Parasitology Research

, Volume 108, Issue 6, pp 1501–1506 | Cite as

The European eel—the swim bladder–nematode system provides a new view of the invasion paradox

  • Carlos Martínez-Carrasco
  • Emmanuel Serrano
  • Rocio Ruiz de Ybáñez
  • José Peñalver
  • José Antonio García
  • Alfonsa García-Ayala
  • Sergé Morand
  • Pilar Muñoz
Original Paper


It is widely assumed that the likelihood of invasion decreases with increased species richness in the recipient community. However, the invasion paradox supports a negative and a positive relationship between native biodiversity and the success of an invader. Here, we show that for a host–parasite system (Anguilla anguilla as host and Anguillicoloides crassus as parasitic invader), invasion increases with native micro- and macroparasitic species richness. In fact, about 30% of the A. crassus intensity in eels could be explained by the number of both micro- and macroparasite species. This pattern could be due to the fact that A. crassus exploits a niche (the swim bladder) that is unoccupied by native parasite species and by the Th1/Th2 trade-off between native microparasites and the invader. We conclude that the host–parasite system resistance to invasion may depend on both niche availability and the Th1/Th2 trade-off. As well, we encourage researchers to incorporate native parasite richness as a risk factor in epidemiological models of A. crassus.


Species Richness Parasite Community Akaike Information Criterion Correct Parasite Invasion Parasite Diversity 
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.



This work was supported by Fundación Séneca, Coordination Centre for Research (grant 04538/GERM/06). The authors wish to thank E. Romero for his assistance with the eel sampling and D. Riquelme for his technical assistance with parasite processing. E. Serrano is supported by the Juan de la Cierva postdoctoral programme of the MICINN, Spain.


  1. Álvarez-Pellitero P (2008) Fish immunity and parasite infections: from innate immunity to immunoprophylactic prospects. Vet Immunol Immunopathol 126:171–198PubMedCrossRefGoogle Scholar
  2. Bordes F, Morand S (2009) Parasite diversity: an overlooked metric of parasite pressures? Oikos 118:801–806CrossRefGoogle Scholar
  3. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: A practical information-theoretic approach. Springer, New YorkGoogle Scholar
  4. 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
  5. Case TJ (1990) Invasion resistance arises in strongly interacting species-rich model competition communities. Proc Natl Acad Sci USA 87:9610–9614PubMedCrossRefGoogle Scholar
  6. Dunstan PK, Johnson CR (2004) Invasion rates increase with species richness in a marine epibenthic community by two mechanisms. Oecologia 138:285–292PubMedCrossRefGoogle Scholar
  7. Fazio G, Sasal P, Lecomte-Finiger R, Da Silva C, Fumet B, Moné H (2008) Macroparasite communities in European eels, Anguilla anguilla, from French Mediterranean lagoons, with special reference to the invasive species Anguillicola crassus and Pseudodactylogyrus spp. Knowl Managt Aquatic Ecosyst 1:390–391Google Scholar
  8. Fazio G, Mone H, Da Silva C, Simon-Levert G, Allienne JF, Lecomte-Finiger R, Sasal P (2009) Changes in gene expression in European eels (Anguilla anguilla) induced by infection with swim bladder nematodes (Anguillicola crassus). J Parasitol 95:808–816PubMedCrossRefGoogle Scholar
  9. Fenton A, Lamb T, Graham AL (2008) Optimality analysis of Th1/Th2 immune responses during microparasite-macroparasite co-infection, with epidemiological feedbacks. Parasitology 135:841–853PubMedGoogle Scholar
  10. Freyholf J, Kottelat M (2008) Anguilla anguilla .IUCN Red List of Threatened Species, version 2010., accesed 28/10/2010
  11. Fridley JD, Stachowicz JJ, Naeem S, Sax DF, Seabloom EW, Smith MD, Stohlgren TJ, Tilman D, von Holle B (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17PubMedCrossRefGoogle Scholar
  12. Graham AL (2008) Ecological rules governing helminth-microparasite coinfection. Proc Natl Acad Sci USA 105:566–570PubMedCrossRefGoogle Scholar
  13. Joerink M, Forlenza M, Ribeiro CMS, de Vries BJ, Savelkoul HFJ, Wiegertjes GF (2006) Differential macrophage polarisation during parasitic infections in common carp (Cyprinus carpio L.). Fish Shellfish Immunol 21:561–571PubMedCrossRefGoogle Scholar
  14. Kennedy CR, Guégan J-F (1996) The number of niches in intestinal helminth communities of Anguilla anguilla: are there enough spaces for parasites? Parasitology 113:293–302CrossRefGoogle Scholar
  15. Moravec F, Taraschewski H (1988) Revision of the genus Anguillicola Yamaguti 1935 (Nematoda: Anguillicolidae) of the swimbladder of eels, including descriptors of two new species, A. novaezelandiae sp. N., and A. papernai sp. N. Folia Parasitol 35:125–146PubMedGoogle Scholar
  16. Pedersen AB, Fenton A (2007) Emphasizing the ecology in parasite community ecology. Trends Ecol Evol 22:133–139PubMedCrossRefGoogle Scholar
  17. Pérez JM, Meneguz PG, Dematteis A, Rossi L, Serrano E (2006) Parasites and conservation biology: the “Ibex-ecosystem”. Biodivers Conserv 15:2033–2047CrossRefGoogle Scholar
  18. Poulin R (2007) Are there general laws in parasite ecology? Parasitology 134:763–776PubMedCrossRefGoogle Scholar
  19. R Development Core Team 2.10.1 (2009) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, accessed 28/10/2010
  20. Rahhou I, Morand S, Lecomte-Finiger R, Sasal P (2005) Biogeographical relationships of the eel parasite Anguillicola crassus revealed by random amplified polymorphic DNA markers (RAPDS). Bull Fr Pêche Piscic 378–379:87–98CrossRefGoogle Scholar
  21. Rolbiecki L (2008) New data on the biology of the introduced exotic nematode Anguillicola crassus Kuwahara, Niimi et Itagaki, 1974 in the eel Anguilla anguilla in Lake Wdzydze (Polish waters). Int J Oceanogr Hidrobiol 37:37–48Google Scholar
  22. Rosenzweig ML (2001) The four questions: what does the introduction of exotic species do to diversity? Evol Ecol Res 3:361–367Google Scholar
  23. Schmidt GD (1986) Handbook of tapeworm identification. CRC Press, Boca RatonGoogle Scholar
  24. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176CrossRefGoogle Scholar
  25. Stachowicz JJ, Byrnes JE (2006) Species diversity, invasion success, and ecosystem functioning: disentangling the influence of resource competition, facilitation, and extrinsic factors. Mar Ecol Prog Ser 311:251–262CrossRefGoogle Scholar
  26. Taraschewski H (2006) Hosts and parasites as aliens. J Helminthol 80:99–128PubMedCrossRefGoogle Scholar
  27. Würtz J, Taraschewski H (2000) Histopatological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus. Dis Aquat Org 39:121–134PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Carlos Martínez-Carrasco
    • 1
  • Emmanuel Serrano
    • 2
  • Rocio Ruiz de Ybáñez
    • 1
  • José Peñalver
    • 3
  • José Antonio García
    • 4
  • Alfonsa García-Ayala
    • 5
  • Sergé Morand
    • 6
  • Pilar Muñoz
    • 1
  1. 1.Departamento de Sanidad Animal, Facultad de VeterinariaUniversidad de MurciaMurciaSpain
  2. 2.Servei d’Ecopatologia de Fauna Salvatge (SEFaS), Departament de Medicina i Cirurgia AnimalsUniversitat Autònoma de BarcelonaBarcelonaSpain
  3. 3.Dirección General de Ganadería y PescaComunidad Autónoma de la Región de MurciaMurciaSpain
  4. 4.Departamento de Sanidad AnimalUniversidad Complutense de MadridMadridSpain
  5. 5.Departamento de Biología Celular e HistologíaUniversidad de MurciaMurciaSpain
  6. 6.Institut des Sciences de l’EvolutionUniversité de Montpellier 2MontpellierFrance

Personalised recommendations