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Mollusks (Gastropoda) as Intermediate Hosts of Cattles' Trematodes (Trematoda) in Conditions of Dnipro Basin's Small Ponds (Northern Ukraine).


The parasitic system is a special biosystem based on the trophic relationship between the parasite and the host (Beklemishev, 1970). The functioning of parasitic systems, in particular, the regulation of the relationship between their members, is ensured by a whole complex of environmental factors (Antipov et al., 2018; Kennedy, 1978; Krasnoshchekov, 1996).

Trematodes (Treamentoda: Digenea) are extremely common in tropical and subtropical climates (including Bolivia, Ecuador, Peru, Cuba, Egypt, Turkey, Iran), as well as in the European Union, Russia and Ukraine. Intermediate hosts of trematodes are freshwater gastropods (Caminade et al., 2015; Canete et al., 2004; Caron et al., 2014; El-Shazly et al., 2012; Gorokhov et al., 2010; Khoramian et al., 2014; Lopez et al., 2012; Novobilsky et al., 2013; Rondelaud et al., 2015; Stadnichenko, 2006).

Trematodes, which parasitize in the organs of the digestive system of cattle (in particular in the duodenum, the liver and the sections of the multi-chamber stomach) are an important epizootic danger to the cattle breeding of these countries (Munguia-Xochihua et al., 2007). In this context, separate representatives of the following species should be singled out: Fasciola hepatica (F. hepatica) (Linnaeus, 1758), Paramphistomum ichikawai (Fukui, 1922), Paramphistomum cervi (Schrank, 1790) and Liorchis scotiae (Willmott, 1950).

Gastropods mollusks (Gastropoda) the most numerous class in the Mollusca type (Linnaeus, 1758), which has about 60.000-75.000 species (Zhadin, 1926). Among the gastropods, there are very few real parasites, for example: Eulima bilineata (Alder, 1848), parasite of bottom marine animals (Ophiuroidea; Grey, 1840) from the type of echinoderms (Echinodermata; Klein, 1734) (Nekhaev, 2011).

However, many species of gastropods are included to the life cycle of helminths and the epizootic chain of domestic animals' invasive diseases, in particular Fasciola and Paramphistomum invasion of cattle.

According to their biology, freshwater mollusks are natural inhabitants of large and small ponds involved in water purification and are indicator species for determining the degree of anthropogenic loading of biotopes. The fauna of mollusks depends to a large extent on the propagation of certain types of higher vegetation and depth of water bodies, velocity, temperature and pH of water in the pond (Bennema et al., 2011; Sargison et al., 2016; Zhytova and Kornyushyn, 2017).

In Ukraine, the northern Polissya regions, geographical center of which is in the territory of Kyiv and Zhytomyr regions, are characterized by the largest species diversity of gastropods in the small rivers of the Dnipro basin (Zhytova and Kornyushyn, 2017). It causes a severe enzootic situation with Trematoda invasions of large and small ruminants in this zone.

So, the study of the epizootology of ruminant animals' trematodoses and freshwater fauna is closely interrelated and the provision of quality products and profitability of cattle breeding in endemic areas is impossible without comprehensive knowledge about ecology of the gastropods.

Materials and Methods

The research protocol of the current study was approved by the Ethic Committee of the Zhytomyr National Agroecological University (Approval number: 2016/07).

Freshwater mollusks were collected during 2016-2017 from river basins and their tributaries-rivers Teteriv and Sluch (Zhytomyr region), Bucha, Ros, Skvira (Kiev region). Particular attention was paid to the study of the malakofauna of lakes and swamps, which are located on the territory of these regions. Points of mollusks' collecting are shown on the map (Figure 1).

In general, more than one thousand specimens of molluscs from the family Lymnaeidae (2 species), Valvatidae (1 species), Planorbidae (2 species), Viviparidae (1 species) and Succineidae (1 species) were investigated. Cameral processing of materials was carried out in accordance with the recommendations of Zdun (1961). The molluscs were harvested using common methods (Stadnichenko, 2006). Identification of the species of mollusks was carried out according to external conchological features (Stadnichenko, 2004).

For histological study of the most common species of mollusks--Lymnaea stagnalis (L. stagnalis) (Linne, 1758), Planorbarius corneus (P. corneus) (Linne, 1758), hepatopancreas was taken from which were made preparations for parasitological microscopic examination. The presence of partenites (rediae) and larvae (cercariae) in the body of mollusks was determined using a microscope "XS-6320 (MICROmed, Poltava, Ukraine)". The intensity of the invasion was assessed visually according to the following criteria: weak-larvae defeat less than 1/10 volume of hepatopancreas; average-from 1/10 to 1/2; and strong--more than 1/2.

Results and Discussion

From the biotopes of groundwater ponds of the Dnipro basin in Kiev and Zhytomyr regions, we collected and identified 6 species of freshwater mollusks: L. stagnalis (Linnaeus, 1758); L. truncatula (Muller, 1774); P. corneus (Linnaeus, 1758); P. planorbis (Linnaeus, 1758); Viviparus contectus (Millet, 1813); Valvata (V.) piscinalis (Muller, 1774), and 1 terrestrial species--Succinea (S.) pfeifferi (Rossmassler, 1834).

Dominant species were L. truncatula, L. stagnalis, and P. corneus with a population density of 4-9 specimens/[m.sup.2] in the spring, in the summer of 14-20 specimens/[m.sup.2], and in the autumn, 1-3 specimens/[m.sup.2]. Other species occurred singly, 1-3 specimens/[m.sup.2]. For trematodes (Trematoda: Digenea) of ruminants, as intermediate hosts can serve: L. truncatula--for Fasciola hepatica

(Figure 2); L. stagnalis (Figure 3), L. truncatula and P. corneus (Figure 4)--for pathogens Paramphistomidae sp.; S. pfeifferi (Figure 5), sometimes may be an intermediate host of the dicrocoeliosis' pathogen (Dicrocoelium lanceatum) (Charlier et al., 2016; Dreyfuss et al., 1999; Faltynkova et al., 2008; Hodasi, 1972; Vignoles et al., 2016; Zhytova and Kornyushyn 2012).

Mollusk V. piscinalis can be the first intermediate host for trematodes Ichthyocotylurus pileatus (Rudolphi, 1802) and Diplostomum baeri (Dubois, 1937), the additional hosts of which are freshwater fish, and the definitive--gulls. According to the fact that there is no literature data about the distribution of ruminant trematodes' larvae in V. piscinalis, microscopic examination of these mollusks' hepatopancreas was not carried out. Our studies have confirmed that the ratio of species of molluscs in a certain area and the level of their invasion by partenites and larvae of the trematodes depend on the biotope's characteristics.

Thus, the malakofauna of small flowing (rivers, their tributaries and floodplains) and standing reservoirs (lakes, swamps) of the Dnipro basin of northern Ukraine differed considerably.

The data obtained is illustrated in Table 1, from which it is evident that part of the representatives of the species L. truncatula (up to 36.3%) was affected by rediae and cercariae of F. hepatica (Figure 6); up to 23.5% of L. stagnalis mollusks contained parthenogenetic genera of both F. hepatica and Paramphistomum sp. in hepatopancreas; some specimens of gastropods of the species P. corneus (5.7%) were invasive solely by Paramphistomum sp. trematodes.
        Fasciola hepatica  Paramphistomidae sp.

Cattle       10,8                 1,8
Goats         3,6                 1,2
Sheeps        4,3                 1,9

Figure 7. Average extensiveness of the invasion of large and small
cattle by trematodes in the territory of Kyiv and Zhytomyr regions
during 2016-2017, %

Note: Table made from bar graph.

Taking into account that L. truncatula mollusks are biological hosts exclusively for F hepatica, as well as the fact that they are widely distributed in the ponds of Ukrainian Polissya and the damage by the trematodes' partenites and larvae (especially in biotopes of lakes and swamps), there is a high risk for ruminants about fasciolosis throughout the studied area.

In contrast, the populations of L. stagnalis species of mollusks, which are often infected with rediae and cercariae of F. hepatica and Paramphistomidae sp., are more numerous near rivers than near standing water bodies.

Thus, in the northern regions of Ukraine at ponds of Dnipro basin, the predominant number of cases of cattle contamination by pathogens of paramfistomoses occurs near the rivers, and invasion by fascioles--near any ponds (both flowing and standing).

To establish the scale of the damage by the ruminant animals' trematodes in the investigated area, we have analyzed the official data of the state veterinary service in the Kyiv and Zhytomyr regions for 2016-2017. The analysis results are presented in Figure 7. The high extensiveness of ruminal invasion with Paramphistomidae sp. (1.2-1.9% of all examined animals), and especially F hepatica (3.6-10.8%), confirm the obtained data on the widespread distribution of the diseases in the northern regions of Ukraine.

It is known that 25% invasion of malakofauna with helminths in a particular region is quite sufficient for the preservation and spread of the disease among the favorable domestic animals (Beesley et al., 2017). Just in one mollusc can develop at the same time more than 100 trematodes' cercariae. This is confirmed by our own research, according to which, up to 11% of cattle in the territory of Kyiv and Zhytomyr regions are having fasciolosis. It is not a critical indicator, but it is also not a reason to ignore the problem, since the stationary troubles of farms bring not less economic damage than sudden outbreaks of especially dangerous diseases.

To disrupt the stability of the parasitic system (trematodes-mollusks-ruminants), a sharp change in external environmental factors may occur. For example, the subletal for gastropods is the temperature of water above 27[degrees]C, depending on the type of mollusk (Afanasyev, 1993), due to the population of mollusks in the waters of Central Europe in the summer, it is sometimes significantly reduced. However, representatives of the subclass Pulmonata (Cuvier, 1817), adapted to the sharp fluctuations of temperature, falling into the summer (aestivation period) or winter (hibernation period) lethargy.

In most of the water systems of the Dnipro basin in the north of Ukraine, conditions for the development of freshwater mollusks are quite favorable. The climate of this area is mild, moderately continental. Endemic species of molluscs are evolutionally adapted to possible short-term critical climatic oscillations, as evidenced by the seasonal fluctuations of the number of gastropods in the studied ponds.

Thus, the presence of a permanent population of gastropod mollusks, affected by trematodes' pathogens, in small ponds of the north of Ukraine creates a permanent natural reservoir of fasciolosis and paramfistomatoses. This does not let to allow the cattle to be protected from further invasion without using of complex control measures against helminths.


In the biotope of natural ponds of the Dnipro basin at the northern regions of Ukraine, there are 7 species of gastropods, which are intermediates of ruminant's trematodes: L. stagnalis, L. truncatula, P. corneus, P. planorbis, Viviparus contectus, V. piscinalis and S. pfeifferi. The first three species are dominated by numbers: from 4 to 9 specimens/[m.sup.2] in spring, from 14 to 20 per [m.sup.2] in summer, and from 1 to 3 per [m.sup.2] in autumn.

Intraspecies indices of mollusks' invasiveness by partenites and larvae of the trematodes varied depending on the type of ponds. More often (23.5%) and more intensively the L. stagnalis population was affected by rediae and cercariae of F. hepatica and Paramphistomum sp., while in P. corneus (5.7%) was found only Paramphistomum sp. in rivers' biotopes. Indices of damage to mollusks of the species L. truncatula by the F. hepatica trematodes increased in lakes and swamps (36.3%).

Ethics Committee Approval: Ethics Committee approval was received for this study from the Ethics Committee of Zhytomyr National Agroecological University, Ukraine (Approval number: 2016/07).

Peer-review: Externally peer-reviewed.

Author Contributions: Concept--D.V.F., T.I.B., A.A.A.; Design--D.V.F., O.A.Z., R.V.S.; Supervision--D.V.F., A.A.A., V.P.G.; Resources--V.O.Y.; Materials--D.V.F., O.A.D., V.V.M.; Data Collection and/or Processing--T.I.B., V.P.G., V.S.S.; Analysis and/or Interpretation--D.V.F., T.I.B., B.H.S.; Literature Search--D.V.F., O.A.Z., O.A.D., V.S.S.; Writing Manuscript--D.V.F., T.I.B.; Critical Review--A.A.A., B.H.S.

Acknowledgements: The authors are grateful to Associate Professor Zhitova O.P. from Zhytomyr National Agroecological University for thematic advisory support.

Conflict of Interest: The authors have no conflict of interest to declare.

Financial Disclosure: The authors declared that this study has received no financial support.


Afanasyev, S.A., 1993. Influence of elevated water temperatures on elimination of different-sized Dreissenia. In: Materials of the VI All-Union Conference "The species and its productivity in the range" Minsk, 115.

Antipov, A.A., Bakhur, T.I., Feshchenko, D.V., Romanishina, T.A., Avramenko, N.V., Goncharenko, V.P., Zghozinska, O.A., Solovyova, L.M., Koziy, N.V., Pidborska, R.V., Shahanenko, V.S., Dzhmil, V.I., Tyshkivska, N.V., 2018. Earthworms (Lumbricidae) as intermidiate hosts of lung nematodes (Metastrongylidae) of swine in Kyiv and Zhytomyr regions of Ukraine. Vestnik Zoologii 52, 59-64.

Beesley, N.J., Williams, D.J.L., Paterson, S., Hodgkinson, J., 2017. Fasciola hepatica demonstrates high levels of genetic diversity, a lack of population structure and high gene flow: Possible implications for drug resistance. International Journal for Parasitology 47, 11-20.

Beklemishev, V.N., 1970. Disease Agents as Components of Bio-cenoses. In: Biocenotic Basics of Comparative Parasitology. Moskow, pp. 334-352.

Bennema, S.C., Ducheyne, E., Vercruysse, J., Claerebout, E., Hendrickx, G., Charlier, J., 2011. Relative importance of management, meteorological and environmental factors in the spatial distribution of Fasciola hepatica in dairy cattle in a temperate climate zone. International Journal for Parasitology 41, 225-233.

Caminade, C., Van Dijk, J., Baylis, M., Williams, D., 2015. Modelling recent and future climatic suitability for fasciolosis in Europe. Geospatial Health 9, 301-308.

Canete, R., Yong, M., Sanchez, J., Wong, L., Gutierrez, A., 2004. Population dynamics of intermediate snail hosts of Fasciola hepatica and some environmental factors in San Juan y Martinez municipality, Cuba. Memorias do Instituto Oswaldo Cruz 99, 257-262.

Caron, Y., Martens, K., Lempereur, L., Saegerman, C., Losson, B., 2014. New insight in lymnaeid snails (Mollusca, Gastropoda) as intermediate hosts of Fasciola hepatica (Trematoda, Digenea) in Belgium and Luxembourg. Parasites and Vectors 7, 66.

Charlier, J., Ghebretinsae, A.H., Levecke, B., Ducheyne, E., Claere-bout, E., Vercruysse, J., 2016. Climate-driven longitudinal trends in pasture-borne helminth infections of dairy cattle. International Journal for Parasitology 46, 881-888.

Gorokhov, V.V., Skira, V.N., Klenova, I.F., Taiichinov, U.G., Volichev, A.N., Peshkov, R.A., Maisheva, M.A., Gorokhova, E.V., Melnikova, L.E.E., Simolovskaya, N.A., Ermakov, I.V., 2010. Epizootic situation in the main helminthiases in the Russian Federation. Theory and Practice of Parasitic Animal Diseases 11, 124-131.

Dreyfuss, G., Vignoles, P., Rondelaud, D., Vareille-Morel, C., 1999. Fasciola hepatica: characteristics of infection in Lymnaea truncatula in relation to the number of Miracidia at exposure. Experimental Parasitology 92, 19-23.

El-Shazly, A.M., Nabih, N., Salem, D.A.B., Mohamed, M.Z., 2012. Snail populations in Dakahlia Governorate, Egypt, with special reference to lymnaeids. Egypt Journal of Biology 14, 45-49.

Faltynkova, A., Nasincova, V., Kablaskova, L., 2008. Larval trematodes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in Central Europe: a survey of species and key to their identification. Systematic Parasitology 69, 155-178.

Hodasi, J.K.M., 1972. The output of cercariae of Fasciola hepatica by Lymnaea truncatula and the distribution of metacercariae on grass. Parasitology 64, 53.

Khoramian, H., Arbabi, M., Osqoi, M. M., Delavari, M., Hooshyar, H., Asgari, M., 2014. Prevalence of ruminants fascioliasis and their economic effects in Kashan, center of Iran. Asian Pacific Journal of Tropical Biomedicine 4, 918-922.

Kennedy, K., 1978. Ecological parasitology. Moscow, Mir, p. 230.

Krasnoshchekov, G.P., 1996. Parasitic system: habitat and adaptation of parasites. Tolyatti, 50.

Lopez, M., White, A.C.Jr., Cabada, M.M., 2012. Burden of Fasciola hepatica Infection among Children from Paucartambo in Cusco, Peru. The American Journal of Tropical Medicine and Hygiene 86, 481-485.

Munguia-Xochihua, J.A., Ibarra-Velarde, F., Ducoing-Watty, A., Montenegro-Cristino, N., Quiroz-Romero, H., 2007. Prevalence of Fasciola hepatica (ELISA and fecal analysis) in ruminants from a semi-desert area in the northwest of Mexico. Parasitology Research 101, 127-130.

Nekhaev, I.O., 2011. Two species of parasitic molluscs new for Russian seas. Ruthenica 21, 69-72.

Novobilsky, A., Kasny, M., Beran, L., Rondelaud, D., Hoglund, J., 2013. Lymnaea palustris and Lymnaea fuscus are potential but uncommon intermediate hosts of Fasciola hepatica in Sweden. Parasites and Vectors 6, 251.

Rondelaud, D., Vignoles, P., Dreyfuss, G., 2015. Larval trematode infections in Galba truncatula (Gastropoda, Lymnaeidae) from the Brenne Regional Natural Park, central France. Journal of Helminthology 90, 256-261.

Sargison, N., Francis, E., Davison, C, Bronsvoort, B.M.C., Handel, I., Mazeri, S., 2016. Observations on the biology, epidemiology and economic relevance of rumen flukes (Paramphistomidae) in cattle kept in a temperate environment. Veterinary Parasitology 219, 7-16.

Stadnichenko, A.P., 2004. Prothorovic and calyx (Lymnaeidae, Acroloxidae) of Ukraine. Kiev, Center for Educational Literature, 327.

Stadnichenko, A.P., 2006. Lymnaeidae and Acroloxidae of Ukraine: Methods of collection and study, biology, ecology, useful and harmful meaning: monograph. Zhytomyr, Ruta, 168.

Vignoles, P., Rondelaud, D., Dreyfuss, G., 2016. Aptitude of Lymnaea palustris and L. stagnalis to Fasciola hepatica larval development through the infection of several successive generations of 4-mm-high snails. Parasitology Research 115, 2263-2268.

Zdun, V.I., 1961. Larvae of Trematodes in Freshwater Molluscs of Ukraine. Ukrainian Academy of Sciences Press, Kiev, p. 141.

Zhadin, V.I., 1926. Biology of fresh-water mollusks of ephemeral bodies of water. Russiche Hydrobiologische Zeitschrift, 131.

Zhytova, E.P., Kornyushyn, V.V., 2012. The dynamics of the dimensional and age structure of Lymnaea (L.) stagnalis (Gastropoda, Pulmonata) populations infected with trematode parthenitae and larvae. Visnyk of Lviv University, Biological series 58, 193-201.

Zhytova, E.P., Kornyushyn, V.V., 2017. The role of different mollusk species in maintaining the transmission of polyhostal Trematode species in Ukrainian Polissya waters: the specificity of Trematode parthenogenetic generations to mollusk hosts. Vestnik Zoologii 51, 295-310.

Diana Valeriyivna FESHCHENKO (1) [iD], Tetiana Ivanivna BAKHUR (2*) [iD], Biricik Halil SELCUK (3) [iD], Anatoliy Anatoliyovych ANTIPOV (2) [iD], Oksana Anatoliyivna ZGHOZINSKA (1) [iD], Oksana Anatoliyivna DUBOVA (1) [iD], Valentina Oleksandrivna YEVSTAFYEVA (4) [iD], Volodymyr Petrovich GONCHARENKO (2) [iD], Raisa Volodymyrivna SHAHANENKO (2) [iD], Volodymyr Sergiyovych SHAHANENKO (2) [iD], Vitaliy Vasyliovych MELNYCHUK (4) [iD]

(1) Department of Parasitology, Veterinary-Sanitary Expertise and Zoohygiene, Zhytomyr National Agroecological University, Zhytomyr, Ukraine

(2) Department of Parasitology and Pharmacology, Bila Tserkva National Agrarian University, Bila Tserkva, Kiev, Ukraine

(3) Department of Laboratory Animals, Afyon Kocatepe Universitesi, Afyon, Turkey

(4) Department of Parasitology and Veterinary-Sanitary Expertise, Poltava State Agrarian Academy, Poltava, Ukraine

Cite this article as: Feshchenko, D.V., Bakhur, T.I., Biricik, H.S., Antipov, A.A., Zghozinska, O.A., Dubova, O.A.,Yevstafyeva, V.O., Goncharenko, V.P., Shahanenko, R.V., Shahanenko, V.S., Melnychuk, V.V., 2019. Mollusks (Gastropoda) as Intermediate Hosts of Cattles' Trematodes (Trematoda) in Conditions of Dnipro Basin's Small Ponds (Northern Ukraine).Acta Vet Eurasia 2019; 45: 16-21.

ORCID IDs of the authors: D.V.F. 0000-0002-4811-2488; T.I.B. 0000-0001-8271-8267; B.H.S. 0000-0003-4974-1611; A.A.A. 0000-0003-3955-3377; O.A.Z. 0000-0003-4622-6307; O.A.D. 0000-0002-8303-573X; V.O.Y. 0000-0003-4809-2584; V.P.G. 0000-0002-7279-6146; R.V.S. 0000-0002-5848-1367; V.S.S. 0000-0002-3484-2962; V.V.M. 0000-0003-1927-1065.

Address for Correspondence: Tetiana Ivanivna BAKHUR * E-mail:

Received Date: 6 September 2018 * Accepted Date: 14 February 2019 * DOI: 10.26650/actavet.2019.18009
Table 1. Parasitologic study of mollusks' hepatopancreas (selected from
ponds, Dnipro basin, Northern Ukraine)

                            Extensiveness of the Invasion, %
                     Biotopes of Lakes  Biotopes
Species of Mollusks     and Swamps      of Rivers

L. truncatula
(Muller, 1774)                      F. hepatica
                           36.3          8.3
L. stagnalis
(Linnaeus, 1758)            F. hepatica and Paramphistomidae sp.
                           13.7         23.5
P. corneus
(Linnaeus, 1758)                  Paramphistomidae sp.
                            0            5.7
P. planorbis
(Linnaeus, 1758)                 Paramphistomidae sp.
                            0            0
S. pfeifferi
(Rossmassler, 1834)             Dicrocoelium lanceatum
                            0            0

                           Level of the Invasion
                     Biotopes of Lakes  Biotopes
Species of Mollusks     and Swamps      of Rivers

L. truncatula
(Muller, 1774)                 F. hepatica
                          Average          Weak
L. stagnalis
(Linnaeus, 1758)     F. hepatica and Paramphistomidae sp.
                           Weak           Strong
P. corneus
(Linnaeus, 1758)              Paramphistomidae sp.
                            0              Weak
P. planorbis
(Linnaeus, 1758)              Paramphistomidae sp.
                            0               0
S. pfeifferi
(Rossmassler, 1834)           Dicrocoelium lanceatum
                            0               0
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Title Annotation:Original Article
Author:Feshchenko, Diana Valeriyivna; Bakhur, Tetiana Ivanivna; Selcuk, Biricik Halil; Antipov, Anatoliy An
Publication:Journal of the Faculty of Veterinary Medicine
Date:Jan 1, 2019
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