Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-23T21:27:45.110Z Has data issue: false hasContentIssue false

Parasite communities and infection levels of the invasive Chinese sleeper Perccottus glenii (Actinopterygii: Odontobutidae) from the Naab river basin, Germany

Published online by Cambridge University Press:  04 November 2016

Y. Kvach*
Affiliation:
Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Květná 8, 60365 Brno, Czech Republic
M. Janáč
Affiliation:
Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Květná 8, 60365 Brno, Czech Republic
S. Nehring
Affiliation:
Federal Agency for Nature Conservation, Konstantinstraße 110, 53179 Bonn, Germany
M. Ondračková
Affiliation:
Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Květná 8, 60365 Brno, Czech Republic
P. Jurajda
Affiliation:
Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Květná 8, 60365 Brno, Czech Republic
*

Abstract

The Chinese sleeper (Perccottus glenii), an invasive Asian fish, was first registered in Germany in 2009 (westernmost extent of its invasive range). We sampled Chinese sleepers from two localities on the Bücherlgraben creek (a tributary of the River Naab) in south-eastern Germany in November 2015 and examined them for parasite infection. Twelve taxa were registered, including ciliates (unidentified Trichodina), a monogenean, three cestode species, two digenean taxa, two acanthocephalan species, two nematode species and one mollusc glochidia. Infracommunities consisted of 1–5 species, with 10% of fish uninfected. Three parasite species (Acanthocephalus anguillae, Gyrodactylus luciopercae and Pseudocapillaria tomentosa) were recorded on Chinese sleepers for the first time. The results highlight the important role of the Chinese sleeper as a second intermediate host in the life cycle of heron and grebe parasites. The Chinese sleeper parasite community displayed low homogeneity at both localities sampled, with allogenic parasites (metacercariae and mesocercoids) mostly shared. Differences between localities were mainly caused by autogenic parasites. No invasive parasites associated with the Chinese sleeper were observed in the study area, all parasites being representatives of European fauna. This supports the hypothesis of introduction via the aquarium trade or through transport with commercial fish.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Antal, L., Székely, Cs. & Molnár, K. (2015) Parasitic infections of two fish species, the Caucasian dwarf goby and the Amur sleeper, in Hungary. Acta Veterinaria Hungarica 63, 472484.Google Scholar
Bagge, A.M., Poulin, R. & Valtonen, E.T. (2004) Fish population size, and not density, as the determining factor of parasite infection: a case study. Parasitology 128, 305313.Google Scholar
BO-FfF (2015a) E-Befischung Bücherlgraben 20.01.2015. Report of Bezirk Oberpfalz – Fachberatung für Fischerei, Regensburg.Google Scholar
BO-FfF (2015b) E-Befischung Bücherlgraben und Kranzlohgraben 30.03.2015. Report of Bezirk Oberpfalz – Fachberatung für Fischerei, Regensburg.Google Scholar
Brattey, J. (1983) The effects of larval Acanthocephalus lucii on the pigmentation, reproduction and susceptibility to predation of the isopod Asellus aquaticus . Journal of Parasitology 69, 11721173.Google Scholar
Brooks, D.R. (1980) Allopatric speciation and non-interactive parasite community structure. Systematic Zoology 29, 192203.CrossRefGoogle Scholar
Brown, A.F., Chubb, J.C. & Veltkamp, C.J. (1986) A key to the species of Acanthocephala parasitic in British freshwater fishes. Journal of Fish Biology 28, 327334.Google Scholar
Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.Google Scholar
Cribb, T.H. & Bray, R.A. (2010) Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Systematic Parasitology 76, 17.Google Scholar
Drobiniak, O., Kutsokon, Y. & Kvach, Y. (2014) Trichodinids (Ciliopora: Peritrichia) of Perccottus glenii (Actinopterygii: Odontobutidae) in three Ukrainian rivers. Vestnik Zoologii 48, 231238.CrossRefGoogle Scholar
Dziekońska-Rynko, J. & Dzika, E. (2011) The tapeworm Paradilepis scolecina (Rudolphi, 1819) (Cestoda: Cyclophyllidea) invasion in Great Cormorant [Phalacrocorax carbo sinensis (Blumenbach, 1798)] from the breeding colony in Lake Selment Wielki (northern Poland). Helminthologia 48, 2328.CrossRefGoogle Scholar
Dziekońska-Rynko, J., Mierzejewska, K. & Hliwa, P. (2015) Parasitic helminths in grey heron (Ardea cinerea) chicks. Biologia 70, 279282.CrossRefGoogle Scholar
Emde, S., Kochmann, J., Kuhn, T., Dörge, D.D., Plath, M., Miesen, F.W. & Klimpel, S. (2016) Cooling water of power plant creates ‘hot spots’ for tropical fishes and parasites. Parasitology Research 115, 8598.Google Scholar
Esch, G.W., Shostak, A.W., Marcogliese, D.J. & Goater, T.M. (1990) Patterns and processes in helminth parasite communities: an overview. pp. 119 in Esch, G.W., Bush, A.O. & Aho, J.M. (Eds) Parasite communities: pattern and processes. London, Chapman & Hall.Google Scholar
Gedeon, K., Grüneberg, C., Mitschke, A., Sudfeldt, C., Eickhorst, W., Fischer, S., Flade, M., Frick, S., Geiersberger, I., Koop, B., Kramer, M., Krüger, T., Roth, N., Ryslavy, T., Stübing, S., Sudmann, S.R., Steffens, R., Vökler, F. & Witt, K. (2014) Atlas Deutscher Brutvogelarten. Münster, Stiftung Vogelmonitoring Deutschland und Dachverband Deutscher Avifaunisten.Google Scholar
Georgiev, B., Biserkov, V. & Genov, T. (1986) In toto staining method for cestodes with iron acetocarmine. Helminthologia 23, 279281.Google Scholar
Golvan, Y.J. (1969) Systématique des acanthocéphales (Acanthocephala Rudolphi 1801). L'Ordre des Palaeacanthocephala Meyer 1931. La Super-famille des Echinorhynchoidea (Cobbold 1876) Golvan et Houin 1963. Mémoires du Muséum National d'Histoire Naturelle, Seria A (Zoologie) 57, 5373.Google Scholar
Gusev, A.V., Dubinina, M.N., Raikova, E.V., Khotenkovskiy, I.A., Pugachev, O.N. & Ergens, R. (1985) Paraziticheskiye mnogokletochnye. Part 1. Monogenea. pp. 1425 in Bauer, O.N. (Ed.) Opredelitel parazitov presnovodnykh ryb fauny SSSR. Vol. 2. Leningrad, Nauka.Google Scholar
Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001) PAST: paleontological statistics software package for education and data analysis. Palaentologica Electronica 4, 4.Google Scholar
Hanzelová, V., Dudiňák, V. & Oros, M. (2007) Seasonality and maturation of alien invasive tapeworm Amurotaenia perccotti (Cestodae: Nippotaeniidae) in Slovakia. Parassitologia 49, 341.Google Scholar
Holmes, J.C. & Price, P.W. (1986) Communities of parasites. pp. 187213 in Anderson, D.J. & Kikkawa, J. (Eds) Community biology: pattern and processes. Oxford, Blackwell.Google Scholar
Kelly, D.W., Paterson, R.A., Townsend, C.R., Poulin, R. & Tompkins, D.M. (2009) Parasite spillback: a neglected concept in invasion ecology? Ecology 90, 20472056.Google Scholar
Košuthová, L., Koščo, J., Miklisová, D., Letková, V., Košuth, P. & Manko, P. (2008) New data on an exotic Nippotaenia mogurndae (Cestoda), newly introduced to Europe. Helminthologia 45, 8185.Google Scholar
Košuthová, L., Koščo, J., Letková, V., Košuth, P. & Manko, P. (2009) New records of endoparasitic helminths in alien invasive fishes from the Carpathian region. Biologia 64, 776780.Google Scholar
Kottelat, M. & Freyhof, J. (2007) Handbook of European freshwater fishes. Berlin, Publications Kottelat, Cornol and Freyhof.Google Scholar
Kozicka, J. (1971) Cestode larvae of the family Dilepididae Fuhrmann, 1907 parasitizing freshwater fish in Poland. Acta Parasitologica Polonica 19, 8193.Google Scholar
Kuhn, J.A., Kristoffersen, R., Knudsen, R., Jakobsen, J., Marcogliese, D.J., Locke, S.A., Primicerio, R. & Amundsen, P.-A. (2015) Parasite communities of two three-spined stickleback populations in subarctic Norway – effects of a small spatial-scale host introduction. Parasitology Research 114, 13271339.Google Scholar
Kvach, Y. (2012) First record of the Chinese sleeper Perccottus glenii Dybowski, 1877 in the Ukrainian part of the Danube delta. BioInvasion Records 1, 2528.Google Scholar
Kvach, Y. & Stepien, C.A. (2008) Metazoan parasites of introduced round and tubenose gobies in the Great Lakes: support for the ‘enemy release hypothesis’. Journal of Great Lakes Research 34, 2335.Google Scholar
Kvach, Y., Drobiniak, O., Kutsokon, Y. & Hoch, I. (2013) The parasites of the invasive Chinese sleeper Perccottus glenii (Fam. Odontobutidae), with the first report of Nippotaenia mogurndae in Ukraine. Knowledge and Management of Aquatic Ecosystems 409, 05. doi: 10.1051/kmae/2013048.Google Scholar
Kvach, Y., Kutsokon, Y., Stepien, C.A. & Markovych, M. (2016a) Role of the invasive Chinese sleeper Perccottus glenii Dybowski 1877 (Actinopterygii: Odontobutidae) in the distribution of European fish parasites: new data and a review. Biologia 71, 941951.Google Scholar
Kvach, Y., Ondračková, M., Janáč, M. & Jurajda, P. (2016b) Methodological issues affecting the study of fish parasites. 1. Duration of live fish storage prior to dissection. Diseases of Aquatic Organisms 192, 107115.CrossRefGoogle Scholar
Magurran, A.E. (1988) Ecological diversity and its measurement. London, Croom Helm.Google Scholar
Malmberg, G. (1970) The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv för Zoologi 23, 1235.Google Scholar
Marcogliese, D.J. & Cone, D.K. (1991) Do brook charr (Salvelinus fontinalis) from insular Newfoundland have different parasites than their mainland counterparts? Canadian Journal of Zoology 69, 809811.Google Scholar
Mihok, T., Košuth, P., Kočišová, A., Pekárik, L., Bártová, E. & Major, P. (2011) The intestinal parasite Pseudocapillaria tomentosa (Dujardin, 1843) of the invasive fish species topmouth gudgeon, Pseudorasbora parva (Temminck and Schlegel), in Slovakia. Journal of Fish Diseases 34, 711714.Google Scholar
Moravec, F. (2013) Parasitic nematodes of freshwater fishes of Europe. Revised 2nd edn. Prague, Academia.Google Scholar
Nehring, S. & Steinhof, J. (2015) First records of the invasive Amur sleeper, Perccottus glenii Dybowski, 1877 in German freshwaters: a need for realization of effective management measures to stop the invasion. BioInvasion Records 4, 223232.CrossRefGoogle Scholar
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. Parasitology Research 105, 201208.Google Scholar
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, 233243.Google Scholar
Panov, V.E., Alexandrov, B., Arbačiauskas, K., Binimelis, R., Copp, G.H., Grabowski, M., Lucy, F., Leuven, R.S.E.W., Nehring, S., Paunović, M., Semenchenko, V. & Son, M.O. (2009) Assessing the risks of aquatic species invasions via European inland waterways: from concepts to environmental indicators. Integrated Environmental Assessment and Managment 5, 110126.Google Scholar
Poulin, R. & Mouillot, D. (2003) Host introductions and the geography of parasite taxonomic diversity. Journal of Biogeography 30, 837845.Google Scholar
R Core Team. (2015) R: a language and environment for statistical computing. Vienna, R Foundation for Statistical Computing. Available at www.R-project.org (accessed 26 October 2016).Google Scholar
Reshetnikov, A.N. (2013) Spatio-temporal dynamics of the expansion of rotan Perccottus glenii from West-Ukrainian centre of distribution and consequences for European freshwater ecosystems. Aquatic Invasions 8, 193206.CrossRefGoogle Scholar
Reshetnikov, A.N. & Karyagina, A.S. (2015) Further evidence of naturalisation of the invasive fish Perccottus glenii Dybowski, 1877 (Perciformes: Odontobutidae) in Germany and necessity of urgent management response. Acta Zoologica Bulgarica 67, 553556.Google Scholar
Reshetnikov, A.N. & Schliewen, U.K. (2013) First record of the invasive alien fish rotan Perccottus glenii Dybowski, 1877 (Odontobutidae) in the Upper Danube drainage (Bavaria, Germany). Journal of Applied Ichthyology 29, 13671369.Google Scholar
Reshetnikov, A.N., Sokolov, S.G., Chikhlyaev, I.V., Fayzulin, A.I., Kirillov, A.A., Kuzovenko, A.E., Protasova, E.N. & Skomorokhov, M.O. (2013) Direct and indirect interactions between an invasive alien fish (Perccottus glenii) and two native semi-aquatic snakes. Copeia 2013, 103110.Google Scholar
Schenke, G. & Grabow, A. (1965) Deutsche Erstzucht der Amurgrundel. Aquarien Terrarien 12, 292295.Google Scholar
Sitko, J. & Heneberg, P. (2015) Host specificity and seasonality of helminth component communities in central European grebes (Podicipediformes) and loons (Gaviiformes). Parasitology International 64, 377388.Google Scholar
Sivokhop, Y.M. (1998) Pershi znakhidky rotana (Perccottus glenii Dybowski) na Zakarpatti. Abstracts of students’ scientific conference, Biology. No. 3. pp. 44–45. Uzhhorod, University of Uzhhorod (in Ukrainian).Google Scholar
Šlapanský, L., Jurajda, P. & Janáč, M. (2016) Early life stages of exotic gobiids as new hosts for unionid glochidia. Freshwater Biology 61, 979990.Google Scholar
Sokolov, S.G. & Moshu, A.Y. (2013) First data on parasites of Amur sleeper Perccottus glenii Dybowski 1877 (Actinopterygii: Odontobutidae) in water bodies of Republic of Moldova. Izvestiya Samarskogo nauchnogo tsentra Rossiyskoy Akedemii nauk 15, 213–221 (in Russian with English summary).Google Scholar
Sokolov, S.G., Protasova, E.N. & Kholin, S.K. (2011a) Parasites of the introduced Amur sleeper, Perccottus glenii (Osteichthyes): alpha-diversity of parasites and age of the host. Biology Bulletin 38, 500508.Google Scholar
Sokolov, S.G., Protasova, E.N. & Reshetnikov, A.N. (2011b) Parasite fauna of rotan Perccottus glenii Dybowski, 1877 (Osteichthyes, Odontobutidae) in some waterbodies of European Russia. Povolzhskii Ekologicheskii Zhurnal 4, 507522.Google Scholar
Sokolov, S.G., Reshetnikov, A.N. & Protasova, E.N. (2014) A checklist of parasites in non-native populations of rotan Perccottus glenii Dybowski, 1877 (Odontobutidae). Journal of Applied Ichthyology 30, 574596.Google Scholar
Sokolov, S.G., Protasova, E.N. & Reshetnikov, A.N. (2015) First data on parasites of the rotan, Perccottus glenii Dybowski, 1877 (Perciformes: Odontobutidae), from Germany, with a detection of the previously unknown merocercoid of the gryporhynchid cestode Mashonalepis macrosphincter (Fuhrmann, 1909). Acta Zoologica Bulgarica 67, 557560.Google Scholar
Sørensen, T.A. (1948) A new method of establishing groups of equal amplitude in plant sociology based on similarity of species content and its application to analysis of vegetation on Danish commons. Kongelige Danske Videnskabernes Selskabs (Biologiske Skrifter) 5, 134.Google Scholar
Sudarikov, V.J., Lomakin, V.V., Atajev, A.M. & Semenova, N.N. (2006) Metacercariae of flukes (Trematoda) – fish parasites from the Caspian Sea and the Volga delta. pp. 1183 in Be'er, S.A. (Ed.) Metacercariae of flukes (Trematoda) – parasites of hydrobionts of Russia. Vol. 2. Moscow, Nauka (in Russian with English summary).Google Scholar
Taraschewski, H. (1988) Host–parasite interface of fish acanthocephalans. I. Acanthocephalus anguillae (Palaeacanthocephala) in naturally infected fishes: LM and TEM investigations. Diseases of Aquatic Organisms 4, 109119.CrossRefGoogle Scholar
Taraschewski, H. (2006) Hosts and parasites as aliens. Journal of Helminthology 80, 99128.Google Scholar
Torchin, M.E., Lafferty, K.D., Dobson, A.P., McKenzie, V.J. & Kuris, A.M. (2003) Introduced species and their missing parasites. Nature 421, 628629.Google Scholar
Vovk, P.S. (1976) Biologiya dalnevostochnykh rastitelnoyadnykh ryb i ikh khoziaystvennoe ispolzovanie v vodoemakh Ukrainy. 243 pp. Kiev, Naukova Dumka.Google Scholar
Zaichenko, N.V. (2015) Parasite fauna of Amur sleeper Perccottus glenii Dybowski, 1877 (Osteichthyes: Odontobutidae) in some water bodies of Kyiv Oblast. Russian Journal of Biological Invasions 6, 165199.Google Scholar
Zander, C.D. (2004) Four-year monitoring of parasite communities in gobiid fishes of the south-western Baltic. II. Infracommunity. Parasitology Research 93, 1729.Google Scholar
Zander, C.D. (2007) Parasite diversity of sticklebacks from the Baltic Sea. Parasitology Research 100, 287297.Google Scholar
Zander, C.D., Reimer, L.W., Barz, K., Dietel, G. & Strohbach, U. (2000) Parasite communities of the Salzhaff (Northwest Mecklenburg, Baltic Sea). II. Guild communities, with special regard to snails, benthic crustaceans, and small-sized fish. Parasitology Research 86, 359372.CrossRefGoogle ScholarPubMed