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Aliens in Egyptian Mediterranean waters. A check-list of Erythrean fish with new records

The historical role of the Suez Canal as a pathway for migrations between the Red sea and the Mediterranean is recalled. A check-list of 42 immigrant Erythrean fish in Egyptian Mediterranean waters is given. The list comprises four new records. 17 of the immigrant species are commercially exploited, whereas 15 are known from single records. While the Erythrean fish as invasive species are beneficial to local fisheries, in our view, they do not have an important impact upon the ecosystem.


Introduction
The biodiversity of the East Mediterranean has been considerably altered since the opening of the Suez Canal in 1869. As a narrow and shallow water course, it stands as a channel between two marine basins (GRUVEL, 1936). Its biological role however, is out of proportion to its size, although as a habitat and a pathway it remained long inhospitable to marine organisms. Two opposite salinity barriers, the abnormally high salinity of the Bitter Lakes, south, and the Nile dilution, north, stood on their way. With the continuous dissolution of the salt beds in the Lakes and the cessation of the Nile flood, both barriers became weaker. MORCOS (1980) compared the water masses in the Canal in 1955 to the records made in 1871, two years after its opening and found that salinity dropped from about 65 ppm to about 45ppm. Nevertheless, the circulation pattern remained unchanged, the residual current tending to flow from the Red Sea to the Mediterranean for ten months, reversing its flow in August-September. This pattern, added to their greater tolerance to high salinity, favours the northward migration of Erythrean organisms.
The process of immigration into and through the Canal remained incremental but slow, as documented by the early surveys of its ichthyofauna. Some ten years after its opening, KELLER (1882) found 12 fish species in the Canal and shortly after, KRUKENBERG (1888) recorded 15 species (for KRUKENBERG 1888 see NORMAN, 1927). TILLIER in 1902 published a detailed account of the ichthyofauna of the Canal based on a survey extending over several years. He recorded 80 species of which about 40 occurred in the Canal, the others presumably venturing in and out. NORMAN (1927), working on the collection made by the Cambridge Expedition to the Suez Canal in 1924, reported the occurrence of 45 fish species, 24 originated from the Red Sea and 21 from the Mediterranean. From his records and from more recent observations, it appears that 13 of the Red Sea species had already established viable populations in the Mediterranean . On the other hand, five the Mediterranean species such as Engraulis encrassicholus (Linnaeus, 1758), Hippocampus brevirostris (Schinz, 1822), Serranus cabrilla (Linnaeus, 1785), Gobius ocheticus (Norman, 1926) and Epinephelus aeneus (Geoffroy Saint-Hilaire, 1817), succeeded in crossing the Bitter Lakes establishing in the Gulf of Suez.
The important changes that took place in the Levantine basin following the completion of the High Aswan Dam in 1965-67 have created more favourable conditions for the settlement and spread of Erythrean fish and invertebrates in the Mediterranean basin (HALIM et al., 1995;HALIM, 2004). Instead of reaching a plateau as POR (1978) assumed, the process appears to be accelerating.
Later, POR himself reviewed his earlier statement (POR, 1990). TORTONESE (1964) estimated the Indo-Pacific immigrant fish species to be about 30 for a Mediterranean total of about 550. BEN-TUVIA (1985) listed 41 species including the records of MOUNEIMNE (1977). In their Atlas of Exotic fish species in the Mediterranean, GOLANI et al. (2002) reported 59 exotic species for an estimated Mediterranean total of 650, which is almost 10% of the population. The rate of fish invasion has continued unabated since 2002 (GOLANI et al., 2002). By 2007, 18 new alien fish species have been recorded and many have extended their area of distribution (GOLANI et al., 2007). As to Egyptian waters, the check list of EL SAYED (1994) included 31 Erythrean fish species out of a total of 257. After EL SAYED (1994) and taking into account earlier records (NORMAN, 1927;MILLER & FOUDA, 1986) and more recent ones (RIZKALLA, 1997;ALLAM et al., 1999;GAMEE, 2005), Erythrean fish accounted for 38 species. Two species reported from Egyptian waters by TORTONESE (1951), Glaucostegus halavi (Forssk l, 1775) and Carcharhinus melanopterus (Quoy & Gaimard, 1824) have been omitted as their occurrence has not been confirmed.
The present work adds four new records of Erythrean fishes being present along the Mediterranean Egyptian coasts, bringing the list to a total of 42 species. Information on their contribution to fishery is also given.

Material and Methods
The present check-list of Erythrean fish species in Egyptian waters combines dispersed records reported by several authors over the years but it also includes recent, unpublished records made by the second au-a thor (S. RIZKALLA). Species are sorted according to the observed abundance and the frequency of appearance in the fish market. Species which have established successful viable populations are grouped under "A" and "B". Species under A are of commercial value and appear on the fish market, with the exception of the toxic Lagocephalus sceleratus. "Single record" species are put under "C" since the frequency of the presence in the fish market tends to be a function of their economic value. The less valuable species are frequently overlooked, though some might be fairly common. On the other hand the three groups should not to be considered as rigid categories. Some species from group B such Fistularia commersonii and Hemiramphus far are on their way to develop growing populations and will soon need to be included under A. Three species (Herklotsichthys punctatus, Siganus luridus and Callionymus filamentosus) have been placed under category "A" following the survey of AKEL (2005) in Abu Qir bay. Two species namely Glaucostegus halavi (Forssk l, 1775) and Carcharinus melanopterus reported from Egyptian waters by TORTONESE (1951) have been omitted from the check list as their occurrence in Egyptian waters has not been confirmed.
Nomenclature follows the World Register of Marine Species (APPELTANS et al, 2011).

Results
The Erythrean fish species recorded from Egyptian Mediterranean waters until 2010 are given on As a rule, the new-comers to the Mediterranean tended to extend east rather than west from the Canal in the pre-High Dam times, a trend which is expected to change. Nevertheless, some Red Sea immigrants are now common hundreds of kilometres west of Alexandria. This is the case with L. sceleratus and F. commersonii (unpublished records). On the other hand, some Erythrean fish proved to be highly euryhaline, tolerant to a wide salinity range being able to penetrate the low brackish Delta lakes as well as the hypersaline Bardawil lagoon (Table 2, Fig. 1).
Sebastapistes nuchalis (Günther, 1874), which was excluded from the checklist of GOLANI et al. (2002) on the grounds that its single record in Cyprus was based on a misidentification, is now included again in the list of alien Mediterranean species from a single record of EL SAYED, 1994.
New records. Four new Indo-Pacific species were encountered in samples collected by the second author (S.R.) from trawlers, beach-seiners and purse-seiners from 2001 to 2009. Their description agrees with GOLANI et al. (2010).
A relatively large number of specimens (48-103 cm in total length) were caught in 2001 by trawlers west of Alexandria. The species is so far absent from the eastern zone.
a    Specimens of this species (11.0-14.0 cm in total length) were found in 2009 in the catch of trawlers in Abu Qir Bay at 39-47 m of depth. Additional specimens (7.0-10 cm in length) were captured off Rosetta at less than 50 m.
One specimen of 10 cm in total length was caught by day-light purse-seine in coastal waters off Abu Qir in 2007.
Specimens of this species were first caught off Alexandria at a depth of about 80m in 2008. Additional specimens were later caught  off Lake Borullos in the mid-delta at depths from 50-100m (total length range 51-73 cm.). L. sceleratus is now common off the Delta and the Sinai. Proven to be toxic due to tetrodotoxin and is banned.

Discussion
The spread of non-native species into the Mediterranean and their impacts on the host environment is of much concern to ecol-ogists everywhere. In most definitions the term "invasive aliens" is associated with adverse effects, threatening native biological diversity, the ecological stability of the invaded ecosystems and the resulting economic consequences. Some authors consider the spread of "invasive" species and climate change as the two major threats to biodiversity in the marine environment (DUKES, 2003). This ignores other potential impacts such as overharvesting of resources, de-   (1986) struction of habitats or the introduction of harmful pollutants. The terminology used by invasion ecologists reflects their pre-conceived options, ranging from neutral to quasi-hostile, sometimes emotionally charged attitudes. The history of invasion biology  has been reviewed by DAVIS & THOMPSON (2000) and DAVIS (2006). Depending on the author, a species in the invasion literature might be referred to as non-indigenous, introduced, imported, non-native, immigrant, colonizer, alien, exotic or invasive. A list of the "100 Worst Invasives" in the Mediterranean has been compiled by STREFTARIS & ZENETOS (2006).
On the other hand, it should not be forgotten that the spread of new species to new habitats is and has always been a natural and continuous process over the ages. Man has only accelerated this process. The Mediterranean Sea in particular has seen successive waves of introductions. Its fauna and flora consist of a mosaic of formerly alien species of different biogeographic affinities, reflecting its eventful geological history.
OCCHIPINTI-AMBROGI & SAVINI (2003) discussing three case studies such as the lagoon of Venice, the Black Sea and the spread of the alien alga Caulerpa taxifolia in the West Mediterranean, concluded that stress on the marine environment favours the spread of alien species. Invasions are facilitated either in strongly depleted environments subject to anthropogenic stress or in inherently unstable and variable environments having empty niches. However, the case of the Erythrean invasions in the Levantine basin and the waters beyond does not fit entirely with the above hypothesis. Successful invasions also occur in undisturbed environments.
The Suez Canal has created a gradient in the biodiversity between the highly rich Red Sea -Indo-Pacific and the impoverished Levantine fauna (HALIM et al., 1995) In Egyptian waters, the reported impact of immigrant fish species is based on assumptions while the benefits are largely economic. In certain cases in our view there is no evidence of measurable conflict. The Erythrean fish Siganus luridus and S. rivulatus which are voracious feeders on green algae (MOHAMED, 1991), do not appear to be in competition with the indigenous Diplodus vulgaris and D. sargus as happens elsewhere (IDIL et al., 2007). In Egyptian waters the last two species are omnivorous, feeding on microcrustaceans, bivalves, fish fry and green algae (WASSIF, 1973). Merluccius merluccius, once abundant on the shelf fishing grounds, appears to have been displaced from its coastal habitat to deeper waters. It is presumably unable to coexist with demersal Erythrean invaders. It is not clear whether this is due to competition for food or to predation on its fry and youngs (unpublished observations).
The most severe case of adverse impact on human health is that of the puffer fish, Lagocephalus sceleratus. First recorded in Gokova Bay, on the south-eastern Aegean Sea coast of Turkey in 2003(AKYOL et al., 2005, it rapidly extended to Egyptian waters where it became abundant in the fish catch. Although sold beheaded and eviscerated, it soon proved to be a serious hazard to consumers, causing paralysis of the mouth and limbs. Four lethal cases occurred in Alexandria following consumption of L.sceleratus due to tetrodotoxin, a poisonous substance. The species figures on the list of the 100 worst invasives (STREFTARIS & ZENETOS, 2006). With the exception of the latter case and of the few instances of native species displacement or regression, the Erythrean immigrants are economically important for Egyptian fisheries.
It is obvious that the focus in most of the "invasion" literature is on the unwanted effects, any beneficial outcome being minimized or overlooked (GALIL, 2007). A parallel list of species without important adverse effects upon the biodiversity and the environmental stability could be sought. Among the ecological benefits derived from immigration and settlement of Erythrean fish in Egyptian waters and possibly in the Levantine basin at large are the enrichment in species and the ensuing improvement of biodiversity. This leads to a more efficient use of the resources presumably leading to an improvement of the ecosystem stability.
The economic returns are undeniable. Among the "100 Beneficial Invasives" should be included the species listed under A in Table 1. The Erythrean Scomberomorus commerson increased in the catch from 550 ton/year in 2000 to 1500 ton/year in 2007, valued at about 15 million LE. Likewise the Siganus spp increased in the catch from 600 t/y to 1146 and the Synodontids from 1300 to 2000 t/y in the same period, the native and non-native species included (GAFRD, 2009). Several examples can be given demonstrating that the increased species richness has been of economic benefit.
An objective approach to the issue of non-native species migration to new environments and its consequences has to recognize that the problem is case-specific.