Advertisement

The Rhine as Hotspot of Parasite Invasions

  • Bernd SuresEmail author
  • Milen Nachev
  • Daniel Grabner
Chapter
Part of the Parasitology Research Monographs book series (Parasitology Res. Monogr., volume 12)

Abstract

The Rhine has been severely impacted by non-indigenous free-living and parasite species, largely triggered by the connection of the Ponto-Caspian and the Central European area due to the inauguration of the Main-Danube Canal in 1992. In the present review, we give a brief summary of species invasions in the Rhine with a focus on non-indigenous free-living and parasite species and related changes in species communities that have been recorded in the last decades. Among the most relevant invaders, we find the “killer shrimp,” Dikerogammarus villosus, and various species of gobiids. Together with non-indigenous hosts, several parasite species were introduced and stayed mostly with their original host, e.g., the monogenean Gyrodactylus proterorhini on gobiids and the acanthocephalan Paratenuisentis ambiguus in its specific non-indigenous intermediate host Gammarus tigrinus. Other parasites colonized indigenous host species after their introduction (parasite spillover), e.g., the monogeneans Pseudodactylogyrus bini and Pseudodactylogyrus anguillae, the nematode Anguillicola crassus, the tapeworm Schyzocotyle acheilognathi, and acanthocephalans of the genus Pomphorhynchus. As both A. crassus and Pomphorhynchus sp. use non-indigenous gobies as paratenic hosts, we also find an example of parasite spillover in the Rhine. Furthermore, in cases of co-infection of the same host, Pomphorhynchus sp. cysts in the gobies serve as a “refuge” for the larvae of A. crassus, which probably increases the efficiency of transmission to the eel final host. Therefore, this combination of an invasive host species and the two parasites is a unique example of an invasional meltdown. Finally, we illustrate the drastic changes in parasite communities caused by interactions of indigenous and non-indigenous species and their parasites, using the examples of eel and gobies as host species.

Keywords

Rhine history Fish parasites Invading fish species Richness in species 

References

  1. Adámek Z, Andreji J, Gallardo JM (2007) Food habits of four bottom-dwelling gobiid species at the confluence of the Danube and Hron rivers (South Slovakia). Int Rev Hydrobiol 92:554–563CrossRefGoogle Scholar
  2. Amin OM, Thielen F, Münderle M, Taraschewski H, Sures B (2008) Description of a new echinorhynchid species (Acanthocephala) from the European eel, Anguilla anguilla, in Germany, with a key to species of Acanthocephalus in Europe. J Parasitol 94:1299–1304PubMedCrossRefGoogle Scholar
  3. Bakke TA, Harris PD, Cable J (2007) The biology of gyrodactylid monogeneans: the “Russian-Doll Killers”. Adv Parasitol 64:161–376PubMedCrossRefGoogle Scholar
  4. Bašić T, Britton JR, Jackson MC, Reading P, Grey J (2014) Angling baits and invasive crayfish as important trophic subsidies for a large cyprinid fish. Aquat Sci 77:153–160CrossRefGoogle Scholar
  5. 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.  https://doi.org/10.1139/F02-098 CrossRefGoogle Scholar
  6. Borcherding J, Staas S, Krüger S, Ondračková M, Šlapanský L, Jurajda P (2011a) Non-native Gobiid species in the lower River Rhine (Germany): recent range extensions and densities. J Appl Ichthyol 27:153–155CrossRefGoogle Scholar
  7. Borcherding J, Gertzen S, Staas S (2011b) First record of Pontian racer goby, Babka gymnotrachelus (Gobiidae: Teleostei), in the River Rhine, Germany. J Appl Ichtyol 27:1399–1400CrossRefGoogle Scholar
  8. Buchmann K (1988) Epidemiology of pseudodactylogyrosis in an intensive eel-culture system. Dis Aquat Org 5:81–85CrossRefGoogle Scholar
  9. Buchmann K, Mellergaard S, Køie M (1987) Pseudodactylogyrus infections in eel: a review. Dis Aquat Org 3:51–57CrossRefGoogle Scholar
  10. Bullock WL, Samuel G (1975) Paratenuisentis gen. n. for Tanaorhamphus ambiguus Van Cleave 1921 (Acanthocephala), with reconsideration of the Tenuisentidae. J Parasitol 61:105–109PubMedCrossRefGoogle Scholar
  11. Christison KW, Baker GC (2007) First record of Pseudodactylogyrus anguillae (Yin & Sproston, 1948) (Monogenea) from South Africa. Afr Zool 42(2):279–285CrossRefGoogle Scholar
  12. Cone DK, Marcogliese DJ (1995) Pseudodactylogyrus anguillae on Anguilla rostrata in Nova Scotia: an endemic or an introduction? J Fish Biol 47:177–178Google Scholar
  13. Corkum LD, Sapota MR, Skora KE (2004) The round goby, Neogobius melanostomus, a fish invader on both sides of the Atlantic Ocean. Biol Invasions 6:173–181CrossRefGoogle Scholar
  14. Dangel KC, Keppel M, Tabujew K, Sures B (2014) Effects of Anguillicola novaezelandiae on the levels of cortisol and hsp70 in the European eel. Parasitol Res 113:3817–3822.  https://doi.org/10.1007/s00436-014-4049-8 CrossRefPubMedGoogle Scholar
  15. Dangel KC, Keppel M, Le TTY, Grabner D, Sures B (2015) Competing invaders: performance of two Anguillicola species in Lake Bracciano. Int J Parasitol Parasit Wildl 4:119–124CrossRefGoogle Scholar
  16. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife - threats to biodiversity and human health. Science 287:443–449PubMedCrossRefGoogle Scholar
  17. David GM, Staentzel C, Schlumberger O, Perrot-Minnot M-J, Beisel J, Hardion L (2018) A minimalist macroparasite diversity in the round goby of the upper Rhine reduced to an exotic acanthocephalan lineage. Parasitology 145:1020–1026PubMedCrossRefGoogle Scholar
  18. De Charleroy D, Grisez L, Thomas K, Belpaire C, Ollevier F (1990) The life cycle of Anguillicola crassus. Dis Aquat Org 8:77–84CrossRefGoogle Scholar
  19. Dezfuli BS, Lui A, Squerzanti S, Lorenzoni M, Shinn AP (2011) Confirmation of the hosts involved in the life cycle of an acanthocephalan parasite of Anguilla anguilla (L.) from Lake Piediluco and its effect on the reproductive potential of its amphipod intermediate host. Parasitol Res 110:2137–2143PubMedCrossRefGoogle Scholar
  20. Dick JTA, Platvoet D (2000) Invading predatory crustacean Dikerogammarus villosus eliminates both native and exotic species. Proc R Soc Lond B 267:977–983CrossRefGoogle Scholar
  21. 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(6):229–236Google Scholar
  22. 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:e53218PubMedPubMedCentralCrossRefGoogle Scholar
  23. Emde S, Kochmann J, Kuhn T, Plath M, Klimpel S (2014a) Getting what is served? Feeding ecology influencing parasite-host interactions in invasive round goby Neogobius melanostomus. PLoS One 9:e109971PubMedPubMedCentralCrossRefGoogle Scholar
  24. Emde S, Rueckert S, Kochmann J, Knopf K, Sures B, Klimpel S (2014b) Nematode eel parasite found inside acanthocephalan cysts - a “Trojan horse” strategy? Parasit Vectors 7:504PubMedPubMedCentralGoogle Scholar
  25. Emde S, Kochmann J, Kuhn T, Dörge DD, Plath M, Miesen FW, Klimpel S (2016) Cooling water of power plant creates “hot spots” for tropical fishes and parasites. Parasitol Res 115:85–98PubMedCrossRefGoogle Scholar
  26. Ergens R (1967) New species of the genus Gyrodactylus (Monogenoidea) from the Danube basin. Folia Parasitol 14:377–379Google Scholar
  27. Freyhof J, Huckstorf V (2006) Conservation and management of aquatic genetic resources: a critical checklist of German freshwater fishes, pp 113–126Google Scholar
  28. Gaevskaya AV, Dmitrieva EV (1997) Overview of Black Sea monogenean fauna. Ekologija morja 6:7–17Google Scholar
  29. Giger W (2007) Brandkatastrophe in Schweizerhalle 1986 - Rückblick und Bilanz. UWSF - Z Umweltchem Ökotox 19(1):11–23CrossRefGoogle Scholar
  30. Golovin PP (1977) Monogeneans of eel during its culture using heated water. Investigation of Monogenoidea in U.S.S.R. Zoological Institute, U.S.S.R. Academy of Sciences, Leningrad, pp 144–150Google Scholar
  31. Haas G, Brunke M, Streit B (2002) Fast turnover in dominance of exotic species in the Rhine River determines biodiversity and ecosystem function: an affair between amphipods and mussels. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe: distribution, impacts and management. Kluwer, Dordrecht, pp 426–432CrossRefGoogle Scholar
  32. Hayward CJ, Iwashita M, Crane JS, Ogawa K (2001) First report of the invasive eel pest Pseudodactylogyrus bini in North American eels. Dis Aquat Org 44:53–60PubMedCrossRefGoogle Scholar
  33. Hine PM, Kennedy CR (1974) Observations on the distribution, specificity and pathogenicity of the acanthocephalan Pomphorhynchus laevis (Müller). J Fish Biol 6:521–535.  https://doi.org/10.1111/j.1095-8649.1974.tb04569.x CrossRefGoogle Scholar
  34. Hohenadler MAA, Honka KI, Emde S, Klimpel S, Sures B (2018a) First evidence for a possible invasional meltdown among invasive fish parasites. Sci Rep 8:15085PubMedPubMedCentralCrossRefGoogle Scholar
  35. Hohenadler MAA, Nachev M, Thielen F, Taraschewski H, Grabner D, Sures B (2018b) Pomphorhynchus laevis: an invasive species in the river Rhine? Biol Invasions 20:207–217CrossRefGoogle Scholar
  36. Hohenadler MAA, Nachev M, Freese M, Pohlmann JD, Hanel R, Sures B (2019) How Ponto-Caspian invaders affect local parasite communities of native fish. Parasitol Res:1–13Google Scholar
  37. Huyse T, Vanhove MPM, Mombaerts M, Volckaert FAM, Verreycken H (2015) Parasite introduction with an invasive goby in Belgium: double trouble? Parasitol Res 114:2789–2793PubMedCrossRefGoogle Scholar
  38. Internationale Kommission zum Schutz des Rheins (IKSR, 2015) Die Biologie des Rheins Synthesebericht zum Rhein-Messprogramm Biologie 2012/2013 und nationale Bewertungen gemäß WRRL. Bericht Nr. 232, KoblenzGoogle Scholar
  39. Jakob 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 32:757–804CrossRefGoogle Scholar
  40. Johnson PTJ, Thieltges DW (2010) Diversity, decoys and the dilution effect: how ecological communities affect disease risk. J Exp Biol 213:961–970.  https://doi.org/10.1242/jeb.037721 CrossRefPubMedGoogle Scholar
  41. Jude DJ, Reider RH, Smith GR (1992) Establishment of Gobiidae in the Great Lakes Basin. Can J Fish Aquat Sci 49:416–421CrossRefGoogle Scholar
  42. Jurajda P, Černý J, Polačik M, Valová Z, Janáč M, Blažek R, Ondračková M (2005) The recent distribution and abundance of non-native Neogobius fishes in the Slovak section of the River Danube. J Appl Ichthyol 21:319–323CrossRefGoogle Scholar
  43. Kakareko T, Plachocki D, Kobak J (2009) Relative abundance of Ponto-Caspian gobiids in the lower Vistula River (Poland) 3- to 4 years after first appearance. J Appl Ichthyol 25:647–651CrossRefGoogle Scholar
  44. Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056PubMedCrossRefGoogle Scholar
  45. Kennedy CR (1993) Introductions, spread and colonization of new localities by fish helminth and crustacean parasites in the British Isles: a perspective and appraisal. J Fish Biol 43:287–301CrossRefGoogle Scholar
  46. Kennedy CR (1994) The ecology of introductions. In: Pike AW, Lewis JW (eds) Parasitic diseases of fish. Samara, Tresaith, pp 189–208Google Scholar
  47. Kennedy CR (2006) Ecology of the Acanthocephala. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  48. Kennedy CR, Broughton PF, Hine PM (1978) The status of brown and rainbow trout, Salmo trutta and S. gairdneri as hosts of the acanthocephalan, Pomphorhynchus laevis. J Fish Biol 13:265–275.  https://doi.org/10.1111/j.1095-8649.1978.tb03434.x CrossRefGoogle Scholar
  49. Keppel M, Dangel KC, Sures B (2016) The Hsp70 response of Anguillicola species to host-specific stressors. Parasitol Res 115:2149–2154PubMedCrossRefGoogle Scholar
  50. Kikuchi H (1929) Two new species of Japanese trematodes belonging to Gyrodactylidae. Annot Zool Jpn 12:175–186Google Scholar
  51. Kirk RS (2003) The impact of Anguillicola crassus on European eels. Fish Manag Ecol 10:385–394CrossRefGoogle Scholar
  52. Kiskároly M, Čanković M (1967) Pomphorhynchus bosniacus nov. sp. aus Barben Barbus barbus (L.) des Save-Gebietes. Zool Anz 182:69–74Google Scholar
  53. Kley A, Maier G (2006) Reproductive characteristics of invasive gammarids in the Rhine-Main-Danube catchment, South Germany. Limnologica 36:79–90.  https://doi.org/10.1016/j.limno.2006.01.002 CrossRefGoogle Scholar
  54. 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 80:129–136.  https://doi.org/10.1079/JOH2006353 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Kopp K, Jokela J (2007) Resistant invaders can convey benefits to native species. Oikos 116:295–301.  https://doi.org/10.1111/j.0030-1299.2007.15290.x CrossRefGoogle Scholar
  56. Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Kottelat, Cornol and Freyhof, Berlin, p 646Google Scholar
  57. Kováč V, Copp GH, Sousa RP (2009) Life-history traits of invasive bighead goby Neogobius kessleri from the middle Danube with a prediction of who will win the goby competition. J Appl Ichthyol 25:33–37CrossRefGoogle Scholar
  58. Krasnovyd V, Kvach Y, Drobiniak O (2012) The parasite fauna of the gobiid fish (Actinopterygii, Gobiidae) in the Sukhyi Lyman, Black Sea. Vestnik Zoologii 46:1–8CrossRefGoogle Scholar
  59. Krisp H, Maier G (2005) Consumption of macroinvertebrates by invasive and native gammarids: a comparison. J Limnol 64(1):55–59CrossRefGoogle Scholar
  60. Kuchta R, Choudhury A, Scholz T (2018) Asian fish tapeworm: the most successful invasive parasite in freshwaters. Trends Parasitol 34:511–523PubMedCrossRefGoogle Scholar
  61. Kvach Y (2002) The round goby’s parasites in native habitats and in a place of invasion. Oceanol Hydrobiol St 31:51–57Google Scholar
  62. Kvach Y (2004) The metazoan parasites of gobiids in the Dniester Estuary (Black Sea) depending on water salinity. Oceanol Hydrobiol Stud 33:47–56Google Scholar
  63. Kvach Y (2005) A comparative analysis of helminth faunas and infection of ten species of gobiid fishes (Actinopterigii: Gobiidae) from the North-Western Black Sea. Acta Ichtyol Piscat 35(2):103–110CrossRefGoogle Scholar
  64. Kvach Y, Skóra KE (2007) Metazoa parasites of the invasive round goby Apollonia melanostoma (Neogobius melanostomus) (Pallas) (Gobiidae: Osteichthyes) in the Gulf of Gdańsk, Baltic Sea, Poland: a comparison with the Black Sea. Parasitol Res 100(4):767–774PubMedCrossRefPubMedCentralGoogle Scholar
  65. Kvach Y, Boldryev V, Lohner R, Stepien CA (2015) The parasite community of gobiid fishes (Actinopterigyii: Gobiidae) from the lower Volga River region. Biologia 70:948–957CrossRefGoogle Scholar
  66. Lavrinčíková M, Kováč V (2007) Invasive round goby Neogobius melanostomus from the Danube mature at small size. J Appl Ichthyol 23:276–278CrossRefGoogle Scholar
  67. Lelek A, Köhler C (1990) Restoration of fish communities of the Rhine River two years after a heavy pollution wave. Regul Rivers Res Manag 5:57–66CrossRefGoogle Scholar
  68. Marcogliese DJ, Cone DK (1993) What metazoan parasites tell us about the evolution of American and European eels. Evolution 47:1632–1635PubMedCrossRefGoogle Scholar
  69. McHugh KJ, Weyl OLF, Smit NJ (2017) Parasite diversity of African longfin eel Anguilla mossambica Peters with comments on host response to the monogenean Pseudodactylogyrus anguillae (Yin and Sproston). J Fish Dis 40:959–961PubMedCrossRefGoogle Scholar
  70. Médoc V, Rigaud T, Motreuil S, Perrot-Minnot M-J, Bollache L (2011) Paratenic hosts as regular transmission route in the acanthocephalan Pomphorhynchus laevis: potential implications for food webs. Naturwissenschaften 98:825–835.  https://doi.org/10.1007/s00114-011-0831-y CrossRefPubMedGoogle Scholar
  71. Mierzejewska K, Martyniak A, Kakareko T, Dzika E, Stańczak K, Hliwa P (2011) Gyrodactylus proterorhini Ergens, 1967 (Monogenoidea, Gyrodactylidae) in gobiids from the Vistula River - the first record of the parasite in Poland. Parasitol Res 108:1147–1151PubMedCrossRefGoogle Scholar
  72. Mierzejewska K, Kvach Y, Woźniak M, Kosowska A, Dziekońska-Rynko J (2012) Parasites of an Asian Fish, the Chinese sleeper Perccottus glenii, in the Wloclawek reservoir on the lower Vistula River, Poland: in search of the key species in the host expansion process. Comp Parasitol 79:23–29CrossRefGoogle Scholar
  73. Nachev M, Sures B (2009) The endohelminth fauna of barbel (Barbus barbus) correlates with water quality of the Danube River in Bulgaria. Parasitology 136:545–552PubMedCrossRefGoogle Scholar
  74. Naidenova NN (1974) Parasite fauna of gobiid fishes of the Black Sea and Sea of Azov. Naukova Dumka, KievGoogle Scholar
  75. Nehring S (2003) Gebietsfremde Arten aus in den deutschen Gewässern – ein Risiko für die Biodiversität – Schriftenreihe des Bundesministeriums für Verbraucherschutz, Ernährung und Landwirtschaft. Reihe A: Angewandte Wissenschaft 498:40–52Google Scholar
  76. Oesterwind D, Bock C, Förster A, Gabel M, Henseler C, Kotterba P, Menge M, Myts D, Winkler HM (2017) Predator and prey: the role of the round goby Neogobius melanostomus in the western Baltic. Mar Biol Res 13:188–197CrossRefGoogle Scholar
  77. Ondračková M (2016) Gyrodactylus proterorhini in its non-native range: distribution and ability to host-switch in freshwaters. Parasitol Res 115(8):3153–3162PubMedCrossRefGoogle Scholar
  78. Ondračková M, Trichkova T, Jurajda P (2006) Present and historical occurrence of metazoan parasites in Neogobius kessleri (Pisces: Gobiidae) in the Bulgarian section of the Danube River. Acta Zool Bulg 58(3):399–406Google Scholar
  79. Ondračková M, Šimková A, Civáňová K, Vyskočilová M, Jurajda P (2012) Parasite diversity and microsatellite variability in native and introduced populations of four Neogobius species (Gobiidae). Parasitology 139:1493–1505PubMedCrossRefGoogle Scholar
  80. Ondračková M, Valová Z, Hudcová I, Michálková V, Šimková A, Borcherding J, Jurajda P (2015) Temporal effects on host-parasite associations in four naturalized goby species living in sympatry. Hydrobiologia 746:233–243CrossRefGoogle Scholar
  81. Özer A (2007) Metazoan parasite fauna of the round goby Neogobius melanostomus Pallas, 1811 (Perciformes: Gobiidae) collected from the Black Sea coast at Sinop, Turkey. J Nat His 41(9–12):483–492CrossRefGoogle Scholar
  82. Palstra AP, Heppener DFM, van Ginneken VJT, Székely C, van Den Thillart GEEJ (2007) Swimming performance of silver eels is severely impaired by the swim-bladder parasite Anguillicola crassus. J Exp Mar Bio Ecol 352:244–256CrossRefGoogle Scholar
  83. Parker D, Weyl OLF, Taraschewski H (2011) Invasion of a South African Anguilla mossambica (Anguillidae) population by the alien gill worm Pseudodactylogyrus anguillae (Monogenea). Afr Zool 46:371–377Google Scholar
  84. Pelster B (2015) Swimbladder function and the spawning migration of the European eel Anguilla anguilla. Front Physiol 6:1–10Google Scholar
  85. Perrot-Minnot M-J, Guyonnet E, Bollache L, Lagrue C (2019) Differential patterns of definitive host use by two fish acanthocephalans occurring in sympatry: Pomphorhynchus laevis and Pomphorhynchus tereticollis. Int J Parasitol Parasit Wildl 8:135–144.  https://doi.org/10.1016/j.ijppaw.2019.01.007 CrossRefGoogle Scholar
  86. Pinkster S, Smit H, Brandse-de Jong N (1977) The introduction of the alien amphipod Gammarus tigrinus Sexton, 1939, in the Netherlands and its competition with indigenous species. Crustaceana Suppl 4:91–105Google Scholar
  87. Pitronaci S (2016) Parasitengemeinschaften des Karpfens aus dem Rhein. Staatsexamensarbeit, Universität Duisburg-EssenGoogle Scholar
  88. 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. Int J Parasitol Parasit Wildl 8:145–155CrossRefGoogle Scholar
  89. Rewicz T, Grabowski M, MacNeil C, Bacela-Spychalska K (2014) The profile of a ‘perfect’ invader – the case of killer shrimp, Dikerogammarus villosus. Aquat Invasions 9:267–288.  https://doi.org/10.3391/ai.2014.9.3.04 CrossRefGoogle Scholar
  90. Sasal P, Taraschewski H, Valade P, Grondin H, Wielgoss S, Moravec F (2008) Parasite communities in eels of the Island of Reunion (Indian Ocean): a lesson in parasite introduction. Parasitol Res 102:1343–1350PubMedCrossRefGoogle Scholar
  91. Shears JA, Kennedy CR (2005) The life cycle of Paraquimperia tenerrima: a parasite of the European eel Anguilla anguilla. J Helminthol 79:169–176PubMedCrossRefGoogle Scholar
  92. Skóra KE, Stolarski J (1993) New fish species in the Gulf of Gdansk, Neogobius sp. [cf. Neogobius melanostomus (Pallas 1811)]. Bull Sea Fish Inst 1(128):83–84Google Scholar
  93. Špakulová M, Perrot-Minnot M-J, Neuhaus B (2011) Resurrection of Pomphorhynchus tereticollis (Rudolphi, 1809) (Acanthocephala: Pomphorhynchidae) based on new morphological and molecular data. Helminthologia 48:268–277CrossRefGoogle Scholar
  94. Steele DH, Steele VJ (1972) The biology of Gammarus (Crustacea, Amphipoda) in the northwestern Atlantic. VI. Gammarus tigrinus Sexton. Can J Zool 50(8):1063–1068.  https://doi.org/10.1139/z72-144 CrossRefGoogle Scholar
  95. Stemmer B (2008) Flussgrundel im Rhein-Gewässersystem. Natur in NRW 4/08:57–60Google Scholar
  96. Sures B (2011) Parasites of animals. In: Simberloff D, Rejmánek M (eds) Encyclopedia of biological invasions. University of California Press, Berkeley, pp 500–503Google Scholar
  97. Sures B, Knopf K (2004) Parasites as a threat to freshwater eels? Science 304:208–209CrossRefGoogle Scholar
  98. Sures B, Streit B (2001) Eel parasite diversity and intermediate host abundance in the River Rhine, Germany. Parasitology 123:185–191PubMedCrossRefGoogle Scholar
  99. Sures B, Knopf K, Wurtz 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 119:323–330PubMedCrossRefGoogle Scholar
  100. Sures B, Knopf K, Kloas W (2001) Induction of stress by the swimbladder nematode Anguillicola crassus in European eels, Anguilla anguilla, after repeated experimental infection. Parasitology 123:179–184.  https://doi.org/10.1017/S003118200100823X CrossRefPubMedGoogle Scholar
  101. Sures B, Nachev M, Pahl M, Grabner D, Selbach C (2017) Parasites as drivers of key processes in aquatic ecosystems: facts and future directions. Exp Parasitol 180:141–147.  https://doi.org/10.1016/j.exppara.2017.03.011 CrossRefPubMedGoogle Scholar
  102. Taraschewski H (2006) Hosts and parasites as aliens. J Helminthol 80:99–128PubMedCrossRefGoogle Scholar
  103. Taraschewski H, Moravec F, Lamah T, Anders K (1987) Distribution and morphology of two helminths recently introduced into European eel populations: Anguillicola crassus (Nematoda Drancunculoidea) and Paratenuisentis ambiguus (Acanthocephala, Tenuisentidae). Dis Aquat Org 3:167–176CrossRefGoogle Scholar
  104. Telfer S, Bown KJ, Sekules R, Begon M, Hayden T, Birtles R (2005) Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130:661–668.  https://doi.org/10.1017/S0031182005007250 CrossRefPubMedGoogle Scholar
  105. Thiel R, Horn L, Knörr C, Tonn M (2014) Analyse der ökologischen Einnischung der invasiven Schwarzmundgrundel in relevanten Brack und Süßgewässerhabitaten Schleswig Holsteins. Final Report. Landesamt für Landwirtschaft, Umwelt und ländliche Räume Schleswig Holstein, p 199Google Scholar
  106. 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 81:179–189PubMedCrossRefGoogle Scholar
  107. Thielen F, Weibel U, Hirt J, Münderle M, Marten M, Taraschewski H, Sures B (2008) Ichthyofauna in the upper Rhine River close to the city of Karlsruhe as determined by the analysis of fish impingement by cooling-water intakes of a power plant. Limnologica 38:76–85CrossRefGoogle Scholar
  108. Thieltges DW, Reise K, Prinz K, Jensen KT (2008) Invaders interfere with native parasite–host interactions. Biol Invasions 11:1421–1429CrossRefGoogle Scholar
  109. Tittizer T, Krebs F (1996) Ökosystem-Forschung: Der Rhein und seine Auen. Springer, Berlin, p 468CrossRefGoogle Scholar
  110. Tittizer T, Schöll F, Banning M, Haybach A, Schleuter M (2000) Aquatic neozoan invertebrates in the inland water ways of the Federal Republic of Germany. Lauterbornia 39:1–72Google Scholar
  111. Torchin M, Lafferty K, Dobson A (2003) Introduced species and their missing parasites. Nature 421:628–630PubMedCrossRefGoogle Scholar
  112. van Beek GCW (2006) The round goby Neogobius melanostomus first recorded in Netherlands. Aquat Invasions 1:42–43CrossRefGoogle Scholar
  113. van Kessel N, Dorenbosch M, Spikmans F (2009) First record of Pontian monkey goby, Neogobius fluviatilis (Pallas, 1814), in the Dutch Rhine. Aquat Invasions 4:421–424CrossRefGoogle Scholar
  114. Villeneuve C De HV (1996) Western Europe’s artery: the Rhine. Nat Resour J 36:441–454Google Scholar
  115. Wilken RD (2006) The recovered Rhine and its history. In: Knepper TP (ed) The Rhine: the handbook of environmental chemistry, vol 5L. Springer, BerlinCrossRefGoogle Scholar
  116. Würtz J, Taraschewski H (2000) Histopathological changes in the swimbladder wall of the European eel Anguilla anguilla due to infections with Anguillicola crassus. Dis Aquat Org 39:121–134PubMedCrossRefGoogle Scholar
  117. Würtz J, Taraschewski H, Pelster B (1996) Changes in gas composition in the swimbladder of the European eel (Anguilla anguilla) infected with Anguillicola crassus (Nematoda). Parasitology 112:233–238PubMedCrossRefGoogle Scholar
  118. Würtz J, Knopf K, Taraschewski H (1998) Distribution and prevalence of Anguillicola crassus (Nematoda) in eels Anguilla anguilla of the rivers Rhine and Naab, Germany. Dis Aquat Org 32:137–143PubMedCrossRefGoogle Scholar
  119. Zittel M, Grabner D, Wlecklik A, Sures B, Leese F, Taraschewski H, Weigand AM (2018) Cryptic species and their utilization of indigenous and non-indigenous intermediate hosts in the acanthocephalan Polymorphus minutus sensu lato (Polymorphidae). Parasitology 145:1421–1429PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Aquatic Ecology and Centre for Water and Environmental ResearchUniversity of Duisburg-EssenEssenGermany
  2. 2.Department of ZoologyUniversity of JohannesburgJohannesburgSouth Africa

Personalised recommendations