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1 BIHAREAN BIOLOGIST Univeristy of Oradea, Faculty of Sciences, Department of Biology Univeristatii str. No.1, Oradea , Romania Publisher: University of Oradea Publishing House url: index.html Contact BIHAREAN BIOLOGIST (International journal of biology) ACCEPTED PAPER - Online until proofing - Authors: Oksana V. TRAVINA; Yulia V. BESPALAYA; Olga V. AKSENOVA; Alexander R. SHEVCHENKO; Svetlana E. SOKOLOVA Title: Infection of Dreissena polymorpha (Bivalvia: Dreissenidae) with Phyllodistomum macrocotyle (Digenea: Gorgoderidae) in the Severnaya Dvina River Basin, Northern Russia Journal: Biharean Biologist Article number: e Status: awaiting proofing How to cite: Travina O.V., Bespalaya Y.V., Aksenova O.V., Shevchenko A.R., Sokolova S.E. (2019): Infection of Dreissena polymorpha (Bivalvia: Dreissenidae) with Phyllodistomum macrocotyle (Digenea: Gorgoderidae) in the Severnaya Dvina River Basin, Northern Russia. Biharean Biologist 13: e Date published:

2 Infection of Dreissena polymorpha (Bivalvia: Dreissenidae) with Phyllodistomum macrocotyle (Digenea: Gorgoderidae) in the Severnaya Dvina River Basin, Northern Russia Oksana V. TRAVINA 1, Yulia V. BESPALAYA 1,2 *, Olga V. AKSENOVA 1,2, Alexander R. SHEVCHENKO 1,2 and Svetlana E. SOKOLOVA N. Laverov Federal Center for Integrated Arctic Research, Russian Academy of Sciences, Severnaya Dvina Emb. 23, Arkhangelsk, Russian Federation. 2 Northern (Arctic) Federal University, Severnaya Dvina Emb. 17, Arkhangelsk, Russian Federation. *Corresponding author, Yu. Bespalaya, jbespalaja@yandex.ru Abstract. The infection of D. polymorpha with sporocysts of P. macrocotyle in the Northern Dvina River Basin, Northern Russia has been detected for the first time and represents the northern most record of the host-specific parasite. The average shell length of infected zebra mussels was 26.0 mm. As is typical for the parasite, prevalence of infection was low (i.e., <1%) and juveniles of D. polymorpha were not observed to be infected. Key words: Dreissena polymorpha, invasive species, Severnaya Dvina River Basin, infection, Phyllodistomum macrocotyle Running Title. Infection of Dreissena polymorpha The zebra mussel, Dreissena polymorpha (Pallas 1771), is a successful invasive species coming from the freshwater regions of the Caspian area which has spread widely throughout Europe and North America (Burlakova et al. 2006, Peñarrubia et al. 2016). The 2

3 northernmost boundary of D. polymorpha distribution is the Northern Dvina River (Starobogatov & Andreeva 1994). The first record of the species in the Northern Dvina River dates to the beginning of the twentieth century (Skorikov 1903). It was found that when the zebra mussel invaded the freshwaters, it can became the absolute dominant species among benthic organisms and periphyton, both in abundance and biomass (Karatayev et al. 1997). The zebra mussel is often a host for a number of invertebrates (Karatayev et al. 2000). Hence, for D. polymorpha, 34 taxa of parasites, including ciliates, trematodes, nematodes, chironomids, oligochaetes, mites and leeches have been reported (Molloy et al. 1997). Among them, the parthenites of trematodes in the genus Phyllodistomum occupy a special status due to their high pathogenicity (Tyutin et al. 2005). The cosmopolitan genus Phyllodistomum Braun, 1899 contains more than 110 species, most of which as adults inhabit the urinary bladders and/or ureters of teleost fishes (Petkevičiūtė et al. 2014). Phyllodistomum spp. have been reported in populations of D. polymorpha throughout Europe (Molloy et al. 1996, 1997, Karatayev et al. 2000). At the same time, to our knowledge, D. polymorpha infection with Phyllodistomum in the Northern Dvina River Basin had not been previously studied. The aim of the present study was to investigate the infection by trematodes of the genus Phyllodistomum in D. polymorpha populations in the watercourses of the Northern Dvina River Basin. Samples of D. polymorpha were collected from the Northern Dvina (64 22' N, 40 59' E), Juras (64 34' N, ' E), Lyavlya (64 23' N, 41 00' E), and Solombalka (64 34' N, 40 31' E) rivers in the periods of June-August 2016 and June-August The samples of D. polymorpha were gathered using a rectangular hand net (dimensions 0.28 m 0.5 m, mesh size 200 µm), Petersen grab (0.024 m 2 ) and also manual collection from various substrates, 3

4 fixed networks, etc. The samples were washed using a hydrobiological sieve (mesh size 0.56 mm), placed in an ice container, and delivered alive to the laboratory for further examination. The gills and visceral mass were removed from the shell and the whole body was dissected and examined for the presence of trematodes using a stereomicroscope Leica M165 C with a digital camera (Leica DFC 425). Histological examination was not performed (Burlakova et al. 2006). A total of 446 mussels were examined. Identification of trematode sporocysts was carried out on the basis of previous published works (Zdun et al. 1994, Molloy et al. 1997). The materials are stored in the collection of the Russian Museum of the Biodiversity Hotspots of the N. Laverov Federal Center for Integrated Arctic Research of Russian Academy of Sciences, Arkhangelsk, Russia. Phyllodistomum macrocotyle (Lühe, 1909) sporocyst infection was recorded in 3 individuals of D. polymorpha from Juras River (Fig. 1). The overall percentage of infected individuals of D. polymorpha by P. macrocotyle was <1%. The shell length of infected zebra mussels was mm [average length: 26.0 mm (SD: 4.0)]. Juveniles of D. polymorpha were not infected by trematodes. Sporocysts were oval and mm in length (Fig. 1b). Sporocysts of P. macrocotyle were recorded from zebra mussels in one of the four sampled populations. In the past, Phyllodistomum trematodes found in D. polymorpha were also referred to as P. folium, P. dogieli, or P. angulatum, but recent molecular work has shown that these latter three species names have been incorrectly used, and that P. macrocotyle is the only valid Phyllodistomum species thus far documented from D. polymorpha (Petkevičiùte et al. 2014). It is well known that D. polymorpha is the intermediate host of P. macrocotyle sporocysts (Molloy et al. 1997, Burlakova et al. 2006). Mollusks are infected by freeswimming miracidium larvae, which subsequently give rise to a number of parthenogenetic generations of sporocysts (Mastitsky 2003). Mature sporocysts containing metacercariae are 4

5 shed from the gills and float through the water (Molloy et al. 1997). For its complete life cycle, P. macrocotyle requires only one other host, namely, a fish (Molloy et al. 1997). It was found that the D. polymorpha individuals that were infected with P. macrocotyle showed a decrease in mass compared with uninfected individuals. In addition, the concentration of toxic substances such as Cd and Pb was found to be higher in infected D. polymorpha (Davids & Kraak 1991). In fish, Phyllodistomum spp. are localized in the ureters and bladder (Petkevičiùte et al. 2014), causing blockage of the ducts and inflammatory processes (Mastitsky 2003). The infection of fish by trematodes of the genus Phyllodistomum in the Severnaya Dvina River Basin was reported for the first time by Gnedin, Savin in 1930 (Jushkov & Ivashevsky 1999). The authors found that the definitive hosts for the trematode Phyllodistomum spp. are pike, grayling, ruff, perch, freshwater sculpin, chub, dace, ide, minnow, crucian, rudd, roach, bleak, and verkhovka. Currently, Phyllodistomum has been recorded from D. polymorpha in the Netherlands, Poland, Belarus, Russia, Ukraine, and Kazakhstan (Molloy et al. 1996, Tyutin et al. 2005), and our observation in the Juras River represents the northernmost record of this host-specific parasite. The percentage of D. polymorpha infection with P. macrocotyle sporocysts is typically low, often < 1% (Molloy et al. 1996, Karatayev et al. 2000), which in accordance with the results of the present study. To our knowledge, the present study provides the first information on the infection of D. polymorpha by sporocysts of P. macrocotyle in the Northern Dvina River Basin. Taking into account that the zebra mussel is characterized by a fast growth rate, high fecundity and abundance, it is necessary to conduct further studies of parasites and endosymbionts of D. polymorpha in the region using histological and methods in molecular genetics Acknowledgements 5

6 The authors express their gratitude to Lyubov E. Burlakova, Alexander Y. Karataev, and Daniel P. Molloy for their advice and assistance in identifying the sporocyst trematode. The authors would like to acknowledge two anonymous reviewers for their comments and suggestions which substantially improved the manuscript. This research was supported by grant no mol_a of the Russian Foundation for Basic Research and the study of distribution of D. polymorpha was supported by grant no of the Russian Foundation for Basic Research. 6

7 References Burlakova, L.E., Karatayev, A.Y., Padilla, D.K. (2006): Changes in the distribution and abundance of Dreissena polymorpha within lakes through time. Hydrobiologia 571: Jushkov, V.F., Ivashevsky, G.A. (1999): Parasites of vertebrates animals of European North - East of Russia. The catalogue. Institute of biology Komi Scientific center Uro RAS, Syktyvkar [In Rusian]. Karatayev, A.Y., Burlakova, L.E., Padilla, D.K. (1997): The effects of Dreissena polymorpha (Pallas) invasion on aquatic communities in Eastern Europe. Journal of Shellfish Research 16: Karatayev, A.Y., Burlakova, L.E., Molloy, D.P., Volkova, L.K. (2000): Endosymbionts of Dreissena polymorpha (Pallas) in Belarus. International Review of Hydrobiology 85: Kraak, M.H.S., Davids, C. (1991): The effect of the parasite Phyllodistomum macrocotyle (Trematoda) on heavy metal concentrations in the freshwater mussel Dreissena polymorpha. Netherlands Journal of Zoology 41: Mastitsky, S.E. (2004): Distribution of trematode Phyllodistomum folium (Digenea: Gorgoderidae) among populations of the mollusc Dreissena polymorpha (Pallas) in Belarus. pp: In: Proceedings of the international conference of young scientists and students «Sakharov s readings 2003: ecological problems of the XXI century». Trioleta Press. [in Russian with English summary]. Molloy, D.P., Roitman, V.A., Shields, J.D. (1996): Survey of the parasites of zebra mussels (Bivalvia: Dreissenidae) in northwestern Russia, with comments on records of parasitism in Europe and North America. Journal of Helminthology 63:

8 Molloy, D.P., Karatayev, A.Y., Burlakova, L.E., Kurandina, D.P., Laruelle, F. (1997): Natural enemies of zebra mussels: predators, parasites, and ecological competitors. Reviews in Fisheries Science 5: Mordukhay-Boltovskoy, F.D. (1975): Metodika izucheniya biogeotsenozov vnutrennikh vodoemov (Method of studying the biogeocenoses of inland water bodies ed.), Nauka, Moscow. [In Rusian]. Peñarrubia, L., Vidal, O., Viñas, J., Pla, C., Sanz, N. (2016): Genetic characterization of the invasive zebra mussel (Dreissena polymorpha) in the Iberian Peninsula. Hydrobiologia 779: Petkevičiùte, R, Stunženas, V., Stanevičiùte, G., Zhokhov, A.E. (2015): European Phyllodistomum (Digenea, Gorgoderidae) and phylogenetic affinities of Cercaria duplicata based on rdna and karyotypes. Zoologica Scripta 44: Skorikov, A.S. (1903): The Modern Distribution of Dreissena polymorpha (Pallas) in Russia. Ezhegodnik Volzh. bioll. st. (Yearbook of the Volga Biol. St.), Saratov [In Rusian]. Starobogatov, J. I., Andreeva, C.I. (1994): Areal and it s history. pp In: Starobogatov, J. I. (eds.), Freshwater zebra mussel Dreissena polymorpha (Pall.) (Bivalvia, Dreissenidae). Systematics, ecology, practical meaning. Nauka Press. [in Russian]. Tyutin, A.V., Shcherbina, G.H., Medyantseva, E.N. (2005): Long-term dynamics of infection with Dreissena polymorpha (Bivalvia, Dreissenidae) by trematode parthenites in upper Volga Reservoirs pp In: Rivier I.K., Shcherbina, G.Kh., Krylov A.V. (eds.). Biological resources of fresh water: invertebrates. Rybinsk printing house. [In Rusian]. Zdun, V.I., Kiselene, V.K., Karatayev, A.Y., Makarova G.E. (1994): Parasites. pp In: Starobogatov, J.I. (eds.). Freshwater zebra mussel Dreissena polymorpha (Pall.) (Bivalvia, Dreissenidae). Systematics, ecology, practical meaning. Nauka Press[in Russian]. 8

9 158 Figures Figure 1. Dreissena polymorpha infected by sporocysts of Phyllodistomum macrocotyle: (A- B) sporocyst of P. macrocotyle on the gills of D. polymorpha (Juras River); (C-D) - dissected sporocysts. 9