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.
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
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
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
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
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
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
Brown AF (1987) Anatomical variability and secondary sexual characteristics in Pomphorhynchus laevis (Müller, 1776) (Acanthocephala). Syst Parasitol 9:213–219
Brown AF, Thompson DBA (1986) Parasite manipulation of host behavior, acanthocephalans and shrimps in the laboratory. J Biol Educ 20:121–127
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056
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
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
Kennedy CR (2006) Ecology of the Acanthocephala. Cambridge University Press, Cambridge, pp 35–41
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasion. Trends Ecol Evol 19:385–390
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
Ricciardi A (2006) Patterns of invasion in the Laurentian Great Lakes in relation to changes in vector activity. Divers Distrib 12:425–433
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
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
Schmidt GD, Nickol BB (1985) Biology of the Acanthocephala. Cambridge University Press, Cambridge, pp 273–305
Šlapanský L, Jurajda P, Janáč M (2016) Early life stages of exotic gobiids as new hosts for unionid glochidia. Freshw Biol 61:979–990
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
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
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
Sures B, Streit B (2001) Eel parasite diversity and intermediate host abundance in the River Rhine, Germany. Parasitology 123:185–191
Sures B, Taraschewski H, Jackwerth E (1994) Lead accumulation in Pomphorhynchus laevis and its host. J Parasitol 80:355–357
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
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
Taraschewski H (2000) Host-parasite interactions in Acanthocephala: a morphological approach. Adv Parasitol 46:1–179
Taraschewski H (2006) Hosts and parasites as aliens. J Helminthol 80:99–128
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
Tompkins DM, Poulin R (2006) Parasites and biological invasions. Biol Invasion N Z 186:67–84
van Beek GCW (2006) The round goby Neogobius melanostomus first recorded in the Netherlands. Aquat Invasions 1:42–43
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
van Riel MC, van Velde G, Bij de Vaate A (2011) Dispersal of invasive species by drifting. Curr Zool 57:818–827
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
Acknowledgements
Special thanks goes to the Deutsche Bundesstiftung Umwelt (DBU) for a Ph.D. fellowship to Michael Hohenadler.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-017-1527-9