INTRODUCTION

Trematodes, also called “blood flukes” (Digenea: Schistosomatoidea), parasitizing the blood vessels of vertebrates, are allocated into three families; each family corresponds to a certain group of definitive hosts. Schistosomes (Schistosomatidae) infect birds and mammals; they are considered the most studied group of trematodes (Brant et al., 2006). Spirorchids (Spirorchiidae) are parasites of marine and freshwater turtles. Trematodes of the family Aporocotylidae Odhner, 1900 parasitize marine and freshwater fish. Blood flukes in fish usually develop with the participation of one intermediate host, which can be a species from gastropods, bivalves, and polychaetes (Peoples, 2013). They parasitize the cartilaginous and bony marine, estuarine, and freshwater fish throughout the world, mainly localized in the blood, body cavity, and (infrequently) other organs (Alama-Bermejo et al., 2011). At present, aporocotylids comprise 165 species assigned to 39 genera (Orélis-Ribeiro et al., 2014; Warren and Bullard, 2019). New genera and species of this family are being found at a relatively high rate compared to that for other families of fish trematodes; diversity in it is apparently underestimated (Cribb and Bray, 2011). Nevertheless, this family remains a very poorly studied trematode. Blood flukes in freshwater fish are insufficiently studied when compared with the marine fish trematode. Thus, only 6 of 39 genera of aporocotylids are blood parasites of the freshwater fish. Species of the genus Acipensericola Bullard, Snyder, Jensen et Overstreet, 2008 parasitize the freshwater sturgeon species in North America (Warren et al., 2017). Representatives of the genera Plehniella Szidat, 1951; Cladocaecum Orélis-Ribeiro & Bullard, 2016; Kritsky Orélis-Ribeiro & Bullard, 2016; and Nomasanguinicola Truong & Bullard, 2013 infect catfish species (Siluriformes) in South America, West Asia, and Southeast Asia (Truong and Bullard, 2013; Orélis-Ribeiro, Bullard, 2015). The largest genus Sanguinicola Plehn, 1907 includes species known as freshwater, marine, and estuarine fish. Freshwater sanguinicola species are recorded in fish on every continent except Australia. Five species of Aporocotylidae—Sanguinicola armata Plehn, 1905; S. inermis Plehn, 1905; S. intermedia Ejsmont, 1926; S. volgensis (Rasin, 1929) McIntosh, 1934; and S. rutili Simon-Martin, Rojo-Vazquez & Simon-Vicente, 1987—are described in the freshwater fish of Europe. In addition, some of these trematodes were found in fish and snails in the water bodies of Central Asia and West Siberia (the Ob-Irtysh River basin). No molecular genetic test was performed for any of these species.

This paper presents data on the spreading, host distribution, and fish infection with freshwater aporocotylids; their diversity; and snail infection with cercariae.

The deficiency in information on trematodes of the genus Sanguinicola can be explained by the fact that sanguinicolae are small transparent worms 1–2 mm in length localized in the fish heart, gill vessels, and kidneys. It is difficult to remove these organs accurately. When the blood vessels break, trematodes exit from them and escape; therfore, it is rather difficult to find them, especially upon low intensities of invasion. Rather commonly, researchers cannot find the trematodes themselves, but indicate eggs that are detectable through the gill filament vessels of fish. It is quite possible that sanguinicolae are rarely found because blood vessels and the heart are rarely observed within routine parasitology testing in fish. It cannot be excluded that most sanguinicolae are occasionally detected. Any of those indicated above can be proven by the fact that sanguinicolae found in snails and underyearling in some water bodies were not observed in adult fish. Thus, the underyearling of roach, ide, and pikepearch were infected with sanguinicolae (Kulemina, 1969), while sanguinicolae were not detected in adult fish (Shul’man and Kulemina, 1969). The report of Stenko (1979) provides data on the large infection of snails Lymnaea auricularia L., 1758 with sanguinicolae in various water bodies on the Crimean Peninsula, while these trematodes were not found in the fish there (Miroshnichenko, 2008). Further examples may be provided.

Distribution

The literature source data on the fish and snail infection show that European Sanguinicolae are widely distributed across Europe and Central Asia (Kazakhstan, Uzbekistan, and Kyrgyzstan). In addition, they are found in the southern part of West Siberia (Ob River basin) and in Caucasus (Fig. 1). The northern boundary of their distribution narrowly fails to reach the Article Circle (Mezen and Pechora Rivers) (Ekimova, 1962, 1976; Dorovskikh, 1997). S. inermis has been reported in wild carp from the Zeya River in the Amur River basin (Strelkov, 1971). The recently described Sanguinicola rutili has the most limited distribution, with evidence gathered so far only from Spain (Simon-Martin et al., 1987). Three species of sanguinicolae (S. armata, S. inermis, and S. volgensis) are found in fish in England; in addition, S. inermis is an introduced species (Kirk and Lewis, 1994).

Fig. 1.
figure 1

Map of the locations of Sanguinicola found in the freshwater fish (●) and snails () in Europe and some countries in Asia.

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A comparison of the records of trematodes found in fish and snails (Fig. 1) shows a considerable discrepancy in the distribution of both host parasites. Thus, the snails of five species infected with sanguinicola cercariae were found in different water bodies across the whole territory of Kazakhstan (Butenko, 1967; Smirnova and Irbasheva, 1967; Belyakova, 1975, 1981; Belyakova and Mazina, 1990). Adult S. inermis trematodes within the territory of Kazakhstan were found only in the carp on a fish farm near Alma-Ata (Agapova, 1966) and in the wild carp and the ide in the Bukhtarma Reservoir (Bragina, 1972). In Crimea, snails infected with cercariae were found in five different water bodies of high infection, up to 71.4% (Stenko, 1979). However, sanguinicolae were not found in fish in the Crimean Peninsula (Miroshnichenko, 2008). Sanguinicolae in fish and snails occur in water bodies and watercourses of different types: firths (Dogel and Petrushevsky, 1933; Mekhraliev and Mikailov, 1982), lakes, and lowland and upland rivers (Belyakova, 1975; Olenev, 1979; Ermolenko et al., 1998).

Life Cycles

Life cycles of European Sanguinicola species studied to a level alowing us to assign their cercariae and adults to a certain species are well-described for a limited number of species. Cercariae and sporocysts of S. armata found in the snail Lymnaea stagnalis (L., 1758) are described (Sendersky et al., 2002; Sendersky and Dobrovolsky, 2004). The authors found infected L. stagnalis snails in a pond inhabited by only one fish, the crucian Carassius carassius (L., 1758). The trematodes found in the crucian were determined as S. armata. The life cycles and morphology of the Sanguinicola inermis cercariae and maritae in the Cyprinus carpio (L.) and Lymnaea peregra (О.F. Müller, 1774) species experimentally infected have been studied (Kirk and Lewis, 1993). Moreover, the life cycle of Sanguinicola rutili has been studied (Simon-Martin et al., 1987). A description of cercariae, sporocysts, and maritae isolated from the snail Ancylus fluviatilis (О.F. Müller, 1774) and the fish Achondrostoma arcasii Steindachner, 1866 is reported in the paper.

Distribution and Host Range

It has been traditionally considered that European Sanguinicolae generally parasitize the Cyprinidae. An analysis of the literature source data has shown (Table 1) that this is only partly true. S. volgensis has a wide range of hosts (12 species); this species is more frequently recorded in pike. In addition, S. volgensis is found in Percidae (ruff, perch, and pikeperch) and eight species of Cyprinidae. S. inermis has a wide range of hosts (13 species); with a few exceptions, they are generally assigned to Cyprinidae (the wild carp is most frequent). S. armata, parasitaizing ten fish species, generally the Tench, may be called a species typical for the Cyprinidae. A similar so-called “Cyprinida” species is the S. intermedia, more frequently occurring in crucians and found only in four fish species. The endemic S. rutili species is found only in the Spanish roach Achondrostoma arcasii (Steindachner, 1866) in Spain. Table 1 presents a list of fish species infested with trematodes indicated as Sanguinicola sp. Among the hosts, the catfish Silurus glanis L., 1758 (trematode fragments are found); the stone loach Barbatula barbatula L., 1758; and the Peled Coregonus peled Gmelin, 1789 are recorded. An analysis of the European Sanguinicola records can prove that they parasitize fish of seven families: Cyprinidae (18 species), Esocidae (pike), Balitoridae (bearded stone loach), Cobitidae (loach), Percidae (perch, ruff, and pikeperch), Siluridae (catfish), and Coregonidae (peled); overall, they comprise 26 fish species.

Table 1.   Distribution and fish infection with freshwater trematodes of the genus Sanguinicola
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The record of Sanguinicola sp. found in the peled from the Pechora River has been reported (Ekimova, 1976). However, the peled is not found in the Pechora River, according to the data of ichthyologists (Reshetnikov, 2003). If the fish species was incorrectly identified, it could be the broad whitefish Coregonus nasus Pallas, 1776, which inhabit the Pechora River. Sanguinicola sp. found in the common whitefish caught in the Pechora River can probably be considered occasional, since these trematodes are not found in the other European and North Asian Salmonidae. However, Salmonidae (taimen and lenok) are recorded as the hosts of sanguinicolae in the Amur River basin (Strelkov, 1971; Ermolenko et al., 1998). Five species of Sanguinicola parasitizing the Salmonidae are known in North America (Warren et al., 2017).

The stone loach Barbatula barbatula L., 1758 is probably a nonrandom host choice by Sanguinicola sp., since it is a single record in Europe (Shevchenko, 1956). Sanguinicolae are found in the Siberian stone loach B. toni Dybowski, 1869 within the Primorie maritime region (Sanguinicola sp.) (Ermolenko, 2004) and Japan (S. hasegawai Shimazu, 2013) (Shimazu, 2013) and the Tibetan stone loach Triplophysa stoliczkai Steindachner, 1866 within Uzbekistan (S. inermis) (Bykhovskaya and Kulakova, 1987). In addition, a singular record of Sanguinicola sp. in catfish in the Volga River delta (Kurochkin, 1968) does not seem random, since aporocotylids in the Siluridae are found in Africa, West Asia, and Southeast Asia (Truong and Bullard, 2013).

The experimental datasets on the life cycles can provide more information on the specificity of Canguinicolae. The in vitro cultivation of S. inermis has proven that the specific host of this species is carp (wild carp). Trematodes infected tench only in the case of a high level of infection with cercariae. The crucian carp appeared unsusceptible to the invasion of the cercaria S. inermis (Kirk, Lewis, 1992).

Characteristics of Fish Infection

It is rather difficult to determine the importance of the quantitative variables for infection, since they are dependent on the sample size, which can frequently be small. Data analysis shows that the prevalence (P) of fish by sanguinicolae is generally low (Table 1). Examples of rare occasions when prevalence exceeds 30% are associated with the small sample sizes or the fish P assessment by trematode eggs found in the gills. In addition, the high P was usually recorded in the limnephilus fish (crusian, tench, and wild carp) in lakes and reservoirs. The intensity of infection (II) is also low, generally no more than several units; >10 worms per fish is quite rare (Table 1). Very high II (>100 units per fish) is measured only in carps, probably of large sizes (Strelkov, 1971; Kirk and Lewis, 1994). It is considered that sanguinicolae are more frequently found in fish of the southern regions. With respect to S. volgensis, this statement is not proven by the data in Table 1. It is partly true for wild carp infection with S. inermis; however, the wild carp itself is a thermophilic fish more frequently found in southern regions.

There is almost no open data on fish infection associated with age. The analysis of large datasets on the wild carp infection with S. inermis reveals no age dependency ratio (Kirk and Lewis, 1994). A high level of infection was observed in both juveniles and old fish (10+). These authors have revealed that two species of sanguinicolae (S. volgensis and S. inermis) may simultaneously parasitize the fish. With respect to the other datasets (Scheuring, 1922), S. inermis is found in larger quantitities in juvenile carp, rather than in old fish. Sanguinicolae infect fish at the early life stages. Young Sanguinicola sp. found in the branchial artery of roach larvae at the age of 59 days, in ide larvae at the age of 34–35 days (Lopukhina and Strelkov, 1972b; Yunchis, 1972). Other data shows that sanguinicolae infect roach larvae 8–11 mm in body length at the age of 10 days, ide larvae of 18–22 mm body length at the age of 25 days, and pikeperch larvae 7–12.5 mm in body length at the age of 15–20 days (Kulemina, 1969). The carp larvae at the pond fish farms are usually infected with S. inermis at the age of 29–30 days (Chechina, 1959).

Snail Hosts

Pulmonate gastropods and prosobranchs of the families Lymnaeidae, Planorbidae, Valvatidae, Neritidae, Lithoglyphidae, Bithyniidae, and Melanopsidae, totally comprising 24 species (the number of species may be lower due to adjusting the variations in the systematics of snails), are registered as the first intermediate hosts of European sanguinicolae (Table 2). Among the listed families, the sanguinicola sporocysts and cercariae were more frequently found in lymneids (Lymnaea stagnalis; L. pereger; L. palustris; L. corvus Gmelin, 1791; Radix ovata; R. auricularia; and R. auricularia m. lagotis) and melanopsids (Melanopsis premorsa L., 1758; Fagotia acicularis Férussac, 1823; F. esperi Férussac, 1823; Microcolpia ucrainica Starobogatov, Alexenko & Levina, 1992; M. canaliculata Bourguignat, 1884; and M. potamoctebia Bourguignat, 1870). The sanguinicolid hosts recorded were represented by three species among valvatidae (Valvata piscinalis O.F. Müller, 1774; V. macrostoma Mörch, 1864; and V. pulchella Studer, 1789) and two species among bithyniidae (Bithynia tentaculata L., 1758 and B. leachii Sheppard, 1823). Among lithoglyphidae, neritidae, and planorbidae, they were represented by one species each (Lithoglyphus naticoides C. Pfeiffer, 1828; Theodoxus fluviatilus L., 1758; and Ancylus fluviatilis, respectively).

Table 2.   Distribution and infection of snails with cercariae of freshwater trematodes of the genus Sanguinicola
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Some cercariae found in the snails were identified as S. inermis, S. armata, and S. intermedia, while the others were given temporary or symbolic names by the authors (Table 2).

Morphology of cercariae is too poorly studued. Therefore, most of the cercariae found in hosts are unindentified as species. Thus, M.N. Chernogorenko (1976) identified five cercaria species isolated from seven snail species, which are different in morphology and body sizes.

Articles providing drawings of cercaria and data on their sizes (Ejsmont, 1926; Khan, 1961; Butenko, 1967; Olenev, 1979; Simon-Martin et al., 1987; Belyakova and Mazina, 1990; Kirk and Lewis, 1993; Sendersky and Dobrovolsky, 2004; Faltynkova et al., 2007) deal with snails assigned to a small number of species of all studied species. They include only Lymnaea stagnalis, L. peregra, Radix ovata, R. auricularia, Valvata macrostoma, V. piscinalis, Melanopsis premorsa, Ancylus fluviatilis, and Bithynia leachi. The morphology of sanguinicolid cercariae released from the other species of snails is not studued. Therefore, the true diversity of the cercariae Sanguinicola parasitizing the snails remains unknown.

According to a quantitative assessment, the snail infestation with sanguinicolae at cercarial stages is low in total (Table 2). The infection of small species of the families Valvatidae, Neritidae, Lithoglyphidae, Bithyniidae, and Melanopsidae is no more than 10%, despite the large sizes of the analyzed samples. The large species of lymneids are infected even more weakly. Stenko (1979) reports about the very heavy infection (71.4%) of Lymnaea auriculari in the water bodies of the Crimean Peninsula; however, there is no information on quantity of the analyzed snails in the article.

It is very difficult to define the specificities of sporocysts and cercariae in relation to snails based on faunistic data. Thus, cercareae under the name Sanguinicola inermis were found in several species of lymneids and Bithynia tentaculata, while cercaria S. armata were found in Lymnaea stagnalis and Bithynia leachi (Table 2). The limited data on their life cycles can indicate that Sanguinicola inermis may be developed only in Lymnaea peregra and L. auricularia, while L. stagnalis is unsusceptible to the invasion of Sanguinicola inermis (Kirk and Lewis, 1992). Taking into consideration the specificity of S. inermis in relation to wild carp and the data in Table 2, it becomes clear why snails Lymnaea peregra and L. auricularia infected by Sanguinicola (and probably S. inermis) are found only in the southern regions, where wild carp inhabit the natural freshwater environments.

According to a quantitative assessment, the snail infection with sanguinicolae at cercarial stages is low in total (Table 2). Infection of small species of the families Valvatidae, Neritidae, Lithoglyphidae, Bithyniidae, and Melanopsidae is no more than 10%, despite the large sizes of the samples. The large species of lymneids are infested even more weakly. Stenko (1979) reports about the very heavy infestation (71.4%) of Lymnaea auriculari in the water bodies of the Crimean Peninsula; however, there is no information on the quantity of the analyzed snails in the article.

Molecular genetic data on the larval stages of sanguinicolae from snails are sparse. Research has begun on genotyping sanguinicolae that invade various species of freshwater snails (Khrisanfova et al., 2013, 2019).

CONCLUSIONS

European freshwater trematodes of the genus Sanguinicola remain an insufficiently studied group of trematodes. Research into these trematodes seems not to be going anywhere. It is considered definite that only five species of sanguinicolae parasitize European fish. Research over the last 20 years has proven the existence of well-known species parasitizing some species of fish and snails in different water bodies. This review is taken as an attempt to compile as much data as possible on the distribution and biology of these trematodes. The toughest challenge associated with studying the freshwater sanguinicolae is a lack of knowledge of true diversity of this group. Assessing open data sources has shown that the number of species of sanguinicola cercariae found in the snails is larger than the number of species described as adult trematodes. In addition, the morphological description of almost all known cercariae cannot be considered sufficient. Taking into account that the parthenogenetic generation of trematodes is very specific in relation to the host, with few exceptions, it may be assumed that a great number of species of sanguinicolae parasitize the snails of 24 species that are recorded as hosts of sanguinicolae known at the moment. Fish of 26 species assigned to seven families and four orders were identified as hosts of European sanguinicolae. The richness of more than five known species of blood flukes may be expected with such an abundant diversity of hosts. All information available in literature sources on the distribution of sanguinicolae throughout the host range, based on faunistic data, shows that each of them, except for Sanguinicola rutili, parasitizes several or many fish species. However, the example described above for S. inermis in vitro cultivation can prove that this species is very specific and parasitizes fish of one–two species. This is probably true in relation to the other known but undescribed species of sanguinicolae.