Addressing anthropogenically induced changes in fish communities through community-level or ecosystem-level indicators is imperative to the proper management of fisheries (Jennings 2005). In Mediterranean bottom trawling, this need is obviated by the multi-species nature of the fishery (Caddy et al. 1995) and the rapid biogeographic changes caused by Red Sea invasion that the local ichthyofauna is undergoing (Edelist et al. 2013). These render single-species indicators such as those proposed by Froese (2004) rather less practical and less indicative of the general state of the fishery or the ecosystem. Groundfish trawl surveys for assessing changes in various aspects of the community’s composition, structure and function are widely used in the Mediterranean. They have provided us with much knowledge in recent years but their development and implementation as viable tools for fishery management still lag far behind those in northern European seas. Various metrics can be considered as tell-tale variables although few are as indicative and simple to understand as the Large Fish Index (LFI). This indicator is defined as the biomass fraction of fish above a pre-determined length threshold (i.e. “large” fish), expressed as a proportion of the total fish biomass (Heslenfeld and Enserink 2008, Greenstreet et al. 2011). This metric is sensitive to decreases in large fish biomass, which might be caused by overfishing, as well as to increases in small fish biomass caused by reduced predation by large fish (Fung et al. 2012). Therefore, the LFI responds to both the direct and indirect effects of fishing (Greenstreet et al. 2011). It has been adopted by the Oslo-Paris convention (OSPAR) as an indicator for fish community health as part of the Ecosystem Approach to Fisheries Management (Heslenfeld and Enserink 2008) and is listed as an indicator of “good environmental status” by the EU MSFD in descriptor 4, under which member states are required to strive for good environmental status by the year 2020 (Fung et al. 2012). It has been successfully used in the North Sea (where it is most developed – see Greenstreet et al. 2011), the Celtic Sea (Shephard et al. 2011), the Baltic Sea and the Grand Banks (ICES 2011). As part of the EU MFSD the LFI was also very recently introduced in the western Mediterranean as part of the MEDITS surveys (Ordines et al. 2013). Here we wish to demonstrate the possible implementation of LFI in the eastern Mediterranean and discuss prerequisite adjustments mandated by the nature of trawl catches in the new and rapidly changing Levantine environment.

The Levantine Sea is a highly oligotrophic body of water, with high salinity and temperatures (e.g. Herut et al. 2000). These characteristics are perceived to be the main natural reason for the low fishery yields of the region (Caddy et al. 1995) and may also be associated with Levantine Nanism, characterized as “the smaller size and early maturation of several species in the Levant compared to conspecifics of the same sex and age in the northern and western Mediterranean” (Sonin et al. 2007). Mediterranean fish markets are thus culturally accustomed to and appreciative of smaller fishes, especially those harvested by the trawl fishery. This is accentuated in the Levant, where the main bottom trawl target species (e.g. goatfishes, pandoras, bogue) rarely attain sizes larger than 25 cm total length and are typically landed at only 10-15 cm (Appendix 1. also see Edelist et al. 2011). The most striking phenomenon shaping species composition in the Levant is bioinvasion of tropical fauna through the Suez Canal and (Edelist et al. 2013), but its impacts on size spectra is yet unstudied. While smallness of the local fishes is a known fact, it is yet unknown whether it should be attributed solely to Levantine Nanism, or whether (and to what extent) excessive or unsustainable fishing is a contributing factor.

A sustainable fishery is expected to extract large animals, which have had time to reproduce and contribute to the gene pool (Pauly et al. 1998). Large fishes provide ecosystem services to humans (e.g. nutrition and employment), whereas small fish extraction represents economic wastage and inefficiency as well as an ecological crippling of future stocks. It therefore stands to reason that bottom trawling, long criticized for its low selectivity and extraction of small fish, is the chosen fishing method for implementation of the LFI. This is not the first time that trawling data have been proposed as an indicator for the state of fisheries in the Mediterranean. For example, the ratios of diversity and/or trophic level of the discarded and landed fractions of the catch were suggested by Tsagarakis et al. (2008) as such an indicator. Rochet and Trenkel (2003), however, found that multi-species indicators based on empirical population indicators (such as the LFI) were more reliable than indicators based on food web modelling. Moreover, the LFI itself can be highly indicative of trophic changes in demersal fish communities, since ontogenetic change and inter-specific variation in diet are strongly linked to predator body size (Greenstreet et al. 2010). The present study aims to demonstrate that the LFI can be implemented in the Levantine Sea, and describes how it can be tailored and adapted to the smaller size spectra of its fish.

Our 2008-2012 surveys yielded 72812 bony fish length measurements, out of which 70461 (96.7%) were below 20 cm, and 72150 (99%) were below 30 cm. In the North Sea, Greenstreet et al. (2011) for example, found that 95% of the trawled fish (by number) were shorter than 30 cm, underscoring the lack of large fishes in the Levantine assemblage. The LFI₂₀ and LFI₃₀ values were 0.3 and 0.15 respectively (Fig. 2), meaning that 70% and 85% of the fished biomass originates in fishes smaller than 20 cm and 30 cm, respectively.

As Mediterranean trawlers rely more on juvenile fishes than Atlantic ones (Caddy 2009), the Mediterranean catch composition is expected to depend greatly on seasonality. This is, indeed, echoed in our results, as LFI values declined during the summer recruitment season by 0.05-0.2 (Fig. 3). This analysis was unavailable when the LFI was applied to data obtained from the 20 mm mesh MEDITS surveys, in which the annual analysis was the main application allocated to the LFI within the EU MSFD for the Mediterranean (Ordines et al. 2013).

We also calculated the LFI separately for each year (Fig. 4). While LFI values seem to have improved over the study period, the low values for 2008 and high values for 2012 are a function of the seasonal variance in sampling and thus reflect seasonal rather than annual trends.

The ‘smallness’ of Levantine fish assemblages may also be rooted in invasive species. Of the 72812 fishes measured in this study, 56307 (58.4%) were Lessepsian Migrants—Nonindigenous fishes of Indo-Pacific origin. The three most common species in this study, accounting together for 30% of the specimens, were nonindigenous: 1) The tiny (typically 5-10 cm total length) pony fish Equulites klunzingeri, which almost creates its own new size class in the Mediterranean (Fig. 5); 2) The commercially important goatfish Upeneus moluccensis, rather smaller than its displaced indigenous confamilials, Mullus barbatus and M. surmuletus; 3) The venomous catfish Plotosus lineatus, which exploded in population (Edelist et al. 2012a) since its recent introduction a decade ago. While not nearly as short as the ponyfish (with L_max of >20 cm), the slender catfish is very light compared to its length, and considerably negatively impacts the LFI. Unlike the goatfish, which is only discarded when smaller than 8-9 cm, the ponyfish and the catfish are wholly discarded.

In sizes of 12.5-18 cm, indigenous species slightly outnumber nonindigenous ones, but many indigenous species are also by-caught in small sizes of 5-10 cm total length (Fig. 3). These are mainly juvenile porgies (Pagellus spp.), goatfishes (Mullus spp.) and Bogue (Boops boops), extracted in large abundance every spring and summer during their recruitment.

In Figure 2 we present (dashed line) a more sustainable LFI contour based on the arbitrarily set values of LFI₂₀=0.5 and LFI₃₀=0.3, which we consider as reasonable for the Levant. These values are higher than the actual values by about the same proportion as target LFI values of the North Sea are higher than actual values (i.e. the target values are 1.5-2 times the actual values, see Greenstreet et al. 2011 and Fung et al. 2012). We propose them as indicative reference points that represent a healthy Levantine trawl fishery. Fishes 20 to 30 cm long thus abound in the Mediterranean in the same range of LFI values as 40-cm-long fishes do in the North Sea. We therefore suggest that considering the smallness of the Levantine species assemblage, 0.5 for 20 cm and 0.3 for 30 cm can similarly be considered as benign levels for this region. The 40 cm value proposed for the North Sea was set to maximize the LFI sensitivity to fishing pressure rather than to recruitment events and other ex-fishery factors (Greenstreet et al. 2011). The recruitment of (mainly indigenous) Mediterranean species occurs in the summer, following spawning (Edelist et al. 2011, 2012b). This is when juveniles reach sizes large enough (typically 5-13 cm) to be caught in the ~40 mm diamond mesh nets dragged by the Israeli trawl fleet.

Ex-fishery factors contributing to small sizes in Levantine fishes

Rochet et al. (2010) propose that an exploited groundfish community can be viewed as a three-level food chain with two upper levels that are target catch, while the lower level is subject mostly to environmental variation. Metrics relying on the lower level are therefore often criticized for their dependence on natural events (Rochet et al. 2010). However, the LFI was found to be comparably robust to such perturbations (Greenstreet et al. 2011, ICES 2011) as biomass is less sensitive to changes in the lower level components of the catch. The fish assemblage of the eastern Mediterranean is ‘naturally’ small, but there is another way in which it varies significantly from that of the western Mediterranean.

The faunistic invasion via the Suez Canal has profoundly and irreversibly altered the composition of the Levantine ichthyofauna (Edelist et al. 2013). Indigenous species now occupy ever deeper strata, as they are being displaced by Indo-Pacific species along bathymetric axes and fishwise, Levantine shallows are now almost tropical. For example, Edelist et al. (2013) have shown that nonindigenous fish accounted for 84% of the abundance and 66% of the biomass in waters shallower than 30 m in Israel. The difference between these percentages alludes to the small body size of migrants and also coincides with the upper, warmest layer in the water column. Surely the long-term impacts of this unidirectional process must be weighed carefully upon analysis of the LFI indicator.

One main natural cause in explaining overall diminished sizes in Levantine fishes is undoubtedly Bergmann’s rule, stating that within a broadly distributed species, specimens from cooler climates tend to be larger than conspecifics from warmer climates (Bergmann 1847). The waters of the eastern Mediterranean are warmer by ~6-9ºC than those of the western basin (Nykjaer 2009) and Levantine fishes are thus expected to be smaller not only than those from the North Sea, but also than those from the western Mediterranean. Another reason for this lies in the extreme natural oligotrophy of the region, previously suggested as the main reason for Levantine Nanism (Sonin et al. 2007). This is possibly exacerbated by damming of the Nile River in Aswan in 1964, which curtailed the annual flooding of this once giant river, cut its freshwater flow to less than 10% of previous levels, and eliminated phytoplankton blooms associated with the nutrients swept into the Mediterranean by floods (Oczkowski et al. 2009). Here we propose that a third factor is contributing to the small size of the assemblage - the influx of nonindigenous Indo-Pacific species through the Suez Canal.