Parasitology Research

, Volume 101, Issue 6, pp 1647–1655 | Cite as

Cestode parasitism in invasive and native brine shrimps (Artemia spp.) as a possible factor promoting the rapid invasion of A. franciscana in the Mediterranean region

  • B. B. GeorgievEmail author
  • M. I. Sánchez
  • G. P. Vasileva
  • P. N. Nikolov
  • A. J. Green
Original Paper


Artemia franciscana is an invasive crustacean expanding its range in hypersaline wetlands in the Mediterranean region and replacing native Artemia parthenogenetica and Artemia salina. Native brine shrimps are known as intermediate hosts of cestodes; infected individuals exhibit changes in their behaviour and appearance, thus facilitating the parasite transmission to the avian hosts by predation. To assess whether invasive brine shrimps participate in the cestode life cycles to the same extent as the native species, we examined the natural infections in seven populations of Artemia spp. along the southern coast of Spain and Portugal: three populations of each A. franciscana and A. parthenogenetica and one population of A. salina. Ten cestode species were found in A. parthenogenetica, while only six were recorded in each of A. salina and A. franciscana. The overall infection was consistently higher in native than in invasive populations. For a particular cestode species, the prevalence or abundance was significantly higher in a native population for 54 pairwise comparisons and only higher for an invasive population for 4 pairwise comparisons. These results suggest that cestodes may influence competitive interactions between native and invasive brine shrimps, thus partly explaining the invasive success of A. franciscana.


Intermediate Host Brine Shrimp Invasive Population Salt Pond Enemy Release Hypothesis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are grateful to Francisco Hortas for his help in the field studies in the vicinities of Cádiz. Professor F. Amat (Instituto de Acuicultura de Torre de la Sal, CSIC, Castellón, Spain) kindly commented on an earlier version of the manuscript. This study was carried out in the framework of a cooperative program between the Bulgarian Academy of Sciences and the Consejo Superior de Investigaciones Cientificas (Project 2004BG0013).


  1. Amat F, Gozalbo A, Navarro JC, Hontoria F, Varó I (1991) Some aspects of Artemia biology affected by cestode parasitism. Hydrobiologia 212:39–44CrossRefGoogle Scholar
  2. Amat F, Hontoria F, Ruiz O, Green AJ, Sánchez MI, Figuerola J, Hortas F (2005) The American brine shrimp Artemia franciscana as an exotic invasive species in the Western Mediterranean. Biol Invasions 7:37–47CrossRefGoogle Scholar
  3. Anderson RC (1972) The ecological relationships of meningeal worm and native cervids in North America. J Wildl Dis 8:304–310PubMedGoogle Scholar
  4. Baxevanis AD, Kappas I, Abatzopoulos TJ (2006) Molecular phylogenetics and asexuality in the brine shrimp Artemia. Mol Phylogenet Evol 40:724–738PubMedCrossRefGoogle Scholar
  5. BirdLife International (2005) BirdLife’s online World Bird Database: the site for bird conservation. Version 2.0. BirdLife International, Cambridge, UK.
  6. Browne RA (1980) Competition experiments between parthenogenetic and sexual strains of the brine shrimp, Artemia salina. Ecology 61:471–474CrossRefGoogle Scholar
  7. Browne RA, Halanych KM (1989) Competition between sexual and parthenogenetic Artemia: a re-evaluation (Branchiopoda, Anostraca). Crustaceana 57:57–71CrossRefGoogle Scholar
  8. Browne RA, Sallee SE, Grosch DS, Segreti WO, Purser SM (1984) Partitioning genetic and environmental components of reproduction and lifespan of Artemia. Ecology 65:949–960CrossRefGoogle Scholar
  9. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583PubMedCrossRefGoogle Scholar
  10. Combes C (1996) Parasites, biodiversity and ecosystem stability. Biodivers Conserv 5:953–962CrossRefGoogle Scholar
  11. Dobson AP (1988) Restoring island ecosystems: the potential of parasites to control introduced mammals. Conserv Biol 2:31–39CrossRefGoogle Scholar
  12. Drake JM (2003) The paradox of the parasites: implications for biological invasion. Proc R Soc Lond Ser B (Suppl) 270:S133–S135CrossRefGoogle Scholar
  13. Gabrion C, MacDonald-Crivelli G, Boy V (1982) Dynamique des populations larvaires du cestode Flamingolepis liguloides dans une population d’Artemia en Camargue. Acta Oecol 3:273–293Google Scholar
  14. Georgiev BB, Sánchez MI, Green AJ, Nikolov PN, Vasileva GP, Mavrodieva RS (2005) Cestodes from Artemia parthenogenetica (Crustacea, Branchiopoda) in the Odiel Marshes, Spain: a systematic survey of cysticercoids. Acta Parasitol 50:105–117Google Scholar
  15. Green AJ, Sánchez MI, Amat F, Figuerola J, Hontoria F, Ruiz O, Hortas F (2005) Dispersal of invasive and native brine shrimps Artemia (Anostraca) via waterbirds. Limnol Oceanogr 50:737–742CrossRefGoogle Scholar
  16. Hatcher MJ, Dick JTA, Dunn AM (2006) How parasites affect interactions between competitors and predators? Ecol Letters 9:1–19CrossRefGoogle Scholar
  17. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  18. Krakau M, Thieltges DW, Reise K (2006) Native parasites adopt introduced bivalves of the North Sea. Biol Invasions 8:919–925CrossRefGoogle Scholar
  19. Lafferty KD, Smith KF, Torchin ME, Dobson AP, Kuris AM (2005) The role of infectious diseases in natural communities. What introduced species tell us? In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution and biogeography. Sinauer Associates, Sunderland, MA, pp 111–134Google Scholar
  20. MacNeil C, Fielding NJ, Dick JTA, Briffa M, Prenter J, Hatcher MJ, Dunn AM (2003) An acanthocephalan parasite mediates intraguild predation between invasive and native freshwater amphipods (Crustacea). Freshw Biol 48:2085–2093CrossRefGoogle Scholar
  21. Maksimova AP (1976) A new cestode, Fimbriarioides tadornae sp. n., from Tadorna tadorna and its development in the intermediate host (in Russian). Parazitologia 10:17–24PubMedGoogle Scholar
  22. Martí R, del Moral JC (eds) (2002) La invernada de aves acuáticas en España. Organismo Autónomo Parques Nacionales, Ministerio de Medio Ambiente: MadridGoogle Scholar
  23. Masero JA, Pérez-Hurtado A (2001) Importance of supratidal habitats for maintaining overwintering shorebirds populations: how redshanks use tidal mudflats and adjacent saltworks in Southern Europe. Condor 103:21–30CrossRefGoogle Scholar
  24. Miller RG (1991) Simultaneous Statistical Inference. Springer, Berlin Heidelberg New YorkGoogle Scholar
  25. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627PubMedCrossRefGoogle Scholar
  26. Molnár K (2006) Some remarks on parasitic infections of the invasive Neogobius spp. (Pisces) in the Hungarian reaches of the Danube River, with a description of Goussia szekelyi sp. n. (Apicomplexa: Eimeriidae). J Appl Ichthyol 22:395–400CrossRefGoogle Scholar
  27. Ondračková M, Dávidová M, Pečínková M, Blažek R, Gelnar M, Valová Z, Černý J, Jurajda P (2005) Metazoan parasites of Neogobius fishes in the Slovak section of the River Danube. J Appl Ichthyol 21:345–349CrossRefGoogle Scholar
  28. Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390PubMedCrossRefGoogle Scholar
  29. Ramsar Sites Information Service (2006)
  30. Robert F, Gabrion C (1991) Cestodoses de l’avifaune Camarguaise. Rôle d’Artemia (Crustacea, Anostraca) et stratégies de rencontre hôte–parasite. Ann Parasit Hum Comp 66:226–235Google Scholar
  31. Sánchez MI, Georgiev BB, Nikolov PN, Vasileva GP, Green AJ (2006a) Red and transparent brine shrimps (Artemia parthenogenetica): comparative study of their cestode infections. Parasitol Res 100:111–114PubMedCrossRefGoogle Scholar
  32. Sánchez MI, Green AJ, Castellanos EM (2006b) Temporal and spatial variation of an aquatic invertebrate community subjected to avian predation at the Odiel salt pans (SW Spain). Arch Hydrobiol 166:199–223CrossRefGoogle Scholar
  33. Sánchez MI, Georgiev BB, Green AJ (2007) Avian cestodes affect the behaviour of their intermediate host Artemia parthenogenetica: an experimental study. Behav Processes 74:293–299PubMedCrossRefGoogle Scholar
  34. Snedecor G, Cochran WG (1989) Statistical Methods. Iowa State University Press, Ames, IowaGoogle Scholar
  35. StatSoft (1999) Statistica 5.5. StatSoft, TulsaGoogle Scholar
  36. Thiéry A, Robert F, Gabrion C (1990) Distribution des populations d’Artemia et de leur parasite Flamingolepis liguloides (Cestoda, Cyclophyllidea), dans les salins du littoral méditerranéen français. Can J Zool 68:2199–2204Google Scholar
  37. Tompkins DM, Greenman JV, Robertson PA, Hudson PJ (2000) The role of shared parasites in the exclusion of wildlife hosts: Heterakis gallinarum in the ring-necked pheasant and the grey partridge. J Anim Ecol 69:829–840CrossRefGoogle Scholar
  38. Tompkins DM, White AR, Boots M (2003) Ecological replacement of native red squirrels by invasive greys driven by disease. Ecol Lett 6:189–196CrossRefGoogle Scholar
  39. Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190CrossRefGoogle Scholar
  40. Torchin ME, Lafferty KD, Kuris AM (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions 3:333–345CrossRefGoogle Scholar
  41. Torchin ME, Lafferty KD, Kuris AM (2002) Parasites and marine invasions. Parasitology 124:S137–S151CrossRefGoogle Scholar
  42. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630PubMedCrossRefGoogle Scholar
  43. Wolfe LM (2002) Why alien invaders succeed: support for the Escape-from-Enemy Hypothesis. Am Nat 160:705–711CrossRefPubMedGoogle Scholar
  44. Wurtsbaugh WA, Gliwicz ZM (2001) Limnological control of brine shrimp population dynamics and cyst production in the Great Salt Lake, Utah. Hydrobiologia 466:119–132CrossRefGoogle Scholar
  45. Young RT (1952) The larva of Hymenolepis californicus in the brine shrimp (Artemia salina). J Wash Acad Sci 42:385–388Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • B. B. Georgiev
    • 1
    • 2
    Email author
  • M. I. Sánchez
    • 3
    • 4
  • G. P. Vasileva
    • 1
  • P. N. Nikolov
    • 1
  • A. J. Green
    • 3
  1. 1.Central Laboratory of General EcologyBulgarian Academy of SciencesSofiaBulgaria
  2. 2.Department of ZoologyNatural History MuseumLondonUK
  3. 3.Estación Biológica de Doñana (CSIC)Pabellón del PerúSpain
  4. 4.GEMI/UMR CNRS-IRD 2724, Equipe: “Evolution des Systèmes Symbiotiques”, IRDMontpellier, Cedex 5France

Personalised recommendations