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The Dynamics of Trematode Occurrence in Two Permanent Settlements of the Ponto-Azov Mollusk Lithoglyphus naticoides (C. Pfeiffer, 1828) (Gastropoda, Hydrobiidae) at the Northeastern Border of Its Range

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Abstract

The freshwater gastropod mollusk Lithoglyphus naticoides (C. Pfeiffer, 1828) is one of the most successful alien species in water bodies of the Volga River basin. One of the negative consequences of its spread is range expansion of trematode species, some of which are highly pathogenic to fish and fish-eating birds and mammals. The aim of this study is to analyze the features of formation of the trematode fauna in settlements of L. naticoides at the northeastern border of its range (Rybinsk Reservoir). It is found that the first permanent settlement of L. naticoides formed in 2005–2010 in coastal shallow waters in the lower part of the Volga reach of the reservoir. The mollusk did not spread rapidly throughout the entire water area of the reservoir outside the Volga reach zone with relatively high mineral water content. However, in 2011–2019, a new large settlement of L. naticoides was recorded in the upper fast-flow part of the Volga reach. A relatively low density of mature individuals in the settlements of L. naticoides (up to 50 ind./m2) allows at least five trematode species to complete their life cycle: Apophallus muehlingi (Jägerskiöld, 1899), Apophallus (=Rossicotrema) donicus (Skrjabin et Lindtrop, 1919), Parasymphylodora markewitschi Kulakowskaja, 1947, Nicolla skrjabini (Iwanitzky, 1928), and Sanguinicola volgensis (Razin, 1929). The prevalence of parthenitae of certain species depends on the reservoir water level regime, although the overall infestation of L. naticoides can exceed 90%. The slow-flowing lower part of the Volga reach is characterized by the dominance of P. markewitschi and trematodes of the genus Apophallus; the upper section, which is close to the river type, is dominated by N. skrjabini and S. volgensis. In the future, in the Rybinsk Reservoir, we can expect naturalization of other trematode species associated with L. naticoides within its range.

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REFERENCES

  1. Arbačiauskas, K., Višinskienė, G., Smilgevičienė, S., and Rakauskas, V., Non-indigenous macroinvertebrate species in Lithuanian fresh waters, Part 1: Distributions, dispersal and future, Knowl. Manage. Aquat. Ecosyst., 2011, vol. 402, pp. 1201–1218. https://doi.org/10.1051/kmae/2011075

    Article  Google Scholar 

  2. Bij de Vaate, A., Jazdzewski, K., Ketelaars, H.A.M., Gollasch, S., and Van der Velde, G., Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe, Can. J. Fish. Aquat. Sci., 2002, vol. 59, pp. 1159–1174. https://doi.org/10.1139/F02-098

    Article  Google Scholar 

  3. Biserova, L.I., Parasitological aspects of alien species invasions, Tr. Vseross. Nauchno-Issled. Inst. Rybn. Khoz. Okeanogr., 2010, vol. 148, pp. 137–141.

    Google Scholar 

  4. Biserova, L.I., Trematodes Apophallus muehlingi and Rossicotrema donicum are parasites of fish in the Volga delta (ecological features and ichthyoparasitosis caused by them), Extended Abstract of Cand. Sci. (Biol.) Dissertation, Moscow: Inst. Parasitol., Russ. Acad. Sci., 2005.

  5. Bush, A.O., Lafferty, K.D., Lotz, J.M., and Shostak, A.W., Parasitology meets ecology on its own terms: Margolis et al. revisited, J. Parasitol., 1997, vol. 83, no. 4, pp. 575–583. https://doi.org/10.2307/3284227

    Article  CAS  Google Scholar 

  6. Butkus, R., Šidagytė, E., Rakauskas, V., and Arbačiauskas, K., Distribution and current status of nonindigenous mollusc species in Lithuanian inland waters, Aquat. Invasions, 2014, vol. 9, no. 1, pp. 95–103. https://doi.org/10.3391/ai.2014.9.1.08

    Article  Google Scholar 

  7. Falniowski, A., Hydrobioidea of Poland (Prosobranchia: Gastropoda), Folia Malacol., 1987, vol. 1, no. 1, pp. 11–122. https://doi.org/10.12657/folmal.001.001

    Article  Google Scholar 

  8. Ivanov, V.M., Genesis of epizootics involving introduced species of helminths, mammals and mollusks, Russ. J. Ecol., 2008, vol. 39, no. 2, pp. 136–139. https://doi.org/10.1007/s11184-008-2010-8

    Article  Google Scholar 

  9. Izvekova, G.I. and Tyutin, A.V., Occurrence of partenites in mollusks and the influence that metacercaria of Apophallus muehlingi (Jägerskiöld, 1899) and Posthodiplostomum cuticola (Nordmann, 1832) has on some biochemical parameters in fish, Inland Water Biol., 2011, vol. 4, no. 3, pp. 367–372. https://doi.org/10.1134/S1995082911030114

    Article  Google Scholar 

  10. Martemyanov, V.I., Threshold cation concentrations in water determining the range limits of alien gastropod mollusk Lithoglyphus naticoides in the Rybinsk Reservoir, Russ. J. Biol. Invasions, 2013, vol. 4, no. 1, pp. 60–67. https://doi.org/10.1134/S2075111713010074

    Article  Google Scholar 

  11. Mouthon, J., Lithoglyphus naticoides (Pfeiffer) (Gastropoda: Prosobranchia): Distribution in France, population dynamics and life cycle in the Saône River at Lyon (France), Ann. Limnol.–Int. J. Limnol., 2007, vol. 43, no. 1, pp. 53–59. https://doi.org/10.1051/limn:2007027

    Article  Google Scholar 

  12. Odening, K., Der Entwicklungszyklus von Apophallus muehlingi (Trematoda: Opisthorchiida: Heterophyidae) in Berlin, Z. Parasitenkd., 1970, vol. 33, pp. 194–210. https://doi.org/10.1007/BF00259490

    Article  CAS  Google Scholar 

  13. Panov, V.E., Alexandrov, B., Arbačiauskas, K., Binimelis, R., Copp, G.H., Grabowski, M., Lucy, F., Leuven, R.S., Nehring, S., Paunović, M., Semenchenko, V.P., and Son, M.O., Assessing the risk of aquatic species invasions via European inland waterways: From concepts to environmental indicators, Integr. Environ. Assess. Manage., 2009, vol. 5, no. 1, pp. 110–126. https://doi.org/10.1897/IEAM_2008-034.1

    Article  CAS  Google Scholar 

  14. Perova, S.N., Pryanichnikova, E.G., and Tyutin, A.V., Expansion of the range of the Black Sea snail Lithoglyphus naticoides (C. Pfeiffer, 1828) (Mollusca: Gastropoda: Lithoglyphidae) and associated trematode species in the Upper Volga, Inland Water Biol., 2018, vol. 11, no. 2, pp. 234–235. https://doi.org/10.1134/S1995082918020165

    Article  Google Scholar 

  15. Pirogov, V.V., On the finding of Lithoglyphus naticoides in the Volga delta, Zool. Zh., 1972, vol. 51, no. 6, pp. 912–913.

    Google Scholar 

  16. Samye opasnye invazionnye vidy Rossii (TOP-100) (The Most Dangerous Invasive Species in Russia (TOP-100)), Dgebuadze, Yu.Yu., Petrosyan, V.G., and Khlyap, L.A., Eds., Moscow: KMK, 2018.

  17. Sokal, R.R. and Rohlf, F.J., Biometry. The Principals and Practice of Statistics in Biological Research, New York: W.H. Freeman, 1995.

    Google Scholar 

  18. Stanevičiūtė, G., Petkevičiūtė, R., and Kiselienė V., Digenean parasites in prosobranch snail Lithoglyphus naticoides population with the morphological description of Echinochasmus sp. cercaria, Ekologija, 2008, vol. 54, no. 4, pp. 251–255. https://doi.org/10.2478/v10055-008-0037-6

    Article  Google Scholar 

  19. The River Volga and Its Life, Mordukhai-Boltovskoi, F.D., Ed., Hague: Springer, 1979. https://doi.org/10.1002/iroh.19800650315

  20. Tyutin, A.V. and Kiyashko, V.I., Fish parasites, in Struktura i funktsionirovanie ekosistemy Rybinskogo vodokhranilishcha v nachale XXI veka (Structure and Functioning of the Ecosystem of the Rybinsk Reservoir at the Beginning of the XXI Century), Lazareva, V.I., Ed., Moscow: Inst. Biol. Vnutr. Vod, Ross. Akad. Nauk, 2018, pp. 294–297.

  21. Tyutin, A.V. and Medyantseva, E.N., On the causes of range extension of the trematode Apophallus muehlingi (Jägerskiöld, 1899) in the Volga Basin, Biol. Vnutr. Vod, 2008, no. 2, suppl., pp. 41–46.

  22. Tyutin, A.V., Medyantseva, E.N., Gremyachikh, V.A., and Komov, V.T., Host–parasite relationships in the plerocercoids of Ligula intestinalis (L.) (Cestoda: Pseudophyllidea)—carp fish system and the mercury accumulation in the muscles of hosts, Parazitologiya, 2019, vol. 53, no. 3, pp. 241–250. https://doi.org/10.1134/S0031184719030062

    Article  Google Scholar 

  23. Tyutin, A.V. and Slynko, Yu.V., The first finding of the Black Sea snail Lithoglyphus naticoides (Gastropoda) and its associated species-specific trematoda in the Upper Volga basin, Russ. J. Biol. Invasions, 2010, vol. 1, no. 1, pp. 45–49. https://doi.org/10.1134/S2075111710010091

    Article  Google Scholar 

  24. Tyutin, A.V., Verbitsky, V.B., Verbitskaya, T.I., and Medyantseva, E.N., Parasites of alien aquatic animals in the Upper Volga basin, Russ. J. Biol. Invasions, 2013, vol. 4, no. 1, pp. 54–59. https://doi.org/10.1134/S2075111713010098

    Article  Google Scholar 

  25. Tyutin, A.V. and Izvekova, G.I., Infections of mollusks and fish by the trematode Apophallus muehlingi (Jägerskiöld, 1899) and its interrelations with intermediate hosts, Inland Water Biol., 2013, vol. 6, no. 1, pp. 52–56. https://doi.org/10.1134/S1995082912030157

    Article  Google Scholar 

  26. Yakovlev, V.A., Akhmetzyanova, N.S., and Yakovleva, A.V., Distributional patterns and size-weight parameters of Lithoglyphus naticoides (Gastropoda: Hydrobiidae) in the upper reach of the Kuibyshev Reservoir, Russ. J. Biol. Invasions, 2010, vol. 1, no. 4, pp. 313–322. https://doi.org/10.1134/S2075111710040090

    Article  Google Scholar 

  27. Yakovleva, G.A., Lebedeva, D.I., and Ieshko, E.P., The first finding of Apophallus muehlingi (Jägerskiöld, 1899), Lühe, 1909 (Trematoda, Heterophyidae) in Karelia, Russ. J. Biol. Invasions, 2016, vol. 7, no. 2, pp. 200–204. https://doi.org/10.1134/s2075111716020144

    Article  Google Scholar 

  28. Yanygina, L.V., Regional features of alien macroinvertebrate invasion into the water ecosystems of the Ob River Basin, Contemp. Probl. Ecol., 2016, vol. 9, no. 3, pp. 384–390. https://doi.org/10.1134/S1995425516030161

    Article  Google Scholar 

  29. Zhokhov, A.E., Molodozhnikova, N.M., and Pugacheva, M.N., Dispersal of invading trematodes Nicolla skrjabini (Iwanitzky, 1928) and Plagioporus skrjabini Kowal, 1951 (Trematoda: Opecoelidae) in the Volga, Russ. J. Ecol., 2006, vol. 37, no. 5, pp. 363–365. https://doi.org/10.1134/S1067413606050110

    Article  Google Scholar 

  30. Zhokhov, A.E., Pugacheva, M.N., Molodozhnikova, N.M., and Berechikidze, I.A., Alien parasite species of the fish in the Volga River basin: A review of data on the species number and distribution, Russ. J. Biol. Invasions, 2019, vol. 10, no. 2, pp. 136–152. https://doi.org/10.1134/S2075111719020140

    Article  Google Scholar 

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Funding

This work was carried out within the framework of the State Tasks of the Russian Federation (nos. 121051100109-1 and 121051100100-8).

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Authors and Affiliations

  1. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, 152742, Borok, Russia

    A. V. Tyutin, E. N. Medyantseva & D. A. Morozova

  2. Darwin State Biosphere Nature Reserve, 162723, Borok, Russia

    D. A. Morozova

  3. Demidov Yaroslavl State University, 150003, Yaroslavl, Russia

    V. A. Tyutin

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  1. A. V. Tyutin
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  2. E. N. Medyantseva
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Correspondence to A. V. Tyutin, E. N. Medyantseva or D. A. Morozova.

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Translated by T. Kuznetsova

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Tyutin, A.V., Medyantseva, E.N., Morozova, D.A. et al. The Dynamics of Trematode Occurrence in Two Permanent Settlements of the Ponto-Azov Mollusk Lithoglyphus naticoides (C. Pfeiffer, 1828) (Gastropoda, Hydrobiidae) at the Northeastern Border of Its Range. Russ J Biol Invasions 13, 537–543 (2022). https://doi.org/10.1134/S2075111722040130

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