Skip to main content
Log in

Pomphorhynchus laevis: An invasive species in the river Rhine?

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Acanthocephalans of the globally distributed genus Pomphorhynchus have been intensively studied during the past decades. In Europe, Pomphorhynchus species have shown a certain degree of variability in their morphological characteristics and behavior. Nowadays two different Pomphorhynchus species, namely P. laevis and P. tereticollis, have been described for different waterbodies in Western and Central Europe. However, until now it appears that both species do not co-occur at the same time in the same habitat. We assume that due to their very similar morphology some of the individuals that were identified based on their morphological characteristics as either of the two species might have been misidentified in previous studies. To avoid this possible source of error, we used molecular marker (ITS 1, COX genes) to identify Pomphorhynchus individuals from European eels that were sampled within a time period of 12 years from the Rhine River to elucidate the distribution of the two species in Western and Central Europe. Our results together with a re-examination of former studies provide evidence that P. laevis might have been introduced together with potential host species (intermediate, paratenic, and/or definitive) from the Ponto-Caspian region, and that it outcompeted and repelled the endemic P. tereticollis from the mainstream of the river. Our results also provide first evidence on the former coexistence of both Pomphorhynchus species in the river Rhine.

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.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alexandrov B, Boltachev A, Kharchenko T, Lyashenko A, Son M, Tsarenko P, Zhukinsky V (2007) Trends of aquatic alien species invasions in Ukraine. Aquat Invasions 2:215–242

    Google Scholar 

  • Almqvist G, Strandmark AK, Appelber M (2010) Has the invasive round goby caused new links in Baltic food webs? Environ Biol Fishes 89:79–93

    Google Scholar 

  • Baldauf SA, Thünken T, Frommen JG, Bakker TCM, Heupel O, Kullmann H (2007) Infection with an acanthocephalan manipulates an amphipod’s reaction to a fish predator’s oudors. Int J Parasitol 37:61–65

    PubMed  Google Scholar 

  • Bij de Vaate A, Jazdzewski K, Ketelaars HAM, Gollasch S, Van der Velde G (2002) Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Can J Fish Aquat Sci 59:1159–1174

    Google Scholar 

  • Bollache L, Devin S, Wattier R, Chovet M, Beisel JN, Moreteau JC, Rigaud T (2004) Rapid range extension of the Ponto-Caspian amphipod Dikerogammarus villosus in France: potential consequences. Arch Hydrobiol 160:57–66

    Google Scholar 

  • Borcherding J, Staas S, Krüger S, Ondrackova M, Slapansky L, Jurajda P (2011) 3 Non-native Gobiid species in the lower River Rhine (Germany): recent range extensions and densities. J Appl Ichthyol 27:153–155

    Google Scholar 

  • Brown AF (1987) Anatomical variability and secondary sexual characteristics in Pomphorhynchus laevis (Müller, 1776) (Acanthocephala). Syst Parasitol 9:213–219

    Google Scholar 

  • Brown AF, Thompson DBA (1986) Parasite manipulation of host behavior, acanthocephalans and shrimps in the laboratory. J Biol Educ 20:121–127

    Google Scholar 

  • Brown AF, Chubb JC, Veltkamp CJ (1986) A key to the species of Acanthocephala parasitic in British freshwater fishes. J Fish Biol 28:327–334

    Google Scholar 

  • Buckner SC, Nickol BB (1975) Morphological variation of Moniliformis moniliformis (Bremser, 1811) Travassos 1915 and Moniliformis clarki (Ward, 1917) Chandler 1921. J Parasitol 61:996–998

    PubMed  CAS  Google Scholar 

  • Campbell LM, Thacker R, Barton D, Muir DCG, Greenwood D, Hecky RE (2009) Re-engineering the eastern Lake Erie littoral food web: the trophic function of non-indigenous Ponto-Caspian species. J Great Lakes Res 35:224–231

    Google Scholar 

  • Chen W, Bierbach D, Plath M, Streit B, Klaus S (2012) Distribution of amphipod communities in the Middle to Upper Rhine and five of its tributaries. Biol Invasions Rec 1:263–271

    Google Scholar 

  • Copp GH, Bianco PG, Bogutskaya NG, Eros T, Falka I, Ferreira MT, Fox MG, Freyhof J, Gozlan RE, Grabowska J, Kovac V, Moreno-Amich R, Naseka AM, Penaz M, Povz M, Przybylski M, Robillard M, Russell IC, Stakenas S, Sumer S, Vila-Gispert A, Wiesner C (2005) To be, or not to be, a non-native freshwater fish? J Appl Ichthyol 21:242–262

    Google Scholar 

  • Dezfuli BS, Maynard BJ, Wellnitz TA (2003) Activity levels and predator detection by amphipods infected with an acanthocephalan parasite, Pomphorhynchus laevis. Folia Parasitol 50:129–134

    Google Scholar 

  • Dietrich JP, Morrison BJ, Hoyle JA (2006) Alternative ecological pathways in the eastern Lake Ontario food web—round goby in the diet of lake trout. J Great Lakes Res 32:395–400

    Google Scholar 

  • Djikanovic V, Gacic Z, Cakic P (2010) Endohelminth fauna of barbel Barbus barbus (L. 1758) in the Serbian section of the Danube River, with dominance of acanthocephalan Pomphorhynchus laeavis. Bull Eur Assoc Fish Pathol 30:229–236

    Google Scholar 

  • Emde S, Rueckert S, Palm HW, Klimpel S (2012) Invasive Ponto-Caspian amphipods and fish increase the distribution range of the acanthocephalan Pomphorhynchus tereticollis in the river Rhine. PLoS ONE 7(12):e53218

    PubMed  PubMed Central  CAS  Google Scholar 

  • Emde S, Rueckert S, Kochmann J, Knopf K, Sures B, Klimpel S (2014) Nematode eel parasite found inside acanthocephalan cysts—a “Trojan horse” strategy? Parasites Vectors 7:504

    PubMed  PubMed Central  Google Scholar 

  • Engelbrecht H (1957) Einige Bemerkungen zu Pomphorhynchus laevis (Zoega in Müller, 1776) als Parasit in Pleuronectes flesus und Pleuronectes platessa. Zentralblatt für Bakteriologie und Parasitenkunde Infektionskrankheiten 168:474–479

    CAS  Google Scholar 

  • Franceschi N, Bauer A, Bollache L, Rigaud T (2008) The effects of parasite age and intensity on variability in acanthocephalan-induced behavioural manipulation. Int J Parasitol 38:1161–1170

    PubMed  CAS  Google Scholar 

  • Gallardo B, Aldridge DC (2013) Priority setting for invasive species management: risk assessment of Ponto-Caspian invasive species into Great Britain. Ecol Appl 23:352–364

    PubMed  Google Scholar 

  • Johnson JH, Ross RM, McCullough RD, Mathers A (2010) Diet shift of double-crested cormorants in eastern Lake Ontario associated with the expansion of the invasive round goby. J Great Lakes Res 36:242–247

    Google Scholar 

  • Kalchhauser I, Mutzner P, Hirsch PE, Burkhardt-Holm P (2013) Arrival of round goby Neogobius melanostomus (Pallas, 1814) and bighead goby Ponticola kessleri (Günther, 1861) in the High Rhine (Switzerland). Biol Invasions Rec 2:79–83

    Google Scholar 

  • Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056

    PubMed  CAS  Google Scholar 

  • Kennedy CR (1984) The status of flounders, Platichthys flesus L., as hosts of the Acanthocephalan Pomphorhynchus laevis (Müller) and its survival in marine conditions. J Fish Biol 24:135–149

    Google Scholar 

  • Kennedy CR (1989) Discontinuous distributions of the fish acanthocephalans Pomphorhynchus laevis and Acanthocephalus anguillae in Britain and Ireland: an hypothesis. J Fish Biol 34:607–619

    Google Scholar 

  • Kennedy CR (2006) Ecology of the Acanthocephala. Cambridge University Press, Cambridge, pp 35–41

    Google Scholar 

  • Kennedy CR, Broughton PF, Hine PM (1977) The status of brown and rainbow trout, Salmo trutta and S. gairdneri as hosts of acanthocephalan, Pomphorhynchus laevis. J Fish Biol 13:265–275

    Google Scholar 

  • Kinzler W, Kley A, Mayer G, Waloszek D, Maier G (2009) Mutual predation between and cannibalism within several freshwater gammarids: Dikerogammarus villosus versus one native and three invasives. Aquat Ecol 43:457–464

    Google Scholar 

  • Kornis M, van der Zanden J, Mercado-Silva N (2012) Twenty years of invasion: a review of round goby Neogobius melanostomus biology, spread and ecological implications. J Fish Biol 80:235–285

    PubMed  CAS  Google Scholar 

  • Král’ová-Hromadová I, Tietz DF, Shinn AP, Špakulová M (2003) ITS rDNA sequences of Pomphorhynchus laevis (Zoega in Müller, 1776) and P. lucyi William & Rogers, 1984 (Acanthocephala: Palaeacanthocephala). Syst Parasitol 56:141–145

    PubMed  Google Scholar 

  • Kvach Y, Skóra KE (2007) Metazoa parasites of the invasive round goby Apollonia melanostoma (Neogobius melanostomus) (Pallas) (Gobiidae: Osteichthyes) in the Gulf of Gdansk, Baltic Sea, Poland: a comparison with the Black Sea. Parasitol Res 100:767–774

    PubMed  Google Scholar 

  • Lundström A (1942) Die Acanthocephalan Schwedens. [The Swedish Acanthocephala.] Dissertation. University of Lund

  • Meyer A (1932) Acanthocephala. I. In: Bronn HG (ed) Klassen und Ordnungen des Tierreichs, 4th edn. Akademische Verlagsgellschaft, Leipzig, pp 1–332

    Google Scholar 

  • Molloy S, Holland C, O’Regan M (1995) Population biology of Pomphorhynchus laevis in brown trout from two lakes in the west of Ireland. J Helminthol 69:229–235

    PubMed  CAS  Google Scholar 

  • Munro MA, Whitfield PJ, Diffley R (1989) Pomphorhynchus laevis (Müller) in the flounder, Platichthys flesus L., in the tidal River Thames: population structure, microhabitat utilization and reproductive status in the field and under conditions of controlled salinity. J Fish Biol 35:719–735

    Google Scholar 

  • Munro MA, Reid A, Whitfield PJ (1990) Genomic divergence in the ecologically differentiated English freshwater and marine strains of Pomphorhynchus laevis (Acanthocephala: Palaeacanthocephala): a preliminary investigation. Parasitology 101:451–454

    Google Scholar 

  • Nachev M, Sures B (2009) The endohelminth fauna of barbel (Barbus barbus) correlates with water quality of the Danube River in Bulgaria. Parasitology 136:545–552

    PubMed  CAS  Google Scholar 

  • Nachev M, Zimmermann S, Rigaud T, Sures B (2010) Is metal accumulation in Pomphorhynchus laevis dependent on parasite sex or infrapopulation size? Parasitology 137:1239–1248

    PubMed  CAS  Google Scholar 

  • O’Mahony EM, Bradley DG, Kennedy CR, Holland CV (2004) Evidence for the hypothesis of strain formation in Pomphorhynchus laevis (Acanthocephala): an investigation using mitochondrial DNA sequences. Parasitology 29:341–347

    Google Scholar 

  • Ondračková M, Trichkova T, Jurajda P (2006) Present and historical occurrence of metazoan parasites in Neogobius kessleri (Gobiidae) in the Bulgarian section of the Danube River. Acta Zool Bulg 58:399–406

    Google Scholar 

  • Ondračková M, Dávidová M, Blažek R, Gelnar M, Jurajda P (2009) The interaction between an introduced fish host and local parasite fauna: Neogobius kessleri in the middle Danube River. Parasitol Res 105:201–208

    PubMed  Google Scholar 

  • Peeler EJ, Oidtmann BC, Midtlyng PJ, Miossec L, Gozlan RE (2011) Non-native aquatic animals introductions have driven disease emergence in Europe. Biol Invasions 13:1291–1303

    Google Scholar 

  • Pereiraa NN, Colomboc FB, Chávezc MIA, Brinatib HL, Carreñoc MNP (2016) Challenges to implementing a ballast water remote monitoring system. Ocean Coast Manag 131:25–38

    Google Scholar 

  • Perrot-Minnot MJ (2004) Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). Int J Parasitol 34:45–54

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Rewicz T, Grabowski M, MacNeil C, Bącela-Spychalska K (2014) The profile of a ‘perfect’ invader—the case of killer shrimp, Dikerogammarus villosus. Aquat Invasions 9:267–288

    Google Scholar 

  • Ricciardi A (2006) Patterns of invasion in the Laurentian Great Lakes in relation to changes in vector activity. Divers Distrib 12:425–433

    Google Scholar 

  • Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Integr Comp Biol 37:621–632

    Google Scholar 

  • Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annu Rev Ecol Syst 31:481–531

    Google Scholar 

  • Schmidt GD, Nickol BB (1985) Biology of the Acanthocephala. Cambridge University Press, Cambridge, pp 273–305

    Google Scholar 

  • Šlapanský L, Jurajda P, Janáč M (2016) Early life stages of exotic gobiids as new hosts for unionid glochidia. Freshw Biol 61:979–990

    Google Scholar 

  • Smrzlić VI, Valić D, Kapetanović D, Filipović Marijić V, Gjurčević E, Teskeredžić E (2015) Pomphorhynchus laevis (Acanthocephala) from the Sava River basin: new insights into strain formation, mtDNA-like sequences and dynamics of infection. Parasitol Int 64:243–250

    Google Scholar 

  • Špakulová M, Perrot-Minnot MJ, Neuhaus B (2011) Resurrection of Pomphorhynchus tereticollis (Rudolphi, 1809) (Acanthocephala: Pomphorhynchidae) based on new morphological and molecular data. J Helminthol 48:268–277

    Google Scholar 

  • Sures B (2014) Ecology of the acanthocephala. In: Schmidt-Rhaesa A (ed) Handbook of zoology. Gastrotricha, Cycloneuralia and Gnathifera, 3rd edn. de Gruyter, Berlin, pp 337–344

    Google Scholar 

  • Sures B, Streit B (2001) Eel parasite diversity and intermediate host abundance in the River Rhine, Germany. Parasitology 123:185–191

    PubMed  CAS  Google Scholar 

  • Sures B, Taraschewski H, Jackwerth E (1994) Lead accumulation in Pomphorhynchus laevis and its host. J Parasitol 80:355–357

    PubMed  CAS  Google Scholar 

  • Sures B, Knopf K, Würtz J, Hirt J (1999) Richness and diversity of parasite communities in European eels Anguilla anguilla of the River Rhine, Germany, with special reference to helminth parasites. Parasitology 119:323–330

    PubMed  Google Scholar 

  • Tain L, Perrot-Minnot MJ, Cézilly F (2006) Altered host behaviour and brain serotonergic activity caused by acanthocephalans: evidence for specificity. Proc Biol Sci 273:3039–3045

    PubMed  PubMed Central  CAS  Google Scholar 

  • Taraschewski H (2000) Host-parasite interactions in Acanthocephala: a morphological approach. Adv Parasitol 46:1–179

    PubMed  CAS  Google Scholar 

  • Taraschewski H (2006) Hosts and parasites as aliens. J Helminthol 80:99–128

    PubMed  CAS  Google Scholar 

  • Thielen F, Münderle M, Taraschewski H, Sures B (2007) Do eel parasites reflect the local crustacean community? A case study from the Rhine river system. J Helminthol 81:179–189

    PubMed  Google Scholar 

  • Tompkins DM, Poulin R (2006) Parasites and biological invasions. Biol Invasion N Z 186:67–84

    Google Scholar 

  • van Beek GCW (2006) The round goby Neogobius melanostomus first recorded in the Netherlands. Aquat Invasions 1:42–43

    Google Scholar 

  • van Riel MC, van Velde G, Bij de Vaate A (2003) Pomphorhynchus spec. (Acanthocephala) uses the invasive amphipod Chelicorophium curvispinum (G. O. Sars, 1895) as an intermediate host in the river Rhine. Crustaceana 76:241–246

    Google Scholar 

  • van Riel MC, van Velde G, Bij de Vaate A (2011) Dispersal of invasive species by drifting. Curr Zool 57:818–827

    Google Scholar 

  • Westram AM, Baumgartner C, Keller I, Jokela J (2011) Are cryptic host species also cryptic to parasites? Host specificity and geographical distribution of acanthocephalan parasites infecting freshwater Gammarus. Infect Genet Evol 11:1083–1090

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Special thanks goes to the Deutsche Bundesstiftung Umwelt (DBU) for a Ph.D. fellowship to Michael Hohenadler.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. A. A. Hohenadler.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hohenadler, M.A.A., Nachev, M., Thielen, F. et al. Pomphorhynchus laevis: An invasive species in the river Rhine?. Biol Invasions 20, 207–217 (2018). https://doi.org/10.1007/s10530-017-1527-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-017-1527-9

Keywords

Navigation