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Comparative Analysis of Predatory Behavior of Invasive Alien Dikerogammarus villosus (Sowinsky, 1894) and Native Gammarus varsoviensis Jazdzewski, 1975 Amphipods

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Abstract

Alien species of amphipods were registered in Belarus in the early 2000s. Over many years of observing the structure of the riverine macrozoobenthos community, a decrease in the frequency of occurrence of indigenous amphipod species in the southern part of Belarus was noted. In order to find an explanation of the current process, a laboratory experiment was conducted to study the predatory effect of the invasive alien (Dikerogammarus villosus (Sowinsky, 1894)) and native (Gammarus varsoviensis Jazdzewski, 1975) species of amphipods on some macrozoobenthos groups to compare the values of predation rates of amphipods and interspecific interaction of the two amphipod species. During the experiments on the food selectivity, it was found that invasive alien and native species of amphipods consumed the same number of macrozoobenthos groups. The maximum values of the predation rate of amphipods were determined when they consumed water louse and mayfly larvae; there were no statistically significant differences found. The average values of the predation rate of the invasive alien species were lower when it consumed adults of G. varsoviensis than young of G. varsoviensis. On the basis of the experimental data, it can be assumed that the direct predatory pressure of D. villosus or another similar alien species of amphipods (for example, D. haemobaphes (Eichwald, 1841)) is one of the main reasons for the disappearance of G. varsoviensis from the river sections where it was previously found.

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REFERENCES

  1. Arbačiauskas, K., Amphipods of the Nemunas River and the Curonian Lagoon, the Baltic Sea basin: where and which native freshwater amphipods persist?, Acta Zool. Lituan., 2008, no. 18, pp. 10–16. https://doi.org/10.2478/v10043-008-0002-3

    Article  Google Scholar 

  2. Arbačiauskas, K., Ataskaita “Europos bendrijos svarbos rusiu bukles ir invaziniu augalu ir gyvunu rusiu tyrimu atlikimo paslaugos, Technines specifikacijos XI dallies, 2014–2015 metais įvertinti ir prognozuoti šių invazinių bestuburių gyvū nų rū šių—kietašarvės šoniplaukos (Pontogammarus robustoides), ežerinės mizidės (Paramysis lacustris)—paplitimo ir gausumo parametrus bei ju pokycius,” Sutartis Nr. 28TP-2014-90-ES (2014.10.29), 2015.

  3. Arbačiauskas, K., Višinskienė, G., and Smilgevičienė, S., Non-indigenous macroinvertebrate species in Lithuanian fresh waters. Part 1: Distributions, dispersal and future, Knowl. Manag. Aquat. Ecosyst., 2011, no. 402, p. 12. https://doi.org/10.1051/kmae/2011075

  4. Barkov, D.V. and Kurashov, E.A., Selectivity of nutrition, digestibility of food and nutritional needs of the Baikal invader Gmelinoides fasciatus (Stebbing, 1899) in Lake Ladoga, Biol. Vnutr. Vod, 2011, no. 4, pp. 58–63.

  5. Bij de Vaate, A. and Klink, A., Dikerogammarus villosus Sowinski (Crustacea: Gammaridae) a new immigrant in the Dutch part of the Lower Rhine, Lauterbornia, 1995, no. 20, pp. 51–54.

  6. Bij de Vaate, A., Jazdzewski, K., Ketelaars, H.A.M., et al., Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe, Can. J. Fish. Aquat. Sci., 2002, no. 59, pp. 1159–1174.

    Article  Google Scholar 

  7. Bollache, L., Devin, S., Wattier, R.A., et al., Rapid range extension of the Ponto-Caspian amphipod Dikerogammarus villosus (Crustacea, Amphipoda) in France: potential consequences, Arch. Hydrobiol., 2004, no. 160, pp. 57–66.

  8. Borza, P., Huber, T., Leitner, P., et al., How to coexist with the “killer shrimp” Dikerogammarus villosus? Lessons from other invasive Ponto-Caspian peracarids, Aquat. Conserv., Mar. Freshw. Ecosyst., 2018, no. 28, pp. 1441–1450. https://doi.org/10.1002/aqc.2985

    Article  Google Scholar 

  9. Chesson, J., The estimation and analysis of preference and its relationship to foraging models, Ecology, 1983, vol. 64, no. 5, pp. 1297–1304.

    Article  Google Scholar 

  10. Copilaş-Ciocianu, D., and Arbačiauskas, K., First record of Dikerogammarus bispinosus Martynov, 1925 in Kazakhstan: invasive or overlooked native in the Caspian Sea basin? BioInvasions Rec., 2018, vol. 7, no. 3, pp. 285–291. https://doi.org/10.3391/bir.2018.7.3.09

    Article  Google Scholar 

  11. Devin, S. and Beisel, J.-N., Biological and ecological characteristics of invasive species: a gammarid study, Biol. Invasions, 2007, no. 9, pp. 13–24.

    Article  Google Scholar 

  12. Dick, J.T.A. and Platvoet, D., Invading predatory crustacean Dikerogammarus villosus eliminates both native and exotic species, Proc. R. Soc. Lond., 2000, no. 267, pp. 977–983. https://doi.org/10.1098/rspb.2000.1099

    Article  CAS  Google Scholar 

  13. Dick, J.T.A., Platvoet, D., and Kelly, D.W., Predatory impact of the freshwater invader Dikerogammarus villosus (Crustacea: Amphipoda), Can. J. Fish. Aquat. Sci., 2002, no. 59, pp. 1078–1084.

    Article  Google Scholar 

  14. Dodd, J.A., Dick, J.T.A., Alexander, M.E., et al., Predicting the ecological impacts of a new freshwater invader: functional responses and prey selectivity of the “killer shrimp,” Dikerogammarus villosus, compared to the native Gammarus pulex,Freshw. Biol., 2014, no. 59, pp. 337–352. https://doi.org/10.1111/fwb.12268

    Article  Google Scholar 

  15. Dumnicka, E., Konopacka, A., and Ż urek, R., Changes in the benthic fauna composition in the Upper Vistula over the last 50 years—the consequences of the water pollution reduction and alien species invasion, Int. J. Oceanogr. Hydrobiol., 2018, vol. 47, no. 3, pp. 303–312.

    Article  CAS  Google Scholar 

  16. Elliott, J.M., The drift distances and time spent in the drift by freshwater shrimps, Gammarus pulex, in a small stony stream, and their implications for the interpretation of downstream dispersal, Freshw. Biol., 2002, vol. 47, no. 8, pp. 1403–1417.

    Article  Google Scholar 

  17. Grabowski, M., Bą cela, K., and Konopacka, A., How to be an invasive gammarid (Amphipoda: Gammaroidea)—comparison of life history traits, Hydrobiologia, 2007, no. 590, pp. 75–84.

    Article  Google Scholar 

  18. Grabowski, M., Jaż dżewski, K., and Konopacka, A., Alien Crustacea in Polish waters—Amphipoda, Aquat. Invasions, 2007, vol. 2, no. 1, pp. 25–38. http://www.academia.edu/396529

    Article  Google Scholar 

  19. Grabowski, M., Mamos, T., Rewicz, T., et al., Gammarus varsoviensis Jazdzewski, 1975 (Amphipoda, Gammaridae): a long overlooked species in Ukrainian rivers, North-West. J. Zool., 2012a, vol. 8, no. 1: 121201.

    Google Scholar 

  20. Grabowski, M., Rewicz, T., Konopacka, A., et al., Cryptic invasion of Baltic lowlands by freshwater amphipod of Pontic origin, Aquat. Invasions, 2012b, vol. 7, no. 3, pp. 337–346. https://doi.org/10.3391/ai.2012.7.3.005

    Article  Google Scholar 

  21. Hellmann, C., Schöll, F., Worischka, S., Becker, J., and Winkelmann, C., River-specific effects of the invasive amphipod Dikerogammarus villosus (Crustacea: Amphipoda) on benthic communities, Biol. Invasions, 2017, vol. 19, no. 1, pp. 381–398. https://doi.org/10.1007/s10530-016-1286-z

    Article  Google Scholar 

  22. Hellmann, C., Worischka, S., Mehler, E., et al., The trophic function of Dikerogammarus villosus (Sowinsky, 1894) in invaded rivers: a case study in the Elbe and Rhine, Aquat. Invasions, 2015, vol. 10, no. 4, pp. 385–397.

    Article  Google Scholar 

  23. IUCN guidelines for the prevention of biodiversity loss caused by alien invasive species, The 51st Meet. IUCN, Council Species Survival Commission, IUCN, 2000.

  24. Jazdzewski, K., Remarks on Gammarus lacustris G. O. Sars, 1863, with description of Gammarus varsoviensis n. sp. (Crustacea, Amphipoda), Bijd. Dierkunde, 1975, no. 45, pp. 71–86.

  25. Karatayev, A.Y., Mastitsky, S.E., Burlakova, L.E., et al., Past, current, and future of the central European corridor for aquatic invasions in Belarus, Biol. Invasions, 2008, vol. 10, no. 2, pp. 215–232.

    Article  Google Scholar 

  26. Kinzelbach, R., Neozoans in European waters—exemplifying the worldwide process of invasion and species mixing, Cell. Mol. Life Sci., 1995, vol. 51, no. 5, pp. 526–538.

    Article  CAS  Google Scholar 

  27. Kinzler, W., Kley, A., Maier, G., et al., Mutual predation between and cannibalism within several freshwater gammarids: Dikerogammarus villosus versus one native and three invasives, Aquat. Ecol., 2009, vol. 43, no. 2, pp. 457–464.

    Article  Google Scholar 

  28. Kley, A. and Maier, G., Life history characteristics of the invasive freshwater gammarids Dikerogammarus villosus and Echinogammarus ischnus in the River Main and the Main-Donau canal, Arch. Hydrobiol., 2003, vol. 156, no. 4, pp. 457–469.

    Article  Google Scholar 

  29. Kley, A. and Maier, G., An example of niche partitioning between Dikerogammarus villosus and other invasive and native gammarids: a field study, J. Limnol., 2005, vol. 64, no. 1, pp. 85–88.

    Article  Google Scholar 

  30. Koester, M. and Gergs, R., No evidence for intraguild predation of Dikerogammarus villosus (Sowinsky, 1894) at an invasion front in the Untere Lorze, Switzerland, Aquat. Invasions, 2014, vol. 9, no. 4, pp. 489–497. https://doi.org/10.3391/ai.2014.9.4.07

    Article  Google Scholar 

  31. Koester, M., Schneider, M., Hellmann, C., et al., Is the invasive amphipod Dikerogammarus villosus the main factor structuring the benthic community across different types of water bodies in the River Rhine system? Limnologica, 2018, vol. 71, pp. 44–50.https://doi.org/10.1016/j.limno.2018.06.001

    Article  Google Scholar 

  32. Konopacka, A., Life history of Gammarus varsoviensis Jazdzewski, 1975 from Kampinoski National Park (Central Poland), Zool. Pol., 1988, vol. 35, nos. 1–4, pp. 165–177.

  33. Krisp, H. and Maier, G., Consumption of macroinvertebrates by invasive and native gammarids: a comparison, J. Limnol., 2005, vol. 64, no. 1, pp. 55–59.

    Article  Google Scholar 

  34. Leppakoski, E., Gollasch, S., and Olenin, S., Invasive Aquatic Species of Europe Distribution, Impacts and Management, Dordrecht: Kluwer, 2002. https://doi.org/10.1007/978-94-015-9956-6

    Book  Google Scholar 

  35. Lipinskaya, T. and Radulovici, A., DNA barcoding of alien Ponto-Caspian amphipods from the Belarusian part of the Central European invasion corridor, Genome, 2017, vol. 60, no. 11, pp. 963–964. https://doi.org/10.1139/gen-2017-0178

    Article  Google Scholar 

  36. Lipinskaya, T., Radulovici, A., and Makaranka, A., First DNA-barcoding based record of Echinogammarus trichiatus (Martynov, 1932) (Crustacea, Gammaridae) in Belarus, BioInvasions Rec., 2018, vol. 7, no. 1, pp. 55–60.

    Article  Google Scholar 

  37. MacNeil, C., Dick, J.T.A., Elwood, R.W., et al., The trophic ecology of freshwater Gammarus (Crustacea: Amphipoda); problems and perspectives concerning the functional feeding group concept, Biol. Rev., 1997, vol. 72, no. 3, pp. 349–364.

    Article  Google Scholar 

  38. MacNeil, C., Platvoet, D., Dick, J.T.A., et al., The Ponto-Caspian ‘killer shrimp’, Dikerogammarus villosus (Sowinsky, 1894), invades the British Isles, Aquat. Invasions, 2010, vol. 5, no. 4, pp. 441–444.

    Article  Google Scholar 

  39. Makarenko, A.I., Dimensional characteristics of alien and native species of amphipods in Belarus, Vesti Nats. Akad. Nauk Belarusi, 2015, no. 1, pp. 100–105.

  40. Makarenko, A.I. and Vezhnovets, V.V., Modern distribution of alien and native species of the Amphipoda latreille, 1816 in Belarus, Vesti Nats. Akad. Nauk Belarusi, 2014, no. 4, pp. 95–99.

  41. Makarenko, A.I. and Vezhnovets, V.V., Biotopic confinement of alien and native species of crustaceans (Amphipoda, Crustacea) in the water bodies of Belarus, Zh. Beloruss. Gos. Univ., Ser. Ekol., 2018, no. 4, pp. 29–41.

  42. Mastitsky, S.E. and Makarevich, O.A., Distribution and abundance of Ponto-Caspian amphipods in the Belarusian section of the Dnieper River, Aquat. Invasions, 2007, vol. 2, no. 1, pp. 39–44.

    Article  Google Scholar 

  43. Monakov, V.A., Nutrition of freshwater invertebrates, in Bokoplavy (Amphipoda), Monakov, V.A. and Strelkov, A.A., Eds., Moscow, 1998, pp. 188–193.

    Google Scholar 

  44. Monakov, A.V., Feeding of Freshwater Invertebrates, Ghent: Kenobi Productions, 2003.

    Google Scholar 

  45. Rewicz, T., Wattier, R., Grabowski, M., et al., Out of the Black Sea: phylogeography of the invasive killer shrimp Dikerogammarus villosus across Europe, PLoS One, 2015, vol. 10, no. 2: e0118121.https://doi.org/10.1371/journal.pone.0118121

    Article  Google Scholar 

  46. Sala, O.E., Chapin, F.S., Armesto, J.J., et al., Global biodiversity scenarios for the year 2100, Science, 2000, vol. 287, no. 5459, pp. 1770–1774. https://doi.org/10.1126/science.287.54.59.1770

    Article  CAS  PubMed  Google Scholar 

  47. Semenchenko, V.P., Vezhnovets, V.V., and Lipinskaya, T.P., Alien species of Ponto-Caspian amphipods (Crustacea, Amphipoda) in the Dnieper River basin (Belarus), Russ. J. Biol. Invasions, 2013, vol. 4, pp. 269–275. https://doi.org/10.1134/S2075111713040097

    Article  Google Scholar 

  48. Semenchenko, V.P., Rizevsky, V.K., Mastitsky, S.E., et al., Checklist of aquatic alien species established in large river basins of Belarus, Aquat. Invasions, 2009, vol. 4, no. 2, pp. 337–347.

    Article  Google Scholar 

  49. Semenchenko, V., Son, M.O., Novitski, R., et al., Checklist of non-native benthic macroinvertebrates and fish in the Dnieper River basin, BioInvasions Rec., 2016, vol. 5, no. 3, pp. 185–187. https://doi.org/10.3391/bir.2016.5.3.10

    Article  Google Scholar 

  50. Šidagyt\({\dot {e}}\), E., Solovjova, S., Šniaukštait\({\dot {e}}\), V., et al., The killer shrimp Dikerogammarus villosus (Crustacea, Amphipoda) invades Lithuanian waters, South-Eastern Baltic Sea, Oceanologia, 2017, vol. 59, no. 1, pp. 85–91.https://doi.org/10.1016/j.oceano.2016.08.004

    Article  Google Scholar 

  51. Stoffels, B.E.M.W., Tummers, J.G., van der Velde, G., et al., Assessment of predatory ability of native and non-native freshwater gammarideans: a rapid test with water fleas as prey, Curr. Zool., 2011, vol. 57, no. 6, pp. 836–843.

    Article  Google Scholar 

  52. Van der Velde, G., Leuven, R.S.E.W., Platvoet, D., et al., Factors influencing predatory behaviour in an invasive gammaridean species, Dikerogammarus villosus and some related species, Biol. Invasions, 2009, vol. 11, no. 9, pp. 2043–2054.

    Article  Google Scholar 

  53. Van der Velde, G., Rajagopal, S., Kelleher, B., et al., Ecological impact of crustacean invaders: general considerations and examples from the Rhine River, Proc. Fourth Int. Crustacean Congr., Rotterdam: Balkema, 2000, pp. 3–34.

  54. Van Riel, M.C., van der Velde, G., Rajagopal, S., et al., Trophic relationships in the Rhine food web during invasion and after establishment of the Ponto-Caspian invader Dikerogammarus villosus,Hydrobiologia, 2006, vol. 565, no. 1, pp. 39–58.

    Article  Google Scholar 

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ACKNOWLEDGMENTS

We are grateful to Corresponding Member of the National Academy of Sciences of Belarus, Professor V.P. Semenchenko (head of the Laboratory of Hydrobiology, Scientific and Practical Center for Bioresources of the National Academy of Sciences of Belarus) for valuable advice during the planning of the experiment and writing the article, as well as to the reviewer for valuable comments that allowed us to improve the text of the article.

Funding

This study was financially supported by the Belarusian Republican Foundation for Fundamental Research (project no. B17M-019 of April 18, 2017).

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Correspondence to T. P. Lipinskaya or A. I. Makarenko.

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STATEMENT ON THE WELFARE OF ANIMALS

All experimental protocols were carried out in accordance with EU Directive 86/609/EEC on the Protection of Animals Used for Experimental and Other Scientific Purposes and according to the rules approved by the Order of the Presidium of the USSR Academy of Sciences of April 2, 1980, no. 12000-496 and the order of the USSR Ministry of Higher Education of September 13, 1984, no. 22. All efforts were undertaken to use only the minimum number of animals necessary to obtain reliable scientific data.

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Translated by D. Martynova

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Lipinskaya, T.P., Makarenko, A.I. Comparative Analysis of Predatory Behavior of Invasive Alien Dikerogammarus villosus (Sowinsky, 1894) and Native Gammarus varsoviensis Jazdzewski, 1975 Amphipods. Russ J Biol Invasions 10, 349–357 (2019). https://doi.org/10.1134/S2075111719040052

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