Skip to main content Accessibility help
×
Home

Parasite diversity and microsatellite variability in native and introduced populations of four Neogobius species (Gobiidae)

  • M. ONDRAČKOVÁ (a1), A. ŠIMKOVÁ (a2), K. CIVÁŇOVÁ (a2), M. VYSKOČILOVÁ (a2) and P. JURAJDA (a1)...

Summary

Species introduced into new areas often show a reduction in parasite and genetic diversity associated to the limited number of founding individuals. In this study, we compared microsatellite and parasite diversity in both native (lower Danube) and introduced populations of 4 Ponto-Caspian gobies, including those (1) introduced from within the same river system (middle Danube; Neogobius kessleri and N. melanostomus), and (2) introduced from a different river system (River Vistula; N. fluviatilis and N. gymnotrachelus). Microsatellite data confirmed the lower Danube as a source population for gobies introduced into the middle Danube. Both native and introduced (same river system) populations of N. kessleri and N. melanostomus had comparable parasite species richness and microsatellite diversity, possibly due to multiple and/or continual migration/introduction of new individuals and the acquisition of local parasites. Reduced parasite species richness and microsatellite diversity were observed in introduced (different river system) populations in the Vistula. A low number of colonists found for N. fluviatilis and N. gymnotrachelus in the Vistula potentially resulted in reduced introduction of parasite species. Insufficient adaptation of the introduced host to local parasite fauna, together with introduction into an historically different drainage system, may also have contributed to the reduced parasite fauna.

Copyright

Corresponding author

*Corresponding author: Institute of Vertebrate Biology, v.v.i., Academy of Sciences of the Czech Republic, Květná 8, 603 65 Brno, Czech Republic. Tel: 00420 543422522. Fax: 00420 543211346. E-mail: audrey@sci.muni.cz

References

Hide All
Ahnelt, H., Bănărescu, P., Spolwind, R., Harka, A. and Waidbacher, H. (1998). Occurrence and distribution of three gobiid species (Pisces: Gobiidae) in the middle and upper Danube region – example of different dispersal patterns? Biologia (Bratislava) 53, 661674.
Borcherding, J., Staas, S., Krueger, S., Ondračková, M., Šlapanský, L. and Jurajda, P. (2011). Non-native Gobiid species in the lower River Rhine (Germany): recent range extensions and densities. Journal of Applied Ichthyology 27, 153155. doi: 10.1111/j.1439-0426.2010.01662.x.
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.
Chapuis, M. P. and Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24, 621631.
Colautti, R. I., Ricciardi, A., Grigorovich, I. A. and MadIsaac, H. J. (2004). Is invasion success explained by the enemy release hypothesis? Ecology Letters 7, 721733. doi: 10.1093/molbev/msl191.
Crawley, M. J. (2007). The R Book. Wiley, Hoboke, Switzerland.
Dunn, A. M. (2009). Parasites and biological invasions. Advances in Parasitology 68, 161184. doi: 10.1016/S0065-308X(08)00607-6.
Ergens, R. and Lom, J. (1970). Causative Agents of Fish Diseases. Academia, Prague, Czech Republic.
Francová, K., Ondračková, M., Polačik, M. and Jurajda, P. (2011). Parasite fauna of native and non-native populations of Neogobius melanostomus (Pallas, 1814) (Gobiidae) in the longitudinal profile of the Danube River. Journal of Applied Ichthyology 27, 879886. doi: 10.1111/j.1439-0426.2010.01582.x.
Gozlan, R. E., Britton, J. R., Cowx, I. and Copp, G. H. (2010). Current knowledge on non-native freshwater fish introductions. Journal of Fish Biology 76, 751786. doi: 10.1111/j.1095-8649.2010.02566.x.
Grabowska, J., Pietraszewski, D. and Ondračková, M. (2008). Tubenose goby Proterorhinus marmoratus (Pallas, 1814) has joined three other Ponto-Caspian gobies in the Vistula River (Poland). Aquatic Invasions 3, 261265. doi: 10.3391/ai.2008.3.2.20.
Gulugin, S. Y. and Kunitsky, D. F. (1999). New data on spread genus Neogobius: N. fluviatilis, N. melanostomus, N. gymnotrachelus. Thesis of International Scientific Conference, Kaliningrad, Vol. 1: 5. (in Russian).
Hammer, R., Harper, D. A. T. and Ryan, P. D. (2001). PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4, 19.
Hanfling, B. (2007). Understanding the establishment success of non-indigenous fishes: lessons from population genetics. Journal of Fish Biology 71, 115135. doi: 10.1111/j.1095-8649.2007.01685.x.
Hanski, I. (1982). Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38, 210221.
Holmes, J. C. (1996). Helminth communities in marine fishes. In Parasite Communities: Patterns and Processes (ed. Esch, G. W., Bush, A. O. and Aho, J. M.), pp. 101130. Chapman & Hall, London, UK.
Jude, D. J., Reider, R. H. and Smith, G. R. (1992). Establishment of Gobiidae in the Great Lakes Basin. Canadian Journal of Fisheries Aquatic Sciences 49, 416421.
Jurajda, P., Černý, J., Polačik, M., Valová, Z., Janáč, M., Blažek, R. and Ondračková, M. (2005). The recent distribution and abundance of non-native Neogobius fishes in the Slovak section of the River Danube. Journal of Applied Ichthyology 21, 319323.
Kakacheva-Avramova, D., Margaritov, N. and Grupcheva, G. (1978). Fish parasites in the Bulgarian stretch of the Danube River. In Limnology of Bulgarian Stretch of the Danube River, BAS, pp. 250271. Publishing House of the Bulgarian Academy of Sciences, Sofia, Bulgaria.
Kakareko, T., Plachocki, D. and Kobak, J. (2009). Relative abundance of Ponto-Caspian gobiids in the lower Vistula River (Poland) 3- to 4 years after first appearance. Journal of Applied Ichthyology 25, 647651. doi: 10.1111/j.1439/0426.2009.01301.x.
Keane, R. M. and Crawley, M. J. (2002). Exotic plants invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17, 164170. doi: 10.1111/j.1095-8649.2007.01685.x.
Kelly, D. W., Patterson, R. A., Townsend, C. R., Poulin, R., Tompkins, D. M. (2009). Parasite spillback: A neglected concept in invasion ecology? Ecology 90, 20472056. doi: 10.1111/j.1365-2427.2009.02228.x.
Kirkpatrick, M. and Barton, N. H. (1997). Evolution of a species’ range. American Naturalist 150, 123.
Kottelat, M. and Freyhof, J. (2007). Handbook of European Freshwater Fish. Publications Kottelat, Cornol, Switzerland.
Koval, V. P. (1959). Digenetic trematodes in fish of the Dnieper River. Voprosy Ekologii 3, 167216 (in Russian).
Koval, V. P., Bagushchenko, A. M., Seregina, L. Y. and Pashkevichute, A. S. (1975). Parasite fauna of fish in Kachovka Reservoir in the fourteenth year of its existence. Visnik Kyivskogo Universiteta Seria Biologii 17, 105108 (in Ukrainian).
Koval, V. P. and Gerus, M. M. (1968). The parasite fauna of the Kachovka Reservoir in the eleventh year of its existence. Visnik Kyivskogo Universiteta Seria Biologii 10, 149152. (in Ukrainian).
Koval, V. P., Pashkevichute, A. S., Boshko, O. G., Kovalenko, A. A. and Stavrobskyi, K. B. (1973). Parasite fauna of fish in Kachovka Reservoir in the sixteenth year of its existence. Visnik Kyivskogo Universiteta Seria Biologii 15, 135138 (in Ukrainian).
Kvach, Y. (2004). The metazoa parasites of gobiids in the Dniester estuary (Black Sea) depending on water salinity. Oceanological and Hydrobiological Studies 33, 4756.
Lively, C. M. and Dybdahl, M. F. (2000). Parasite adaptation to locally common host genotypes. Nature, London 405, 679681. doi: 10.1038/35015069.
MacLeod, C. J., Paterson, A. P., Tompkins, D. M. and Duncan, R. P. (2010). Parasites lost – do invaders miss the boat or drown on arrival? Ecology Letters 13, 516527. doi: 10.1111/j.1461-0248.2010.01446.x.
Magurran, A. E. (2004). Measuring Biological Diversity. Blackwell Science Ltd, Bodmin, Cornwall, UK.
Markevich, O. P. (1949). The helminth fauna in fish from the Dnieper River in the Kanev region. Trudy Kanivskogo Biogeographicheskego Zapovidnika 7, 7384 (in Ukrainian).
Neilson, M. E. and Stepien, C. A. (2011). Historic speciation and recent colonization of Eurasian monkey gobies (Neogobius fluviatilis and N. pallasi) revealed by DNA sequences, microsatellites, and morphology. Diversity and Distribution 17, 688702. doi: 10.1111/j.1472-4642.2011.00762.x.
Niewiadomska, K. (2003). Parasites of Fishes in Poland (Digenea). Polskie Towarzystwo Parazytologiczne, Warszawa, Poland (in Polish).
Ohayon, J. L. and Stepien, C. A. (2007). Genetic and biogeographic relationships of the racer goby Neogobius gymnotrachelus (Gobiidae: Teleostei) from introduced and native Eurasian locations. Journal of Fish Biology 71 (Suppl. C), 360370. doi: 10.1111/j.1095-8649.2007.01659.x.
Olenin, S. (2002). Black Sea – Baltic Sea invasion corridors. In Alien Marine Organisms Introduced by Ships in the Mediterranean and Black Seas (ed. Briand, F.), pp. 2933. Comission Internationale pour l'Exploration Scientifique de la mer Mediterranee, Monaco, CIESM Workshops Monograph, Monaco.
Ondračková, M., Dávidová, M., Blažek, R., Gelnar, M. and 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. doi: 10.1007/s00436-009-1384-2.
Ondračková, M., Dávidová, M., Pečínková, M., Blažek, R., Gelnar, M., Valová, Z., Černý, J. and Jurajda, P. (2005). Metazoan parasites of Neogobius fishes in the Slovak section of the River Danube. Journal of Applied Ichthyology 21, 345349.
Peakall, R. and Smouse, P. E. (2006). GENEALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288295. doi: 10.1093/jhered/esm064.
Polačik, M., Janáč, M., Jurajda, P., Adámek, Z., Ondračková, M., Trichkova, T. and Vassilev, M. (2009). Invasive gobies in the Danube: invasion success facilitated by availability and selection of superior food resources. Ecology of Freshwater Fish 18, 640649. doi: 10.1111/j.1600-0633.2009.00383.x.
Pojmanska, T., Niewiadomska, K. and Okulewicz, A. (2007). Parasitic Helminths of Poland – Species, Hosts, Grey Areas. Polskie Towarzystwo Parazytologiczne, Warszawa, Poland.
Poulin, R. (2007). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, NJ, USA.
Poulin, R. and Mouillot, D. (2003). Host introductions and the geography of parasite taxonomic diversity. Journal of Biogeography 30, 837845. doi: 10.1046/j.1365-2699.2003.00868.x.
Poulin, R., Paterson, R. A., Townsend, C. R., Tompkins, D. M. and Kelly, D. W. (2011). Biological invasions and the dynamics of the endemic diseases in freshwater ecosystems. Freshwater Biology 56, 676688. doi: 10.1111/j.1365-2427.2010.02425.x.
Raymond, M. and Rousset, F. (1995). GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248249.
Rousset, F. (2008). Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8, 103106. doi: 10.1111/j.1471-8286.2007.01931.x.
Sakai, A. K., Allendorf, F. W., Holt, J. S., Lodge, D. M., Molofsky, J., With, K. A., Baughman, S., Cabin, R. J., Cohen, J. E., Ellstrand, N. C., McCauley, D. E., O'Neil, P., Parker, I. M., Thompson, J. N. and Weller, S. G. (2001). The population biology of invasive species. Annual Review of Ecology and Systematics 32, 305332.
Simberloff, D. and Gibbons, L. (2004). Now you see them, now you don't! – Population crashes of established introduced species. Biological Invasions 6, 161172. doi: http://dx.doi.org/10.1023/B:BINV.0000022133.49752.46.
Timi, J. T., Lanfranchi, A. L. and Luque, J. L. (2010). Similarity in parasite communities of the teleost fish Pinguipes brasilianus in the southwestern Atlantic: Infracommunities a tool to detect geographical patterns. International Journal for Parasitology 40, 243254. doi: 10.1016/j.ijpara.2009.07.006.
Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J. and Kuris, A. M. (2003). Introduced species and their missing parasites. Nature, London 421, 628630.
van Beek, G. C. W. (2006). The round goby Neogobius melanostomus first recorded in the Netherlands. Aquatic Invasions 1, 4243. doi: 10.3391/ai.2006.1.1.10.
Vyskočilová, M., Ondračková, M., Šimková, A. and Martin, J.-F. (2007). Isolation and characterization of microsatellites in Neogobius kessleri (Perciformes, Gobiidae) and cross-species amplification within the family Gobiidae. Molecular Ecology Notes 7, 701704. doi: 10.1111/j.1471-8286.2007.01682.x.
Wiesner, C. (2005). New records of non-indigenous gobies (Neogobius sp.) in the Austrian Danube. Journal of Applied Ichthyology 21, 324327. doi: 10.1111/j.1439-0426.2005.00681.x.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed