, Volume 822, Issue 1, pp 229–235 | Cite as

Eastern spread of the invasive Artemia franciscana in the Mediterranean Basin, with the first record from the Balkan Peninsula

  • Zsófia Horváth
  • Christophe Lejeusne
  • Francisco Amat
  • Javier Sánchez-Fontenla
  • Csaba F. Vad
  • Andy J. Green
Primary Research Paper


In the last 30 years since its first appearance in Portugal, the North-American Artemia franciscana has successfully invaded hypersaline habitats in several Mediterranean countries. Here, we review its spread in the Mediterranean Basin since its first occurrence in the 1980s and report its first occurrence in Croatia, based on both morphological identification (adults) and genetic evidence (cysts). The haplotypes we found in the population from this new locality (two of which were new to both the native and invaded ranges of A. franciscana) suggest either direct or secondary introduction from the main harvested cyst sources (Great Salt Lake or San Francisco Bay, USA) and indicate that some genetic native diversity in the species has not yet been captured by existing studies. Our finding means that the species has reached the eastern shores of the Adriatic Sea and therefore is now present on the Balkan Peninsula. We detected that its eastward spread is still continuing, posing a fundamental threat to remaining populations of native Artemia species in Eastern Europe, which highlights the need for preventive measures.


Invasive species Artemia franciscana Salt works Mediterranean 



The molecular analyses were funded by the Ministerio de Ciencia e Innovación (Proyecto CGL2010-16028) and the CSIC (PIC2015FR4) in Spain, and the CNRS-funded PICS program (PICS07360) in France. The authors thank the staff of Solana Nin for granting access to the sites.

Supplementary material

10750_2018_3683_MOESM1_ESM.docx (43 kb)
Supplementary material 1 (DOCX 44 kb)


  1. Abatzopoulos, T. J., C. D. Triantaphyllidis & C. D. Kastritsis, 1987. Preliminary studies on some Artemia populations from northern Greece. Artemia Research and Its Applications 1: 107–114.Google Scholar
  2. Amat, F., F. Hontoria, O. Ruiz, A. J. Green, M. I. Sanchez, J. Figuerola & F. Hortas, 2005. The American brine shrimp as an exotic invasive species in the western Mediterranean. Biological Invasions 7: 37–47.CrossRefGoogle Scholar
  3. Amat, F., F. Hontoria, J. C. Navarro, N. Vieira & G. Mura, 2007. Biodiversity loss in the genus Artemia in the Western Mediterranean Region. Limnetica 26: 387–404.Google Scholar
  4. Ben Naceur, H., A. B. R. Jenhani & M. S. Romdhane, 2010. Biological characterization of the new invasive brine shrimp Artemia franciscana in Tunisia: Sabkhet Halk El-Menzel. International Journal of Biology and Life Sciences 6: 3.Google Scholar
  5. Browne, R. A. & K. M. Halanych, 1989. Competition between sexual and parthenogenetic Artemia: a re-evaluation (Branchiopoda, Anostraca). Crustaceana 57: 57–71.CrossRefGoogle Scholar
  6. Clement, M., D. Posada & K. A. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659.CrossRefPubMedGoogle Scholar
  7. Eaton, A. D., L. S. Clesceri, E. W. Rice, A. E. Greenberg & M. A. H. Franson, 2005. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, DCGoogle Scholar
  8. Eimanifar, A., B. Marden, M. S. Braun & M. Wink, 2015. Analysis of the genetic variability of Artemia franciscana Kellogg, 1906 from the Great Salt Lake (USA) based on mtDNA sequences, ISSR genomic fingerprinting and biometry. Marine Biodiversity 45: 311–319.CrossRefGoogle Scholar
  9. Green, A. J., M. I. Sánchez, F. Amat, J. Figuerola, F. Hontoria, O. Ruiz & F. Hortas, 2005. Dispersal of invasive and native brine shrimps Artemia (Anostraca) via waterbirds. Limnology and Oceanography 50: 737–742.CrossRefGoogle Scholar
  10. Hall, T. A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic Acids Symposium Series: 95–98,
  11. Hontoria, F. & F. Amat, 1992. Morphological characterization of adult Artemia (Crustacea, Branchiopoda) from different geographical origins. American populations. Journal of Plankton Research 14: 1461–1471.CrossRefGoogle Scholar
  12. Leigh, J. W. & D. Bryant, 2015. popart: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6: 1110–1116.CrossRefGoogle Scholar
  13. Lejeusne, C., A. Saunier, N. Petit, M. Béguer, M. Otani, J. T. Carlton, C. Rico & A. J. Green, 2014. High genetic diversity and absence of founder effects in a worldwide aquatic invader. Scientific Reports 4: 5808.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Montero-Pau, J., A. Gómez & J. Muñoz, 2008. Application of an inexpensive and high-throughput genomic DNA extraction method for the molecular ecology of zooplanktonic diapausing eggs. Limnology and Oceanography: Methods 6: 218–222.Google Scholar
  15. Moscatello, S., G. Belmonte & G. Mura, 2002. The co-occurrence of Artemia parthenogenetica and Branchinella spinosa (Branchiopoda: Anostraca) in a saline pond of south eastern Italy. Hydrobiologia 486: 201–206.CrossRefGoogle Scholar
  16. Muñoz, J., 2009. Implicaciones de la dispersión actual e histórica para la biología evolutiva y conservación de Artemia y otros invertebrados acuáticos con estadio de diapausa. PhD thesis, Spain.Google Scholar
  17. Muñoz, J. & F. Pacios, 2010. Global biodiversity and geographical distribution of diapausing aquatic invertebrates: the case of the cosmopolitan brine shrimp, Artemia (Branchiopoda, Anostraca). Crustaceana 83: 465.CrossRefGoogle Scholar
  18. Muñoz, J., A. Gómez, A. J. Green, J. Figuerola, F. Amat & C. Rico, 2008. Phylogeography and local endemism of the native Mediterranean brine shrimp Artemia salina (Branchiopoda: Anostraca). Molecular Ecology 17: 3160–3177.CrossRefPubMedGoogle Scholar
  19. Muñoz, J., F. Amat, A. J. Green, J. Figuerola & A. Gómez, 2013. Bird migratory flyways influence the phylogeography of the invasive brine shrimp Artemia franciscana in its native American range. PeerJ: e200.Google Scholar
  20. Muñoz, J., A. Gómez, J. Figuerola, F. Amat, C. Rico & A. J. Green, 2014. Colonization and dispersal patterns of the invasive American brine shrimp Artemia franciscana (Branchiopoda: Anostraca) in the Mediterranean region. Hydrobiologia 726: 25–41.CrossRefGoogle Scholar
  21. Mura, G. & B. Brecciaroli, 2004. Use of morphological characters for species separation within the genus Artemia (Crustacea, Branchiopoda). Hydrobiologia 520: 179–183.CrossRefGoogle Scholar
  22. Mura, G., A. D. Baxevanis, G. M. Lopez, F. Hontoria, I. Kappas, S. Moscatello, G. Fancello, F. Amat & T. J. Abatzopoulos, 2005. The use of a multidisciplinary approach for the characterization of a diploid parthenogenetic Artemia population from Torre Colimena (Apulia, Italy). Journal of Plankton Research 27: 895–907.CrossRefGoogle Scholar
  23. Mura, G., I. Kappas, A. D. Baxevanis, S. Moscatello, Q. D’Amico, G. M. Lopez, F. Hontoria, F. Amat & T. J. Abatzopoulos, 2006. Morphological and molecular data reveal the presence of the invasive Artemia franciscana in Margherita di Savoia salterns (Italy). International Review of Hydrobiology 91: 539–554.CrossRefGoogle Scholar
  24. Petrović, A., 1991. The karyotype of the parthenogenetic Artemia (Crustacea) from Secovlje, Yugoslavia. Genetica 83: 289–291.CrossRefGoogle Scholar
  25. Redón, S., F. Amat, M. I. Sánchez & A. J. Green, 2015. Comparing cestode infections and their consequences for host fitness in two sexual branchiopods: alien Artemia franciscana and native A. salina from syntopic-populations. PeerJ 3: e1073.Google Scholar
  26. Reynolds, C., N. A. Miranda & G. S. Cumming, 2015. The role of waterbirds in the dispersal of aquatic alien and invasive species. Diversity and Distributions 21: 744–754.CrossRefGoogle Scholar
  27. Sánchez, M. I., F. Hortas, J. Figuerola & A. J. Green, 2012. Comparing the potential for dispersal via waterbirds of a native and an invasive brine shrimp. Freshwater Biology 57: 1896–1903.CrossRefGoogle Scholar
  28. Sánchez, M. I., I. Paredes, M. Lebouvier & A. J. Green, 2016. Functional role of native and invasive filter-feeders, and the effect of parasites: learning from hypersaline ecosystems. PloS ONE 11: e0161478.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Sánchez, M. I., M. Mata, F. Hortas & S. Redón, 2017. El último despertar de Artemia: crónica de una extinción anunciada. Quercus 377: 30–38.Google Scholar
  30. Scalone, R. & N. Rabet, 2013. Presence of Artemia franciscana (Branchiopoda, Anostraca) in France: morphological, genetic, and biometric evidence. Aquatic Invasions 8: 67–76.CrossRefGoogle Scholar
  31. Triantaphyllidis, G., T. Abatzopoulos & P. Sorgeloos, 1998. Review of the biogeography of the genus Artemia (Crustacea, Anostraca). Journal of Biogeography 25: 213–226.CrossRefGoogle Scholar
  32. Van Stappen, G., H. Yu, X. Wang, S. Hoffman, K. Cooreman, P. Bossier & P. Sorgeloos, 2007. Occurrence of allochthonous Artemia species in the Bohai Bay area, PR China, as confirmed by RFLP analysis and laboratory culture tests. Fundamental and Applied Limnology/Archiv für Hydrobiologie 170: 21–28.CrossRefGoogle Scholar
  33. Vanhaecke, P., W. Tackaert & P. Sorgeloos, 1987. The biogeography of Artemia: an updated review. Artemia Research and Its Applications 1: 129–155.Google Scholar
  34. Viana, D. S., L. Santamaría, T. C. Michot & J. Figuerola, 2013. Migratory strategies of waterbirds shape the continental-scale dispersal of aquatic organisms. Ecography 36: 430–438.CrossRefGoogle Scholar
  35. Waterkeyn, A., B. Vanschoenwinkel, S. Elsen, M. Anton-Pardo, P. Grillas & L. Brendonck, 2010. Unintentional dispersal of aquatic invertebrates via footwear and motor vehicles in a Mediterranean wetland area. Aquatic Conservation: Marine and Freshwater Ecosystems 20: 580–587.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.WasserCluster LunzLunz am SeeAustria
  2. 2.Doñana Biological Station EBD-CSICSevilleSpain
  3. 3.Sorbonne Université (UPMC Paris 06), CNRS, Station Biologique de Roscoff, UMR 7144 AD2MRoscoffFrance
  4. 4.Instituto de Acuicultura de Torre de la Sal (CSIC)Ribera de CabanesSpain

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