Advertisement

Hydrobiologia

, Volume 829, Issue 1, pp 217–235 | Cite as

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

  • Markéta OndračkováEmail author
  • Lucie Všetičková
  • Zdeněk Adámek
  • Lukáš Kopeček
  • Pavel Jurajda
Primary Research Paper
  • 62 Downloads

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.

Keywords

Western tubenose goby Plasticity Habitats Diet Parasites 

Notes

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.

Supplementary material

10750_2018_3833_MOESM1_ESM.docx (348 kb)
Supplementary material 1 (DOCX 347 kb)

References

  1. 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
  2. Armitage, P. D., 1995. Chironomidae as food. In Armitage, P. D., P. S. Cranston & L. C. V. Pinder (eds.), The Chironomidae. Springer, Dordrecht.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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
  11. Ergens, R. & J. Lom, 1970. Agents of Fish Parasitic Diseases. Academia, Prague: 384.Google Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.PubMedGoogle Scholar
  17. 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
  18. 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.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. Jacobs, J., 1974. Quantitative measurement of food selection. Oecologia 14: 413.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. Kadlec, D., A. Šimková, J. Jarkovský & M. Gelnar, 2003. Parasite communities of freshwater fish under flood conditions. Parasitology Research 89: 272–283.PubMedGoogle Scholar
  28. Keane, R. M. & M. J. Crowley, 2002. Exotic plant invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17: 164–170.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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
  31. 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.CrossRefGoogle Scholar
  32. Kottelat, M. & J. Freyhof, 2007. Handbook of European Freshwater Fish. Publications Kottelat, Cornol.Google Scholar
  33. 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
  34. Kvach, Y. & M. C. Oğuz, 2009. Communities of metazoan parasites of two fishes of the Proterorhinus genus (Actinopterygii: Gobiidae). Helminthologia 46: 168–176.CrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. Lucký, Z., S. Navrátil & M. Jirásková, 1989. The health status of commercial fish in the Mušov Lake. Acta Veterinaria Brno 58: 53–90.CrossRefGoogle Scholar
  38. 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
  39. Matesanz, S., T. Horgan-Kobelski & S. E. Sultan, 2012. Phenotypic plasticity and population differentiation in an ongoing species invasion. PLoS ONE 7: e44955.CrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. Ondračková, M., 2016. Gyrodactylus proterorhini in its non-native range: distribution and ability to host-switch in freshwaters. Parasitology Research 115: 3153–3162.CrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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.CrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. 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.CrossRefGoogle Scholar
  49. 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
  50. 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/
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. Šlapanský, L., P. Jurajda & M. Janáč, 2016. Early life stages of exotic gobiids as new hosts for unionid glochidia. Freshwater Biology 61: 979–990.CrossRefGoogle Scholar
  54. StatSoft, 2017. http://www.statsoft.cz/
  55. 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.CrossRefGoogle Scholar
  56. Telfer, S. & K. Bown, 2012. The effects of invasion on parasite dynamics and communities. Functional Ecology 26: 1288–1299.CrossRefGoogle Scholar
  57. 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.CrossRefGoogle Scholar
  58. 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.CrossRefGoogle Scholar
  59. 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.CrossRefGoogle Scholar
  60. Vojtek, J., 1964. Zur Kenntnis des Entwicklungszyklus von Apatemon cobitidis (Linstow, 1890). Zeitschrift Fur Parasitenkunde 24: 578–599.CrossRefGoogle Scholar
  61. 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.CrossRefGoogle Scholar
  62. 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.CrossRefGoogle Scholar
  63. 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.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Institute of Vertebrate BiologyThe Czech Academy of SciencesBrnoCzech Republic

Personalised recommendations