Skip to main content
Log in

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

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Amat F, Gozalbo A, Navarro JC, Hontoria F, Varó I (1991) Some aspects of Artemia biology affected by cestode parasitism. Hydrobiologia 212:39–44

    Article  Google Scholar 

  • 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 7:37–47

    Article  Google Scholar 

  • Anderson RC (1972) The ecological relationships of meningeal worm and native cervids in North America. J Wildl Dis 8:304–310

    PubMed  CAS  Google Scholar 

  • Baxevanis AD, Kappas I, Abatzopoulos TJ (2006) Molecular phylogenetics and asexuality in the brine shrimp Artemia. Mol Phylogenet Evol 40:724–738

    Article  PubMed  CAS  Google Scholar 

  • BirdLife International (2005) BirdLife’s online World Bird Database: the site for bird conservation. Version 2.0. BirdLife International, Cambridge, UK. http://www.birdlife.org

  • Browne RA (1980) Competition experiments between parthenogenetic and sexual strains of the brine shrimp, Artemia salina. Ecology 61:471–474

    Article  Google Scholar 

  • Browne RA, Halanych KM (1989) Competition between sexual and parthenogenetic Artemia: a re-evaluation (Branchiopoda, Anostraca). Crustaceana 57:57–71

    Article  Google Scholar 

  • Browne RA, Sallee SE, Grosch DS, Segreti WO, Purser SM (1984) Partitioning genetic and environmental components of reproduction and lifespan of Artemia. Ecology 65:949–960

    Article  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  PubMed  CAS  Google Scholar 

  • Combes C (1996) Parasites, biodiversity and ecosystem stability. Biodivers Conserv 5:953–962

    Article  Google Scholar 

  • Dobson AP (1988) Restoring island ecosystems: the potential of parasites to control introduced mammals. Conserv Biol 2:31–39

    Article  Google Scholar 

  • Drake JM (2003) The paradox of the parasites: implications for biological invasion. Proc R Soc Lond Ser B (Suppl) 270:S133–S135

    Article  Google Scholar 

  • 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 3:273–293

    Google Scholar 

  • 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 50:105–117

    Google Scholar 

  • 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 50:737–742

    Article  Google Scholar 

  • Hatcher MJ, Dick JTA, Dunn AM (2006) How parasites affect interactions between competitors and predators? Ecol Letters 9:1–19

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Krakau M, Thieltges DW, Reise K (2006) Native parasites adopt introduced bivalves of the North Sea. Biol Invasions 8:919–925

    Article  Google Scholar 

  • 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 111–134

    Google Scholar 

  • 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 48:2085–2093

    Article  Google Scholar 

  • Maksimova AP (1976) A new cestode, Fimbriarioides tadornae sp. n., from Tadorna tadorna and its development in the intermediate host (in Russian). Parazitologia 10:17–24

    PubMed  CAS  Google Scholar 

  • Martí R, del Moral JC (eds) (2002) La invernada de aves acuáticas en España. Organismo Autónomo Parques Nacionales, Ministerio de Medio Ambiente: Madrid

  • 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 103:21–30

    Article  Google Scholar 

  • Miller RG (1991) Simultaneous Statistical Inference. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627

    Article  PubMed  CAS  Google Scholar 

  • 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 22:395–400

    Article  Google Scholar 

  • 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 21:345–349

    Article  Google Scholar 

  • Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390

    Article  PubMed  Google Scholar 

  • Ramsar Sites Information Service (2006) http://www.wetlands.org/RSDB/default.htm

  • 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 66:226–235

    Google Scholar 

  • 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 100:111–114

    Article  PubMed  Google Scholar 

  • 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 166:199–223

    Article  CAS  Google Scholar 

  • Sánchez MI, Georgiev BB, Green AJ (2007) Avian cestodes affect the behaviour of their intermediate host Artemia parthenogenetica: an experimental study. Behav Processes 74:293–299

    Article  PubMed  Google Scholar 

  • Snedecor G, Cochran WG (1989) Statistical Methods. Iowa State University Press, Ames, Iowa

    Google Scholar 

  • StatSoft (1999) Statistica 5.5. StatSoft, Tulsa

    Google Scholar 

  • 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 68:2199–2204

    Google Scholar 

  • 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 69:829–840

    Article  Google Scholar 

  • Tompkins DM, White AR, Boots M (2003) Ecological replacement of native red squirrels by invasive greys driven by disease. Ecol Lett 6:189–196

    Article  Google Scholar 

  • Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190

    Article  Google Scholar 

  • Torchin ME, Lafferty KD, Kuris AM (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions 3:333–345

    Article  Google Scholar 

  • Torchin ME, Lafferty KD, Kuris AM (2002) Parasites and marine invasions. Parasitology 124:S137–S151

    Article  Google Scholar 

  • Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630

    Article  PubMed  CAS  Google Scholar 

  • Wolfe LM (2002) Why alien invaders succeed: support for the Escape-from-Enemy Hypothesis. Am Nat 160:705–711

    Article  PubMed  Google Scholar 

  • Wurtsbaugh WA, Gliwicz ZM (2001) Limnological control of brine shrimp population dynamics and cyst production in the Great Salt Lake, Utah. Hydrobiologia 466:119–132

    Article  Google Scholar 

  • Young RT (1952) The larva of Hymenolepis californicus in the brine shrimp (Artemia salina). J Wash Acad Sci 42:385–388

    Google Scholar 

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B. B. Georgiev.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Georgiev, B.B., Sánchez, M.I., Vasileva, G.P. et al. 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. Parasitol Res 101, 1647–1655 (2007). https://doi.org/10.1007/s00436-007-0708-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-007-0708-3

Keywords

Navigation