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Ecological plasticity of tubenose goby, a small invader in South Moravian waters

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Abstract

The western tubenose goby Proterorhinus semilunaris, an invasive Ponto-Caspian fish species, has established populations in a wide range of habitat types in the Dyje/Morava river basin (Danube basin; Czech Republic). In this study, we assessed tubenose goby tolerance to environmental variables potentially contributing to its spread and performance in new habitats. Of the seven aquatic habitats examined (lowland rivers, brooks, backwaters, oxbow lakes, borrow pits, reservoirs and carp aquaculture ponds), all except small brooks proved suitable for survival and reproduction, with habitat size the only limiting factor. Diet analysis indicated chironomid larvae as preferred prey, though tubenose gobies were able to switch to other food items under specific conditions (e.g. high macrozoobenthos density), suggesting feeding plasticity. Fish condition was positively correlated with individual diet range, but not with parasite burden. Eighteen metazoan parasite taxa were identified, greatly exceeding the known parasite fauna from the species’ native range. Parasite species richness decreased significantly with fish host dominance. Foraging plasticity, the ability to occupy different habitats and cope with parasitism observed in this study all may have important implications for tubenose goby dispersal success and invasiveness.

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References

  • Adámek, Z., P. Jurajda, V. Prášek & I. Sukop, 2010. Seasonal diet pattern of non-native tubenose goby (Proterorhinus semilunaris) in a lowland reservoir (Mušov, Czech Republic). Knowledge and Management in Aquatic Ecosystems 397: 1–12.

    Google Scholar 

  • Armitage, P. D., 1995. Chironomidae as food. In Armitage, P. D., P. S. Cranston & L. C. V. Pinder (eds.), The Chironomidae. Springer, Dordrecht.

    Chapter  Google Scholar 

  • Błońska, D., J. Grabowska, J. Kobak, Ł. Jermacz & K. Bącela-Spychalska, 2015. Feeding preferences of an invasive Ponto-Caspian goby for native and non-native gammarid prey. Freshwater Biology 60: 2187–2195.

    Article  Google Scholar 

  • Borcherding, J., S. Staas, S. Krüger, M. Ondračková, L. Šlapanský & P. Jurajda, 2011. Non-native gobiid species in the lower river Rhine (Germany): recent range extensions and densities. Journal of Applied Ichthyology 27: 153–155.

    Article  Google Scholar 

  • Borcherding, J., M. Dolina, L. Heermann, P. Knutzen, S. Kruger, S. Matern, R. van Treeck & S. Gertzen, 2013. Feeding and niche differentiation in three invasive gobies in the Lower Rhine, Germany. Limnologica 43: 49–58.

    Article  Google Scholar 

  • Bush, A. O., K. D. Lafferty, J. M. Lotz, A. W. Shostak, et al., 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83: 575–583.

    Article  CAS  Google Scholar 

  • Cone, R. S., 1989. The need to reconsider the use of condition indices in fishery sciences. Transactions of the American Fisheries Society 118: 510–514.

    Article  Google Scholar 

  • Costedoat, C., N. Pech, M. D. Salducci, R. Chappaz & A. Gilles, 2005. Evolution of mosaic hybrid zone between invasive and endemic species of Cyprinidae through space and time. Biological Journal of the Linnean Society 85: 135–155.

    Article  Google Scholar 

  • Dávidová, M., R. Blažek, T. Trichkova, E. Koutrakis, O. Gaygusuz, E. Ercan & M. Ondračková, 2011. The role of the European bitterling (Rhodeus amarus, Cyprinidae) in parasite accumulation and transmission in riverine ecosystems. Aquatic Ecology 45: 377–387.

    Article  Google Scholar 

  • Dezvuli, B., S. Volponi, I. Beltrami & R. Poulin, 2002. Intra- and interspecific density-dependent effects on growth in helminth parasites of the cormorant, Phalacrocorax carbo sinensis. Parasitology 124: 537–544.

    Google Scholar 

  • Ergens, R. & J. Lom, 1970. Agents of Fish Parasitic Diseases. Academia, Prague: 384.

    Google Scholar 

  • Erős, T., A. Sevcsik & B. Tóth, 2005. Abundance and night-time habitat use patterns of Ponto-Caspian gobiid species (Pisces, Gobiidae) in the littoral zone of the River Danube, Hungary. Journal of Applied Ichthyology 21: 350–357.

    Article  Google Scholar 

  • Essian, D. A., J. G. Chipault, B. M. Lafrancois & J. B. K. Leonard, 2016. Gut content analysis of Lake Michigan waterbirds in years with avian botulism type E mortality, 2010–2012. Journal of Great Lakes Research 42: 1118–1128.

    Article  Google Scholar 

  • French, J. R. P. & D. J. Jude, 2001. Diets and diet overlap of nonindigenous gobies and small benthic native fishes co-inhabiting the St. Clair River, Michigan. Journal of Great Lakes Research 27: 300–311.

    Article  Google Scholar 

  • Gaygusuz, C. G., A. S. Tarkan & O. Gaygusuz, 2010. The diel changes in feeding activity, microhabitat preferences and abundance of two freshwater fish species in small temperate streams (Omerli, Istanbul). Ekoloji 19: 15–24.

    Article  Google Scholar 

  • Gelnar, M., Š. Šebelová, L. Dušek, B. Koubková, P. Jurajda & S. Zahrádková, 1997. Biodiversity of parasites in freshwater environment in relation to pollution. Parassitologia 39: 189–199.

    CAS  PubMed  Google Scholar 

  • Gendron, A. D. & D. J. Marcogliese, 2017. Enigmatic decline of a common fish parasite (Diplostomum spp.) in the St. Lawrence River: evidence for a dilution effect induced by the invasive round goby. International Journal for Parasitology: Parasites and Wildlife 6: 402–411.

    Google Scholar 

  • Grabowska, J., D. Pietraszewski & M. Ondračková, 2008. Tubenose goby Proterorhinus marmoratus (Pallas, 1814) has joined three other Ponto-Caspian gobies in the Vistula River (Poland). Aquatic Invasions 3: 261–265.

    Article  Google Scholar 

  • Irons, K. S., G. G. Sass, M. A. McClelland & J. D. Stafford, 2007. Reduced condition factor of two native fish species coincident with invasion of non-native Asian carps in the Illinois River, U.S.A. Is this evidence for competition and reduced fitness? Journal of Fish Biology 71: 258–273.

    Article  Google Scholar 

  • Jacobs, J., 1974. Quantitative measurement of food selection. Oecologia 14: 413.

    Article  Google Scholar 

  • Jakubas, D. & A. Mioduszewska, 2005. Diet composition and food consumption of the grey heron (Ardea cinerea) from breeding colonies in northern Poland. European Journal of Wildlife Research 51: 191–198.

    Article  Google Scholar 

  • Janáč, M., Z. Valová & P. Jurajda, 2012. Range expansion and habitat preferences of nonnative 0+ tubenose goby (Proterorhinus semilunaris) in two lowland rivers in the Danube basin. Fundamental and Applied Limnology / Archiv fur Hydrobiology 181: 73–85.

    Article  Google Scholar 

  • Janáč, M., J. Bryja, M. Ondračková, J. Mendel & P. Jurajda, 2017. Genetic structure of three invasive gobiid species along the Danube-Rhine invasion corridor: similar distributions, different histories. Aquatic Invasions 12: 551–564.

    Article  Google Scholar 

  • Johnson, J. H., R. M. Ross, R. D. McCullough & A. Mathers, 2010. Diet shift of double-crested cormorants in Eastern Lake Ontario associated with the expansion of the invasive round goby. Journal of Great Lakes Research 36: 242–247.

    Article  Google Scholar 

  • Jude, D. J. & S. F. DeBoe, 1996. Possible impacts of gobies and other introduced species on habitat restoration efforts. Canadian Journal of Fisheries and Aquatic Sciences 53: 136–141.

    Article  Google Scholar 

  • Jude, D. J., R. H. Reider & G. R. Smith, 1992. Establishment of gobiidae in the Great Lakes Basin. Canadian Journal of Fisheries and Aquatic Sciences 49: 416–421.

    Article  Google Scholar 

  • Kadlec, D., A. Šimková, J. Jarkovský & M. Gelnar, 2003. Parasite communities of freshwater fish under flood conditions. Parasitology Research 89: 272–283.

    PubMed  Google Scholar 

  • Keane, R. M. & M. J. Crowley, 2002. Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17: 164–170.

    Article  Google Scholar 

  • Kocovsky, P. M., J. A. Tallman, D. J. Jude, D. M. Murphy, J. E. Brown & C. A. Stepien, 2011. Expansion of tubenose gobies Proterorhinus semilunaris into western Lake Erieand potential effects on native species. Biological Invasions 13: 2775–2784.

    Article  Google Scholar 

  • Kokeš, J. & D. Němejcová, 2006. Methodology of Running Waters Macrozoobenthos Sampling and Sample Processing Using the Perla Method. T. G. Masaryk Water Research Institute, v.v.i., Praha.

    Google Scholar 

  • Kornis, M. S., N. Mercado-Silva & M. J. Vander Zanden, 2012. Twenty years of invasion: a review of round goby Neogobius melanostomus biology, spread and ecological implications. Journal of Fish Biology 80: 235–285.

    Article  CAS  Google Scholar 

  • Kottelat, M. & J. Freyhof, 2007. Handbook of European Freshwater Fish. Publications Kottelat, Cornol.

    Google Scholar 

  • Koubková, B. & V. Baruš, 2000. Metazoan parasites of the recently established tubenose goby (Proterorhinus marmoratus: Gobiidae) population from the South Moravian reservoir, Czech Republic. Helminthologia 37: 89–95.

    Google Scholar 

  • Kvach, Y. & M. C. Oğuz, 2009. Communities of metazoan parasites of two fishes of the Proterorhinus genus (Actinopterygii: Gobiidae). Helminthologia 46: 168–176.

    Article  Google Scholar 

  • Kvach, Y., M. Ondračková & P. Jurajda, 2016. First report of metacercariae of Cyathocotyle prussica parasitising a fish host in the Czech Republic, Central Europe. Helminthologia 53: 257–261.

    Article  Google Scholar 

  • Kvach, Y., M. Ondračková, M. Janáč & P. Jurajda, 2018. Methodological issues affecting the study of fish parasites. III. Effect of fish preservation method. Diseases of Aquatic Organisms 127: 213–224.

    Article  CAS  Google Scholar 

  • Lucký, Z., S. Navrátil & M. Jirásková, 1989. The health status of commercial fish in the Mušov Lake. Acta Veterinaria Brno 58: 53–90.

    Article  Google Scholar 

  • Lusk, S. & K. Halačka, 1995. The first finding of the tubenose goby, Proterorhinus marmoratus, in the Czech Republic. Folia Zoologica 44: 90–92.

    Google Scholar 

  • Matesanz, S., T. Horgan-Kobelski & S. E. Sultan, 2012. Phenotypic plasticity and population differentiation in an ongoing species invasion. PLoS ONE 7: e44955.

    Article  CAS  Google Scholar 

  • McMahon, R. F., 2002. Evolutionary and physiological adaptations of aquatic invasive animals: r selection versus resistence. Canadian Journal of Fisheries and Aquatic Sciences 59: 1235–1244.

    Article  Google Scholar 

  • Mikl, L., Z. Adámek, L. Všetičková, M. Janáč, K. Roche, L. Šlapanský & P. Jurajda, 2017. Response of benthic macroinvertebrate assemblages to round (Neogobius melanostomus, Pallas 1814) and tubenose (Proterorhinus semilunaris, Heckel 1837) goby predation pressure. Hydrobiologia 785: 219–232.

    Article  CAS  Google Scholar 

  • Mombaerts, M., H. Verreycken, F. A. M. Volckaert & T. Huyse, 2014. The invasive round goby Neogobius melanostomus and tubenose goby Proterorhinus semilunaris: two introduction routes into Belgium. Aquatic Invasions 9: 305–314.

    Article  Google Scholar 

  • Ondračková, M., 2016. Gyrodactylus proterorhini in its non-native range: distribution and ability to host-switch in freshwaters. Parasitology Research 115: 3153–3162.

    Article  Google Scholar 

  • Ondračková, M., K. Francová, M. Dávidová, M. Polačik & P. Jurajda, 2010. Condition status and parasite infection of Neogobius kessleri and N. melanostomus (Gobiidae) in their native and non-native area of distribution of the Danube River. Ecological Research 25: 857–866.

    Article  Google Scholar 

  • Ondračková, M., I. Hudcová, M. Dávidová, Z. Adámek, M. Kašný & P. Jurajda, 2015a. Non-native gobies facilitate the transmission of Bucephalus polymorphus (Trematoda). Parasites & Vectors 8: 382.

    Article  Google Scholar 

  • Ondračková, M., Z. Valová, I. Hudcová, V. Michálková, A. Šimková, J. Borcherding & P. Jurajda, 2015b. Temporal effects on host-parasite associations in four naturalized goby species living in sympatry. Hydrobiologia 746: 233–243.

    Article  Google Scholar 

  • Panov, V. E., B. Alexandrov, K. Arbačiauskas, R. Binimelis, G. H. Copp, M. Grabowski, F. Lucy, R. S. Leuven, S. Nehring, M. Paunović, V. Semenchenko & M. O. Son, 2009. Assessing the risks of aquatic species invasions via european inland waterways: from concepts to environmental indicators. Integrated Environmental Assessment and Management 5: 110–126.

    Article  CAS  Google Scholar 

  • Peeler, E. J., B. C. Oidtmann, P. J. Midtlyng, L. Miossec & R. E. Gozlan, 2011. Non-native aquatic animals introductions have driven disease emergence in Europe. Biological Invasions 13: 1291–1303.

    Article  Google Scholar 

  • Prášek, V. & P. Jurajda, 2005. Expansion of Proterorhinus marmoratus in the Morava River basin (Czech Republic, Danube R. watershed). Folia Zoologica 54: 189–192.

    Google Scholar 

  • R Core Team, 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Austria. ISBN 3-900051-07-0. http://www.Rproject.org/

  • Roche, K. F., M. Janáč, L. Šlapanský, L. Mikl, L. Kopeček & P. Jurajda, 2015. A newly established round goby (Neogobius melanostomus) population in the upper stretch of the River Elbe. Knowledge and Management in Aquatic Ecosystems 416: 33.

    Article  Google Scholar 

  • Sakai, A. K., F. W. Allendorf, J. S. Holt, D. M. Lodge, J. Molofsky, K. A. With, S. Baughman, R. J. Cabin, J. E. Cohen, N. C. Ellstrand, D. E. McCauley, P. O’Neil, I. M. Parker, J. N. Thompson & S. G. Wheller, 2001. The population biology of invasive species. Annual Review of Ecology and Systematics 32: 305–332.

    Article  Google Scholar 

  • Šlapanský, L., P. Jurajda & M. Janáč, 2016. Early life stages of exotic gobiids as new hosts for unionid glochidia. Freshwater Biology 61: 979–990.

    Article  Google Scholar 

  • StatSoft, 2017. http://www.statsoft.cz/

  • Strayer, D. L., 2010. Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshwater Biology 55: 152–174.

    Article  Google Scholar 

  • Telfer, S. & K. Bown, 2012. The effects of invasion on parasite dynamics and communities. Functional Ecology 26: 1288–1299.

    Article  Google Scholar 

  • Torchin, M. E., K. D. Lafferty, A. P. Dobson, V. J. McKenzie & A. M. Kuris, 2003. Introduced species and their missing parasites. Nature 421: 628–630.

    Article  CAS  Google Scholar 

  • Vašek, M., T. Jůza, M. Čech, M. Kratochvíl, M. Prchalová, J. Frouzová, M. Říha, M. Tušer, J. Seďa & J. Kubečka, 2011. The occurrence of non-native tubenose goby Proterorhinus semilunaris in the pelagic 0+ year fish assemblage of a central European reservoir. Journal of Fish Biology 78: 953–961.

    Article  Google Scholar 

  • Vašek, M., L. Všetičková, K. Roche & P. Jurajda, 2014. Diet of two invading gobiid species (Proterorhinus semilunaris and Neogobius melanostomus) during the breeding and hatching season: no field evidence of extensive predation on fish eggs and fry. Limnologica – Ecology and Management of Inland Waters 46: 31–36.

    Article  Google Scholar 

  • Vojtek, J., 1964. Zur Kenntnis des Entwicklungszyklus von Apatemon cobitidis (Linstow, 1890). Zeitschrift Fur Parasitenkunde 24: 578–599.

    Article  CAS  Google Scholar 

  • Všetičková, L., M. Janáč, M. Vašek, K. Roche & P. Jurajda, 2014. Non-native western tubenose gobies Proterorhinus semilunaris show distinct site, sex and age-related differences in diet. Knowledge and Management in Aquatic Ecosystems 414: 10.

    Article  Google Scholar 

  • Všetičková, L., M. Janáč, K. Roche & P. Jurajda, 2015. Assessment of possible diel and sex-related differences in round goby (Neogobius melanostomus) diet. Folia Zoologica 64: 104–111.

    Article  Google Scholar 

  • Zander, C. D., U. Strohbach & S. Groenewold, 1993. The importance of gobies (Gobiidae, Teleostei) as hosts and transmitters of parasites in the SW Baltic. Helgoländer Meeresuntersuchungen 47: 81–111.

    Article  Google Scholar 

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Acknowledgements

This study received financial support through the European Centre of Ichthyoparasitology – Centre of Excellence, Grant Agency of the Czech Republic, Project No. P505/12/G112. We thank our colleagues from the Institute of Vertebrate Biology for their help with fish sampling and parasite collection. The authors acknowledge Dr. Kevin Roche (Institute of Vertebrate Biology, Czech Academy of Sciences) for his help with proofreading the English text.

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Correspondence to Markéta Ondračková.

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Ondračková, M., Všetičková, L., Adámek, Z. et al. Ecological plasticity of tubenose goby, a small invader in South Moravian waters. Hydrobiologia 829, 217–235 (2019). https://doi.org/10.1007/s10750-018-3833-3

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