The taxonomic survey of the fauna of cercariae (Platyhelminthes, Trematoda) in the mollusks of Uzbekistan
The article provides a list of trematodes cercariae found in the molluscs of Uzbekistan based on the analysis and generalisation of well-known data published in the period between 1934 and 2019. Currently, the list comprises 50 cercaria species belonging to 38 genera, 19 families and 11 orders of tr...
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| Published in: | Zoodiversity (Vestnik Zoologii) |
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| Date: | 2020 |
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| author | Shakarbaev, Ulugbek Akramova, Firuza Azimov, Djalaliddin |
| author_facet | Shakarbaev, Ulugbek Akramova, Firuza Azimov, Djalaliddin |
| author_institution_txt_mv | [
{
"author": "Ulugbek Shakarbaev",
"institution": "Abdulakimovich",
"orcid": "0000-0002-1475-2583"
},
{
"author": "Firuza Akramova",
"institution": null,
"orcid": "0000-0002-4603-3698"
},
{
"author": "Djalaliddin Azimov",
"institution": null,
"orcid": "0009-0008-8161-0084"
}
] |
| author_orcid_str_mv | 0000-0002-1475-2583 0000-0002-4603-3698 0009-0008-8161-0084 |
| author_sort | Shakarbaev, Ulugbek |
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| container_issue | 6 |
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| container_title | Zoodiversity (Vestnik Zoologii) |
| container_volume | 54 |
| datestamp_date | 2026-08-20T12:37:32Z |
| description | The article provides a list of trematodes cercariae found in the molluscs of Uzbekistan based on the analysis and generalisation of well-known data published in the period between 1934 and 2019. Currently, the list comprises 50 cercaria species belonging to 38 genera, 19 families and 11 orders of trematodes, the adult forms of which parasitise vertebrates (fish, amphibians, birds and mammals), including the human being. The cercariae were discovered in 38 mollusc species belonging to Gastropoda and Bivalvia. The discovered larvae comprised 12 groups of cercariae. |
| doi_str_mv | 10.15407/zoo2020.06.505 |
| first_indexed | 2025-07-17T12:35:42Z |
| format | Article |
| fulltext |
UDC 594.381.595.122
THE TAXONOMIC SURVEY OF THE CERCARIAL FAUNA
(PLATYHELMINTHES, TREMATODA) IN THE MOLLUSKS OF
UZBEKISTAN
U. A. Shakarbaev1, F. D. Akramova1, D. A. Azimov1
1 Institute of Zoology, Academy of Sciences of the Republic of Uzbekistan,
232 Bogishamol st., Tashkent, 100053 Uzbekistan
E-mail: ushakarbaev@mail.ru
U. A. Shakarbaev (https://orcid.org/0000-0002-1475-2583)
F. D. Akramova (https://orcid.org/0000-0002-4603-3698)
D. A. Azimov (https://orcid.org/0000-0002-2674-9242)
Th e Taxonomic Survey of the Cercarial Fauna (Platyhelminthes, Trematoda) in the Mollusks
of Uzbekistan. Shakarbaev, U. A., Akramova, F. D., Azimov, D. A. — Th e article provides a list of
trematodes cercariae found in the mollusks of Uzbekistan based on the analysis and generalisation of well-
known data published in the period between 1934 and 2019. Currently, the list comprises 50 trematode
species belonging to 38 genera, 22 families of trematodes, the adult forms of which parasitise vertebrates
(fi sh, amphibians, birds and mammals), including the human being. Th e cercariae were discovered in
38 mollusk species belonging to Gastropoda and Bivalvia. Th e discovered larvae comprised 12 morphotype
groups of cercariae.
Key words : cercariae, fauna, trematodes, mollusks, parasites, Uzbekistan.
Introduction
Th e research into mollusks’ participation in the life cycle of trematodes has a long history. Th e fi rst
studies are known to be carried out in the mid-17th century in Europe. Later, the research transferred to
other continents. Th e results of the studies of the cercarial fauna parasitising molluscs in diff erent countries
of the world have been generalised in the works of various researchers (Zdun, 1961, 1962; Nasir and Erasmus,
1964; Ito, 1964; Ginetsinskaya, 1968; Yamaguti, 1975; Chernogorenko, 1983; Nasir, 1984; Scholz et al., 2000;
Ostrowski de Núňez and Gil de Pertierra, 2004; Bartoli and Gibson, 2007; Mukherjee, 2007; Żbikowska and
Nowak, 2009; Cichy et al., 2011; Pinto and Melo, 2013). No doubt, the works mentioned above contributed
greatly to the further deeper research into the biodiversity of cercariae in many regions of the world.
Similar research has been accomplished in Uzbekistan. Th e works of Dogel and Bykhovsky (1934) are
oft en mentioned in relation to cercaria larvae in the fi sh of the Aral Sea. Th e authors of this article studied
Zoodiversity, 54(6): 505–522, 2020
DOI 10.15407/zoo2020.06.505
Parasitology
506 U. A. Shakarbaev, F. D. Akramova, D. A. Azimov
545 specimens of mollusks, in which they discovered several species of cercariae and metacercariae belonging
to the families Bucephalidae, Brachylaimidae, Plagiorchidae, Echinostomatidae and Strigеidae. For over 80
years researchers from Uzbekistan and other countries have been reporting on mollusks in Uzbekistan infected
with diff erent kinds of cercarial larvae. Th e results of their studies have been published in various scientifi c
periodicals and scientifi c literature. Almost all of them published in Uzbek or Russian, they are practically
inaccessible to foreign specialists. Th erefore, to make a general survey of the cercarial fauna in the mollusks
of Uzbekistan is highly important. We suppose that the publication of the survey in English will contribute to
deeper relations between Uzbek scientists and experts from a number of countries around the world, as well as
a better exchange of information on the study of trematodes’ life cycles.
Material and methods
Th e material of this work has been composed of the results of numerous studies of freshwater and
terrestrial mollusks as trematodes’ intermediate hosts in the aquatic and terrestrial ecosystems of Uzbekistan.
Th e studies were begun in 1934 and are still continuing now (2019). At the same time we have worked on
published articles dedicated to the cercarial larvae of the mollusks of Uzbekistan kept at diff erent libraries of the
former Soviet countries, mainly Russia, Ukraine and Uzbekistan. Besides, through various interviews we have
collected data from the publications of specialists from Uzbekistan and other countries of the former USSR we
have no access to.
In total we have studied about 100 articles dedicated to research into the cercarial fauna of certain species
and groups of trematodes found in freshwater and terrestrial mollusks. Th e taxonomic diversity of intermediate
host mollusks is given in conformity with the following systems (Zhadin, 1952; Starobogatov, 1970; Pazilov,
Azimov, 2003; Kruglov, 2005).
Th e list of cercariae developing in the mollusks of Uzbekistan is presented in conformity with the
classifi cation of Lühe (1909) and subsequent additions (Dawes, 1968; Zdun, 1961; Ginetsinskaya, 1968;
Chernogorenko, 1983).
It should be noted that the higher taxon system for trematodes from the subclass Digenea Carus, 1863 —
its orders and suborders has undergone considerable changes over the last 20 years. It is necessary to pay tribute
to those who have done that large amount of work. Th e most transformed are two orders — Plagiorchiida La
Rue, 1957 and Diplostomida Olson, Cribb, Tkach, Bray and Littlewood, 2003 (Gibson et al., 2002; Olson at al.,
2003; Jones et al., 2005; Bray et al., 2008; Kostadinova and Pérez-del-Olmo, 2014; Pérez-Ponce de León and
Hernández-Mena, 2019), which have considerably grown in size and changed in content. Th e structure of these
orders is highly disputable. According to Taxonomy Browser (2020), the number of orders has grown to 4:
Azigiida, Plagiorchiida, Diplostomida and Strigeidida. Th e higher taxons, orders and suborders of Trematoda
Digenea are interpreted in various ways, and there is no uniform opinion on that. Th e proposed order and
suborder systems of Trematoda Digenea are too formal and require amendments.
We provide the list of trematode cercariae in Uzbekistan in conformity with the system proposed for the
subclass Digenea by Key to the Trematoda (2002, 2005, 2008, Vol. 1–3).
Th at said, we retain a right to interpret the Bilharziellidae (Price, 1929: subfam.) as a sovereign family
uniting bilharziae, parasites of birds.
Characterising the species composition of the cercariae of certain taxonomic groups of trematodes, we
gave detailed data on the species recorded in the territory of Uzbekistan. Th is work gives information on the
intermediate hosts and groups of vertebrate hosts of each of these species. Each species of cercaria is classifi ed
and referred to a certain group of cercariae; each geographic place this or that cercaria species was found in is
marked, and for each species references to literary sources are given. Most of the data was obtained through the
study of mollusks infected in a natural way, in water or on land. Most of the cercaria species were identifi ed. For
some objective reasons a part of the cercariae were not diff erentiated. In our work they are classifi ed as cercariae
with unknown systematic positions.
Results
Th e bibliographic review is based on the analysis of about 100 scientifi c articles
published between 1934 and 2019 relating to cercarial larvae of trematode found in the
freshwater and terrestrial mollusks of Uzbekistan. A large number of mollusks belonging
to 2 classes, Gastropoda and Bivalvia, have been studied for the period mentioned, a part of
them being trematodes’ intermediate hosts. Th e total number of mollusc species involved
in trematodes’ life cycles is 38. Th e mollusks were infected by cercariae of 50 trematode
species (see the table below) belonging to 38 genera and 22 families of trematodes, the
mature forms of which parasitise fi sh, amphibians, birds and mammals (Shakarboyev et
al, 2012).
507Th e Taxonomic Survey of the Cercarial Fauna in the Mollusks of Uzbekistan
TREMATODE CERCARIAE FOUND IN THE MOLLUSKS OF UZBEKISTAN
Phylum Platyhelminthes Gegenbaur, 1859
Class Trematoda Rudolphi, 1808
Subclass Digenea Carus, 1863
BRACHYLAIMIDAE TRAVASSOS, 1922
Brachylaima fuscata (Rudolphi, 1819)
Intermediate host: Oxyloma elegans, Deroceras sturanui, Macrochamys sogdiana
(Gastropoda: Succineidae, Agriolimacidae, Ariophantidae).
Cercarial morphotype group: cercariaeum.
T a b l e . Th e taxonomic composition and species diversity of the cercariae discovered in the molluscs of
Uzbekistan (based on works published between 1934 and 2019)
Family Genus Number of species
Brachylaimidae Brachylaima 2
Hasstilesiidae Hasstilesia 1
Bucephalidae Bucephalus 1
Rhipidocotyle 1
Clinostomidae Clinostomum 1
Cyclocoeliidae Cyclocoelium 1
Diplostomidae Diplostomum 3
Codonocephalus 1
Neodiplostomum 1
Tylodelephus 1
Strigeidae Strigea 1
Cotylurus 1
Apatemon 1
Schistosomatidae Schistosoma 1
Bilharziellidae Bilharziella 1
Trichobilharzia 2
Ornithobilharzia 1
Dendritobilharzia 2
Gigantobilharzia 2
Aporocotylidae Sanguinicola 1
Echinostomatidae Echinostoma 1
Echinoparyphium 2
Hypoderaeum 1
Fasciolidae Fasсiola 2
Philophthalmidae Philophthalmus 1
Paramphistomidae Calicophoron 2
Liorchis 1
Gastrothylacidae Gastrothylax 1
Notocotylidae Notocotylus 4
Gorgoderidae Gorgodera 1
Dicrocoeliidae Dicrocoelium 1
Corrigia 1
Eurytrema 1
Plagiorchiidae Haplometra 1
Telorchiidae Opisthioglyphe 1
Haematoloechidae Haematoloechus 1
Skrjabinoeces 1
Pleurogenidae Pleurogenes 1
22 38 50
508 U. A. Shakarbaev, F. D. Akramova, D. A. Azimov
Habitat: terrestrial.
Defi nitive hosts: birds.
Localities: northeastern and southern regions.
References: Davronov (1999), Shakarboyev et al. (2012).
Brachylaima sp.
Intermediate host: Xeropicta candaharica (Gastropoda: Hygromiidae).
Cercarial morphotype group: cercariaeum.
Habitat: terrestrial.
Defi nitive hosts: birds.
Localities: Fergana Valley, northeastern part.
References: Tukhmanyants, Shakhurina (1971), Shakarboyev et al. (2012).
HASSTILESIIDAE HALL, 1916
Hasstilesia ovis (Orloff , Erschoff et Badanin, 1937)
Intermediate host: Pupilla muscorum, Vallonia costata (Gastropoda: Pupillidae,
Vallonidae).
Cercarial morphotype group: cercariaeum.
Habitat: terrestrial.
Defi nitive hosts: mammals.
Locality: Fergana Valley.
References: Gvozdev & Soboleva (1972), Shakarboyev et al. (2012).
BUCEPHALIDAE POCHE, 1907
Bucephalus polymorphus Baer, 1827
Intermediate host: Anodonta cygnea (Bivalvia: Unionidae).
Cercarial morphotype group: gasterostome.
Habitat: freshwater.
Defi nitive hosts: fi sh.
Locality: the Syrdarya river.
Reference: Butenko (1967).
Rhipidocotyle companula (Dujardin, 1845)
Intermediate host: Anodonta piscinalis (Bivalvia: Unionidae).
Cercarial morphotype group: gasterostome.
Habitat: freshwater.
Defi nitive hosts: fi sh.
Locality: Republic of Karakalpakstan (the Aral Sea).
Reference: Arystanov (1976).
CLINOSTOMIDAE LÜHE, 1901
Clinostomum complanatum (Rudolphi, 1814)
Intermediate host: Lymnaea stagnalis (Gastropoda: Lymnaeidae).
Cercarial morphotype group: cercariaeum.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
CYCLOCOELIIDAE STOSSICH, 1902
Cyclocoelum sp.
Intermediate host: Plаnorbis plаnorbis (Gastropoda: Planоrbidae).
509Th e Taxonomic Survey of the Cercarial Fauna in the Mollusks of Uzbekistan
Cercarial morphotype group: cercariaeum.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
DIPLOSTOMIDAE POIRIER, 1886
Diplostomum spathaceum (Rudolphi, 1819)
Intermediate host: Lymnaea auricularia, L. stagnalis, L. subdisjuncta (Gastropoda:
Lymnaeidae).
Cercarial morphotype group: strigeid.
Habitat: freshwater.
Defi nitive hosts: birds.
Localities: Republic of Karakalpakstan, northeastern and eastern regions.
References: Nasimov (1967), Tukhmanyants, Shakhurina (1971), Arystanov (1976),
Azimov, Kabilov (1977), Nurullayev (1991), Davronov (1999), Shakarboyev et al. (2012),
Shakarbaev et al. (2013, 2014 b).
Diplostomum helveticum (Dubois, 1929)
Intermediate host: Lymnaea auricularia, L. stagnalis (Gastropoda: Lymnaeidae).
Cercarial morphotype group: strigeid.
Habitat: freshwater.
Defi nitive hosts: birds.
Localities: northeastern and central regions.
References: Azimov, Kabilov (1977), Shakarboyev et al. (2012), Shakarbaev et al.
(2013, 2014 b).
Diplostomum indisticum (Guberlet, 1923)
Intermediate host: Lymnaea auricularia (Gastropoda: Lymnaeidae).
Cercarial morphotype group: strigeid.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
Codonocephalus urnigerus (Rudolphi, 1899)
Intermediate host: Lymnaea stagnalis (Gastropoda: Lymnaeidae).
Cercarial morphotype group: strigeid.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
Neodiplostomum sp.
Intermediate host: Plаnorbis plаnorbis (Gastropoda: Planоrbidae).
Cercarial morphotype group: strigeid.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
Tylodelphus clavata (von Nordmann, 1832)
Intermediate host: Lymnaea auricularia (Gastropoda: Lymnaeidae).
Cercarial morphotype group: strigeid.
510 U. A. Shakarbaev, F. D. Akramova, D. A. Azimov
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
STRIGEIDAE RAILLIET, 1919
Strigea falconis Szidat, 1928
Intermediate host: Plаnorbis plаnorbis (Gastropoda: Planоrbidae).
Cercarial morphotype group: strigeid.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: Tashkent Province.
Reference: Arystanov (1976).
Cotylurus cornutus (Rudolphi, 1808)
Intermediate host: Lymnaea auricularia, L. stagnalis, L. truncatula (Gastropoda:
Lymnaeidae).
Cercarial morphotype group: strigeid.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: northeastern part.
References: Nasimov (1967), Tukhmanyants, Shakhurina (1971), Arystanov (1976),
Azimov, Kabilov (1977), Shakarbaev et al. (2013, 2014 a, b).
Apatemon gracilis (Rudolphi, 1808)
Intermediate host: Lymnaea auricularia, L. stagnalis, L. palustris (Gastropoda:
Lymnaeidae).
Cercarial morphotype group: strigeid.
Habitat: freshwater.
Defi nitive hosts: birds.
Localities: northeastern and central parts.
References: Nasimov (1967), Azimov, Kabilov (1977), Shakarbaev et al. (2013, 2014 b).
SCHISTOSOMATIDAE STILES ET HASSAL, 1898
Schistosoma turkestanicum Skrjabin, 1913
Intermediate host: Lymnaea auricularia (Gastropoda: Lymnaeidae).
Cercarial morphotype group: brevifurcate.
Habitat: freshwater.
Defi nitive hosts: mammals.
Localities: northeastern and northwestern parts.
References: Azimov (1975, 1978, 1985, 1986), Azimov et al. (2014), Arystanov (1968 a,
b, 1969 b, 1976), Shakarboyev et al. (2012), Shakarbaev et al. (2013, 2014 b).
BILHARZIELLIDAE (PRICE, 1929: SUBFAM)
Bilharziella polonica (Kowalewsky, 1895)
Intermediate host: Plаnorbis plаnorbis, Anisus septemgyratus (Gastropoda: Planоrbidae).
Cercarial morphotype group: brevifurcate.
Habitat: freshwater.
Defi nitive hosts: birds.
Localities: Republic of Karakalpakstan, northeastern, central and southern regions.
References: Nasimov (1967), Arystanov (1976), Azimov, Kabilov (1977), Davronov
(1999), Akramova, Shakarboyev (2005), Akramova (2011), Shakarboyev et al. (2012),
511Th e Taxonomic Survey of the Cercarial Fauna in the Mollusks of Uzbekistan
Shakarbaev et al. (2014 a).
Trichobilharzia ocellata (La Valette, 1855)
Intermediate host: Lymnaea auricularia, Melanoides kainarensis (Gastropoda:
Lymnaeidae, Th iaridae).
Cercarial morphotype group: brevifurcate.
Habitat: freshwater.
Defi nitive hosts: birds.
Localities: northwestern, northeastern, central, eastern and southern regions.
References: Nasimov (1967), Tukhmanyants, Shakhurina (1971), Arystanov (1976),
Azimov, Kabilov (1977), Nurullayev (1991), Davronov (1999), Akramova (2005, 2008,
2011), Shakarboyev et al. (2012), Shakarbaev et al. (2013, 2014 b).
Trichobilharzia sp.
Intermediate host: Lymnaea corvus (Gastropoda: Lymnaeidae).
Cercarial morphotype group: brevifurcate.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: northeastern region.
Reference: Akramova (2011).
Ornithobilharzia canaliculata (Rudolphi, 1819)
Intermediate host: Lymnaea auricularia, L. stagnalis (Gastropoda: Lymnaeidae).
Cercarial morphotype group: brevifurcate.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: northeastern region.
References: Azimov, Kabilov (1977), Akramova, Azimov (2005), Akramova (2011).
Dendritobilharzia loossi Skrjabin, 1924
Intermediate host: Anisus spirorbis (Gastropoda: Planоrbidae).
Cercarial morphotype group: brevifurcate.
Habitat: freshwater.
Defi nitive hosts: birds.
Localities: northeastern and northwestern regions.
References: Azimov, Kabilov (1977), Azimov (1986), Akramova (2005, 2011),
Akramova et al. (2007, 2009 b, 2011), Shakarboyev et al. (2012), Shakarbaev et al. (2014 a).
Dendritobilharzia purverulenta (Braun, 1901)
Intermediate host: Plаnorbis plаnorbis (Gastropoda: Planоrbidae).
Cercarial morphotype group: brevifurcate.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: northeastern region.
References: Azimov, Kabilov (1977), Azimov (1986), Akramova et al., (2009 b),
Akramova (2011).
Gigantobilharzia acotylea Odhner, 1910
Intermediate host: Anisus spirorbis, Physa fontinalis (Gastropoda: Planоrbidae,
Physidae).
Cercarial morphotype group: brevifurcate.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: northeastern region.
References: Azimov, Kabilov (1977), Akramova (2008, 2011), Akramova et al. (2009 a,
512 U. A. Shakarbaev, F. D. Akramova, D. A. Azimov
2010), Shakarboyev et al. (2012), Shakarbaev et al. (2014 a).
Gigantobilharzia sp.
Intermediate host: Physa fontinalis, Anisus spirorbis, (Gastropoda: Physidae,
Planоrbidae).
Cercarial morphotype group: brevifurcate.
Habitat: freshwater.
Defi nitive hosts: birds.
Locality: northeastern part.
References: Azimov, Kabilov (1977), Akramova (2011).
APOROCOTYLIDAE ODHNER, 1912
Sanguinicola inermis Plehn, 1905
Intermediate host: Lymnaea auricularia, L. peregra (Gastropoda: Lymnaeidae).
Cercarial morphotype group: furcocercaria.
Habitat: freshwater.
Defi nitive hosts: fi sh.
Localities: Republic of Karakalpakstan, northeastern and southern regions.
References: Nasimov (1967), Tukhmanyants, Shakhurina (1971), Azimov, Kabilov
(1977), Davronov (1999), Shakarboyev et al. (2012), Shakarbaev et al. (2013, 2014 b).
TECHINOSTOMATIDAE LOOSS, 1899
Echinostoma revolutum (Frochlich, 1802)
Intermediate host: Lymnaea auricularia, L. corvus, L. stagnalis, Plаnorbis plаnorbis,
Anisus converiusculus, A. spirorbis (Gastropoda: Lymnaeidae, Planоrbidae).
Cercarial morphotype group: echinostome.
Habitat: freshwater.
Defi nitive hosts: birds.
Localities: Republic of Karakalpakstan, Fergana Valley, northeastern regions.
References: Nasimov (1967), Tukhmanyants, Shakhurina (1971), Arystanov (1976),
Azimov, Kabilov (1977), Davronov (1999), Shakarboyev (2009), Shakarbaev et al. (2013,
2014 a, b).
Echinoparyphium aconiatum Dietz, 1909
Intermediate host: Lymnaea auricularia, L. corvus, L. stagnalis, Plаnorbis plаnorbis
(Gastropoda: Lymnaeidae, Planоrbidae).
Cercarial morphotype group: echinostome.
Habitat: freshwater.
Defi nitive hosts: birds.
Localities: northeastern and northwestern regions.
References: Nasimov (1967), Arystanov (1976), Azimov, Kabilov (1977), Shakarboyev
(2009), Shakarbaev et al. (2014 a).
Echinoparyphium recurvatum (Linstow, 1873)
Intermediate host: Lymnaea auricularia (Gastropoda: Lymnaeidae).
Cercarial morphotype group: echinostome.
Habitat: freshwater.
Defi nitive hosts: birds.
Localities: Republic of Karakalpakstan, northeastern region.
References: Nasimov (1967), Arystanov (1976), Azimov, Kabilov (1977), Shakarbaev
et al. (2013, 2014 a, b).
Hypoderaeum conoideum (Bloch, 1782)
513Th e Taxonomic Survey of the Cercarial Fauna in the Mollusks of Uzbekistan
Intermediate host: Lymnaea auricularia, L. corvus, L. stagnalis, L. subdisjuncta
(Gastropoda: Lymnaeidae).
Cercarial morphotype group: echinostome.
Habitat: freshwater.
Defi nitive hosts: birds.
Localities: Republic of Karakalpakstan, Tashkent and Syrdarya Provinces.
References: Nasimov (1967), Arystanov (1976), Azimov, Kabilov (1977), Davronov
(1999), Shakarboyev et al. (2012), Shakarbaev et al. (2013, 2014 b).
FASCIOLIDAE RAILLIET, 1895
Fasсiola hepatica Linnaeus, 1758
Intermediate host: Lymnaea truncatula (Gastropoda: Lymnaeidae).
Cercarial morphotype group: gymnocephalous.
Habitat: freshwater.
Defi nitive host group: mammals.
Localities: Andizhan, Namangan, Fergana, Tashkent, Syrdarya, Jizakh, Kashkadarya
and Surkhandarya Provinces.
References: Salimov (1965, 1989), Nasimov (1967), Tukhmanyants, Shakhurina
(1971), Azimov, Kabilov (1977), Nurullayev (1991), Davronov (1999), Azimov et al. (2006),
Shakarboyev (2009), Shakarbaev et al. (2013).
Fasсiola gigantica (Cobbold, 1856)
Intermediate host: Lymnaea auricularia, L. bactriana, L. subdisjuncta, L. impure
(Gastropoda: Lymnaeidae).
Cercarian group: gymnocephalous.
Habitat: freshwater.
Defi nitive host group: mammals.
Localities: Republic of Karakalpakstan, Khorezm, Kashkadarya, Surkhandarya,
Syrdarya, Tashkent and Samarkand Provinces.
References: Nasimov (1967), Gekhtin (1967), Arystanov (1976), Azimov, Kabilov
(1977), Salimov (1989), Nurullayev (1991), Davronov (1999), Kojabayev (2001), Salimov et
al. (1986), Shakarboyev (2009), Shakarbaev et al. (2013, 2014 a, b).
PHILOPHTHALMIDAE LOOSS, 1899
Philophthalmus lucipetus (Rudolphi, 1819)
Intermediate host: Melanoides kainarensis (Gastropoda: Melanoididae (= Th iaridae)).
Cercarian group: megalurous.
Habitat: freshwater.
Defi nitive host group: birds.
Locality: Samarkand Province.
References: Shakarbayev et al. (2016).
PARAMPHISTOMIDAE FISCHOEDER, 1901
Calicophoron calicophorum (Fischoeder, 1901)
Intermediate host: Plаnorbis plаnorbis, Anisus spirorbis, Gyraulus ehrenbergi
(Gastropoda: Planоrbidae).
Cercarian group: amphistome.
Habitat: freshwater.
Defi nitive host group: mammals.
Localities: Republic of Karakalpakstan, Khorezm, Surkhandarya, Syrdarya, Tashkent
and Samarkand Provinces.
References: Nasimov (1967), Tukhmanyants, Shakhurina (1971), Khaydarov (1974),
Azimov, Kabilov (1977), Khamrayev (1983), Nikitin (1968), Kojabayev (2001), Shakarboyev
514 U. A. Shakarbaev, F. D. Akramova, D. A. Azimov
et al. (2012), Shakarbaev et al. (2014 a).
Calicophoron erschowi (Fischoeder, 1901)
Intermediate host: Plаnorbis plаnorbis, Gyraulus ehrenbergi, G. gredleri (Gastropoda:
Planоrbidae).
Cercarian group: amphistome.
Habitat: freshwater.
Defi nitive host group: mammals.
Localities: Surkhandarya, Kashkadarya, Samarkand and Tashkent Provinces.
References: Khamrayev (1983), Nikitin (1968), Davronov (1999), Shakarboyev et al.
(2012), Shakarbaev et al. (2014 a).
Liorchis scotiae (Willmott, 1950)
Intermediate host: Plаnorbis plаnorbis (Gastropoda: Planоrbidae).
Cercarian group: amphistome.
Habitat: freshwater.
Defi nitive host group: mammals.
Localities: central, northwestern and northeastern regions.
References: Nikitin (1968), Azimov et al. (1998), Shakarboyev et al. (2012).
GASTROTHYLACIDAE STILES ET GOLDBERGER, 1910
Gastrothylax crumenifer (Creplin, 1847)
Intermediate host: Plаnorbis sieversi, Gyraulus ehrenbergi, G. albus (Gastropoda:
Planоrbidae).
Cercarian group: amphistome.
Habitat: freshwater.
Defi nitive host group: mammals.
Localities: central, northwestern and northeastern parts of the country.
References: Nikitin (1968), Kojabayev (2001), Shakarboyev et al. (2012).
NOTOCOTYLIDAE LÜHE, 1901
Notocotylus attenuatus (Rudolphi, 1809)
Intermediate host: Lymnaea auricularia, L. bactriana, L. corvus (Gastropoda:
Lymnaeidae).
Cercarian group: monostome.
Habitat: freshwater.
Defi nitive host group: birds.
Localities: northwestern and northeastern parts of Uzbekistan.
References: Nasimov (1967), Arystanov (1969 a, b, 1970, 1976, 1980), Azimov, Kabilov
(1977), Shakarboyev et al. (2012), Shakarbaev et al. (2013, 2014 a, b).
Notocotylus ephemera (Nitzsch, 1817)
Intermediate host: Plаnorbis plаnorbis (Gastropoda: Planоrbidae).
Cercarian group: monostome.
Habitat: freshwater.
Defi nitive host group: birds.
Localities: Republic of Karakalpakstan, Fergana Valley, northeastern part.
References: Nasimov (1967), Arystanov (1969 a, 1976, 1980), Azimov, Kabilov (1977),
Shakarboyev et al. (2012).
Notocotylus sp. 1
Intermediate host: Bithynia caeurlans (Gastropoda: Bulinidae).
Cercarian group: monostome.
515Th e Taxonomic Survey of the Cercarial Fauna in the Mollusks of Uzbekistan
Habitat: freshwater.
Defi nitive host group: birds.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
Notocotylus sp. 2
Intermediate host: Th eodoxus pallasi (Gastropoda: Neretidae).
Cercarian group: monostome.
Habitat: freshwater.
Defi nitive host group: birds.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
GORGODERIDAE LOOSS, 1901
Gorgodera pagenstecheri (Ssinitzin, 1905)
Intermediate host: Sphaerium corneum, Pisidium abtusale (Bivalvia: Pisidiidae).
Cercarian group: amphistome.
Habitat: freshwater.
Defi nitive host group: amphibians.
Locality: Fergana Valley.
Reference: Tukhmanyants, Shakhurina (1971).
DICROCOELIIDAE LOOSS, 1889
Dicrocoelium dendriticum (Rudolphi, 1819)
Intermediate host: Leucozonella rufi spira, Xeropicta candaharica, Bradybaena
phaezona, Ponsadenia semenovi, Subzebrinus labieleus, Pseudonapaeus sogdianus
(Gastropoda: Hygromiidae, Bradybaenidae, Buliminidae).
Cercarian group: microcercous.
Habitat: terrestrial.
Defi nitive host group: mammals.
Localities: eastern, northeastern, central and southern regions of Uzbekistan.
References: Salimov (1965, 1974, 1989, 1991), Ernazarov (1972), Tukhmanyants,
Shakhurina (1971), Sultanov et al. (1975), Shakarboyev et al. (2012).
Corrigia corrigia (Braun, 1901)
Intermediate host: Candaharia rutellum, Bradybaena phaezona (Gastropoda:
Parmacellidae, Bradybaenidae).
Cercarian group: cercariaeum.
Habitat: terrestrial.
Defi nitive host group: birds.
Locality: southern regions.
Reference: Davronov (1999).
Eurytrema pancreaticum (Giard et Billet, 1892)
Intermediate host: Bradybaena phaezona (Gastropoda: Bradybaenidae).
Cercarian group: microcercous.
Habitat: terrestrial.
Defi nitive host group: mammals.
Locality: Fergana Valley.
References: Sultanov et al. (1975), Shakarboyev et al. (2012).
516 U. A. Shakarbaev, F. D. Akramova, D. A. Azimov
PLAGIORCHIIDAE LÜHE, 1901
Haplometra cylindracea (Zeder, 1800)
Intermediate host: Lymnaea stagnalis (Gastropoda: Lymnaeidae).
Cercarian group: xiphidiocercaria.
Habitat: freshwater.
Defi nitive host group: amphibians.
Localities: central and northeastern regions.
References: Nasimov (1967), Shakarbaev et al. (2013, 2014 b).
HAEMATOLOECHIDAE FREITAS & LENT, 1939
Haematoloechus variegatus (Rudolphi, 1819)
Intermediate host: Plаnorbis plаnorbis (Gastropoda: Planоrbidae).
Cercarian group: xiphidiocercaria.
Habitat: freshwater.
Defi nitive host group: amphibians.
Localities: Republic of Karakalpakstan, Fergana Valley.
References: Tukhmanyants, Shakhurina (1971), Arystanov (1976).
Skrjabinoeces similis (Looss, 1899)
Intermediate host: Plаnorbis plаnorbis (Gastropoda: Planоrbidae).
Cercarian group: xiphidiocercaria.
Habitat: freshwater.
Defi nitive host group: amphibians.
Localities: Fergana Valley, central and northeastern parts of Uzbekistan.
References: Nasimov (1967), Tukhmanyants, Shakhurina (1971), Shakarbaev et al.
(2013, 2014 a).
TELORCHIIDAE LOOSS, 1899
Opisthioglyphe ranae (Froelich, 1791)
Intermediate host: Lymnaea auricularia, L. bactriana, L. stagnalis (Gastropoda:
Lymnaeidae).
Cercarian group: xiphidiocercaria.
Habitat: freshwater.
Defi nitive host group: amphibians.
Localities: Republic of Karakalpakstan, central and northeastern regions.
References: Nasimov (1967), Arystanov (1976), Shakarboyev et al. (2012), Shakarbaev
et al. (2013, 2014 b).
PLEUROGENIDAE LOOSS, 1899
Pleurogenes claviger (Rudolphi, 1819)
Intermediate host: Plаnorbis plаnorbis (Gastropoda: Planоrbidae).
Cercarian group: xiphidiocercaria.
Habitat: freshwater.
Defi nitive host group: amphibians.
Locality: Fergana Valley.
Reference: Tukhmanyants, Shakhurina (1971).
CERCARIAN GROUPS OF UNIDENTIFIED SPECIES
(species inquirendae)
Amphistome
Intermediate host: Lymnaea auricularia.
517Th e Taxonomic Survey of the Cercarial Fauna in the Mollusks of Uzbekistan
Habitat: freshwater.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
Xiphidiocercaria
Intermediate host: Lymnaea auricularia, L. stagnalis.
Habitat: freshwater.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
Xiphidiocercaria
Intermediate host: Lymnaea auricularia.
Habitat: freshwater.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
Xiphidiocercaria
Intermediate host: Lymnaea stagnalis.
Locality: Republic of Karakalpakstan.
Reference: Butenko (1967).
Brevifurcate
Intermediate host: Lymnaea auricularia.
Locality: Republic of Karakalpakstan.
Reference: Arystanov (1976).
Brevifurcate
Intermediate host: Plаnorbis plаnorbis.
Locality: the Syrdarya River.
Reference: Butenko (1967).
Discussion
Trematodes are common in the biocoenoses of Uzbekistan, where they are represented
by about 200 species. Th ey are entirely parasitic organisms. Trematodes’ defi nitive hosts
are various vertebrates, such as fi sh, amphibians, birds and mammals (Shakarboyev et al.,
2012). Th ey concentrate in various organs in the defi nitive host’s body. Some species and
groups cause serious helminthiases in domestic and game animals and the human.
Th e class Trematoda is divided into two subclasses — Aspidogastrea Faust and Tang,
1936 and Digenea Carus, 1863 (Gibson et al., 2002). All the trematode cercarial larvae
covered by this work belong to the subclass Digenea.
Th e enormous research made into of the cercarial fauna developing in the mollusks
of Uzbekistan’s aquatic and terrestrial biocenoses has a long history. For the fi rst time
mollusks as trematodes’ intermediate hosts were studied in the biocenoses of this region in
the 30s of the 20th century (Dogel & Bykhovsky, 1934).
In the years that followed the research was continued and spread to the aquatic and
terrestrial biocenoses of the adjoining territories. Th e results were presented in numerous
articles published in Russian, which, therefore, proved inaccessible to foreign parasitologists.
Currently, aft er 80 years of research (1934–2019), there are about 100 scientifi c
articles dedicated to the fauna of trematodes living in the aquatic and terrestrial mollusks
of Uzbekistan. Th ese publications demonstrate that the trematode cercariae of mollusks
have been studied quite properly in the water bodies of the lower course of the Amu River
(Arystanov, 1967, 1968 a, b, 1969 а, b, 1970, 1971, 1976), where 41 cercaria species have
been recorded. Th e infection rate among mollusks ranged between 0.02 % and 37.2 %,
depending on the season and type of a water body.
518 U. A. Shakarbaev, F. D. Akramova, D. A. Azimov
Th ere have been 21 cercaria species discovered in mollusks of the classes Gastropoda
and Bivalvia inhabiting the water bodies of the Syrdarya and Zarafshan Rivers. Th e average
infection rate among the studied mollusks was 3.43 % (Nasimov, 1967).
Th e freshwater and terrestrial mollusks of the Fergana Valley (Andizhan, Namangan
and Fergana Provinces) were recorded to be the hosts of 28 cercaria species. Th e infection
rate among the freshwater mollusks was 4.3 %, among the terrestrial ones — 1.0 %
(Tukhmanyants, Shakhurina, 1971). Th ere were 12 cercaria species recorded in the south
of Uzbekistan (Davronov, 1999).
Th ere were also a number of scientists who carried out comprehensive research into
the life cycles of trematode groups most pathogenic for animals and the human being.
Th e experts determined the rate of infection with fl uke cercariae among freshwater and
terrestrial mollusks (Salimov, 1965, 1974, 1989, 1991; Salimov et al., 1986; Ernazarov, 1972;
Azimov et al., 2014; Akramova, 2011; Shakarboyev et al., 2012; Shakarbaev et al., 2013,
2014 a, b).
We specifi ed the life cycles of a number of trematode species in Uzbekistan:
Brachylaima fuscata, Diplostomum spathaceum, Schistosoma turkestanicum, Bilharziella
polonica, Trichobilharzia ocellata, Dendritobilharzia loossi, Gigantobilharzia acotylea,
Sanguinicola inermis, Fasсiola hepatica, Fasсiola gigantica, Calicophoron calicophorum,
Calicophoron erschowi, Gastrothylax crumenifer, Notocotylus attenuates, Dicrocoelium
dendriticum, Eurytrema pancreaticum. We were the fi rst to provide the descriptions of
life cycles and biology of three species — Calicophoron erschowi, Dendritobilharzia loossi,
Gigantobilharzia acotylea (Khamrayev, 1983; Akramova et al., 2007, 2010, 2011, 2017).
Th us, the research into the fauna of cercariae and the larval stage of trematodes that
has been so far carried out in the territory of Uzbekistan is absolutely insuffi cient. Th e total
number of cercaria species established in the course of the research both in freshwater and
terrestrial mollusks is 50. Th e cercarial fauna of freshwater mollusks comprises 44 species,
while only 6 species of cercarial from the families Dicrocoeliidae and Brachylaimidae
have been recorded in terrestrial mollusks. It should be noted that by the present time
187 species of adult forms of trematodes have been recorded to parasitise the vertebrates of
Uzbekistan (Sultanov et al., 1975; Shakarboyev et al., 2012; Azimov et al., 2014). Th e species
diversity of cercariae discovered in the studied mollusks was much poorer, amounting to
26.7 % of the total number of adult forms of trematodes. Moreover, the same situation can
be observed in the natural rate of infection with cercariae of diff erent groups of trematodes
among mollusks. According to the malacologists of Uzbekistan, the country’s mollusc
fauna comprises 386 species (Zhadin, 1952; Starobogatov, 1970; Izzatullayev, 1987; Pazilov,
2005; Pazilov, Azimov, 2003), of which 214 are freshwater and 172 — terrestrial. Only
38 species of the total number have been recorded to be infected with cercariae, which
is 9.8 %. According to this data, only a small portion of the mollusc species were infected
with cercarial larvae, which makes us think about the necessity of deeper research into the
relations between mollusks and trematodes on a vast area of Uzbekistan with the use of the
molecular genetic methods in order to specify the cercariae’s species diversity. Nevertheless,
analysing the existing materials we can distinguish two types of cercaria communities: the
ones inhabiting acquatic biocenoses and those living in terrestrial ones. Th ere are at least
four strategies cercariae use to infect defi nitive hosts. Th e fi rst strategy is utilised by cercaria
species of the families Fasciolidae, Paramphistomidae, Gastrothylacidae and Notocotylidae,
which encyst on underwater substrates. Adolescariae enter the organism of a defi nitive host
with food. Th e second strategy is characteristic of most of cercariae, which use vertebrate
and invertebrate animals as the second intermediate hosts to turn into metacercariae
(the Echinostomatidae, Cyclocoeliidae, Clinostomidae, Plagiorchiidae, Telorchiidae,
Dicrocoeliidae, Strigeidae, Diplostomidae, Brachylaimidae and Bucephalidae). Defi nitive
hosts become infected through eating the second intermediate host with metacercariae
inside. Th e third group of cercarial are quite active penetrating into their defi nitive host
519Th e Taxonomic Survey of the Cercarial Fauna in the Mollusks of Uzbekistan
through its skin (the Schistosomatidae, Bilharziellidae and Aporocotylidae). Th e fourth
strategy is rather passive, when fl oating cercariae get into their defi nitive host with water
through the mouth or infraorbitally, or when the host eats substrate with an adolescaria
(metacercaria) in it (the Philophthalmidae).
As for the last strategy, it should be noted that earlier a number of experts discovered
the possibility for a defi nitive host to be infected with cercariae or adolescariae of the
Philophthalmidae (Galaktionov, Dobrovolsky, 1998; Pinto and Melo, 2013). Th is strategy
should be defi ned as a mixed-type strategy, as it combines two strategies described above
(Prokofyev, 2006; Prokofyev and Galaktionov, 2009).
Th e above described strategies used by certain groups of cercariae are accomplished
through a number of responses, mainly photo-, geo- and chemotropism developed in the
course of the evolution of parasite-host relations contributing to the concentration of larvae
in the area with the best opportunities to meet hosts.
Conclusion
Th e territory of Uzbekistan is a habitat for 50 trematode species cercarial larvae species
from 22 families. Th ey infect certain species of freshwater and terrestrial mollusks. Th e core
of the fauna of cercariae is formed of cercarial larvae developing in freshwater mollusks
(44 species).
Th e defi nitive hosts of the mentioned cercariae are vertebrates — fi sh, amphibians,
birds and mammals.
It should be noted that the groups of cercariae described above are common for the
biogeocenoses of Uzbekistan, and the trematode-mollusk relations are quite stable. Th e risk
of infection with certain trematodes is very high for animals. In this connection mollusks
infected with trematode cercariae should be constantly monitored, which may allow us to
understand parasite-host relations better and to study the life cycles, ecology and taxonomy
of these parasites, on the one hand, and to develop the methods of preventing trematodoses
in animals and the human being, on the other hand.
Author’s great thankful to Dr. Hudson Alves Pinto, Deparment of Parasitology, Institute of Biological
Science, Federal University of Minas Gerais for valuable comments and editing the English version of the
manuscript.
Th e authors thank E. B. Shakarboyev and V. I. Golovanov for their help in collecting articles on the
cercarial larvae of Uzbekistan’s fauna. Th e work was supported by grants given by the Academy of Sciences of
the Republic of Uzbekistan for fundamental studies.
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Received 15 October 2020
Accepted 15 December 2020
|
| id | oai:ojs.akademperiodyka.org.ua:article-68 |
| institution | Zoodiversity |
| issn | 2707-7268 |
| keywords_txt_mv | |
| language | English |
| last_indexed | 2026-08-21T01:01:45Z |
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| spelling | oai:ojs.akademperiodyka.org.ua:article-682026-08-20T12:37:32Z The taxonomic survey of the fauna of cercariae (Platyhelminthes, Trematoda) in the mollusks of Uzbekistan Shakarbaev, Ulugbek Akramova, Firuza Azimov, Djalaliddin fauna cercariae trematodes molluscs parasites Uzbekistan The article provides a list of trematodes cercariae found in the molluscs of Uzbekistan based on the analysis and generalisation of well-known data published in the period between 1934 and 2019. Currently, the list comprises 50 cercaria species belonging to 38 genera, 19 families and 11 orders of trematodes, the adult forms of which parasitise vertebrates (fish, amphibians, birds and mammals), including the human being. The cercariae were discovered in 38 mollusc species belonging to Gastropoda and Bivalvia. The discovered larvae comprised 12 groups of cercariae. Publishing House "Akademperiodyka" of the National Academy of Sciences of Ukraine 2020-12-07 Article Article application/pdf https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/68 10.15407/zoo2020.06.505 Zoodiversity; Vol. 54 No. 6 (2020): Zoodiversity Zoodiversity (Vestnik Zoologii); Том 54 № 6 (2020): Zoodiversity 2707-7268 2707-725X 10.15407/zoo2020.06 en https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/68/57 Copyright (c) 2020 Zoodiversity https://creativecommons.org/licenses/by-nc-nd/4.0 |
| spellingShingle | Shakarbaev, Ulugbek Akramova, Firuza Azimov, Djalaliddin The taxonomic survey of the fauna of cercariae (Platyhelminthes, Trematoda) in the mollusks of Uzbekistan |
| title | The taxonomic survey of the fauna of cercariae (Platyhelminthes, Trematoda) in the mollusks of Uzbekistan |
| title_full | The taxonomic survey of the fauna of cercariae (Platyhelminthes, Trematoda) in the mollusks of Uzbekistan |
| title_fullStr | The taxonomic survey of the fauna of cercariae (Platyhelminthes, Trematoda) in the mollusks of Uzbekistan |
| title_full_unstemmed | The taxonomic survey of the fauna of cercariae (Platyhelminthes, Trematoda) in the mollusks of Uzbekistan |
| title_short | The taxonomic survey of the fauna of cercariae (Platyhelminthes, Trematoda) in the mollusks of Uzbekistan |
| title_sort | taxonomic survey of the fauna of cercariae (platyhelminthes, trematoda) in the mollusks of uzbekistan |
| topic_facet | fauna cercariae trematodes molluscs parasites Uzbekistan |
| url | https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/68 |
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