Parasites of the invasive Chinese sleeper Percсottus glenii (Actinopterygii: Odontobutidae) in the region of the first introduction of the Carpathian population

Yuriy Kvach, Yuliya Kutsokon, Michal Janáč, Ihor Dykyy, Natalia Dzyziuk, Ivanna Dudliv, Kateryna Nazaruk

Paper category: Original research paper
Corresponding author: Yuriy Kvach (yuriy.kvach@gmail.com)
DOI: https://doi.org/10.26881/oahs.2022.1.01
Received: 06/08/2021
Accepted: 03/09/2021
Full text: here

Citation (APA style): Kvach,Y.,Kutsokon,Y.,Janáč,M.,Dykyy,I.,Dzyziuk,N.,Dudliv,I. & Nazaruk,K.(2022).Parasites of the invasive Chinese sleeper Perccottus glenii (Actinopterygii: Odontobutidae) in the region of the first introduction of the Carpathian population. Oceanological and Hydrobiological Studies,51(1) 1-9. https://doi.org/10.26881/oahs.2022.1.01

Abstract

Parasites of the invasive Chinese sleeper (Perccottus glenii) were studied in five different localities at the site of the first introduction of the Carpathian population of this fish. We recorded eight taxa of parasites in Lviv water bodies. The monogenean Gyrodactylus perccotti and the cestode Nippoteania perccotti were recorded in all five lakes studied. These parasites represent Far East species introduced together with their host. Also the copepod Neoergasilus japonicus is a Far East parasite introduced to Europe with its aquaculture vector. Differences between the surveyed bodies of water were mainly related to their local seasonal conditions and watershed characteristics. The current data confirm the presence of co-introduced populations of G. perccotti and N. perccotti, which probably affects the future invasiveness of their host. Due to low acquisition of local parasites, we cannot confirm any significant effect of invasive fish on local parasite assemblages in this region. However, the presence of the non-indigenous copepod, N. japonicus, requires additional attention in the future.

References

Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26(1), 32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Antal, L., Székely, C., & Molnár, K. (2015). Parasitic infections of two invasive fish species, the Caucasian dwarf goby and the Amur sleeper, in Hungary. Acta Veterinaria Hungarica, 63(4), 472–484. https://doi.org/10.1556/004.2015.044 PMID:26599094
Bogutskaya, N. G., Naseka, A. M., Shedko, S. V., Vasil’eva, E. D., & Chereshnev, I. A. (2008). The fishes of the Amur River: Updated check-list and zoogeography. Ichthyological Exploration of Freshwaters, 19(4), 301–366.
Brattey, J. (1986). Life history and population biology of larval Acanthocephalus lucii (Acanthocephala: Echinorhynchidae) in the isopod Asellus aquaticus. The Journal of Parasitology, 72(5), 633–645. https://doi.org/10.2307/3281450 PMID:3806315
Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology, 83(4), 575–583. https://doi.org/10.2307/3284227 PMID:9267395
Catalano, S. R., Whittington, I. D., Donnellan, S. C., & Gillanders, B. M. (2014). Parasites as biological tags to assess host population structure: Guidelines, recent genetic advances and comments on a holistic approach. International Journal for Parasitology. Parasites and Wildlife, 3(2), 220–226. https://doi.org/10.1016/j.ijppaw.2013.11.001 PMID:25197624
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(1), 1–7. https://doi.org/10.1007/s11230-010-9229-z PMID:20401574
Drobiniak, O., Kutsokon, Y., & Kvach, Y. (2014). Trichodinids (Ciliopora: Peritrichia) of Perccottus glenii (Actinopterygii: Odontobutidae) in three Ukrainian rivers. Vestnik Zoologii, 48(3), 231–237. https://doi.org/10.2478/vzoo-2014-0026
Emde, S., Rueckert, S., Kochmann, J., Knopf, K., Sures, B., & Klimpel, S. (2014). Nematode eel parasite found inside acanthocephalan cysts—A “Trojan horse” strategy? Parasites & Vectors, 7, 504. https://doi.org/10.1186/s13071-014-0504-8 PMID:25403767
European Commission. (2017). List of Invasive Alien Species of Union concern. Publications Office of the European Union.
Fedoniuk, O. V. (2005). Holoveshka amurska (Perccottus glenii) v umovakh vodoym Lvivshchyny. In Biodiversity and role of zoocenosis in natural and anthropogenic ecosystems: Extended abstracts of the ІІІ International Conference, Dnipropetrovsk, October 4–6, 2005 (pp. 102–104). Dnipropetrovsk National University. [in Ukrainian]
Georgiev, B., Biserkov, V., & Genov, T. (1986). In toto staining method for cestodes with iron acetocarmine. Helminthologia, 23, 279–281.
Goedknegt, M. A., Feis, M. E., Wegner, K. M., Luttikhuizen, P. C., Buschbaum, C., Camphuysen, K. C. J., van der Meer, J., & Thieltges, D. W. (2016). Parasites and marine invasions: Ecological and evolutionary perspectives. Journal of Sea Research, 113, 11–27. https://doi.org/10.1016/j.seares.2015.12.003
Grabowska, J., Kvach, Y., Rewicz, T., Pupins, M., Kutsokon, I., Dykyy, I., Antal, L., Zięba, G., Rakauskas, V., Trichkova, T., Čeirāns, A., & Grabowski, M. (2020). First insights into the molecular population structure and origins of the invasive Chinese sleeper, Perccottus glenii, in Europe. NeoBiota, 57, 87–107. https://doi.org/10.3897/neobiota.57.48958
Hudson, P. L., & Bowen, C. A., II. (2002). First record of Neoergasilus japonicus (Poecilostomatoida: Ergasilidae), a parasitic copepod new to the Laurentian Great Lakes. The Journal of Parasitology, 88(4), 657–663. https://doi.org/10.1645/0022-3395(2002)088[0657:FRONJP]2.0.CO;2 PMID:12197110
Koinova, I. B., & Chorna, A.-K. (2019). [Lviv reservoirs: Current geo-ecological status and opportunities for its improvement] [in Ukrainian with English summary]. Man and Environment. Issues of Neoecology, 32, 6–15. https://doi.org/10.26565/1992-4224-2019-32-01
Košuthová, L., Letková, V., Koščo, J., & Košuth, P. (2004). First record of Nippotaenia mogurndae Yamaguti and Miyata, 1940 (Cestoda: Nippotaeniidea), a parasite of Perccottus glenii Dybowski, 1877, from Europe. Helminthologia, 41(1), 55–57.
Kutsokon, I. (2017). The Chinese sleeper (Perccottus glenii Dybowski, 1877) in Ukraine: New data on distribution. Journal of Applied Ichthyology, 33(6), 1100–1107. https://doi.org/10.1111/jai.13454
Kutsokon, I., Tkachenko, M., Bondarenko, O., Pupins, M., Snigirova, A., Berezovska, V., Čeirāns, A., & Kvach, Y. (2021). The role of invasive Chinese sleeper Perccottus glenii Dybowski, 1877 in the Ilgas Nature Reserve ecosystem: An example of a monospecific fish community. BioInvasions Records, 10(2), 396–410. https://doi.org/10.3391/bir.2021.10.2.18
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. https://doi.org/10.1051/kmae/2013048
Kvach, Y., Karavanskyi, Y., Tkachenko, P., & Zamorov, V. (2021). First record of the invasive Chinese sleeper, Perccottus glenii Dybowski, 1877 (Gobiiformes: Odontobutidae) in the Black Sea. BioInvasions Records, 10(2), 411–418. https://doi.org/10.3391/bir.2021.10.2.19
Kvach, Y., Kutsokon, I., Roman, A., Čeirāns, A., Pupins, M., & Kirjušina, M. (2020). Parasite acquisition by the invasive Chinese sleeper (Perccottus glenii Dybowski, 1877) (Gobiiformes: Odontobutidae) in Latvia and Ukraine. Journal of Applied Ichthyology, 36(6), 785–794. https://doi.org/10.1111/jai.14100
Kvach, Y., Kutsokon, Y., Stepien, C. A., & Markovych, M. (2016a). Role of the invasive Chinese sleeper Perccottus glenii (Actinopterygii: Odontobutidae) in the distribution of fish parasites in Europe: New data and a review. Biologia, 71(8), 941–951. https://doi.org/10.1515/biolog-2016-0112
Kvach, Y., Ondračková, M., Janáč, M., & Jurajda, P. (2016b). Methodological issues affecting the study of fish parasites. I. Duration of live fish storage prior to dissection. Diseases of Aquatic Organisms, 119(2), 107–115. https://doi.org/10.3354/dao02990 PMID:27137069
Kvach, Y., Ondračková, M., Kutsokon, Y., & Dzyziuk, N. (2018). New record of monogenean parasites on non-indigenous fishes in the Ukrainian Danube delta. BioInvasions Records, 7(1), 65–72. https://doi.org/10.3391/bir.2018.7.1.10
MacKenzie, K. (1983). Parasites as biological tags in fish population studies. In T. H. Coaker (Eds.), Advances in Applied Biology, Vol. 7 (pp. 251–331). New York: Academic Press.
Malmberg, G. (1970). The excretory systems and the marginal hooks as a basis for the systematics of Gyrodactylus (Trematoda, Monogenea). Arkiv för Zoologi, 23, 1–235.
Maslovsky, O., Tafiychuk, R., & Lyesnik, V. (2010). Parazytofauna rotana (Perccottus glenii Dybowski) u vodoymakh zakhodu Ukrayiny. In S. Hnatush et al. (eds.), Youth and Progress of Biology: Abstracts book of the VI International Scientific Conference of Students and PhD Students, Lviv, September 21–24, 2010 (pp. 128–129). Lviv: Vydavnytstvo LNU. [in Ukrainian]
Mierzejewska, K., Martyniak, A., Kakareko, T., & Hliwa, P. (2010). First record of Nippotaenia mogurndae Yamaguti and Miyata, 1940 (Cestoda, Nippotaeniidae), a parasite introduced with Chinese sleeper to Poland. Parasitology Research, 106(2), 451–456. https://doi.org/10.1007/s00436-009-1685-5 PMID:19943065
Mierzejewska, K., Kvach, Y., Woźniak, M., Kosowska, A., & Dziekońska-Rynko, J. (2012). Parasites of an Asian fish, the Chinese sleeper Perccottus glenii, in the Włocławek Reservoir on the Lower Vistula River, Poland: In search of the key species in the host expansion process. Comparative Parasitology, 79(1), 23–29. https://doi.org/10.1654/4519.1
Mori, T. (1936). Studies on the geographical distribution of freshwater fishes in Eastern Asia. Toppan Print.
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. BioInvasions Records, 4(3), 223–232. https://doi.org/10.3391/bir.2015.4.3.12
O’Callaghan, I., Harrison, S., Fitzpatrick, D., & Sullivan, T. (2019). The freshwater isopod Asellus aquaticus as a model biomonitor of environmental pollution: A review. Chemosphere, 235, 498–509. https://doi.org/10.1016/j.chemosphere.2019.06.217 PMID:31276864
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R., O’Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs, E., & Wagner, H. (2019). Vegan: Community Ecology Package. R package version 2.5-6, from https://CRAN.R-project.org/package=vegan
Ondračková, M., Fojtů, J., Seifertová, M., Kvach, Y., & Jurajda, P. (2019). Non-native parasitic copepod Neoergasilus japonicus (Harada, 1930) utilizes non-native fish host Lepomis gibbosus (L.) in the floodplain of the River Dyje (Danube basin). Parasitology Research, 118(1), 57–62. https://doi.org/10.1007/s00436-018-6114-1 PMID:30353234
Ondračková, M., Matějusová, I., & Grabowska, J. (2012). Introduction of Gyrodactylus perccotti (Monogenea) into Europe on its invasive fish host, Amur sleeper (Perccottus glenii, Dybowski 1877). Helminthologia, 49(1), 21–26. https://doi.org/10.2478/s11687-012-0004-3
Poulin, R., & Kamiya, T. (2015). Parasites as biological tags of fish stocks: A meta-analysis of their discriminatory power. Parasitology, 142(1), 145–155. https://doi.org/10.1017/S0031182013001534 PMID:24156370
Pupina, A., Pupins, M., Nekrasova, O., Tytar, V., Kozynenko, I., & Marushchak, O. (2018). Species distribution modelling: Bombina bombina (Linnaeus, 1761) and its important invasive threat Perccottus glenii (Dybowski, 1877) in Latvia under global climate change. Environmental Research, Engineering and Management, 74(4), 79–86. https://doi.org/10.5755/j01.erem.74.4.21093
Pupina, A., Pupins, M., Skute, A., Pupina, Ag., & Karklins, A. (2015). The distribution of the invasive fish Amur sleeper, rotan Perccottus glenii Dybowski, 1877 (Osteichthyes, Odontobutidae), in Latvia. Acta Biologica Universitatis Daugavpiliensis, 15(2), 329–341.
Rakauskas, V., Masiulytė, R., & Pikūnienė, A. (2016). Predator-prey interactions between a recent invader, the Chinese sleeper (Perccottus glenii) and the European pond turtle (Emys orbicularis): A case study from Lithuania. Acta Herpetologica, 11(2), 101–109. https://doi.org/10.13128/Acta_Herpetol-18261
R Core Team. (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, from https://www.R-project.org/
Reshetnikov, A. N. (2004). The fish Perccottus glenii: History of introduction to western regions of Eurasia. Hydrobiologia, 522(1-3), 349–350. https://doi.org/10.1023/B:HYDR.0000030060.29433.34
Reshetnikov, A. N. (2010). The current range of Amur sleeper Perccottus glenii Dybowski, 1877 (Odontobutidae, Pisces) in Eurasia. Russian Journal of Biological Invasions, 1(2), 119–126. https://doi.org/10.1134/S2075111710020116
Reshetnikov, A. N. (2013). Spatio-temporal dynamics of the expansion of rotan Perccottus glenii from West-Ukrainian center of distribution and consequences for European freshwater ecosystems. Aquatic Invasions, 8(2), 193–206. https://doi.org/10.3391/ai.2013.8.2.07
Reshetnikov, A. N., & Ficetola, G. F. (2011). Potential range of the invasive fish rotan (Perccottus glenii) in the Holarctic. Biological Invasions, 13(12), 2967–2980. https://doi.org/10.1007/s10530-011-9982-1
Reshetnikov, A. N., Sokolov, S. G., & Protasova, E. N. (2011). The host-specific parasite Nippotaenia mogurndae confirms introduction vectors of the fish Perccottus glenii in the Volga river basin. Journal of Applied Ichthyology, 27(5), 1226–1231. https://doi.org/10.1111/j.1439-0426.2011.01792.x
Rusinek, O. T. (1989). O tsykle razvitiya Nippotaenia mogurndae (Cestoda, Nippotaeniidae) – parazita rotana-goloveshki iz delty r. Selengi. In Bioproduktivnost, okhrana i ratsionalnoye izpolzovanie syryevykh resursov rybokhoziaystvennykh vodoyemov Vostochnoy Sibiri: Abstracts of regional conference, Ulan-Ude, March 29–30, 1989 (pp. 60-62). Ulan-Ude: BNTs SO AN SSSR. [in Russian]
Simberloff, D., & von Holle, B. (1999). Positive interactions of nonindigenous species: Invasional meltdown? Biological Invasions, 1(1), 21–32. https://doi.org/10.1023/A:1010086329619
Sokolov, S. G., & Moshu, A. J. (2014). [Goussia obstinata sp. n. (Sporozoa: Eimeriidae), a new coccidian species from intestines of the Amur sleeper Perccottus glenii Dybowski, 1877 (Perciformes: odontobutidae)] [in Russian with English summary]. Parazitologiia, 48(5), 382–392. PMID:25929109
Sokolov, S. G., Shedko, M. B., Protasova, E. N., & Reshetnikov, A. N. (2012). The first record of Henneguya alexeevi (Myxozoa, Myxobolidae) in Europe. [in Russian with English summary]. Vestnik Zoologii, 46(2), 167–172.
Taraschewski, H. (2006). Hosts and parasites as aliens. Journal of Helminthology, 80(2), 99–128. https://doi.org/10.1079/JOH2006364 PMID:16768855
Zaichenko, N. V. (2015). Finding of Gyrodactylus perccotti (Plathelminthes, Gyrodactylidae) in water bodies of Kyiv region. Vestnik Zoologii, 49(2), 181–184. https://doi.org/10.1515/vzoo-2015-0019