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Invading up the food web? Invasive fish in the southeastern Mediterranean Sea

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Abstract

The invasion of Indo-Pacific fish through the Suez Canal has dramatically altered the diversity of fish assemblages on the upper shelf of the southeastern Mediterranean. Yet, their role in the trophodynamics of the novel assemblages has been largely overlooked. In the present study, we investigated the impacts of the alien fish species on the structure of the food web along the Israeli upper shelf soft bottoms, as expressed by their biomass relative abundance, and by comparing the mean and distribution patterns of the trophic levels among the aliens and the local native species. Our study, based on examination of more than 200,000 fishes belonging to 111 species, revealed that at 20-m alien species comprised 54 % of all sampled individuals while comprising 70 % of the biomass; at 40 the alien species comprised 67 % of all sampled individuals and 45 % of the biomass. Overall, the mean weighted trophic level of the aliens was 3.74, while that of the natives was 3.39. Depth was found as an important factor affecting the trophic levels of both native and alien species. At a depth of 20 m, the combined mean weighted trophic level (natives + aliens) was slightly higher than at 40 m (3.61 and 3.56, respectively), although depth impact differed between aliens and natives. Between a depth of 20 and 40 m, the mean weighted trophic level of aliens increased from 3.65 to 3.85, while that of the natives decreased from 3.54 to 3.33. These findings indicate that the local food webs have gone through significant modification, with a trend of increasing dominance of alien fish.

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References

  • Andaloro F, Pipitone C (1997) Food and feeding habits of the amberjack, Seriola dumerili in the Central Mediterranean Sea during the spawning season. Cah Biol Mar 38:91–96

    Google Scholar 

  • Bakhoum SA (2007) Diet overlap of immigrant narrow–barred Spanish mackerel Scomberomorus commerson (Lac., 1802) and the largehead hairtail ribbonfish Trichiurus lepturus (L., 1758) in the Egyptian Mediterranean coast. Anim Biodivers Conserv 30(2):147–160

    Google Scholar 

  • Bariche M, Alwan N, El Assi H, Zurayk R (2009) Diet composition of the lessepsian bluespotted cornetfish Fistularia commersonii in the eastern Mediterranean. J Appl Ichthyol 25(4):460–465

    Article  Google Scholar 

  • Bilecenoğlu M (2016) Demersal Lessepsian fish assemblage structure in the northern Levant and Aegean Seas. J Black Sea Mediterr Env 22(1):46–59

    Google Scholar 

  • Bozec Y, Kulbicki M, Chassot E, Gascuel D (2005) Trophic signature of coral reef fish assemblages: towards a potential indicator of ecosystem disturbance. Aquat Living Resour 18(2):103–109

    Article  Google Scholar 

  • Branch TA, Watson R, Fulton EA, Jennings S, McGilliard CR, Pablico GT, Ricard D, Tracey SR (2010) The trophic fingerprint of marine fisheries. Nature 468(7322):431–435

    Article  CAS  Google Scholar 

  • Chavez FP, Ryan J, Lluch-Cota SE, Niquen CM (2003) From anchovies to sardines and back: multidecadal change in the pacific ocean. Science 299(5604):217–221

    Article  CAS  Google Scholar 

  • Christensen V, Guenette S, Heymans JJ, Walters CJ, Watson R, Zeller D, Pauly D (2003) Hundred year decline of North Atlantic predatory fishes. Fish Fish 4(1):1–24

    Article  Google Scholar 

  • Coll M, Lotze HK, Romanuk TN (2008) Structural degradation in Mediterranean Sea food webs: testing ecological hypotheses using stochastic and mass-balance modelling. Ecosystems 11(6):939–960

    Article  Google Scholar 

  • de Ruiter PC, Neutel AM, Moore JC (1995) Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 269:1257–1260

    Article  Google Scholar 

  • Edelist D, Sonin O, Golani D, Rilov G, Spanier E (2011) Spatiotemporal patterns of catch and discards of the Israeli Mediterranean trawl fishery in the early 1990s: ecological and conservation perspectives. Sci Mar 75(4):641–652

    Article  Google Scholar 

  • Edelist D, Rilov G, Golani D, Carlton JT, Spanier E (2013) Restructuring the sea: profound shifts in the world’s most invaded marine ecosystem. Divers Distrib 19(1):69–77

    Article  Google Scholar 

  • El-Maremie H, El-Mor M (2015) Feeding habits of the Bogue, Boops boops (Linnaeus, 1758) (Teleostei: Sparidae) in Benghazi Coast, Eastern Libya. J Life Sci 9:189–196

    Google Scholar 

  • Fanelli E, Badalamenti F, D’anna G, Pipitone C, Riginella E, Azzurro E (2011) Food partitioning and diet temporal variation in two coexisting sparids, Pagellus erythrinus and Pagellus acarne. J Fish Biol 78(3):869–900

    Article  CAS  Google Scholar 

  • Fanelli E, Azzurro E, Bariche M, Cartes J, Maynou F (2015) Depicting the novel eastern Mediterranean food web: a stable isotopes study following lessepsian fish invasion. Biol Invasions 1–16

  • Froese R, Pauly D (2016) Fishbase. World wide web electronic publication. http://www.fishbase.org. Accessed 22 March 2016

  • Froese R, Garthe S, Piatkowski U, Pauly D (2004) Trophic signatures of marine organisms in the Mediterranean as compared with other ecosystems. Belg J Zool 134:31–36

    Google Scholar 

  • Galil BS, Goren M (2014) Metamorphoses: bioinvasions in the Mediterranean sea. In: Stefano G, Zvi D (eds) The Mediterranean sea: its history and present challenges. Springer, Berlin, p 463

    Chapter  Google Scholar 

  • Galil BS, Marchini A, Occhipinti-Ambrogi A (2016) East is East and west is west? Management of marine bioinvasions in the Mediterranean Sea. Estuar Coast Mar Sci. doi:10.1016/j.ecss.2015.12.021

    Google Scholar 

  • Gertman I, Goldman R, Lunin I, Krivenko E, Ozer T, Katsnelson B (2013) ISRAMAR report for 2012. Israel Marine data: 1–30 Center. Accessed 10 Oct 2015

  • Gilaad R-L (2011) Resource utilization by Indigenous and Migrant fish species in the Eastern Mediterranean. M.Sc. Thesis, Tel Aviv University (in Hebrew)

  • Golani D (1993) The biology of the Red Sea migrant, Saurida undosquamis in the Mediterranean and comparison with the indigenous confamilial Synodus saurus (teleostei: Synodontidae). Hydrobiologia 271(2):109–117

    Article  Google Scholar 

  • Golani D (1994) Niche separation between colonizing and indigenous goatfish (Mullidae) along the Mediterranean coast of Israel. J Fish Biol 45(3):503–513

    Article  Google Scholar 

  • Golani D (2010) Colonization of the Mediterranean by Red Sea fishes via the Suez Canal-Lessepsian migration. In: Golani D, Appelbaum-Golani B (eds) Fish invasions of the Mediterranean Sea: change and renewal. Pensoft Publishers, Sofia-Moscow, pp 145–188

    Google Scholar 

  • Golani D, Ben-Tuvia A (1995) Lessepsian migration and the Mediterranean fisheries of Israel. In: Armantrout NB (ed) Condition of the world’s aquatic habitats. Science Publishers, New Hampshire, pp 279–289

    Google Scholar 

  • Golani D, Galil B (1991) Trophic relationships of colonizing and indigenous goatfishes (Mullidae) in the eastern Mediterranean with special emphasis on decapod crustaceans. Hydrobiologia 218(1):27–33

    Article  Google Scholar 

  • Golani D, Ben-Tuvia A, Galil B (1983) Feeding habits of the Suez Canal migrant squirrelfish, Sargocentron rubrum, in the Mediterranean Sea. Isr J Zool 32(4):194–204

    Google Scholar 

  • Goren M, Galil B (2005) A review of changes in the fish assemblages of Levantine inland and marine ecosystems following the introduction of non-native fishes. J Appl Ichthyol 21(4):364–370

    Article  Google Scholar 

  • Hamida NBH, Hamida OBABH, Jarboui O, Missaoui H (2015) Diet composition and feeding habits of Lithognathus mormyrus (Sparidae) from the Gulf of Gabes (Central Mediterranean). J Mar Biol Assoc UK 1–8‏

  • Kallianiotis A, Torre M, Argyri A (2005) Age, growth, mortality, reproduction, and feeding habits of the striped seabream, Lithognathus mormyrus L. (Pisces, Sparidae) in the coastal waters of the Thracian Sea, Greece. Sci Mar 69(3):391–404

    Article  Google Scholar 

  • Kalogirou S, Corsini M, Kondilatos G, Wennhage H (2007) Diet of the invasive piscivorous fish Fistularia commersonii in a recently colonized area of the eastern Mediterranean. Biol Invasions 9(8):887–896

    Article  Google Scholar 

  • Karachle P, Stergiou K (2008) The effect of season and sex on trophic levels of marine fishes. J Fish Biol 72(6):1463–1487

    Article  Google Scholar 

  • Lassalle G, Gascuel D, Le Loc’h F, Lobry J, Pierce GJ, Ridoux V, Santos MB, Spitz J, Niquil N (2012) An ecosystem approach for the assessment of fisheries impacts on marine top predators: the Bay of Biscay case study. ICES J Mar Sci 96(6):925–938

    Article  Google Scholar 

  • Laurans M, Gascuel D, Chassot E, Thiam D (2004) Changes in the trophic structure of fish demersal communities in west Africa in the three last decades. Aquat Living Resour 17(02):163–173

    Article  Google Scholar 

  • Levitt Y (2012) The impact of depth gradient on the status of alien species along the Mediterranean sea coast of Israel. M.Sc. Thesis, Tel Aviv University (in Hebrew)

  • Lotze HK, Coll M, Dunne JA (2011) Historical changes in marine resources, food-web structure and ecosystem functioning in the Adriatic sea, Mediterranean. Ecosystems 14(2):198–222

    Article  Google Scholar 

  • Lundberg B, Ogorek R, Galil BS, Goren M (2004) Dietary choices of siganid fish at Shiqmona reef, Israel. Isr J Zool 50(1):39–53

    Article  Google Scholar 

  • Neutel AM, Heesterbeek JA, de Ruiter PC, de Ruiter PC (2002) Stability in real food webs: weak links in long loops. Science 296(5570):1120–1123‏

    Article  CAS  Google Scholar 

  • Neutel AM, Heesterbeek JA, van de Koppel J, Hoenderboom G, Vos A, Kaldeway C, de Ruiter PC (2007) Reconciling complexity with stability in naturally assembling food webs. Nature 449(7162):599–602‏

    Article  CAS  Google Scholar 

  • Pauly D, Christensen V (1995) Primary production required to sustain global fisheries. Nature 374(6519):255–257

    Article  CAS  Google Scholar 

  • Pauly D, Palomares M (2005) Fishing down marine food web: it is far more pervasive than we thought. Bull Mar Sci 76(2):197–212

    Google Scholar 

  • Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F Jr (1998) Fishing down marine food webs. Science 279(5352):860–863

    Article  CAS  Google Scholar 

  • Pinnegar JK, Jennings S, O’brien CM, Polunin NVC (2002) Long term changes in the trophic level of the celtic sea fish community and fish market price distribution. J Appl Ichthyol 39(3):377–390

    Google Scholar 

  • Saad AA, Sabour WG (2010) Impact of invasive species on the biodiversity and fish stock; case study: Fistularia commersonii Rüppell, in the Syrian coast. Rapp Comm Int Mer Medit 39:652

    Google Scholar 

  • Sethi SA, Branch TA, Watson R (2010) Global fishery development patterns are driven by profit but not trophic level. Proc Natl Acad Sci USA 107(27):12163–12167

    Article  CAS  Google Scholar 

  • Shapiro J (2008) The fishery and aquaculture of Israel 2007. The State of Israel, Ministry of Agriculture, Department of Fisheries, Tveria, Israel (in Hebrew)

  • Snovsky G, Shapiro J (2001) The fishery and aquaculture of Israel 2000. The State of Israel, Ministry of Agriculture, Department of Fisheries, Tveria, Israel (in Hebrew)

  • Snovsky G, Shapiro J, Zohar G (2002) The fishery and aquaculture of Israel 2001. The State of Israel, Ministry of Agriculture, Department of Fisheries, Tveria, Israel (in Hebrew)

  • Stergiou KI, Karpouzi VS (2002) Feeding habits and trophic levels of Mediterranean fish. Rev Fish Biol Fish 11(3):217–254

    Article  Google Scholar 

  • Stergiou KI, Moutopoulos DK, Hernando J, Erzini K (2007) Trophic signatures of small-scale fishing gears: implications for conservation and management. Mar Ecol Prog Ser 333:117–128

    Article  Google Scholar 

  • Stern N (2010) The impact of invasive species on the soft-bottom fish communities in the eastern Mediterranean. M.Sc. Thesis, Tel Aviv University (in Hebrew)

  • Tecchio S, Coll M, Christensen V, Company JB, Ramirez-Llodra E, Sarda F (2013) Food web structure and vulnerability of a deep-sea ecosystem in the NW Mediterranean sea. Deep Sea Res PT I Oceanogr Res Pap 75:1–15

    Article  Google Scholar 

  • Tsikliras AC, Stergiou KI, Adamopoulos N, Pauly D, Mente E (2014) Shift in trophic level of Mediterranean mariculture species. Conserv Biol 28(4):1124–1128

    Article  Google Scholar 

  • Valero-Rodriguez JM, Toledo-Guedes K, Arechavala-Lopez P, Izquierdo-Gomez D, Sanchez-Jerez P (2015) The use of trophic resources by Argyrosomus regius (Asso, 1801) escaped from Mediterranean offshore fish farms. J Appl Ichthyol 31(1):10–15‏

    Article  Google Scholar 

  • Williams RJ, Martinez ND (2004) Limits to trophic levels and omnivory in complex food webs: theory and data. Am Nat 163(3):458–468

    Article  Google Scholar 

  • Yokeş MB, Goren M, Karhan SÜ, Demir V, Kalkan E, Galil BS, Diamant A (2010) Rapid expansion of recently introduced species populations off the Mediterranean coast of Turkey. Rapp P V Réun Comm Int Explor Sci Mer Méditerr 39:701

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Acknowledgments

The authors are deeply grateful to Captain Levi Ornoy, who ably ran the trawler ‘Moti’; thanks to N. Paz for editing the manuscript and I. Goren for helping with the statistical analysis. This research was funded by the Porter School of Environmental Studies, Tel Aviv University, through funding from the Italian Ministry of the Environment, Land and Sea, R&D Project (2008) (received by M.G., B.S.G. and A.D.) and by the Israel Taxonomy Initiative (2010) (received by M.G.).

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Correspondence to Menachem Goren.

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Goren, M., Galil, B.S., Diamant, A. et al. Invading up the food web? Invasive fish in the southeastern Mediterranean Sea. Mar Biol 163, 180 (2016). https://doi.org/10.1007/s00227-016-2950-7

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