Biological Invasions

, Volume 18, Issue 10, pp 2761–2772 | Cite as

Lag times in Lessepsian fish invasion

  • E. Azzurro
  • F. Maynou
  • J. Belmaker
  • D. Golani
  • J. A. Crooks
Perpectives and paradigms


Insight from theory has shown the usefulness of considering time lags in both plant and animal invasions, but this topic has yet to be fully explored with real examples. Here we define and investigate several types of lags using Red Sea fish invasions of the Mediterranean as a case study. By exploring both conceptual and analytical aspects of time lags, we suggest that this concept can be applied to both the ecology and management of invasions. Through the review of available literature and by compiling a comprehensive geo-referenced database, we show that our understanding of the temporal nature of invasion can be confounded by our varying capability to perceive it. This deep, sometimes inextricable, connection between the temporal nature of a process and its observation represents a critical issue for our understanding of the Lessepsian phenomenon, and is a challenge for invasion biology more generally. While our case study is associated with a very specific date in which the Suez Canal opened, our framework is expected to broaden the notion of time lags in bioinvasions research.


Red Sea Mediterranean Fish Time lags Detection Monitoring 

Supplementary material

10530_2016_1184_MOESM1_ESM.docx (288 kb)
Supplementary material 1 (DOCX 288 kb)


  1. Aagaard K, Lockwood J (2014) Exotic birds show lags in population growth. Divers Distrib 20:547–554CrossRefGoogle Scholar
  2. Akyol O, Ünal V, Ceyhan T, Bilecenoglu M (2005) First confirmed record of the silverside blaasop, Lagocephalus sceleratus (Gmelin, 1789), in the Mediterranean Sea. J Fish Biol 66:1183–1186CrossRefGoogle Scholar
  3. Azzurro E, Soto S, Garofalo G, Maynou F (2012) Fistularia commersonii in the Mediterranean Sea: invasion history and distribution modeling based on presence-only records. Biol Invasions 15:977–990CrossRefGoogle Scholar
  4. Azzurro E, Soto S, Bariche M, Fanelli E, Maynou F (2013) Exotic fish species in the Mediterranean Sea: analysis of occurrence records. Rapp Comm Int Mer Médit 40:598Google Scholar
  5. Azzurro E, Tuset VM, Lombarte A, Maynou F, Simberloff D, Rodríguez-Pérez A, Solé RV (2014) External morphology explains the success of biological invasions. Ecol Lett 17:1455–1463CrossRefPubMedGoogle Scholar
  6. Azzurro E, Goren M, Diamant A, Galil B, Bernardi G (2015) Establishing the identity and assessing the dynamics of invasion in the Mediterranean Sea by the dusky sweeper, Pempheris rhomboidea Kossmann & Räuber, 1877 (Pempheridae, Perciformes). Biol Invasions 17:815–826CrossRefGoogle Scholar
  7. Barbour AB, Allen MS, Frazer TK, Sherman KD (2011) Evaluating the potential efficacy of invasive lionfish (Pterois volitans) removals. PLoS ONE 6(5):e19666CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bariche M, Kazanjian G, Azzurro E (2013) A lag of 25 years: evidence from an old capture of Fistularia commersonii Rüppell, 1838 from Lebanon (Mediterranean Sea). J Appl Ichthyol 3:535–536Google Scholar
  9. Bellard C, Genovesi P, Jeschke JM (2016) Global patterns in threats to vertebrates by biological invasions. Proc R Soc B 283:20152454. doi: 10.1098/rspb.2015.2454 CrossRefPubMedGoogle Scholar
  10. Belmaker J, Brokovich E, China V, Golani D, Kiflawi M (2009) Estimating the rate of biological introductions. Ecology 90:1134–1141CrossRefPubMedGoogle Scholar
  11. Belmaker J, Brokovich E, China V, Golani D, Kiflawi M (2010) Introduction rates of Lessepsian fishes in the Mediterranean. In: Golani D, Applebaum-Golani B (eds) Fish invasions of the Mediterranean Sea, change and renewal. Pensoft, Sofia, pp 35–56Google Scholar
  12. Ben Rais Lasram F, Guilhaumon F, Mouillot D (2010) Global warming and exotic fishes in the Mediterranean Sea: introduction dynamic, range expansion and spatial congruence with endemic species. In: Golani D, Applebaum-Golani B (eds) Fish invasions of the Mediterranean Sea, change and renewal. Pensoft, Sofia, pp 35–56Google Scholar
  13. Ben-Souissi J, Rifi M, Ghanem R, Ghozzi L, Boughedir W, Azzurro E (2014) Lagocephalus sceleratus (Gmelin, 1789) expands through the African coasts towards the Western Mediterranean Sea: a call for awareness. Manag Biol Invasions 5:357–362CrossRefGoogle Scholar
  14. Ben-Tuvia A (1978) Immigration of fishes through the Suez Canal. Fishery Bull 76:249–255Google Scholar
  15. Bernardi G, Azzurro E, Golani D, Miller M (2016) Genomic signatures of rapid adaptive evolution in the bluespotted cornetfish, a Mediterranean Lessepsian invader. Mol Ecol. doi: 10.1111/mec.13682 Google Scholar
  16. Bilecenoglu M (2010) Alien marine fishes of Turkey-an updated review. In: Golani D, Applebaum-Golani B (eds) Fish invasions of the Mediterranean Sea, change and renewal. Pensoft, Sofia, pp 189–217Google Scholar
  17. Bilecenoglu M, Russell BC (2008) Record of Nemipterus randalli Russell, 1986 (Nemipteridae) from Iskenderun Bay, Turkey. Cybium 32:279–280Google Scholar
  18. Blackburn TM, Pisek P, Bacher S, Bacher S, Carlton JT, Duncan RP, Jarosik V, Wilson JRU, Richardson D (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26:333–339CrossRefPubMedGoogle Scholar
  19. Costello CJ, Solow AR (2003) On the pattern of discovery of introduced species. Proc Natl Acad Sci 100:3321–3323CrossRefPubMedPubMedCentralGoogle Scholar
  20. Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12:316–329CrossRefGoogle Scholar
  21. Crooks JA (2011) Lag times. In: Simberloff D, Rejmánek M (eds) Encyclopedia of Biological invasions. University of California Press, Oakland, pp 404–410Google Scholar
  22. Daehler CC (2009) Short lag times for invasive tropical plants: evidence from experimental plantings in Hawai’i. PLoS ONE 4(2):e4462CrossRefPubMedPubMedCentralGoogle Scholar
  23. Essl F, Dullinger S, Rabitsch W, Hulme PE, Hülber K et al (2011) Socioeconomic legacy yields an invasion debt. Proc Natl Acad Sci 108:203–207CrossRefPubMedGoogle Scholar
  24. Fricke R, Golani D, Appelbaum-Golani B (2012) First record of the Indian Ocean anchovy Stolephorus insularis Hardenberg, 1933 (Clupeiformes: Engraulidae) in the Mediterranean. BioInvasions Rec 1(4):303–306CrossRefGoogle Scholar
  25. Galil BS (2006) The marine caravan – the Suez Canal and Erythrean invasion. In: Gollasch S, Galil BS, Cohen AN (eds) Bridging divides. Maritime canals as invasion corridors. Springer, Dordrecht, pp 207–300Google Scholar
  26. Galil B (2009) Taking stock: inventory of alien species in the Mediterranean sea. Biol Invasions 11:359–372CrossRefGoogle Scholar
  27. Galil BS, Boero F, Campbell ML, Carlton JT, Cook E, Fraschetti S et al (2015) ‘Double trouble’: the expansion of the Suez Canal and marine bioinvasions in the Mediterranean Sea. Biol Invasions 17:973–976CrossRefGoogle Scholar
  28. Genovesi P, Scalera R, Brunel S, Roy D, Solarz W (2010) Towards an early warning and information system for invasive alien species (IAS) threatening biodiversity in Europe. EEA, Technical Report 5:1–49Google Scholar
  29. Golani D (2000) The Lessepsian migrant, the Red-eye Round Herring, Etremeus teres (DeKay, 1842), a new record from Cyprus. Zool Middle East 20:61–64CrossRefGoogle Scholar
  30. 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 reneval. Pensoft Publishers, Sofia, pp 145–188Google Scholar
  31. Golani D, Ben-Tuvia A (1985) The biology of the Indo-Pacific squirrelfish, Sargocentron rubrum (Forsskål), a Suez Canal migrant to the eastern Mediterranean. J Fish Biol 27:249–258CrossRefGoogle Scholar
  32. Golani D, Massutí E, Orsi-Relini L, Quignard JP, Dulčić J, Azzurro E. (2013) CIESM atlas of exotic fish species. Accessed 28 June 2015
  33. Golani D, Askarov G, Dashevsky Y (2015) First record of the Red Sea spotted grouper, Epinephelus geoffroyi (Klunzinger, 1870) (Serranidae) in the Mediterranean. BioInvasion Records 2:143–145CrossRefGoogle Scholar
  34. Jørgensen C, Myron E, Peck A, Antognarelli F, Azzurro E et al. (2012) Conservation physiology of marine fishes: advancing the predictive capacity of models. Biol Lett. 8: 900–903. rsbl20120609Google Scholar
  35. Larkin DJ (2012) Lengths and correlates of lag phases in upper-Midwest plant invasions. Biol Invasions 14:827–838CrossRefGoogle Scholar
  36. Le Maitre DC, Richardson DM, Chapman RA (2004) Conservation Physiology of Marine Fishes: advancing the predictive capacity: working for water. S Afr J Sci 100:103–112Google Scholar
  37. Lelli S, Colloca F, Carpentieri P, Russell BC (2008) The threadfin bream Nemipterus randalli Russell, 1986 (Perciformes; Nemipteridae) in the eastern Mediterranean Sea. J Fish Biol 60:1326–1330Google Scholar
  38. Macias D, Garcia-Gorriz E, Stips A (2013) Understanding the causes of recent warming of Mediterranean waters. How much could be attributed to climate change? PLoS ONE 8(11):e81591CrossRefPubMedPubMedCentralGoogle Scholar
  39. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710CrossRefGoogle Scholar
  40. Marras S, Cucco A, Antognarelli F, Azzurro E, Milazzo M, Bariche M, Butenschön M, Kay S, Di Bitetto M, Quattrocchi G, Sinerchia M, Domenici P (2015) Predicting future thermal habitat suitability of competing native and invasive fish species: from metabolic scope to oceanographic modelling. Cons Physiol 3.1:cou059. doi: 10.1093/conphys/cou059 CrossRefGoogle Scholar
  41. McNeely JA (ed) (2001) The great reshuffling: human dimensions of invasive alien species. Gland, Switz./Cambridge, UK: IUCNGoogle Scholar
  42. Parravicini V, Azzurro E, Kulbicki M, Belmaker J (2015) Niche shift can impair the ability to predict invasion risk in the marine realm: an illustration using Mediterranean fish invaders. Ecol Lett 18:246–253CrossRefPubMedGoogle Scholar
  43. Por FD (1971) One hundred years of Suez Canal: a century of Lessepsian migration. Syst Zool 20:138–159CrossRefGoogle Scholar
  44. Raitsos DE, Beaugrand G, Georgopoulos D, Zenetos A, Pancucci-Papadopoulou AM, Theocharis A, Papathanassiou E (2010) Global climate change amplifies the entry of tropical species into the Eastern Mediterranean Sea. Limn Ocean 55:1478–1484CrossRefGoogle Scholar
  45. Ricciardi A (2013) Invasive species. In: Leemans R (ed) Ecological systems. Springer, New York, pp 161–178CrossRefGoogle Scholar
  46. Rilov G, Benayahu Y, Gasith A (2004) Prolonged lag in population outbreak of an invasive mussel: a shifting-habitat model. Biol Invasions 6:347–364CrossRefGoogle Scholar
  47. Russell BC, Golani D, Tikochinski Y (2015) Saurida lessepsianus a new species of lizardfish (Pisces: Synodontidae) from the Red Sea and Mediterranean Sea, with a key to Saurida species in the Red Sea. Zootaxa 3956:559–568CrossRefPubMedGoogle Scholar
  48. Simberloff D, Rejmánek M (eds) (2010) Encyclopedia of biological invasions, vol 3. University of California Press, OaklandGoogle Scholar
  49. Solow AR, Costello CJ (2004) Estimating the rate of species introductions from the discovery record. Ecology 85:1822–1825CrossRefGoogle Scholar
  50. Spanier E (2000) Changes in the ichthyofauna of an artificial reef in the southeastern Mediterranean in one decade. Sci Mar 64:279–284CrossRefGoogle Scholar
  51. Steinitz W (1927) Beitrage zur Kenntnis der Küstenfauna Palästinas. Pubblicazioni della Stazione Zoologica di Napoli 8:311–353Google Scholar
  52. Tillier JE (1902) Le Canal de Suez et sa faune ichthylogique. Mémoires de la Société zoologique de France 15:279–318Google Scholar
  53. Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distrib 14:569–580CrossRefGoogle Scholar
  54. Witte S, Buschbaum C, Van Beusekom JE, Reise K (2010) Does climatic warming explain why an introduced barnacle finally takes over after a lag of more than 50 years? Biol Invasions 12:3579–3589CrossRefGoogle Scholar
  55. Zalasiewic J, Williams M, Steffen W, Crutzen P (2010) The new world of the Anthropocene. Environ Sci Technol 44:2228–2231CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • E. Azzurro
    • 1
  • F. Maynou
    • 2
  • J. Belmaker
    • 3
  • D. Golani
    • 4
  • J. A. Crooks
    • 5
  1. 1.ISPRA, Institute for Environmental Protection and ResearchLeghornItaly
  2. 2.Institut de Ciències del Mar (CSIC)BarcelonaSpain
  3. 3.Department of Zoology, George S. Wise Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael
  4. 4.Department of Evolution, Systematics and EcologyThe Hebrew University of JerusalemJerusalemIsrael
  5. 5.Tijuana River National Estuarine Research ReserveSouthwest Wetlands Interpretive AssociationImperial BeachUSA

Personalised recommendations