Nematode eel parasite found inside acanthocephalan cysts - a "Trojan horse" strategy?

Abstract Background The invasive eel parasite Anguillicoloides crassus (syn. Anguillicola crassus) is considered one of the major causes for the decline of the European eel (Anguilla anguilla) panmictic population. It impairs the swim bladder function and reduces swimming performance of its host. Th...

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Main Authors: Sebastian Emde, Sonja Rueckert, Judith Kochmann, Klaus Knopf, Bernd Sures, Sven Klimpel
Format: Article
Language:English
Published: BMC 2014-11-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-014-0504-8
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author Sebastian Emde
Sonja Rueckert
Judith Kochmann
Klaus Knopf
Bernd Sures
Sven Klimpel
author_facet Sebastian Emde
Sonja Rueckert
Judith Kochmann
Klaus Knopf
Bernd Sures
Sven Klimpel
author_sort Sebastian Emde
collection DOAJ
description Abstract Background The invasive eel parasite Anguillicoloides crassus (syn. Anguillicola crassus) is considered one of the major causes for the decline of the European eel (Anguilla anguilla) panmictic population. It impairs the swim bladder function and reduces swimming performance of its host. The life cycle of this parasite involves different intermediate and paratenic hosts. Despite an efficient immune system of the paratenic fish hosts acting against infections with A. crassus, levels of parasitized eels remain high in European river systems. Recently, the round goby Neogobius melanostomus (Gobiidae) has become dominant in many rivers in Europe and is still spreading at a rapid pace. This highly invasive species might potentially act as an important, so far neglected paratenic fish host for A. crassus. Methods Based on own observations and earlier single sightings of A. crassus in N. melanostomus, 60 fresh individuals of N. melanostomus were caught in the Rhine River and examined to assess the infection levels with metazoan parasites, especially A. crassus. Glycerin preparations were used for parasite identification. Results The parasite most frequently found in N. melanostomus was the acanthocephalan Pomphorhynchus sp. (subadult stage) which occurred mainly encysted in the mesenteries and liver. Every third gobiid (P = 31.7%) was infected by A. crassus larvae (L3) which exclusively occurred inside the acanthocephalan cysts. No intact or degenerated larvae of A. crassus were detected elsewhere in the goby, neither in the body cavity and mesenteries nor in other organs. Affected cysts contained the acanthocephalan larvae and 1-12 (mI =3) living A. crassus larvae. Additionally, encysted larvae of the nematode Raphidascaris acus were detected in the gobies, but only in the body cavity and not inside the acanthocephalan cysts. Conclusions Based on our observations, we suggest that A. crassus might actively bypass the immune response of N. melanostomus by invading the cysts of acanthocephalan parasites of the genus Pomphorhynchus using them as "Trojan horses". Providing that eels prey on the highly abundant round goby and that the latter transfers viable infective larvae of A. crassus, the new paratenic host might have a strong impact on the epidemiology of A. crassus.
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spelling doaj.art-f295f7ee020f416db7802cad9813155c2023-06-04T11:18:34ZengBMCParasites & Vectors1756-33052014-11-01711510.1186/s13071-014-0504-8Nematode eel parasite found inside acanthocephalan cysts - a "Trojan horse" strategy?Sebastian Emde0Sonja Rueckert1Judith Kochmann2Klaus Knopf3Bernd Sures4Sven Klimpel5Goethe-University (GU), Institute for Ecology, Evolution and Diversity; Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft für Naturforschung (SGN)School of Life, Sport and Social Sciences, Edinburgh Napier UniversityGoethe-University (GU), Institute for Ecology, Evolution and Diversity; Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft für Naturforschung (SGN)Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Ecophysiology and AquacultureFaculty of Biology, Department of Aquatic Ecology, University Duisburg-EssenGoethe-University (GU), Institute for Ecology, Evolution and Diversity; Biodiversity and Climate Research Centre (BiK-F), Senckenberg Gesellschaft für Naturforschung (SGN)Abstract Background The invasive eel parasite Anguillicoloides crassus (syn. Anguillicola crassus) is considered one of the major causes for the decline of the European eel (Anguilla anguilla) panmictic population. It impairs the swim bladder function and reduces swimming performance of its host. The life cycle of this parasite involves different intermediate and paratenic hosts. Despite an efficient immune system of the paratenic fish hosts acting against infections with A. crassus, levels of parasitized eels remain high in European river systems. Recently, the round goby Neogobius melanostomus (Gobiidae) has become dominant in many rivers in Europe and is still spreading at a rapid pace. This highly invasive species might potentially act as an important, so far neglected paratenic fish host for A. crassus. Methods Based on own observations and earlier single sightings of A. crassus in N. melanostomus, 60 fresh individuals of N. melanostomus were caught in the Rhine River and examined to assess the infection levels with metazoan parasites, especially A. crassus. Glycerin preparations were used for parasite identification. Results The parasite most frequently found in N. melanostomus was the acanthocephalan Pomphorhynchus sp. (subadult stage) which occurred mainly encysted in the mesenteries and liver. Every third gobiid (P = 31.7%) was infected by A. crassus larvae (L3) which exclusively occurred inside the acanthocephalan cysts. No intact or degenerated larvae of A. crassus were detected elsewhere in the goby, neither in the body cavity and mesenteries nor in other organs. Affected cysts contained the acanthocephalan larvae and 1-12 (mI =3) living A. crassus larvae. Additionally, encysted larvae of the nematode Raphidascaris acus were detected in the gobies, but only in the body cavity and not inside the acanthocephalan cysts. Conclusions Based on our observations, we suggest that A. crassus might actively bypass the immune response of N. melanostomus by invading the cysts of acanthocephalan parasites of the genus Pomphorhynchus using them as "Trojan horses". Providing that eels prey on the highly abundant round goby and that the latter transfers viable infective larvae of A. crassus, the new paratenic host might have a strong impact on the epidemiology of A. crassus.https://doi.org/10.1186/s13071-014-0504-8Anguillicoloides crassusInvasive speciesNeogobius melanostomusLife cycle strategyParasite infectionIntermediate host
spellingShingle Sebastian Emde
Sonja Rueckert
Judith Kochmann
Klaus Knopf
Bernd Sures
Sven Klimpel
Nematode eel parasite found inside acanthocephalan cysts - a "Trojan horse" strategy?
Parasites & Vectors
Anguillicoloides crassus
Invasive species
Neogobius melanostomus
Life cycle strategy
Parasite infection
Intermediate host
title Nematode eel parasite found inside acanthocephalan cysts - a "Trojan horse" strategy?
title_full Nematode eel parasite found inside acanthocephalan cysts - a "Trojan horse" strategy?
title_fullStr Nematode eel parasite found inside acanthocephalan cysts - a "Trojan horse" strategy?
title_full_unstemmed Nematode eel parasite found inside acanthocephalan cysts - a "Trojan horse" strategy?
title_short Nematode eel parasite found inside acanthocephalan cysts - a "Trojan horse" strategy?
title_sort nematode eel parasite found inside acanthocephalan cysts a trojan horse strategy
topic Anguillicoloides crassus
Invasive species
Neogobius melanostomus
Life cycle strategy
Parasite infection
Intermediate host
url https://doi.org/10.1186/s13071-014-0504-8
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