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

Published online by Cambridge University Press:  20 July 2012

M. ONDRAČKOVÁ ,
A. ŠIMKOVÁ ,
K. CIVÁŇOVÁ ,
M. VYSKOČILOVÁ  and
P. JURAJDA
M. ONDRAČKOVÁ*
Affiliation:
Institute of Vertebrate Biology, v.v.i., Academy of Sciences of the Czech Republic, Květná 8, 603 65 Brno, Czech Republic
A. ŠIMKOVÁ
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic
K. CIVÁŇOVÁ
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic
M. VYSKOČILOVÁ
Affiliation:
Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37 Brno, Czech Republic
P. JURAJDA
Affiliation:
Institute of Vertebrate Biology, v.v.i., Academy of Sciences of the Czech Republic, Květná 8, 603 65 Brno, Czech Republic
*
*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
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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.

Keywords

gobymetazoan parasitesmicrosatellitessimilarityspecies introductions
Type
Research Article
Information
Parasitology , Volume 139 , Issue 11 , September 2012 , pp. 1493 - 1505
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

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, 661–674.Google Scholar
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, 153–155. doi: 10.1111/j.1439-0426.2010.01662.x.CrossRefGoogle Scholar
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, 575–583.CrossRefGoogle Scholar
Chapuis, M. P. and Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24, 621–631.CrossRefGoogle ScholarPubMed
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, 721–733. doi: 10.1093/molbev/msl191.CrossRefGoogle Scholar
Crawley, M. J. (2007). The R Book. Wiley, Hoboke, Switzerland.CrossRefGoogle Scholar
Dunn, A. M. (2009). Parasites and biological invasions. Advances in Parasitology 68, 161–184. doi: 10.1016/S0065-308X(08)00607-6.CrossRefGoogle ScholarPubMed
Ergens, R. and Lom, J. (1970). Causative Agents of Fish Diseases. Academia, Prague, Czech Republic.Google Scholar
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, 879–886. doi: 10.1111/j.1439-0426.2010.01582.x.CrossRefGoogle Scholar
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, 751–786. doi: 10.1111/j.1095-8649.2010.02566.x.CrossRefGoogle Scholar
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, 261–265. doi: 10.3391/ai.2008.3.2.20.CrossRefGoogle Scholar
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).Google Scholar
Hammer, R., Harper, D. A. T. and Ryan, P. D. (2001). PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4, 1–9.Google Scholar
Hanfling, B. (2007). Understanding the establishment success of non-indigenous fishes: lessons from population genetics. Journal of Fish Biology 71, 115–135. doi: 10.1111/j.1095-8649.2007.01685.x.CrossRefGoogle Scholar
Hanski, I. (1982). Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38, 210–221.CrossRefGoogle Scholar
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. 101–130. Chapman & Hall, London, UK.Google Scholar
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, 416–421.CrossRefGoogle Scholar
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, 319–323.CrossRefGoogle Scholar
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. 250–271. Publishing House of the Bulgarian Academy of Sciences, Sofia, Bulgaria.Google Scholar
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, 647–651. doi: 10.1111/j.1439/0426.2009.01301.x.CrossRefGoogle Scholar
Keane, R. M. and Crawley, M. J. (2002). Exotic plants invasions and the enemy release hypothesis. Trends in Ecology and Evolution 17, 164–170. doi: 10.1111/j.1095-8649.2007.01685.x.CrossRefGoogle Scholar
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, 2047–2056. doi: 10.1111/j.1365-2427.2009.02228.x.CrossRefGoogle ScholarPubMed
Kirkpatrick, M. and Barton, N. H. (1997). Evolution of a species’ range. American Naturalist 150, 1–23.CrossRefGoogle ScholarPubMed
Kottelat, M. and Freyhof, J. (2007). Handbook of European Freshwater Fish. Publications Kottelat, Cornol, Switzerland.Google Scholar
Koval, V. P. (1959). Digenetic trematodes in fish of the Dnieper River. Voprosy Ekologii 3, 167–216 (in Russian).Google Scholar
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, 105–108 (in Ukrainian).Google Scholar
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, 149–152. (in Ukrainian).Google Scholar
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, 135–138 (in Ukrainian).Google Scholar
Kvach, Y. (2004). The metazoa parasites of gobiids in the Dniester estuary (Black Sea) depending on water salinity. Oceanological and Hydrobiological Studies 33, 47–56.Google Scholar
Lively, C. M. and Dybdahl, M. F. (2000). Parasite adaptation to locally common host genotypes. Nature, London 405, 679–681. doi: 10.1038/35015069.CrossRefGoogle ScholarPubMed
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, 516–527. doi: 10.1111/j.1461-0248.2010.01446.x.CrossRefGoogle ScholarPubMed
Magurran, A. E. (2004). Measuring Biological Diversity. Blackwell Science Ltd, Bodmin, Cornwall, UK.Google Scholar
Markevich, O. P. (1949). The helminth fauna in fish from the Dnieper River in the Kanev region. Trudy Kanivskogo Biogeographicheskego Zapovidnika 7, 73–84 (in Ukrainian).Google Scholar
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, 688–702. doi: 10.1111/j.1472-4642.2011.00762.x.CrossRefGoogle Scholar
Niewiadomska, K. (2003). Parasites of Fishes in Poland (Digenea). Polskie Towarzystwo Parazytologiczne, Warszawa, Poland (in Polish).Google Scholar
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), 360–370. doi: 10.1111/j.1095-8649.2007.01659.x.CrossRefGoogle Scholar
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. 29–33. Comission Internationale pour l'Exploration Scientifique de la mer Mediterranee, Monaco, CIESM Workshops Monograph, Monaco.Google Scholar
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, 201–208. doi: 10.1007/s00436-009-1384-2.CrossRefGoogle ScholarPubMed
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, 345–349.CrossRefGoogle Scholar
Peakall, R. and Smouse, P. E. (2006). GENEALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295. doi: 10.1093/jhered/esm064.CrossRefGoogle Scholar
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, 640–649. doi: 10.1111/j.1600-0633.2009.00383.x.CrossRefGoogle Scholar
Pojmanska, T., Niewiadomska, K. and Okulewicz, A. (2007). Parasitic Helminths of Poland – Species, Hosts, Grey Areas. Polskie Towarzystwo Parazytologiczne, Warszawa, Poland.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, NJ, USA.CrossRefGoogle Scholar
Poulin, R. and Mouillot, D. (2003). Host introductions and the geography of parasite taxonomic diversity. Journal of Biogeography 30, 837–845. doi: 10.1046/j.1365-2699.2003.00868.x.CrossRefGoogle Scholar
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, 676–688. doi: 10.1111/j.1365-2427.2010.02425.x.CrossRefGoogle Scholar
Raymond, M. and Rousset, F. (1995). GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.CrossRefGoogle Scholar
Rousset, F. (2008). Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8, 103–106. doi: 10.1111/j.1471-8286.2007.01931.x.CrossRefGoogle ScholarPubMed
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, 305–332.CrossRefGoogle Scholar
Simberloff, D. and Gibbons, L. (2004). Now you see them, now you don't! – Population crashes of established introduced species. Biological Invasions 6, 161–172. doi: http://dx.doi.org/10.1023/B:BINV.0000022133.49752.46.CrossRefGoogle Scholar
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, 243–254. doi: 10.1016/j.ijpara.2009.07.006.CrossRefGoogle ScholarPubMed
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, 628–630.CrossRefGoogle ScholarPubMed
van Beek, G. C. W. (2006). The round goby Neogobius melanostomus first recorded in the Netherlands. Aquatic Invasions 1, 42–43. doi: 10.3391/ai.2006.1.1.10.CrossRefGoogle Scholar
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, 701–704. doi: 10.1111/j.1471-8286.2007.01682.x.CrossRefGoogle Scholar
Wiesner, C. (2005). New records of non-indigenous gobies (Neogobius sp.) in the Austrian Danube. Journal of Applied Ichthyology 21, 324–327. doi: 10.1111/j.1439-0426.2005.00681.x.CrossRefGoogle Scholar