Parasitology Research

, Volume 118, Issue 9, pp 2543–2555 | Cite as

How Ponto-Caspian invaders affect local parasite communities of native fish

  • M. A. A. HohenadlerEmail author
  • M. Nachev
  • M. Freese
  • J. D. Pohlmann
  • R. Hanel
  • B. Sures
Fish Parasitology - Original Paper


Invasive species are a major threat to ecosystems worldwide. Their effects are versatile and mostly well studied. However, not much is known about the impact of invasion on native parasite communities, although parasites are usually important response variables for ecosystem health. To improve the knowledge on how native fish parasite communities and their dynamics are affected by invasive species and how these processes change local host-parasite interactions over time, we studied different host-parasite systems in four German rivers. Three of these rivers (Rhine, Ems, and Elbe) are heavily invaded by different Ponto-Caspian species such as the amphipod Dikerogammarus villosus and various gobiids such as Neogobius melanostomus and Ponticola kessleri that serve as potential hosts for different local parasite species, while the fourth river (Schwentine) was free of any Ponto-Caspian invaders. Due to the lack of additional uninvaded river systems, literature data on parasite communities before invasion were compared with the post invasion status for the rivers Rhine and Elbe. The results showed differences among the parasite communities of different host species from the three invaded rivers when compared to the Schwentine River. Among the local internal parasite communities, especially the acanthocephalan Pomphorhynchus laevis and the nematode Raphidascaris acus have to be considered as key species associated with invasions from the Ponto-Caspian region. As the examined invasive Ponto-Caspian fish species serves as suitable host for both parasite species, the increases in their infection rates in native fish species are examples of parasite spill back (R. acus) and spill over (P. laevis, at least in the river Rhine). These results were further supported by the analysis of literature data on parasite communities of the past 20 years. Consequences for local parasite communities range from decreased prevalence of native parasites towards an extinction of entire parasite species.


Ponto-Caspian invasion Pomphorhynchus laevis Raphidascaris acus Neogobius melanostomus 



Thanks are due to the Deutsche Bundesstiftung Umwelt (DBU) for a Ph.D. fellowship to Michael Hohenadler.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Statement of ethical approval

Fishes used for this research were sampled in line with the EU Data Collection Framework (European Commission, 2010) and killed in accordance with German animal welfare law (1).

Supplementary material

436_2019_6399_MOESM1_ESM.docx (200 kb)
ESM 1 (DOCX 199 kb)


  1. Aliabadi BK, Juliano SA (2002) Escape from gregarine parasites affects the competitive impact of an invasive mosquito. Biol Invasions 4:283–297Google Scholar
  2. Bernauer D, Jansen W (2006) Recent invasions of alien macroinvertebrates and loss of native species in the upper Rhine River, Germany. Aquat Invasions 2:55–71Google Scholar
  3. 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 Sc 59:1159–1174Google Scholar
  4. 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. Archiv Fur Hydrobiol 160:57–66Google Scholar
  5. Boonstra H, Wiggers R, Swarte M (2016) First record of the Ponto-Caspian amphipod Obesogammarus obesus (Sars, 1894) (Amphipoda: Pontogammaridae) from the Netherlands. Biol Invasions 3:155–158Google Scholar
  6. Borcherding J, Staas S, Krüger S, Ondrackova M, Slapansky L, Jurajda P (2011) Non-native Gobiid species in the lower River Rhine (Germany): recent range extensions and densities. J Appl Ichthyol 27:153–155Google Scholar
  7. Brohmer P, Ehrmann P (1966) Die Tierwelt Mitteleuropas. Quelle and Meyer, LeipzigGoogle Scholar
  8. Bush AO, Lafferty KD, Lotz JM, Shstak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583Google Scholar
  9. Bush AO, Fernandez JC, Esch GW, Seed JR (2001) Parasitism: the diversity and ecology of animal parasites. Cambridge University Press, CambridgeGoogle Scholar
  10. Carlsson M (1997) Sea level and salinity variations in the Baltic Sea - an oceanographic study using historical data. Thesis. Department of Oceanography Goteborg University. ISSN 1400-3813Google Scholar
  11. Carman SM, Janssen J, Jude DJ, Berg MB (2006) Diel interactions between prey behaviour and feeding in an invasive fish, the round goby, in a North American river. Freshw Biol 51:742–755Google Scholar
  12. Colautti RI, Ricciardi A, Grigorovich IA, Maclsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733Google Scholar
  13. Dang C, de Montaudouin X, Bald D, Jude F, Raymond N, Lanceleur L, Paul-Pont I, Caill-Milly N (2009) Testing the enemy release hypothesis: trematode parasites in the non-indigenous Manila clam Ruditapes philippinarum. Hydrobiologia 630:139–148Google Scholar
  14. David GM, Staentzel C, Schlumberger O, Perrot-Minnot MJ, Beisel JN, Hardion L (2018) A minimalist macroparasite diversity in the round goby of the Upper Rhine reduced to an exotic acanthocephalan lineage. Parasitol 145:1020–1026Google Scholar
  15. Diagne C, Ribas A, Charbonnel N, Dalecky A, Tatard C, Gauthier P, Haukisalmi V, Fossati-Gaschignard O, Bâ K, Kane M, Niang Y, Diallo M, Sow A, Piry S, Sembène M, Brouat C (2016) Parasites and invasions: changes in gastrointestinal helminth assemblages in invasive and native rodents in Senegal. Int J Parasitol 46:857–869Google Scholar
  16. Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposesGoogle Scholar
  17. Dunn AM (2009) Parasites and biological invasions. Adv Parasit 68:161–184Google Scholar
  18. 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:e53218Google Scholar
  19. Emde S, Rueckert S, Kochmann J, Knopf K, Sures B, Klimpel S (2014) Nematode eel parasite found inside acanthocephalan cysts – a “Trojan horse” strategy? Parasite Vector 7:504Google Scholar
  20. Essink K, Dekker R (2002) General patterns in invasion ecology tested in the Dutch Wadden Sea: the case of a brackish-marine polychaetous worm. Biol Invasions 4:359–368Google Scholar
  21. 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 38:1161–1170Google Scholar
  22. Francová K, Ondračková M, Polačik M, Jurajda P (2011) Parasite fauna of native and non-native populations of Neogobius melanostomus (Pallas, 1814) (Gobiidae) in the longitudinal profile of the Danube River. J Appl Ichthyol 27:879–886Google Scholar
  23. Freese M, Sühring R, Pohlmann JD, Wolschke H, Magath V, Ebinghaus R, Hanel R (2016) A question of origin: dioxin-like PCBs and their relevance in stock management of European eels. Toxicology 25:41–55Google Scholar
  24. Freese M, Sühring R, Marohn L, Pohlmann JD, Wolschke H, Byer J, Alaee M, Ebinghaus R, Hanel R (2017) Maternal transfer of dioxin-like compounds in artificially matured European eels. Environ Pollut 227:348–356Google Scholar
  25. Froese R, Pauly D Editors. (2018) FishBase. World Wide Web electronic publication., version (06/2018)
  26. Gagne RB, Heins DC, Mcintyre PB, Gilliam JF, Blum MJ (2016) Mutual dilution of infection by an introduced parasite in native and invasive stream fishes across Hawaii. Parasitology 143:1605–1614Google Scholar
  27. Gallardo B, Aldridge DC (2015) Is Great Britain heading for a Ponto-Caspian invasional meltdown? J Appl Ecol 52:41–49Google Scholar
  28. Gebhardt H, Ness A (1997) Fische: die heimischen Süßwasserfische sowie Arten der Nord- und Ostsee. 3., durchgesehene Neuausgabe. BLV Verlag, MünchenGoogle Scholar
  29. Heath MR, Henderson EW, Slesser C, Woodward EMS (1991) High salinity in the North Sea. Nature 352:116Google Scholar
  30. Hiepe T, Lucius R, Gottstein B (2006) Allgemeine Parasitologie – Mit den Grundzügen der Immunologie, Diagnostik und Bekämpfung. MVS Medizinverlage, StuttgartGoogle Scholar
  31. Hohenadler MAA, Nachev M, Thielen F, Taraschewski H, Grabner D, Sures B (2018) Pomphorhynchus laevis: an invasive species in the river Rhine? Biol Invasions 20:207–217Google Scholar
  32. Jacob E, Walter T, Hanel R (2016) A checklist of the protozoan and metazoan parasites of European eel (Anguilla anguilla): checklist of Anguilla anguilla parasites. J Appl Ichthyol 32:1–49Google Scholar
  33. Jakšić G, Jadan M, Piria M (2016) The review of ecological and genetic research of Ponto-Caspian gobies (Pisces, Gobiidae) in Europe. C J Fish 74:110–123Google Scholar
  34. Jůza T, Blabolil P, Baran RD, Barton DC, Cech M, Draštík V, Frouzová J, Holubová M, Ketelaars HAM, Kočvara L, Kubecka J, Muška M, Prchalová M, Říha M, Sajdlova Z, Šmejkal M, Tušer M, Vašek M, Vejřík L, Vejříková I, Wagenvoort AJ, Zak J, Peterka J (2018) Collapse of the native ruffe (Gymnocephalus cernua) population in the Biesbosch lakes (the Netherlands) owing to round goby (Neogobius melanostomus) invasion. Biol Invasions 20:1523–1535Google Scholar
  35. Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056Google Scholar
  36. Kennedy CR (2006) Ecology of the Acanthocephala. Cambridge University Press, Cambridge, pp 35–41Google Scholar
  37. Ketelaars HM (2004) Range extensions of Ponto-Caspian aquatic invertebrates in continental Europe. Aquatic invasions in the Black, Caspian, and Mediterranean seas. Springer, Dordrecht, pp 209–236Google Scholar
  38. 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 43:457–464Google Scholar
  39. Knopf K (2006) The swimbladder nematode Anguillicola crassus in the European eel Anguilla anguilla and the Japanese eel Anguilla japonica: differences in susceptibility and immunity between a recently colonized host and the original host. J Helminthol 80:129–136Google Scholar
  40. Kvach Y, Skora K (2006) The comparative analysis of infection parameters of the round goby Neogobius melanostomus (Pallas) (Gobiidae: Osteichthyes) in the Gulf of Gdańsk, Baltic Sea, Poland, and the Northwestern Black Sea, Ukraine. Acta Ichtiologica Romanica 1:141–152Google Scholar
  41. Kvach Y, Boldyrev V, Lohner R, Stepien CA (2015) The parasite community of gobiid fishes (Actinopterygii: Gobiidae) from the Lower Volga River region. Biologia 70:948–957Google Scholar
  42. Kvach Y, Ondračková M, Janáč M, Jurajda P (2016) Methodological issues affecting the study of fish parasites. I. Duration of live fish storage prior to dissection. Dis Aquat Org 119:107–115Google Scholar
  43. Kvach Y, Ondračková M, Janáč M, Jurajda P (2017) The parasite community of round goby Neogobius melanostomus (Pallas, 1814) (Actinopterygii: Gobiidae) newly introduced into the upper Elbe. Knowl Manag Aquat Ecosyst 418-419Google Scholar
  44. Kvach Y, Ondračková M, Janáč M, Jurajda P (2018) Methodological issues affecting the study of fish parasites. III. Effect of fish preservation method. Dis Aquat Org 127:213–224Google Scholar
  45. Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo D, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546Google Scholar
  46. Lymbery AJ, Morine M, Gholipour Kanani H, Beatty SJ, Morgana DL (2014) Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol Parasites Wildl 2:171–177Google Scholar
  47. Magurran AE (1988) Ecological diversity and its measurement. Springer, DordrechtGoogle Scholar
  48. Micklin P, Aladin N, Plotnikov I (2014) The Aral Sea - the devastation and partial rehabilitation of a Great Lake. Springer, DordrechtGoogle Scholar
  49. Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Envir 6:485–492Google Scholar
  50. Moravec F (1994) Parasitic nematodes of freshwater fishes of Europe. Springer, DordrechtGoogle Scholar
  51. Moravec F (1996) The amphipod Gammarus fossarum as a natural true intermediate host of the nematode Raphidascaris acus. J Parasitol 82:668–669Google Scholar
  52. Moravec F (2004) Metazoan parasites of salmonid fishes of Europe. Academia Czech RepublicGoogle Scholar
  53. Moravec F, Scholz T (2015) Macroparasites and their communities of the European eel Anguilla anguilla (Linnaeus) in the Czech Republic. Folia Parasitol 62:033Google Scholar
  54. Morley NJ (2007) Anthropogenic effects of reservoir construction on the parasite fauna of aquatic wildlife. Eco Health 4:374–383Google Scholar
  55. Morozińska-Gogol J (2013) Parasite communities of European perch, Perca fluviatilis L. (Actinopterygii: Perciformes: Percidae) from lake Łebsko (Central Coast, Poland). Ann Parasitol 59:89–98Google Scholar
  56. Mouritsen KN, Poulin R (2005) Parasites boosts biodiversity and changes animal community structure by trait-mediated indirect effects. Oikos 108:344–350Google Scholar
  57. Münderle M, Taraschewski H, Klar B, Chang CW, Shiao JC, Shen KN, He JT, Lin SH, Tzeng WN (2006) Occurrence of Anguillicola crassus (Nematoda: Dracunculoidea) in Japanese eels Anguilla japonica from a river and an aquaculture unit in SW Taiwan. Dis Aquat Org 71:101–108Google Scholar
  58. Nachev M, Zimmermann S, Rigaud T, Sures B (2010) Is metal accumulation in Pomphorhynchus laevis dependent on parasite sex or infrapopulation size? Parasitology 137:1239–1248Google Scholar
  59. Nehring S (2006) Four arguments why so many alien species settle into estuaries, with special reference to the German river Elbe. Helgol Mar Res 60:127–134Google Scholar
  60. 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 129:341–347Google Scholar
  61. Ondračková M, Dávidová M, Pečínková M, Blažek R, Gelnar M, Černý J, Jurajda P (2005) Metazoan parasites of Neogobius fishes in the Slovak section of the River Danube. J Appl Ichthyol 21:345–349Google Scholar
  62. 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 105:201–208Google Scholar
  63. Ondračková M, Valová Z, Hudcová I, Michálková V, Ŝimková A, Borcherding J, Jurajda P (2015) Temporal effects on host-parasite associations in four naturalized goby species living in sympatry. Hydrobiologia 746:233–243Google Scholar
  64. Perrot-Minnot MJ (2004) Larval morphology, genetic divergence, and contrasting levels of host manipulation between forms of Pomphorhynchus laevis (Acanthocephala). Int J Parasitol 34:45–54Google Scholar
  65. Perrot-Minnot MJ, Špakulová M, Wattier R, Kotlík P, Düşen S, Aydoğdu A, Tougard C (2018) Contrasting phylogeography of two Western Palaearctic fish parasites despite similar life cycles. J Biogeogr 45:101–115Google Scholar
  66. Pimentel D, McNair S, Janecka J, Wightman J, Simmonds C, O’Connell C, Wong E, Russel L, Zern J, Aquino T, Tsomondo T (2001) Economic and environmental threats of alien plant, animal, and microbe invasions. Agric Ecosyst Environ 84:1–20Google Scholar
  67. Piscart C, Bergerot B, Laffaille P, Marmonier P (2010) Are amphipod invaders a threat to regional biodiversity? Biol Invasions 12:853–863Google Scholar
  68. Poulin R (2000) The diversity of parasites. Q Rev Biol 75:277–293Google Scholar
  69. Reier S, Sattmann H, Schwaha T, Harl J, Konecny R, Haring E (2019) An integrative taxonomic approach to reveal the status of the genus Pomphorhynchus Monticelli, 1905 (Acanthocephala: Pomphorhynchidae) in Austria. International Journal for Parasitology: Parasites and Wildlife 8:145–155Google Scholar
  70. Sapota MR (2004) The round goby (Neogobius melanostomus) in the Gulf of Gdańsk – a species introduction into the Baltic Sea. Hydrobiologia 514:219–224Google Scholar
  71. Šlapanský L, Jurajda P, Janac M (2016) Early life stages of exotic gobiids as new hosts for unionid glochidia. Freshw Biol 61:979–990Google Scholar
  72. Špakulová M, Perrot-Minnot MJ, Neuhaus B (2011) Resurrection of Pomphorhynchus tereticollis (Rudolphi, 1809) (Acanthocephala: Pomphorhynchidae) based on new morphological and molecular data. Helminthologia 3:268–277Google Scholar
  73. State authority for nature and environment of the Land Schleswig-Holstein (2008) Seen der SchwentineGoogle Scholar
  74. Sures B (2002) Charakterisierung aquatischer Wirt-Parasit-Interaktionen aus ökologischer und (öko-)toxikologischer Sicht. Habilitation treatise, University of Karlsruhe. KITopen-ID: 2552002Google Scholar
  75. Sures B, Knopf K (2004) Parasites as a threat to freshwater eels? Science 304:208–209Google Scholar
  76. Sures B, Streit B (2001) Eel parasite diversity and intermediate host abundance in the River Rhine, Germany. Parasitology 123:185–191Google Scholar
  77. 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 119:323–330Google Scholar
  78. Sures B, Nachev M, Keppel M, Grabner D, Selbach C (2017) Parasites as drivers of key processes in ecosystems: facts and future perspectives. Exp Parasitol 180:141–147Google Scholar
  79. Taraschewski H (2006) Hosts and parasites as aliens. J Helminthol 80:99–128Google Scholar
  80. Thielen F (2005) Der Einfluss einwandernder Amphipodenarten auf die Parasitozonose des Europäischen Aals (Anguilla anguilla). Dissertation, University KarlsruheGoogle Scholar
  81. Tompkins DM, Poulin R (2006) Parasites and biological invasions. Biol Invasion in New Zealand 186:67–84Google Scholar
  82. Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190Google Scholar
  83. Torchin ME, Lafferty KD, Kuris AM (2002) Parasites and marine invasions. Parasitology 124:137–151Google Scholar
  84. Wielgoss S, Taraschewski H, Meyer A, Wirth T (2008) Population structure of the parasitic nematode Anguillicola crassus, an invader of declining North Atlantic eel stocks. Mol Biol 17:3478–3496Google Scholar
  85. Wolda H (1981) Similarity indices, sample size and diversity. OecoIogia (Berl) 50:296–302Google Scholar
  86. Young HS, Parker IM, Gilbert GS, Guerra AS, Nunn CL (2017) Introduced species, disease ecology, and biodiversity–disease relationships. Trends Ecol Evol 32:41–54Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Aquatic Ecology and Centre for Water and Environmental ResearchUniversity of Duisburg-EssenEssenGermany
  2. 2.Thünen Institute of Fisheries EcologyBremerhavenGermany
  3. 3.Department of ZoologyUniversity of JohannesburgJohannesburgSouth Africa

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