See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/282190358 Common traits associated with establishment and spread of Lessepsian fishes in the Mediterranean Sea Article in Marine Biology · September 2015 DOI: 10.1007/s00227-015-2744-3 CITATIONS READS 6 223 2 authors: Erik Arndt Patrick Joseph Schembri Hochschule Anhalt University of Malta 11 PUBLICATIONS 109 CITATIONS 263 PUBLICATIONS 2,430 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: LIFE BAHAR for N2K View project Alien Species and other Newcomers in Maltese waters View project All content following this page was uploaded by Erik Arndt on 07 October 2015. OAR@UM The user has requested enhancement of the downloaded file. provided by View metadata, citation and similar papers at core.ac.uk CORE brought to you by Mar Biol (2015) 162:2141–2153 DOI 10.1007/s00227-015-2744-3 ORIGINAL PAPER Common traits associated with establishment and spread of Lessepsian fishes in the Mediterranean Sea Erik Arndt1 · Patrick J. Schembri2 Received: 25 February 2015 / Accepted: 14 September 2015 / Published online: 24 September 2015 © Springer-Verlag Berlin Heidelberg 2015 Abstract It was more than 30 years after the opening of the only significant trait influencing dispersal success. This the Suez Canal in 1869 that the first reports on Indo-Pacific trait is likely related to the architecture of the Suez Canal fishes entering the Mediterranean Sea (so-called ‘Lessep- since until the 1970s only species with a very low mini- sian migration’) were published. The number of new mum depth were recorded to have entered the Mediterra- records of Lessepsian fishes remained more or less constant nean, but species occurring in deeper water started to immi- between 1920 and 2000 but increased dramatically after grate after 1980 when the canal was deepened to 19.5 m. that. The accelerated rate of entry was attributed by many The establishment success of Lessepsian fishes was signifi- authors to an increase in the Mediterranean surface water cantly linked to size and spawning type. Benthic spawners temperature. However, the Suez Canal has been repeat- and species with adhesive eggs represent successful colo- edly deepened and widened during the last decades and the nizers. Moreover, successful colonizers are species with a increased immigration rate of Red Sea fishes might also be tendency to form schools, whereas solitary species are less related to reduced dispersal barriers. We analyse the rela- successful. The results show that dispersal and establish- tionship between dispersal and establishment success and ment success of Lessepsian fish immigrants are influenced a pool of different traits for 101 Lessepsian fish species by different ecological traits. using generalized linear models. Our models did not reveal a significant relationship between the sea surface tempera- ture in the native range of immigrant fishes and their dis- Introduction persal or establishment success in the Mediterranean Sea. The minimum depth in which a species was observed was The construction of canals bridges natural barriers to the distribution of aquatic organisms. It allows aquatic organ- Responsible Editor: M. Peck. isms to spread to new geographical areas and often results in important changes to the newly colonized ecosystems and Reviewed by undisclosed experts. their species assemblages (Leppäkoski et al. 2002; Gollasch et al. 2006; Nentwig 2007). This type of human mediated Electronic supplementary material The online version of this invasion has been frequently observed for freshwater canals. article (doi:10.1007/s00227-015-2744-3) contains supplementary material, which is available to authorized users. A well-known example is the Rhine-Main-Danube Canal, connecting not only the catchments of two of the largest * Erik Arndt European rivers but also the Black Sea with the North Sea. [email protected]‑anhalt.de This canal caused one of the most extensive invasion pro- Patrick J. Schembri cesses known for freshwater systems (Tittizer et al. 2000) [email protected] and resulted in severe ecological problems (Haas 2002; 1 Department 1, Anhalt University of Applied Sciences, Leppäkoski et al. 2002; Nentwig 2007). The canals of the Strenzfelder Allee 28, 06406 Bernburg, Germany ‘Chicago Waterway System’ in North America, connecting 2 Department of Biology, University of Malta, Msida the Great Lakes with the Mississippi catchment, had similar MSD 2080, Malta important impacts (Brammeier et al. 2008). 1 3 2142 Mar Biol (2015) 162:2141–2153 Fig. 1 Mean annual immigra- tion rate per decade (except for 1867–1869 and 2010–2014) of Indo-Pacific fish species, sea surface temperature (Celsius) of the Mediterranean Sea (SST) and depth of the Suez Canal (in metres) at various times In the marine realm, beside the Panama canal, one canal declined to approximate that of the Red Sea and the in particular has been of overwhelming importance for physical and physiological barriers to the entry of fish the spread of organisms from one sea to another and thus from the Gulf of Suez were largely removed such that for bringing about profound changes to the ecology of the salinity of the canal no longer hindered successful the affected ecosystems and their species: the Suez Canal immigration into the Mediterranean Sea (Belmaker et al. (Golani 1998; Galil 2006; Rilov and Galil 2009). The 2013). The number of Lessepsian fish species increased importance of this canal has not only been limited to ecol- steadily in the decades following the 1920s but acceler- ogy and biogeography. Because several Indo-Pacific fish ated dramatically after the year 2000 (Fig. 1) and num- species that have immigrated to the Mediterranean Sea are bered 101 species in 2014 (see Table in Supplementary now present at high abundances and are extensively fished, material). this canal has had a considerable influence on the fisheries The accelerating influx of Lessepsian fish species in of the region, and thus on the economy as well (Rilov and the Mediterranean Sea has been the subject of several Galil 2009; EastMed 2010). papers. Most authors invoke climate change and increas- Just over 30 years from the opening of the Suez Canal ing Mediterranean water temperatures as the chief cause in 1869, Tillier (1902) reported Atherinomorus forska- of the increasing numbers of non-indigenous fish species lii from Alexandria (Egypt) and Liza carinata as well being recorded from the Mediterranean since the 1980s as other species from the vicinity of Port Said. Unfortu- (Ben-Tuvia and Golani 1996; Pallaoro and Dulcˇić 2001; nately the exact date of when the first fishes entered the Despalatović et al. 2008). Azzurro (2008) reports a north- Mediterranean is not known, but the reports by Tillier wards shift in the distribution of 51 thermophilic fish spe- (1902) and Norman (1929) imply that these fishes could cies in the Mediterranean Sea, 11 of which are of Indo- have arrived in the Mediterranean much earlier than Pacific origin. If the Mediterranean continues to warm at 1902. At the time, the canal was about 8 m deep and the the present rate, Ben Rais Lasram and Mouillot (2009), ‘Bitter Lakes’ that were incorporated in its route (Small Ben Rais Lasram et al. (2010) and Raitsos et al. (2010) Bitter Lake, Great Bitter Lake, Lake Timsah and Lake expect an increasing immigration of sub-tropical and tropi- Manzala) and were still hypersaline. It was only in the cal Lessepsian species. 1920s after the canal was deepened to 11 m, that a fur- However, the accelerating number of Lessepsian immi- ther influx of Lessepsian species was reported from the grants is not only associated with the increasing water Mediterranean coasts of Israel and Egypt (Steinitz 1927; temperature but is also influenced by changes in the canal Norman 1927, 1929). With further enlargement of the architecture (i.e., depth, width, profile) and the more bal- canal in 1956 (14.0 m), 1980 (19.5 m), 2001 (22.5 m) anced salinity relative to original conditions. Altering the and, most recently, in 2010 (24 m), its depth is now three architecture of the canal, and therefore altering also the times, and the bottom width five and a half times, that of current patterns, may enable the immigration and disper- the original construction (Galil 2006; Suez Canal Author- sal of species which were not able to overcome the barriers ity 2015). The salinity of the ‘Bitter Lakes’ gradually presented by the canal in the past. Therefore, temperature 1 3 Mar Biol (2015) 162:2141–2153 2143 preference is not the only or even the most important factor Materials and methods for the success of Lessepsian fish species. Trait-based approaches allow a more detailed evaluation All 101 Lessepsian fish species reported until October of the characteristics of immigrating fish species, especially 2014 were included in the analysis (see Table in Supple- if they consider not only one species or a species group but mentary material). Sources for this data set are Golani and all available information. Up to now, only a couple of stud- Appelbaum-Golani (2010a) and references cited therein as ies including data on all Lessepsian species have been pub- the fundamental database, and additionally Akamca et al. lished. Golani (1993) focussed on habitat-related traits of 2011; Bariche 2010a, b, 2011, 2012; Bariche and Azzurro Red Sea fishes and concluded that dominance in the equiva- 2012; Bariche and Heemstra 2012; Bariche et al. 2013; lent source habitat is a key contributor to successful coloni- Bilecenoğlu 2012; Çiçek and Bilecenoğlu 2009; Dalyan zation of the Eastern Mediterranean. Ben Rais Lasram et al. et al. 2012; Fricke et al. 2012; Golani and Appelbaum- (2008) examined several ecological characters of Lessep- Golani 2010b; Golani et al.