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Parasitology Research

, Volume 115, Issue 1, pp 85–98 | Cite as

Cooling water of power plant creates “hot spots” for tropical fishes and parasites

  • Sebastian Emde
  • Judith Kochmann
  • Thomas Kuhn
  • Dorian D. Dörge
  • Martin Plath
  • Friedrich W. Miesen
  • Sven Klimpel
Original Paper

Abstract

Thermally altered water bodies can function as “hot spots” where non-native species are establishing self-sustaining populations beyond their tropical and subtropical native regions. Whereas many tropical fish species have been found in these habitats, the introduction of non-native parasites often remains undetected. Here, n = 77 convict cichlids (Amatitlania nigrofasciata) were sampled by electro-fishing at two sites from a thermally altered stream in Germany and examined for parasite fauna and feeding ecology. Stomach content analysis suggests an opportunistic feeding strategy of A. nigrofasciata: while plant material dominated the diet at the warm water inlet (∼30 °C), relative contributions of insects, plants, and crustaceans were balanced 3 km downstream (∼27 °C). The most abundant non-native parasite species was the tropical nematode Camallanus cotti with P = 11.90 % and P = 80.00 % at the inlet and further downstream, respectively. Additionally, nematode larvae of Anguillicoloides crassus and one specimen of the subtropical species Bothriocephalus acheilognathi were isolated. A. nigrofasciata was also highly infected with the native parasite Acanthocephalus anguillae, which could be linked to high numbers of the parasite’s intermediate host Asellus aquaticus. The aim of this study was to highlight the risk and consequences of the release and establishment of ornamental fish species for the introduction and spread of non-indigenous metazoan parasites using the convict cichlid as a model species. Furthermore, the spread of non-native parasites into adjacent fish communities needs to be addressed in the future as first evidence of Camallanus cotti in native fish species was also found.

Keywords

Thermal alteration Invasive species Tropical fish Camallanus cotti Amatitlania nigrofasciata Acanthocephalus anguillae 

Notes

Acknowledgments

The authors would like to thank U. Rose (Erftverband and Erftfischereigenossenschaft) for supporting this study and the permission to conduct surveys at the Gillbach, F. Wegmann (Untere Fischereibehörde Rhein-Erft-Kreis) for the electro-fishing permit, F. Herder (Zoologisches Forschungsmuseum Alexander Koenig) for supporting the study, S. Müller and F. Droppelmann (Zoologisches Forschungsmuseum Alexander Koenig), as well as J. Jourdan and J. Münster (Goethe-University, Senckenberg Gesellschaft für Naturforschung) and Eva Grimm (University of Würzburg) for support during fieldwork and with logistics.

Compliance with ethical standards

Permits and approvals (No. 39.74.20, Stream section Niederaußem - Gill) for electro-fishing were obtained from U. Rose (Erftverband and Erftfischereigenossenschaft) and F. Wegmann (Untere Fischereibehörde Rhein-Erft-Kreis) and included the sampling of fish for research purposes. All fish were immediately euthanized and stored on ice according to the German Animal Protection Law (§ 4) and the ordinance of slaughter and killing of animals (Tierschlachtverordnung § 13). No living or protected animals were used.

Supplementary material

436_2015_4724_MOESM1_ESM.doc (66 kb)
Online Resource 1 Methodology and results of molecular analysis (DOC 65 kb)

References

  1. Aarestrup K, Okland F, Hansen MM et al (2009) Oceanic spawning migration of the European eel (Anguilla anguilla). Science 325:1660. doi: 10.1126/science.1178120 CrossRefPubMedGoogle Scholar
  2. Amundsen P-A, Gabler H-M, Staldvik FJ (1996) A new approach to graphical analysis of feeding strategy from stomach contents data—modification of the Costello (1990) method. J Fish Biol 48:607–614. doi: 10.1111/j.1095-8649.1996.tb01455.x Google Scholar
  3. Brattey J (1986) Life history and population biology of larval Acanthocephalus lucii (Acanthocephala: Echinorhynchidae) in the isopod Asellus aquaticus. J Parasitol 72:633. doi: 10.2307/3281450 CrossRefPubMedGoogle Scholar
  4. Brown AF, Chubb JC, Veltkamp CJ (1986) A key to the species of Acanthocephala parasitic in British freshwater fishes. J Fish Biol 28:327–334CrossRefGoogle Scholar
  5. Busch MW, Kuhn T, Münster J, Klimpel S (2012) Marine crustaceans as potential hosts and vectors for metazoan parasites. In: Mehlhorn H (ed) Arthropods as vectors of emerging diseases. Springer, Berlin, pp 329–360CrossRefGoogle Scholar
  6. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583. doi: 10.2307/3284227 CrossRefPubMedGoogle Scholar
  7. Conn DB (2014) Aquatic invasive species and emerging infectious disease threats: a one health perspective. Aquat Invasions 9:383–390. doi: 10.3391/ai.2014.9.3.12 CrossRefGoogle Scholar
  8. Deacon AE, Ramnarine IW, Magurran AE (2011) How reproductive ecology contributes to the spread of a globally invasive fish. PLoS One 6, e24416. doi: 10.1371/journal.pone.0024416 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Dezfuli BS, Rossetti E, Rossi R, Fano EA (1994) Occurrence of larval Acanthocephalus anguillae (Acanthocephala) in the Asellus aquaticus (Crustacea, Isopoda) from the river Brenta. Boll Zool 61:77–81. doi: 10.1080/11250009409355862 CrossRefGoogle Scholar
  10. Douda K, Lopes-Lima M, Hinzmann M et al (2013) Biotic homogenization as a threat to native affiliate species: fish introductions dilute freshwater mussel’s host resources. Divers Distrib 19:933–942. doi: 10.1111/ddi.12044 CrossRefGoogle Scholar
  11. Dove ADM, Fletcher AS (2000) The distribution of the introduced tapeworm Bothriocephalus acheilognathi in Australian freshwater fishes. J Helminthol 74:121–127. doi: 10.1017/S0022149X00000160 PubMedGoogle Scholar
  12. Dudgeon D, Arthington AH, Gessner MO et al (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163. doi: 10.1017/S1464793105006950 CrossRefPubMedGoogle Scholar
  13. Eldredge LG (2000) Non-indigenous freshwater fishes, amphibians, and crustaceans of the Pacific and Hawaiian islands. In: Sherley G (ed) Invasive species in the Pacific: a technical review and draft regional strategy. South Pacific Regional Environment Programme, Samoa, pp 173–190Google Scholar
  14. 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, e53218. doi: 10.1371/journal.pone.0053218 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Emde S, Kochmann J, Kuhn T et al (2014a) Getting what is served? Feeding ecology influencing parasite-host interactions in invasive round goby Neogobius melanostomus. PLoS One 9, e109971. doi: 10.1371/journal.pone.0109971 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Emde S, Rueckert S, Kochmann J et al (2014b) Nematode eel parasite found inside acanthocephalan cysts—a “Trojan horse” strategy? Parasit Vectors 7:504PubMedPubMedCentralGoogle Scholar
  17. Esmaeli HR, Teimori A, Owfi F et al (2014) Alien and invasive freshwater fish species in Iran: diversity, environmental impacts and management. Iran J Ichthyol 1:61–72Google Scholar
  18. Evans BB, Lester RJ (2001) Parasites of ornamental fish imported into Australia. Bull Eur Assoc Fish Pathol 21:51–55Google Scholar
  19. Font WF, Tate DC (1994) Helminth parasites of native Hawaiian freshwater fishes: an example of extreme ecological isolation. J Parasitol 80:682–688. doi: 10.2307/3283246 CrossRefPubMedGoogle Scholar
  20. Fox MG, Vila-Gispert A, Copp GH (2007) Life-history traits of introduced Iberian pumpkinseed Lepomis gibbosus relative to native populations. Can differences explain colonization success? J Fish Biol 71:56–69. doi: 10.1111/j.1095-8649.2007.01683.x CrossRefGoogle Scholar
  21. Froese R, Pauly D (2015) FishBase. In: World wide web electron. Publ. Wwwfishbaseorg. http://www.fishbase.org/. Accessed 13 Apr 2015
  22. Gollasch S, Nehring S (2006) National checklist for aquatic alien species in Germany. Aquat Invasions 1:245–269. doi: 10.3391/ai.2006.1.4.8 CrossRefGoogle Scholar
  23. Golvan YJ (1969) Systématique des Acanthocéphales (Acanthocephala, Rudolphi 1801). Muséum, ParaisGoogle Scholar
  24. Heitlinger EG, Laetsch DR, Weclawski U et al (2009) Massive encapsulation of larval Anguillicoloides crassus in the intestinal wall of Japanese eels. Parasit Vectors 2:48. doi: 10.1186/1756-3305-2-48 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Herlyn H, Ehlers U (2001) Organisation of the praesoma in Acanthocephalus anguillae (Acanthocephala, Palaeacanthocephala) with special reference to the muscular system. Zoomorphology 121:13–18CrossRefGoogle Scholar
  26. Higgins RP, Thiel H (1988) Introduction to the study of meiofauna. Smithsonian Institution PressGoogle Scholar
  27. Hill J, Cichra C (2005) Eradication of a reproducing population of convict cichlids, Cichlasoma nigrofasciatum (Cichlidae) in north-central Florida. Fla Sci 68:65–74Google Scholar
  28. Höfer S, Staas S (1998) Bericht zur fischereibiologischen Untersuchung des Gillbaches im Bereich Bergheim-Auenheim. Zoologisches Institut der Universität zu Köln, Abt. Allgemeine Ökologie und Limnologie, KölnGoogle Scholar
  29. Hoffmann GL, Schubert G (1984) Some parasite of exotic fishes. In: Courtenay WR Jr, Stauffer JR Jr (eds) Distribution, biology, and management of exotic fishes. The Johns Hopkins University Press, Baltimore, pp 233–261Google Scholar
  30. Holdich DM, Tolba MR (1981) The effect of temperature and water quality on the in vitro development and survival of Asellus aquaticus (Crustacea: Isopoda) eggs. Hydrobiologia 78:227–236CrossRefGoogle Scholar
  31. Holtfreter MC, Moné H, Müller-Stöver I et al (2014) Schistosoma haematobium infections acquired in Corsica, France, August 2013. Euro Surveill 19:20821CrossRefPubMedGoogle Scholar
  32. Hussner A, Lösch R (2005) Alien aquatic plants in a thermally abnormal river and their assembly to neophyte-dominated macrophyte stands (River Erft, Northrhine-Westphalia). Limnol Ecol Manag Inland Waters 35:18–30. doi: 10.1016/j.limno.2005.01.001 CrossRefGoogle Scholar
  33. Hyslop EJ (1980) Stomach contents analysis—a review of methods and their application. J Fish Biol 17:411–429. doi: 10.1111/j.1095-8649.1980.tb02775.x CrossRefGoogle Scholar
  34. Ishikawa T, Tachihara K (2008) Age, growth and maturation of the redbelly tilapia Tilapia zillii introduced into the Haebaru reservoir on Okinawa-Jima Island. Fish Sci 74:527–532. doi: 10.1111/j.1444-2906.2008.01555.x CrossRefGoogle Scholar
  35. Ishikawa T, Tachihara K (2010) Life history of the nonnative convict cichlid Amatitlania nigrofasciata in the Haebaru reservoir on Okinawa-Jima Island, Japan. Environ Biol Fish 88:283–292. doi: 10.1007/s10641-010-9641-x CrossRefGoogle Scholar
  36. Jeschke JM, Strayer DL (2005) Invasion success of vertebrates in Europe and North America. Proc Natl Acad Sci U S A 102:7198–7202CrossRefPubMedPubMedCentralGoogle Scholar
  37. Jourdan J, Miesen FW, Zimmer C et al (2014) On the natural history of an introduced population of guppies (Poecilia reticulata Peters, 1859) in Germany. BioInvasions Rec 3:175–184CrossRefGoogle Scholar
  38. Karvonen A, Kristjánsson BK, Skúlason S et al (2013) Water temperature, not fish morph, determines parasite infections of sympatric Icelandic threespine sticklebacks (Gasterosteus aculeatus). Ecol Evol 3:1507–1517. doi: 10.1002/ece3.568 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kelly DW, Paterson RA, Townsend CR et al (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90:2047–2056CrossRefPubMedGoogle Scholar
  40. Kempkes M (2010) Die Guppys: Gesamtausgabe, Band 1 und 2. Wolf, VerlagsKGGoogle Scholar
  41. Kirk RS (2003) The impact of Anguillicola crassus on European eels. Fish Manag Ecol 10:385–394. doi: 10.1111/j.1365-2400.2003.00355.x CrossRefGoogle Scholar
  42. Klotz W, Miesen FW, Hüllen S et al (2013) Two Asian fresh water shrimp species found in a thermally polluted stream system in North Rhine-Westphalia, Germany. Aquat Invasions 8:333–339CrossRefGoogle Scholar
  43. Knopf K, Lucius R (2008) Vaccination of eels (Anguilla japonica and Anguilla anguilla) against Anguillicola crassus with irradiated L3. Parasitology 135:633–640. doi: 10.1017/S0031182008004162 CrossRefPubMedGoogle Scholar
  44. Korhonen AI, Lagerspetz KYH (1996) Heat shock response and thermal acclimation in Asellus aquaticus. J Therm Biol 21:49–56. doi: 10.1016/0306-4565(95)00020-8 CrossRefGoogle Scholar
  45. Körting W (1975) Larval development of Bothriocephalus sp. (Cestoda: Pseudophyllidea) from carp (Cyprinus carpio L.) in Germany. J Fish Biol 7:727–733CrossRefGoogle Scholar
  46. Kupryanova RA (1954) On the biology of fish nematodes Camallanus lacustris (Zoega, 1776) and Camallanus truncatus (Rudolphi, 1814) (Nematoda: Spirurida). Dokl AN SSSR 97:373–376Google Scholar
  47. Kvach Y, Kornyychuk Y, Mierzejewska K, Rubtsova N, Yurakhno V, Grabowska J, Ovcharenko M (2014) Parasitization of invasive gobiids in the eastern part of the Central trans-European corridor of invasion of Ponto-Caspian hydrobionts. Parasitol Res 113:1605–1624. doi: 10.1007/s00436-009-1384-2 CrossRefPubMedGoogle Scholar
  48. Lavery RJ, Keenleyside MHA (1990) Filial cannibalism in the biparental fish Cichlasoma nigrofasciatum (Pisces: Cichlidae) in response to early brood reductions. Ethology 86:326–338. doi: 10.1111/j.1439-0310.1990.tb00440.x CrossRefGoogle Scholar
  49. Lefebvre F, Fazio G, Crivelli AJ (2012) Anguillicoloides crassus. In: Woo PTK, Buchmann K (eds) Fish parasites: pathobiology and protection. CABI, Wallingford, pp 310–326CrossRefGoogle Scholar
  50. Lever C (1996) Naturalized fishes of the world. Academic, CaliforniaGoogle Scholar
  51. Levsen A, Berland B (2002) The development and morphogenesis of Camallanus cotti Fujita, 1927 (Nematoda: Camallanidae), with notes on its phylogeny and definitive host range. Syst Parasitol 53:29–37. doi: 10.1023/A:1019955917509 CrossRefPubMedGoogle Scholar
  52. Macnab V, Barber I (2012) Some (worms) like it hot: fish parasites grow faster in warmer water, and alter host thermal preferences. Glob Chang Biol 18:1540–1548. doi: 10.1111/j.1365-2486.2011.02595.x CrossRefGoogle Scholar
  53. Mcminn H (1990) Effects of the nematode parasite Camallanus cotti on sexual and non-sexual behaviors in the guppy (Poecilia reticulata). Am Zool 30:245–249. doi: 10.1093/icb/30.2.245 CrossRefGoogle Scholar
  54. Menezes RC, Tortelly R, Tortelly-Neto R et al (2006) Camallanus cotti Fujita, 1927 (Nematoda, Camallanoidea) in ornamental aquarium fishes: pathology and morphology. Mem Inst Oswaldo Cruz 101:683–687CrossRefPubMedGoogle Scholar
  55. Moravec F (1998) Nematodes of freshwater fishes of the neotropical region. Academia PrahaGoogle Scholar
  56. Moravec F (2013) Parasitic nematodes of freshwater fishes of Europe. AcademiaGoogle Scholar
  57. Murray JB, Wingard GL, Phillips EC (2010) Distribution of the non-native gastropod Melanoides tuberculatus in Biscayne National Park, Florida. US Geol Surv Open File Rep 2010:18Google Scholar
  58. Neumann W (1985) Schwimmblasenparasit Anguillicola bei Aalen. Fisch Teichwirt 11:322Google Scholar
  59. Noonan KC (1983) Female mate choice in the cichlid fish Cichlasoma nigrofasciatum. Anim Behav 31:1005–1010. doi: 10.1016/S0003-3472(83)80005-0 CrossRefGoogle Scholar
  60. 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. doi: 10.1007/s00436-009-1384-2 CrossRefPubMedGoogle Scholar
  61. Padilla DK, Williams SL (2004) Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Front Ecol Environ 2:131–138CrossRefGoogle Scholar
  62. Palstra AP, Heppener DFM, van Ginneken VJT et al (2007) Swimming performance of silver eels is severely impaired by the swim-bladder parasite Anguillicola crassus. J Exp Mar Biol Ecol 352:244–256. doi: 10.1016/j.jembe.2007.08.003 CrossRefGoogle Scholar
  63. Paolucci EM, MacIsaac HJ, Ricciardi A (2013) Origin matters: alien consumers inflict greater damage on prey populations than do native consumers. Divers Distrib 19:988–995. doi: 10.1111/ddi.12073 CrossRefGoogle Scholar
  64. Paterson RA, Townsend CR, Poulin R, Tompkins DM (2011) Introduced brown trout alter native acanthocephalan infections in native fish: trout alter native host-parasite dynamics. J Anim Ecol 80:990–998. doi: 10.1111/j.1365-2656.2011.01834.x CrossRefPubMedGoogle Scholar
  65. Paull SH, LaFonte BE, Johnson PTJ (2012) Temperature-driven shifts in a host-parasite interaction drive nonlinear changes in disease risk. Glob Chang Biol 18:3558–3567. doi: 10.1111/gcb.12018 CrossRefGoogle Scholar
  66. Piazzini S, Lori E, Favilli L et al (2010) A tropical fish community in thermal waters of southern Tuscany. Biol Invasions 12:2959–2965. doi: 10.1007/s10530-010-9695-x CrossRefGoogle Scholar
  67. Pinkas L, Oliphant MS, Iverson ILK (1971) Food habits study. Fish Bull 152:5–10Google Scholar
  68. Pool DW, Chubb JC (1985) A critical scanning electron microscope study of the scolex of Bothriocephalus acheilognathi Yamaguti, 1934, with a review of the taxonomic history of the genus Bothriocephalus parasitizing cyprinid fishes. Syst Parasitol 7:199–211CrossRefGoogle Scholar
  69. Prenter J, MacNeil C, Dick JT, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390. doi: 10.1016/j.tree.2004.05.002 CrossRefPubMedGoogle Scholar
  70. Rabitsch W, Milasowszky N, Nehring S et al (2013) The times are changing: temporal shifts in patterns of fish invasions in central European fresh waters. J Fish Biol 82:17–33. doi: 10.1111/j.1095-8649.2012.03457.x CrossRefPubMedGoogle Scholar
  71. Roll U, Dayan T, Simberloff D, Goren M (2007) Characteristics of the introduced fish fauna of Israel. Biol Invasions 9:813–824. doi: 10.1007/s10530-006-9083-8 CrossRefGoogle Scholar
  72. Salgado-Maldonado G (2008) Helminth parasites of freshwater fish from Central America. Zootaxa 1915:29–53Google Scholar
  73. Salgado-Maldonado G (2013) Redescription of Neoechinorhynchus (Neoechinorhynchus) golvani Salgado-Maldonado, 1978 (Acanthocephala: Neoechinorhynchidae) and description of a new species from freshwater cichlids (Teleostei: Cichlidae) in Mexico. Parasitol Res 112:1891–1901. doi: 10.1007/s00436-013-3374-7 CrossRefPubMedGoogle Scholar
  74. Salgado-Maldonado G, Pineda-López RF (2003) The Asian fish tapeworm Bothriocephalus acheilognathi: a potential threat to native freshwater fish species in Mexico. Biol Invasions 5:261–268CrossRefGoogle Scholar
  75. Salgado-Maldonado G, Rubio-Godoy M (2014) Helmintos parásitos de peces de agua dulce introducidos. In: Mendoza R, Koleff P (coords.) Especies acuáticas invasoras en México. Com Nac Para El Conoc Uso Biodivers México, pp 269–285Google Scholar
  76. Sandlund OT, Daverdin RH, Choudhury A et al (2010) A survey of freshwater fishes and their macroparasites in the Guanacaste Conservation Area (ACG), Costa RicaGoogle Scholar
  77. Storey AW, Edward DHD, Gazey P (1991) Surber and kick sampling: a comparison for the assessment of macroinvertebrate community structure in streams of south-western Australia. Hydrobiologia 211:111–121CrossRefGoogle Scholar
  78. Strayer DL (2012) Eight questions about invasions and ecosystem functioning. Ecol Lett 15:1199–1210. doi: 10.1111/j.1461-0248.2012.01817.x CrossRefPubMedGoogle Scholar
  79. Strayer DL, Dudgeon D (2010) Freshwater biodiversity conservation: recent progress and future challenges. J N Am Benthol Soc 29:344–358. doi: 10.1899/08-171.1 CrossRefGoogle Scholar
  80. Studer A, Thieltges D, Poulin R (2010) Parasites and global warming: net effects of temperature on an intertidal host–parasite system. Mar Ecol Prog Ser 415:11–22. doi: 10.3354/meps08742 CrossRefGoogle Scholar
  81. Stumpp M (1975) Untersuchungen zur Morphologie und Biologie von Camallanus cotti (Fujita, 1927). Parasitol Res 46:277–290. doi: 10.1007/BF00418521 Google Scholar
  82. Sures B, Knopf K (2004) Parasites as a threat to freshwater eels? Science 304:209–211. doi: 10.1126/science.304.5668.209 CrossRefPubMedGoogle Scholar
  83. Tachihara K, Tokunaga K, Chimura Y (2002) Alien fishes in Okinawa Island. In: Ecological Society of Japan (ed) Handbook of alien species in Japan. Chijin-Shokan Tokyo Jpn, pp 248–249Google Scholar
  84. Taraschewski H (1988) Host-parasite interface of fish acanthocephalans. I: Acanthocephalus anguillae (Palaeacanthocephala) in naturally infected fishes: LM and TEM investigations. Dis Aquat Organ 4:109–119CrossRefGoogle Scholar
  85. Trujillo-Jiménez P (1998) Trophic spectrum of the cichlids Cichlasoma (Parapetenia) istlanum and Cichlasoma (Arconcentrus) nigrofasciatum in the Amacuzac River, Morelos, Mexico. J Freshw Ecol 13:465–473. doi: 10.1080/02705060.1998.9663643 CrossRefGoogle Scholar
  86. van Ginneken V, Ballieux B, Willemze R et al (2005) Hematology patterns of migrating European eels and the role of EVEX virus. Comp Biochem Physiol Part C Toxicol Pharmacol 140:97–102. doi: 10.1016/j.cca.2005.01.011 CrossRefGoogle Scholar
  87. Vincent AG, Font WF (2003) Seasonal and yearly population dynamics of two exotic helminths, Camallanus cotti (Nematoda) and Bothriocephalus acheilognathi (Cestoda), parasitizing exotic fishes in Waianu Stream, O’ahu, Hawaii. J Parasitol 89:756–760. doi: 10.1645/GE-90R CrossRefPubMedGoogle Scholar
  88. 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 Ecol 17:3478–3495. doi: 10.1111/j.1365-294X.2008.03855.x CrossRefPubMedGoogle Scholar
  89. Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1666. doi: 10.2307/2265769 CrossRefGoogle Scholar
  90. Wu S, Wang G, Gao D et al (2007) Occurrence of Camallanus cotti in greatly diverse fish species from Danjiangkou Reservoir in central China. Parasitol Res 101:467–471. doi: 10.1007/s00436-007-0472-4 CrossRefPubMedGoogle Scholar
  91. 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 112:233–238. doi: 10.1017/S003118200008481X CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Sebastian Emde
    • 1
  • Judith Kochmann
    • 1
  • Thomas Kuhn
    • 1
  • Dorian D. Dörge
    • 1
  • Martin Plath
    • 2
  • Friedrich W. Miesen
    • 3
  • Sven Klimpel
    • 1
  1. 1.Institute for Ecology, Evolution and Diversity, Senckenberg Biodiversity and Climate Research CentreGoethe-University, Senckenberg Gesellschaft für NaturforschungFrankfurt/M.Germany
  2. 2.College of Animal Science and TechnologyNorthwest A&F UniversityYanglingPeople’s Republic of China
  3. 3.Sektion IchthyologieZoologisches Forschungsmuseum Alexander KoenigBonnGermany

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