & Galil, 2009; Edelist et al., 2012), and recent warming of the waters and climatic changes which began in the late 1990s, permitting the invasion of species previously excluded by cooler mediterranean waters (Ben Rais Lasram et al., 2010; Raitsos et al., 2010; see also Cheung et al., 2009 and Sorte et al., 2010 for a broader global picture of the exacerbation of invasions owing to latitudinal shifts mediated by global warming). Despite the magnitude of this incursion, quantitative data facilitating the understanding of its scale, rate and effects on indigenous communities are still missing (Ben Rais Lasram et al., 2008; Rilov & Galil, 2009).

We show here that the number of fish species that have established large permanent populations in the Mediterranean, and the size of some of these populations, far exceed those of any other marine ecosystem and rival the most invaded estuaries. We use trawl data to examine the hypothesis of the lower invasibility of open coasts, and we show that given a strong enough invasion pressure, the abundance and biomass of invasive fish on the open coast can be at the salient expense of indigenous fish, indicating that non-estuarine ecosystems are much more susceptible to large-scale invasion pressures than previously thought.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

Global marine invasion literature was surveyed and critically reviewed to assess the number of invasive brackish and marine fish species in the world's most invaded ecosystems (Fig. 1 and for sources see Table S1 in Supporting Information). Many ecosystems with a single invasion record exist and owing to possible biases introduced by cryptogenic or undiscovered rare species (Carlton & Eldredge, 2009), we chose to focus on invasion hotspots (Sensu Rilov & Crooks, 2009) with four or more established alien marine or brackish fish species. The parameters set by CIESM (Golani et al., 2002) for alien species in the Mediterranean were applied to determine whether invasive species were established. Many invading fishes in the Levant inhabit shallow soft-sediment habitats (Ben Rais Lasram et al., 2008; Rilov & Galil, 2009), making bottom trawling ideal to study their distribution. Historical and modern catch data of Israeli trawlers were used to evaluate trends in abundance, biomass, diversity and TrL of Levantine fishes, and assess potential interactions between invasive and indigenous species. Historical data were collected from 267 trawl hauls from April 1990 to December 1994 at depths of 15–300 m. Current data were collected in 183 hauls conducted between October 2008 and March 2011, covering the same fishing fields and depth range (15–300 m) on the continental shelf and upper slope. Data were extracted from hauls replicating commercial trawl hauls, that is, the skippers were asked to perform their own routes within a given depth, location or time and they are therefore hybrids between fisheries dependent and independent surveys.

image

Figure 1. Number of established invasive marine and brackish fish species reported from invasion hotspots (more than four invasive established species, see Table S1 for details). The Mediterranean column is divided into 55 Indo-Pacific (bottom) and 10 Atlantic (top) species respectively.

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Owing to differences in data collection between the two study periods, the challenges of comparing the two data sets included three main facets: (1) the ability of the vessel to catch fish, affected by vessel size, engine power (HP) and fishing gear used, (2) the post-capture onboard analysis of the catch, that is, sampling methodology and (3) The spatiotemporal effects of haul area, depth and season on catch composition.

  1. Trawl effectiveness in catching fish depends on mesh size, towing speed, horizontal spread of the gear (net width and distance between trawl doors) and the reach of the headline into the vertical distribution profile of fishes in the water column (vertical spread, see Pauly, 1979). In both study periods, 15–22-m Length Over All (LOA) stern trawlers dragged 40-mm diamond mesh nets with sweeps (hauls with shrimp nets using tickler chains and no sweeps were removed from the analyses). Nevertheless, mean engine HP of vessels grew by 33% from 221 in 1990–1994 to 294 in 2008–2011 (Edelist et al., 2011). While this did not result in increased towing speed, which remained constant at three knots, the horizontal opening of the gear (distance between trawl doors) increased from 55–65 m in 1990–1994 to 60–80 m in 2008–2011. Moreover, the vertical reach of nets also increased from 1.2–1.5 m, to 1.5–1.8 m at headline midpoint. Different constants may be used to adjust the headline length and height to the spread of the net. Pauly (1979) for example used 0.67 in Thailand but stated that values may vary widely between studies. The specific spread of the gear in this study was not consistently measured in either period and we therefore chose the median points of 60 and 70 m for horizontal and 1.35 and 1.6 m for vertical spread in 1990–1994 and 2008–2011 respectively. When applying the 0.67 constant used by Pauly (1979) to the vertical opening, these result in a 22% horizontal and 11% vertical increase in swept volume of water. We therefore chose to add 33% to abundance data from 1990 to 1994, which also corresponds to the rise in mean HP between the periods. Furthermore, as pelagic species are most affected by changes in vertical opening of the gear, these were removed from the species specific analyses, as they may be underrepresented in 1990–1994 owing to the lower vertical reach of nets.
  2. The catch sampling protocol from 1990 to 1994 (Edelist et al., 2011) was repeated in 2008–2011. A representative sub-sample from the total catch was obtained from the fish pile onboard with no specific preference given to any direction on deck to assure randomness. All fishes in samples were taxonomically identified to the species level and measured to the nearest 0.5 cm. 1990–1994 data were collected by several surveyors, and hauls with a clear lower taxonomic resolution were subsequently omitted from the database.
  3. primer-e software (Clarke & Gorley, 2006) was used to create a log (x + 1) transformed Bray–Curtis similarity matrix based on species abundance per hour in each haul, calculated by division of abundance in samples by sample proportion and haul time and for 1990–1994 correction according to the 33% catchability coefficient. To identify the factors contributing most to spatiotemporal differences and variability in community composition, we ran a stratified four-way permanova design (Anderson, 2001) on the similarity matrix. Study period and depth contributed considerably more to dissimilarity than season or area (Table S2). Period and depth were subsequently explored in an multidimensional Scaling (MDS) performed to check for community dissimilarity (average distance from each sample to group centroids), which was also suggested by Anderson et al. (2006), to account for beta-diversity differences.

Invasive abundance and biomass proportion, and total TrL and Shannon's species diversity were determined for invasive and indigenous fishes from samples (Fig. 2). Biomass proportions were extrapolated from fish lengths using Length-Weight relationships which we calculated for 107 species. Where not enough specimens could be retained to determine the relationship, it was retrieved from FishBase (Froese & Pauly, 2011) for the nearest location to the Levant. TrLs were similarly assigned to each species from the literature (Stergiou & Karpouzi, 2002; Froese & Pauly, 2011) and then pooled for each sample. After omission of pelagic fishes, demersal species that contributed most to Bray–Curtis dissimilarity between the two periods on the shelf were identified by the simper routine in primer (Clarke & Gorley, 2006). A two-tailed, nonparametric Wilcoxon test was used to test for differences between periods with a Bonferroni correction used to avoid an inflated Type I error rate, where multiple comparisons were performed. Alpha levels were adjusted accordingly to < 0.0125 for the four hypotheses tested in Fig. 2 and < 0.002 for the 25 species comparisons in Fig. 3.

image

Figure 2. Comparison of past and present Levantine trawl surveys over six depth strata. Invasive abundance (a) and biomass (b) on the shelf have significantly increased from 1990–1994 (open bars) to 2008–2011 (solid bars). Trends in Shannon's species diversity (H') (c) and Trophic Level (TrL) (d) were less dramatic and occurred mostly on the slope. Bars represent mean proportion, +one standard error. *P(Wilcoxon) < 0.0125.

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image

Figure 3. Differences between past and present catch on the Levantine shelf. The number of specimens caught per hour of trawling + one standard error for the 25 demersal species which contributed most to dissimilarity between 1990–1994 (open bars) and 2008–2011 (solid bars). The arrival and rapid proliferation of new invasive species (top) are mirrored by declines of indigenous species (bottom), the rarest of which are at the brink of extirpation and underline the shift in community composition over the last two decades. *< 0.002.

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Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

A staggering 84 Indo-Pacific fish species have invaded the eastern Mediterranean since the opening of the Suez Canal in 1869 (updated by us from Golani, 2010 with the most recent invasive record made by Goren et al., 2011). We have found that according to the definitions of Golani et al. (2002), 55 of these invaders (65.5%) have established permanent populations in the Mediterranean, by far more fish invasions than anywhere else in the world (Fig. 1) and that some of the most recent invasions are of colossal proportions.

Remarkably, 27 fish species have invaded in the first decade of the 21st century alone. Thirteen of them are established of which six have experienced population explosions and are among the most common and widespread species in the eastern Mediterranean. We have found significant (Wilcoxon, < 0.0125) twofold increases in invasive fish proportions for the four shelf strata combined (15–100 m, the continental break in Israel occurs at 100–110 m) in only two decades. Abundance increased from 29% to 54% and biomass from 25% to 55%, while for the 15–30-m-depth stratum, they have reached 84% and 66% of the ichthyofauna, respectively (Fig. 2a,b). Nevertheless, despite these profound changes in shelf community composition, we did not find evidence of declines in species diversity or TrL (Fig. 2c,d). Although these functional properties have remained relatively stable on the shelf, community composition has considerably shifted, as evident in Fig. 3 and in the MDS ordination (Fig. 4).

image

Figure 4. Multidimensional Scaling (MDS) plot of community composition changes in time. Each symbol is the centroid of a multitude of hauls from 1990–1994 (empty circles) and 2008–2011 (solid circles). Numbers represent stratum depth (m). Two dimensional stress level of the MDS was 0.04. permanova (Table S2) showed that differences between periods are significant in all strata. In the shallowest stratum (15–30 m), replacement of indigenous species by invasives drives changes. Differences in the upper slope (101–150) reflect species displaced from the shelf into deeper waters.

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Interestingly, TrLs increased in the shallowest stratum during the study period (Fig. 2d), while decreasing on the slope, where invasive fishes are still comparatively rare (Fig. 2a). The shallow increase is attributed mainly to declines in abundance of Pagellus erythrinus (Linnaeus, 1758), and to the recent introduction and massive proliferation of Nemipterus randalli Russell, 1986, Apogon smithi (Kotthaus, 1970), Apogon fasciatus (White, 1790) and Plotosus lineatus (Thunberg, 1787) (Figs 3 & 5), all of which feed at higher TrLs than the displaced Pagellus erythrinus. Deepwater TrL declines are attributed mainly to collapsing stocks of the native piscivorous hake Merluccius merluccius (Linnaeus, 1758), and an increase in omnivorous species, mainly Pagellus erythrinus (Fig. 5).

image

Figure 5. Mean number of specimens caught per hour of trawling in 1990–1994 (white bars) and 2008–2011 (black bars) in six depth strata. Several likely scenarios for indigenous and invasive species are suggested: (1) (a–e) Arrival and rapid population explosion of new invasives, (2) (f–h) a lagged increase in earlier invasive populations, (3) (i,j) moderate declines and bathymetric shifts of common earlier invasives, possibly related to the strong competition on the shallow shelf, (4) (k–p): collapse of common indigenous species, often owing to presumed competition with invasives, (5) (q–u) declines and near extirpation of small indigenous populations.

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The rate and scale of invasions as well as their effects are difficult to evaluate owing to the need for historical native vs. non-native data (Ruiz et al., 1997). For at least one indigenous species, we have data preceding invasion of the apparently displacing invasive. The native Pandora bream Pagellus erythrinus was the most abundant species, contributing most to community similarity (SIMPER) in the shallowest stratum in 1990–1994. In 2008–2011, however, it ranked only 12th and its abundance dropped 10-fold (Fig. 5). Its suspected displacer, Randall's threadfin bream Nemipterus randalli was first found in the Mediterranean in 2005 (Golani & Sonin, 2006) and in 2008–2011 already ranked first in SIMPER of the shallowest stratum. Coinciding with its disappearance from the shallows, the abundance of Pagellus erythrinus grew 8-fold in the 101–150-m stratum (Fig. 5), where it advanced from 26th to 1st in SIMPER. This replacement process can also be observed in commercial landings, as a mean of 87.5 ± 26.3 (SD) tons per year of Pagellus erythrinus was landed by Israeli trawlers between 1949 and 2006, but only 34 and 26 tons were landed in 2009 and 2010, whereas the catch of Nemipterus randalli in these years reached 126 and 147 tons respectively (Ministry of agriculture & rural development of Israel, 1958–2009).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

Non-native fish have invaded the Levant in three main waves: (1) The goatfish Upeneus moluccensis (Bleeker, 1855) and the lizardfish Saurida undosquamis (Richardson, 1848) established large populations following the warm years of 1954–1955 (Ben Yami & Glaser, 1974; Golani et al., 2007) and are still very common today (Figs 3 & 5); (2) 10 more successful establishments occurred during the late 1970s and 1980s (Golani et al., 2007; Ben Rais Lasram et al., 2008), and (3) the most recent invasion episode commenced circa 2000 (Golani et al., 2007; Golani, 2010; Ben Rais Lasram et al., 2008), with several new invasives establishing large populations in recent years (Figs 3, 5). Over the past half-century, and continuing at a steady pace, the marine biodiversity of the Eastern Mediterranean has been considerably shifting, a phenomenon that sets the stage for potentially fundamental alterations to the Sea's ecosystems. The invasion of fishes into the Mediterranean is mirrored by a similarly intense invasion of marine mollusks, crustaceans, foraminifera, Polychaetes and a host of other invertebrates and algae (Rilov & Galil, 2009; Golani, 2010).

The only management strategy previously proposed for Indo-Pacific invasions into the Mediterranean was installation of high-salinity locks in the Suez Canal (Goren & Galil, 2005), a rather impractical suggestion. With regard to fishes, we suggest that the earlier spawning and recruitment seasons of indigenous fishes in the Mediterranean (Golani, 2010; Edelist et al., 2011) present managers with an invaluable opportunity to simultaneously support declining indigenous species and facilitate a more sustainable fishery by enforcing a spring moratorium on fishing. Such bans widely exist throughout the Mediterranean but were implemented only briefly in the Levant (Edelist et al., 2011). Assuming that invaders compete with natives for resources, by allowing natives to reproduce without interference and build considerable populations, the success of invader establishment may be suppressed. This newly suggested benefit should not go unnoticed by regional and local managers.

As with overexploitation of fisheries (Pauly et al., 2002), introductions and extinctions usually displace and deplete predators and lower the mean TrL of marine food webs (Byrnes et al., 2007). The scale of biotic replacement in the Levant (Figs 1,2,3 & 5) would thus be expected to result over time in domination of a few resilient invasives over more numerous indigenous species, leading to declining TrLs (Byrnes et al., 2007) and diversity (McKinney & Lockwood, 1999). For now, however, Levantine invasions have masked both TrL changes and diversity declines by replacing native fish of similar ecological position. We suggest that within the Levantine fish assemblage, invasion has artificially maintained TrLs at a high level (Fig. 2d) by replacing indigenous species with invasives utilizing similar ecological resources in a nutrient-deprived ecosystem near or at its carrying capacity. Likewise, we suggest that the lack of declines in shelf diversity (Fig. 2c) represents a species by species replacement process.

The Mediterranean as a global model for open ocean change

The higher invasibility of estuaries is considered to result from greater alien propagule pressure (owing to the release of species from ballast water and ship fouling), a hydrography that facilitates larval retention, the plasticity of estuarine organisms (of a typically euryhaline and eurythermal nature), a plethora of human-induced alterations to biodiversity and habitat and water quality, and the presumed lower competition in these systems, due in part to the lower natural diversity of estuaries and to the extirpation of the native biota by urbanization and industrialization (Ruiz et al., 1997; Cohen & Carlton, 1998; Wasson et al., 2005; Preisler et al., 2009).

Given that the Mediterranean Sea shares some of these characteristics, does the Levant region serve as a model for the potential of open ocean diversity to be globally and critically altered by invasions? The Mediterranean has endured (for thousands of years) a multitude of anthropogenic disturbances and modifications. It faces great alien propagule pressure (albeit from different vectors, in this case canals which focus on adult vs. larval supply of aliens), and a comparatively younger biogeographic and evolutionary history (like many estuaries) which may render its indigenous biota less adaptable to climatic change, to which the thermophilic Indo-Pacific newcomers may have considerable advantage. In particular, the eastern Mediterranean is demonstrably species poor relative to the much greater diversity of the Indo-Pacific, now made available to the Mediterranean in recent times.

Nevertheless, we argue that the open coasts of the Mediterranean Sea share greater similarities to other seas than to estuaries, and that the remarkable shifts in the Levant ichthyofauna can serve as a global harbinger. Although often described as a ‘semi-enclosed sea,’ the Mediterranean is in fact a heterogeneous, deep-water, open ocean environment that does not compare to enclosed bays, estuaries, or harbours in terms of short-distance (tens of kilometres) retention potential of planktotrophic larvae that would facilitate alien species recruiting near to each other to easily promote population establishment. The Mediterranean is, of course, a high-salinity environment in contrast to the brackish water environments of estuaries. Critically, the biotic composition of the mediterranean open ocean system resembles open marine seas globally, much more than estuaries. Thus, if alien propagule pressure continues to increase globally owing to predicted increases in global shipping (Wonham et al., 2000), aquaculture (Pauly et al., 2002), the private aquarium industry (Carlton & Eldredge, 2009), and other vectors (Rilov & Crooks, 2009) we predict similar increases in open coast fish invasions. Our findings show that while invasions have classically been associated with low-energy estuarine environments, the world's open oceans are not immune to invasions at similar scales that bays, ports, and harbours have experienced. We point, as an example, to the unexpected remarkable success and spread of Pacific lionfish Pterois volitans (Linnaeus, 1758) – released through the expanding aquarium industry vector, in the open coasts of the warm-water western Atlantic Ocean (Whitfield et al., 2002; Albins & Hixon, 2011), where marine fish invasions were previously unknown.

Are fish species extinctions in the Mediterranean's future?

Is species extinction the next phase? Ben Rais Lasram et al. (2010) have predicted that by 2099, 14 endemic mediterranean fish species will become extinct owing to combined effects of climate change and invasion. While marine invasions may not lead to global extinctions (yet), in the Mediterranean they already lead to local, commercial and functional extinctions. Musick (1999) has identified four risk criteria used to assess vulnerability of a fish stock: small range and endemism, specialized habitat requirements, rarity and population decline. No fish species are known to be endemic to the Levant and endemism in the Mediterranean is generally low (Costello et al., 2010). For the trawlable soft-sediment ichthyofauna, small range and specialized habitat requirements play a lesser role, leaving population declines and rarity as potential drivers of extinction. Declines of 70–99% within a decade or three life cycles are proposed to indicate vulnerability (Musick, 1999). We have found changes of this magnitude for Mullus barbatus Linnaeus, 1758 and Mullus surmuletus Linnaeus, 1758, which declined by 85% and 95% respectively (Fig. 3) over two decades. While such abundant species may respond initially by shifting depth (Figs 3 & 5 and see Ben Yami & Glaser, 1974; Golani, 1994; Rilov & Galil, 2009; Golani, 2010), rare species with limited bathymetric range and of already precarious existence may be unable to do so. Rarer indigenous demersal fish species such as Trachinus draco Linnaeus, 1758, Uranuscopus scaber Linnaeus, 1758, Trigla lyra Linnaeus, 1758, Solea solea (Linnaeus, 1758) and Gobius niger Linnaeus, 1758 have experienced declines of 70–100% (Figs 3 & 5) and have become extremely rare in the Levant, possibly due to a species by species replacement by invasives, as proposed for replacement of Trachinus spp. by Plotosus lineatus (see Edelist et al., 2012 and Fig. 5). Before fish invasion began through the Suez Canal, the south-eastern Mediterranean was populated mainly by fishes of Atlantic origin, which are at the margins of their geographic distribution. Such small, disjunct populations are particularly susceptible to extinction. We expect that while non-native species will contribute a larger share to the yield of fisheries, accelerating invasion will also induce further homogenization (McKinney & Lockwood, 1999), indigenous declines and eventually extinctions (Ben Rais Lasram et al., 2010).

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

Invasive species are now the main driver of eastern mediterranean ichthyofaunal changes, profoundly and irreversibly altering community composition more than climate change, pollution, and overexploitation individually. The dominance, number of species and accelerating rate of invasion were argued to make San Francisco Bay and Delta the most invaded estuary in the world (Cohen & Carlton, 1998). As species extirpations increase, we anticipate more extraordinary declines in indigenous biomass, abundance and diversity in the Mediterranean Sea, the world's most invaded marine ecosystem.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

This study was partially supported by grants from the Israeli Ministry of Agriculture and Rural Development, and the Ministry of Environmental Protection (D.E., D.G., E.S.), as well as the Maurice Hatter Grant for Maritime Studies and the Rieger Foundation Fellowship for Environmental Studies (D.E.). We also thank Dr Oren Sonin for collecting the 1990s trawl data, Dr Tamara Shiganova for providing data on fish invasions in the Black and Caspian Seas as well as E. Schwindt, A. Bortolus and A. Solari for contributing data on Argentinean invasions.

References

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  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information
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Biosketch

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

Dor Edelist is a marine ecologist and fisheries scientist researching drivers of change in the fish assemblages of the Eastern Mediterranean. His research focuses on two main subjects: (1) fishing effects on the environment and the state of resources (2) bio-invasion of Indo-Pacific fauna into the Mediterranean. The data he amassed enable him to advocate courses of action to fishery managers and identify long-term trends in the marine environment. His current interests include invasive species, promotion of sustainable fisheries and marine conservation.

Author contributions: D.E. collected and analysed data and wrote the drafts of the manuscript. G.R. performed multivariate analyses and contributed to study design. DG assisted with taxonomic identification of fishes, J.T.C. compiled and edited global data on invasive marine species and led the writing. E.S. was involved in study design and editing of text.

Editor: Robert Cowie

Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Biosketch
  11. Supporting Information

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FilenameFormatSizeDescription
ddi12002-sup-0001-TableS1-S2.docxWord document18KTable S1 Number of marine and brackish water fish species introduced into marine invasion hotspots (4 or more species shown). Table S2 A PERMANOVA model testing the effects of study parameters on species composition.

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