Helminth Fauna in Carnivoran Mammals from Uzbekistan
Helminths, or parasitic worms, are a group of organisms that can infect various animal species, including humans. In Uzbekistan, previous studies on the helminth fauna of mammals have mainly focused on domestic animals and some wildlife species, with little attention given to carnivoran mammals. Thi...
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| author | Safarov, A. Khan, A. Azimov, D. Akramova, F. Saparov, K. Ben Said, M. |
| author_facet | Safarov, A. Khan, A. Azimov, D. Akramova, F. Saparov, K. Ben Said, M. |
| author_institution_txt_mv | [
{
"author": "A. Safarov",
"institution": "State Committee for Veterinary and Livestock Development of the Republic of Uzbekistan",
"orcid": "0000-0002-0987-6063"
},
{
"author": "A. Khan",
"institution": "Bacha Khan University Charsadda, Pakistan ",
"orcid": ""
},
{
"author": "D. Azimov",
"institution": "Institute of Zoology of the Academy of Sciences of the Republic of Uzbekistan",
"orcid": ""
},
{
"author": "F. Akramova",
"institution": "Institute of Zoology of the Academy of Sciences of the Republic of Uzbekistan",
"orcid": ""
},
{
"author": "K. Saparov",
"institution": "Tashkent State Pedagogical University named after Nizami, Uzbekistan ",
"orcid": ""
},
{
"author": "M. Ben Said",
"institution": "Laboratory of Microbiology, National School of Veterinary Medicine of Sidi Thabet, University of Manouba",
"orcid": ""
}
] |
| author_orcid_str_mv | 0000-0002-0987-6063 |
| author_sort | Safarov, A. |
| baseUrl_str | https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/oai |
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| container_issue | 4 |
| container_start_page | |
| container_title | Zoodiversity (Vestnik Zoologii) |
| container_volume | 57 |
| datestamp_date | 2026-08-20T12:37:14Z |
| description | Helminths, or parasitic worms, are a group of organisms that can infect various animal species, including humans. In Uzbekistan, previous studies on the helminth fauna of mammals have mainly focused on domestic animals and some wildlife species, with little attention given to carnivoran mammals. This survey aims to conduct a comprehensive study for the first time in Uzbekistan on the helminth fauna of Carnivora. In this study, helminths were collected from 1002 carnivorans (Canidae, n = 710; Mustelidae, n = 167; and Felidae, n = 125) from five locations in Uzbekistan (Northeastern, Eastern, Central, Southern and Northwestern). A total of 71 species of helminths were identified in domestic and wild carnivores by necropsy and faecal examination, of which 36, 23, 9, and 3 species belonged to the higher taxon Nematoda, Cestoda, Trematoda and Acanthocephala respectively. The highest number of helminth species was recorded in studied Canidae (51 species), followed by Felidae (40 species) and Mustelidae (35 species). The overall infection rate of carnivorans was 79.8 %. Infection intensity ranged from a single to dozens of specimens. The statistical analysis indicated that the diversity of helminth species is significant among members of Canidae, with foxes having 42 species and dogs having 41 species (P < 0.05). Our study proves that the parasitic worm species that inhabit predatory mammals in Uzbekistan are a diverse and complex group that can cause helminthiases, which may be dangerous to livestock and humans. |
| doi_str_mv | 10.15407/zoo2023.04.359 |
| first_indexed | 2025-07-17T12:36:30Z |
| format | Article |
| fulltext |
© Publisher Publishing House "Akademperiodyka" of the NAS of Ukraine, 2023. Th e article is published under
an open access license CC BY-NC-ND (https://creativecommons.org/licenses/by-nc-nd/4.0/)
UDC 619.576.895.122
HELMINTH FAUNA IN CARNIVORAN MAMMALS FROM
UZBEKISTAN
A. Safarov1,*, A. Khan2, D. Azimov3, F. Akramova3, K. Saparov4 & M. Ben Said5,6
1 State Committee of Veterinary and Livestock Development of the Republic of Uzbekistan,
Kichik khalka youli St., 21A,100123, Tashkent, Uzbekistan
2Bacha Khan University Charsadda, Khyber Pakhtunkhwa, Pakistan
3Institute of Zoology of the Academy of Sciences of the Republic of Uzbekistan,
Bogishamol St., 232b, 100053, Tashkent Uzbekistan
4Tashkent State Pedagogical University named aft er Nizami, Bunyodkor St., 27, Tashkent, Uzbekistan
5Laboratory of Microbiology, National School of Veterinary Medicine of Sidi Th abet,
University of Manouba, Manouba 2010, Tunisia
6Department of Basic Sciences, Higher Institute of Biotechnology of Sidi Th abet,
University of Manouba, Manouba 2010, Tunisia
*Corresponding author
E-mail: safarov-alisher@mail.ru (A.S.)
A. Safarov (https://orcid.org/0000-0002-7073-9367)
A. Khan (https://orcid.org/0000-0002-5330-5380)
D. Azimov (https://orcid.org/0009-0008-8161-0084)
F. Akramova (https://orcid.org/0000-0002-4603-3698)
K. Saparov (https://orcid.org/0000-0003-1311-5598)
M. Ben Said (https://orcid.org/0000-0001-5567-4721)
urn:lsid:zoobank.org:pub:AF73EA7E-879F-4819-A2CD-5128423C13FE
Helminth Fauna in Carnivoran Mammals from Uzbekistan. Safarov, A., Khan, A., Azimov, D.,
Akramova, F., Saparov, K., Ben Said, M. — Helminths, or parasitic worms, are a group of organisms
that can infect various animal species, including humans. In Uzbekistan, previous studies on the helminth
fauna of mammals have focused mainly on domestic animals and some wildlife species, with little at-
tention paid to carnivorous mammals. Th is study aims to provide the fi rst comprehensive survey of the
Zoodiversity, 57(4): 359–378, 2023
DOI 10.15407/zoo2023.04.359
360 A. Safarov, A. Khan, D. Azimov, F. Akramova, K. Saparov & M. Ben Said
carnivore helminth fauna in Uzbekistan. In this study, helminths were collected from 1002 carnivorans
(Canidae, n = 710; Mustelidae, n = 167; and Felidae, n = 125) from fi ve locations in Uzbekistan (North-
eastern, Eastern, Central, Southern and Northwestern). A total of 71 helminth species were identifi ed in
domestic and wild carnivores by necropsy and faecal examination, of which 36, 23, 9, and 3 species be-
longed to the higher taxon Nematoda, Cestoda, Trematoda and Acanthocephala respectively. Th e highest
number of helminth species was found in studied Canidae (51 species), followed by Felidae (40 species)
and Mustelidae (35 species). Th e overall infection rate of carnivores was 79.8 %. Infection intensity ranged
from a single specimen to dozens of specimens. Statistical analysis showed that the diversity of helminth
species is signifi cant among members of the Canidae, with foxes having 42 species and dogs having 41
species (P < 0.05). Our study shows that the parasitic worm species that inhabiting carnivorous mammals
in Uzbekistan are a diverse and complex group capable of causing helminthiases, that can be dangerous
to livestock and humans.
Key words : helminths, Carnivora, Canidae, Felidae, Mustelidae, Uzbekistan.
Introduction
Carnivora is one of the most interesting orders of mammals, whose ecological adaptation has reached
the widest range from aquatic to arboreal forms. In this context, carnivores represent a convenient object for
helminthologists, since many issues of the formation of faunal complexes of parasites inherent in certain taxo-
nomic and ecological groups of hosts can be considered on their example (Gibson et al., 2014).
All components of parasitic systems, regardless of their level of organization, are associated to varying
degrees with physical, geographical and biological components that determine the specifi c landscape and hy-
drological conditions of biogeocenoses (Chaĭka SIu, 1998). Th e infl uence of these factors on the qualitative
and quantitative characteristics of the parasitofauna is enhanced by their complex eff ect, which infl uences the
epidemiological processes of parasitic diseases occurring in specifi c areas (Kołodziej-Sobocińska, 2019). In this
context, the link between the helminthofauna of carnivores and other vertebrates, including humans, deserves
special attention (Wells et al., 2018; White and Razgour, 2020).
Mammals of Uzbekistan are represented by 8 orders: Insectivora (Insectivores), Chiroptera (Bats), Lago-
morpha (Hare-like), Rodentia (Rodents), Carnivora (Carnivores), Artiodactyla (Artiodactyls), Perissodactyla
(Ungulates), Tylopoda (Calluses) (Shernazarov et al., 2006; Kashkarov et al., 2020). Th e relationship of the
helminth fauna of carnivorans was established with representatives of the orders Insectivora, Lagomorpha,
Rodentia, Artiodactyla, Perissoactyla, and Tylopoda.
Several researchers including Petrov (1926), Schleicher (1949), and Zhdanova (1949) studied the hel-
minth fauna of dogs in Uzbekistan. Th eir studies revealed 22 species of parasitic worms belonging to the higher
taxa Cestoda, Acanthocephala, and Nematoda were present in the area. Th e authors found that the Taeniidae
and Dipilididae families of cestodes, and the Ancylostomatidae, Ascarididae, and Anisakidae families of nema-
todes, were widely distributed among the dogs they studied.
Th e dominant taxonomic groups in both dog populations were found to be cestodes of the genera Di-
pilidium, Taenia, Echinococcus, Multiceps, and nematodes of the genera Toxoscaris, Toxocara, Ancylostoma.
Materials on the helminthofauna of dogs of Uzbekistan are summarized by Sultanov et al. (1975) in the
monograph “Helminths of domestic mammals of Uzbekistan”, which reports the presence of 32 species of para-
sitic worms in dogs, of which 17 species can parasitize the human body at various stages of development, which
is confi rmed by known literature data (Matchanov et al., 1977; Bronstein and Tokmolaev, 2004; Macpherson et
al., 2013; Azimov et al., 2015; Safarov, 2020; Safarov et al., 2022, 2023).
To date, previous studies have become substantially outdated, which is confi rmed by recent studies on the
helminth fauna of dogs in Uzbekistan (Safarov, 2020; Safarov et al., 2021). Th e data (Delyanova, 1958; Matcha-
nov, 1967) do not support the detection of several species of helminths in dogs (Spirometra erinaceieuropaei,
Diplopylidium nölleri, Mesorchis denticulatus, Brachylaemus sp., Crenosoma vulpis, and Toxocara mystax). Th e
mentioned helminth species in most cases parasitize wild representatives of predatory mammals of Uzbekistan,
which does not contradict previously published works (Irgashev and Sadykov, 1966; Kairov, 1965; 1968; Kos-
chanov, 1972; Safarov et al., 2022).
Among carnivores, a number of species are of great practical importance. Th e fur of river otter, mink and
others is highly valued in domestic and foreign markets. Th ey are, admittedly, hosts of dangerous pathogens of
helminthiasis of animals and humans. However, the list of works on the parasite fauna of Carnivorous mam-
mals of Uzbekistan is relatively small (Muminov, 1963; Kairov, 1965; Koshanov, 1972; Safarov et al., 2021,
2022). At the beginning of the 21st century, only one fundamental monograph by Safarov et al. (2021) was
published, in which the parasites of dogs of the Tashkent megalopolis are considered.
361 Helminth Fauna in Carnivoran Mammals from Uzbekistan
Information on the helminth fauna of individual representatives of carnivorous animals of Karakalpakstan
was signifi cantly updated and supplemented in the dissertation study “Helminths of Carnivorous mammals of
Karakalpakstan” of Berdibaev (2021). However, comprehensive studies of the fauna, distribution features and
helminth ecology of carnivorous mammals in the biogeocenoses of Uzbekistan have not been considered. Giv-
en the importance of this animal group, it is also quite relevant to study in detail their parasite fauna and their
distribution in connection with the peculiarities of the modern ecological context of Uzbekistan.
Th is report showcases the fi ndings of a research study on the fauna and distribution characteristics of hel-
minths among carnivorous mammals in Uzbekistan. Additionally, the report touches upon certain ecological
aspects of helminths. Th e study employed contemporary concepts regarding the classifi cation and naming of
helminths as outlined on the Fauna Europaea website (2020) https://fauna-eu.org.
Material and Methods
Study regions and col lected samples
Over the course of four years, from March 2018 to November 2022, samples were collected from 1002
carnivorous mammals in various regions of Uzbekistan, including North-Eastern, Eastern, Central, Southern,
and North-Western areas (table 1 and fi g. 1). Th e samples were taken from members of three mammal families:
Canidae (710 samples), Mustelidae (167 samples), and Felidae (125 samples), encompassing a range of ages and
both sexes.
Th e samples were obtained from a variety of sources, including animals caught by hunters, those killed in
car accidents (primarily dogs and jackals), and those that died naturally (mostly wild carnivorous mammals).
Additionally, we examined fecal samples from dogs and cats housed at the “Mehr” animal protection organiza-
tion, located in the Piskent district of the Tashkent region in Uzbekistan.
All animals were tested for rabies at the Virology Laboratory of the Republican State Center for Diagnosis
of Animal Diseases and Food Safety before the helminthological examination. Th e carcasses were stored at a
temperature of –20 °C prior to the necropsy. Th e necropsy was conducted using a whole-body post-mortem
examination method, with all organs and tissues examined for the presence of helminths. Muscle samples were
also collected and examined for the presence of Trichinella spp. Th e study was reviewed and approved by the
Center’s ethics committee.
Field work was carried out during the commercial period during the hunting seasons for wild animals —
in autumn and winter. Rare animals — river otter, lynx, steppe cat, were studied in limited numbers, legally
killed or killed by illegal hunting on the territory of southern Uzbekistan. Th e remaining species were obtained
in the territory of North-Eastern, Eastern, Central and North-Western Uzbekistan. At the same time, the ser-
vices of local hunters were used.
Domestic dogs and cats were studied in all seasons of the year in rural areas and settlements using well-
known methods of Parasitology (Zewdu et al., 2010).
Helminths ident i f icat ion
T a b l e 1 . Species composition and number of examined hosts
Family Species Examined
Canidae Golden jackal, Canis aureus 120
Grey wolf, Canis lupus 62
Domestic dog, Canis familiaris 399
Korsak, Vulpes corsac 61
Red fox, Vulpes vulpes 68
Mustelidae Stone Marten, Martes foina 43
American Mink, Mustela vison 26
Least weasel, Mustela nivalis 35
Eurasian Badger, Meles meles 57
River otter, Lutra lutra 6
Felidae Jungle cat, Felis chaus 43
Steppe cat, Felis lybica 11
Domestic cat, Felis catus 66
Lynx, Lynx lynx 5
Total 1002
362 A. Safarov, A. Khan, D. Azimov, F. Akramova, K. Saparov & M. Ben Said
Th e study of collected helminths was conducted according to a generally accepted method — cestodes
and trematodes were stained with carmine or hematoxylin, permanent preparations were prepared from them,
acanthocephalans and nematodes were clarifi ed in a mixture of glycerin and lactic acid (Khalil et al., 1994;
Gibson et al., 2002). Measurement of cestodes, trematodes, acanthocephalans, and nematodes, photographs
and drawings were made using light microscopes Olympus CK2-TR inverted microscope, Lomo research bin-
ocular — ML — 2200, N — 300 m Ningo Yongkin Optics trinocular microscope. Identifi cation of cestodes,
trematodes, acanthocephalans, and nematodes was carried out according to identifi cation keys (Anderson,
Fig. 1. Map showing investigated regions in Uzbekistan. 1— Northeast (Tashkent, Syrdaryn, Jizzakh regions);
2 — East (Fergana, Andijan, Namangan regions); 3 — Central (Samarkand, Bukhara, Navoi regions), 4 —
Southern (Surkhandarya, Kashkadarya regions); 5 — North-Western (Khorezm region).
T a b l e 2 . Helminth infections of investigated predatory mammals in Uzbekistan
Family Species Total Positive Infection rate (% ± C.I.1) P value (Chi2)
Canidae Canis aureus 120 101 84.1 ± 0.064 0.000* (30.91)
Canis lupus 62 50 80.6 ± 0.098 –
Canis familiaris 399 380 95.3 ± 0.021 –
Vulpes corsac 61 49 80.3 ± 0.099 –
Vulpes vulpes 68 63 92.6 ± 0.062 –
Mustelidae Martes foina 43 21 49.0 ± 0.148 0.704 (1.98)
Mustela vison 26 11 42.3 ± 0.19 –
Mustela nivalis 35 16 46.2 ± 0.164 –
Meles meles 57 23 40.2 ± 0.127 –
Lutra lutra 6 4 66.6 ± 0.376 –
Felidae Felis chaus 43 31 74.4 ± 0.133 0.570 (2.01)
Felis lybica 11 7 63.6 ± 0.284 –
Felis catus 66 40 60.5 ± 0.117 –
Lynx lynx 5 4 NC –
Total 1002 800 79.8 ± 0.025 –
Abbrev ia t ions . C.I.1 — 95 % confi dence interval; * — statistically signifi cant, p < 0.05; NC — not
calculated infection rate because the number of examined animals is ≤ 5.
Note . P value and Chi2 between all species are < 0.001 and 106.98, respectively.
363 Helminth Fauna in Carnivoran Mammals from Uzbekistan
T a b l e 3 . Helminths of studied carnivoran mammals of various families
Helminth
higher
taxon
Helminth species
Host family
Canidae Mustelidae Felidae
Cestoda Diphyllobothrium latum + + +
Spirometra erinaceieuropaei + + +
Dipylidium caninum + + +
Diplopylidium nőlleri + – +
Joyeuxiella echinorhynchoides + – –
Joyeuxiella pasqualei – – +
Joyeuxiella rossicum + – +
Taenia hydatigena + + +
Taenia macrocystis + – +
Taenia ovis + – –
Taenia pisiformis + + +
Taenia crassiceps + + +
Taenia laticollis – – +
Taenia martis – + –
Taenia mustelae – + –
Hydatigera krepkogorski + – +
Hydatigera taeniaeformis + + –
Multiceps multiceps + – –
Multiceps skrjabini + – –
Multiceps serialis + – –
Echinococcus multilocularis + – +
Echinococcus granulosus + – +
Mesocestoides lineatus + + +
2000, 2009; Safarov et al., 2021, 2022). Other keys were also used for certain groups of higher taxa (Gibson et
al., 2008).
Stat is t ica l analys is
Th e statistical analysis was performed using Epi Info 7 soft ware (CDC, USA). Th e prevalence and its 95 %
Confi dence Interval (CI) were calculated, and diff erences among groups were assessed by chi-square testing
and considered signifi cant for p ≤ 0.05.
Results
Divers i ty and overal l prevalence of the helminths in carnivorous mam-
mals
The helminth infection of studied animals was found to be quite high which was es-
timated at 79.8 % (table 2). Canis familiaris was statistically the most infected host species
(95.3 %), while Mustela vison was the least infected (40.2 %) (P < 0.001, table 2). In to-
tal, 70 species of helminths belonging to the higher taxon Cestodes, trematodes, acantho-
cephals and Nematodes were identified. In the vast majority of cases, mixed infections by
several types of parasites were recorded in infected animals, with 3 to 9 types of helminths
being found (table 3).
In terms of the helminth species number, the first position is occupied by representa-
tives of canids (Canidae) — 51 species; slightly smaller in felids (Felidae) — 40 species; the
last place in this indicator is occupied by mustelids (Mustelidae) — 35 species (table 3).
Parasites species found in carnivorous mammals of various families are unevenly dis-
tributed as shown in table 4.
364 A. Safarov, A. Khan, D. Azimov, F. Akramova, K. Saparov & M. Ben Said
Trematoda Fasciola hepatica – + –
Plagiorchis elegans + + +
Plagiorchis lutrae – + –
Dicrocoelium dendriticum + – –
Echinochasmus perfoliatus + – –
Euparyphium melis – + –
Mesorchis denticulatus – – +
Alaria alata + + –
Acantho-
cephala
Corynosoma strumosum – + –
Macrocanthorynchus catulinus + + +
Moniliformis moniliformis + + +
Nematoda Capillaria plica + + +
Capillaria putorii + + +
Capillaria mucronata – + +
Th ominx aerophilus + + +
Trichocephalus vulpis + – –
Dioctophyme renale + + +
Strongyloides vulpis + – –
Strongyloides stercoralis + – –
Strongyloides martis – + –
Ancylostoma caninum + + +
Ancylostoma tubaeforme – – +
Uncinaria stenocephala + + +
Crenosoma vulpis + + –
Crenosoma petrowi – – –
Troglostrongylus badanini – – +
Toxascaris leonina + – +
Toxocara canis + – +
Toxocara mystax + – +
Oxynema numidica + – +
Spirura rytipleurites – – +
Petrowospirura lynxi – – +
Cylicospirura subaequalis + – –
Spirocerca arctica + – –
Spirocerca lupi + + –
Vigisospirura potekhini – + –
Vigisospirura skrjabini – + –
Physoloptera praeputialis + – +
Physoloptera sibirica + + +
Gnatostoma spinigerum – + +
Gongylonema pulchrum + – –
Pneumospirura capsulate – + –
Rictullaria affi nis + – +
Rictularia cahirensis + – +
Filaria martis – + –
Dirofi laria immits + – +
Dirofi laria repens + – +
Total number 70 51 35 40
Abbrev ia t ions . +/– — presence or absence of the helminth in animals.
Of the total number of species (51) of helminths of Canidae, cestodes comprised 36 %,
trematodes 9.8 %, Acanthocephals 3.9 % and nematodes 47 %. Practically, similar layouts
are observed in both mustelids and felids. According to table 4, it is observed that nema-
365 Helminth Fauna in Carnivoran Mammals from Uzbekistan
T a b l e 4 . Th e number of helminth species of individual classes in studied carnivorous mammals of
various families
Family
To
ta
l
Parasites of carnivorous mammals
Cestoda Trematoda Acanthocephala Nematoda
N
b
of
sp
ec
ie
s Rate
(% ±
C.I.1)
P value
(Chi2) N
b
of
sp
ec
ie
s Rate
(% ±
C.I.1)
P value
(Chi2) N
b
of
sp
ec
ie
s Rate
(% ±
C.I.1)
P value
(Chi2) N
b
of
sp
ec
ie
s
Rate (% ±
C.I.1)
P value
(Chi2)
Canidae 51 19 37.3 ±
0.13
0.50
(0.43)
5 9.8 ±
0.08
0.52
(0.41)
2 3.9 ±
0.05
0.41
(0.67)
24 47.0 ±
0.13
0.56
(0.32)
Mustelidae 35 10 28.5 ±
0.14
– 5 14.2 ±
0.11
– 3 8.5 ±
0.09
– 18 51.2 ±
0.16
–
Felidae 40 15 37.5 ±
0.15
– 5 15.5 ±
0.1
– 2 5.0 ±
0.06
– 22 50.5 ±
0.15
–
Abbrev ia t ions . Nb of species — number of species; C.I.1 — 95 % confi dence interval.
todes make up the majority of representatives in Canidae, Mustelidae, and Felidae, ac-
counting for 47 %, 81.2 %, and 50.5 %, respectively. Cestodes, on the other hand, constitute,
respectively, 28.5 %, 37.5 %, and 36 % of the representatives in these three animal groups.
Helminthfauna of Canidae
In total 5 canids species (jackal, wolf, domestic dog, corsac and fox) were investigated
in the present study. As mentioned in table 4, 51 species of parasitic worms were recorded
in studied canids, which are unevenly distributed among individual host species.
Helminths of domest ic dog (Canis lupus famil iar i s)
Studied dogs in rural and urban populations of Uzbekistan were significantly infested
with helminths. Of the 399 individuals of examined dogs, helminths were found in 380
(95.3 %) (table 2). The helminths found during their identification turned out to be repre-
sentatives of 32 species belonging to 4 classes — Cestoda, Trematoda, Acanthocephala and
Nematoda (table 5).
Table 6 shows the occurrence of certain associations of the parasitofauna of a domestic
dog with vertebrates of other classes. Of the total number of canine parasites, according to
our own research, the largest number occurs in terrestrial vertebrates in mammals of other
orders (table 6).
Helminths of the jackal (Canis aureus L innaeus , 1758)
In this study of 120 jackal individuals, helminths were found in 101 with an infection
prevalence of 84.1 % (table 2). The intensity of the infection varied from one to dozens of
specimens.
The helminths we found turned out to be representatives of the classes Cestoda,
Trematoda, Acanthocephala and Nematoda. The modern helminth fauna consisted of 26
species: Diphyllobothrium latum (Linnaeus, 1758), Dipylidium caninum (Linnaeus, 1758),
Taenia hydatigena Pallas, 1766, Taenia ovis (Cobbold, 1869), Hydatigera taeniaeformis
(Batsch, 1786), Multiceps multiceps (Leske, 1780), Echinococcus granulosus (Batsch, 1786),
Mesocestoides lineatus (Goeze, 1782), Plagiorchis elegans (Rudolphi, 1802), Alaria alata
(Goeze, 1792), Macrocanthorynchus catulinus Kostylew, 1927, Capillaria plica (Rudolphi,
1819), Capillaria putorii (Rudolphi, 1819), Trichocephalus vulpis Froelich, 1789, Diocto-
phyma renale (Goeze, 1782), Strongyloides vulpis Petrow, 1941, Ancylostoma caninum (Er-
366 A. Safarov, A. Khan, D. Azimov, F. Akramova, K. Saparov & M. Ben Said
colani, 1859), Uncinaria stenocephala (Railliet, 1884), Toxascaris leonina (Linstow, 1902),
Toxocara canis (Werner, 1782), Spirocerca lupi (Rudolphi, 1809), Physoloptera praeputialis
Linstow, 1888, Physoloptera sibirica Petrow et Gorbunov, 1931, Gongylonema pulchrum
Molin, 1857, Dirofilaria immits (Leidy, 1856), and Dirofilaria repens Railliet et Henry, 1911.
T a b l e 5 . Species composition and taxonomic diversity of helminths of investigated domestic dogs in
Uzbekistan
Higher taxon Family Species
Cestoda Diphyllobothridae Diphyllobothrium latum
Dipylididae Dipylidium caninum
Joyeuxiella rossicum
Mesocestoididae Mesocestoides lineatus
Taeniidae Taenia hydatigena
Taenia pisiformis
Multiceps multiceps
Multiceps skrjabini
Hydatigera taeniae formis
Echinococcus granulosus
Trematoda Dicrocoeliidae Dicrocoelium dendriticum
Plagiorchidae Plagiorchis elegans
Alariidae Alaria alata
Acanthocephala Oligacanthorinchidae Macrocanthorynchus catulinus
Nematoda Capillariidae Capillaria plica
Trichocephalidae Trichocephalus vulpis
Dioctophymidae Dioctophyma renale
Strongyloididae Strongyloides stercoralis
Ancylostomatidae Ansylostoma caninum
Uncinaria stenocephala
Crenosomatidae Crenosoma vulpis
Ascarididae Toxascaris leonina
Anisakidae Toxocara canis
Spiruridae Spirocerca lupi
Spirocerca arctica
Physolopteridae Physoloptera preputialis
Physoloptera sibirica
Gongylonematidae Gongylonema pulchrum
Rictulariidae Rictullaria affi nus
Rictullaria cahirensis
Onchocercidae Dirofi laria immitis
Dirofi laria repens
T a b l e 6 . Th e relationship of helminthfauna of dogs and other vertebrates according to the literature
Higher taxon Total
number
Number of helminth species shared between dogs and other vertebrates
Fish Amphibians Reptiles Birds Other orders of mammals
Cestoda 15 2 1 2 1 5
Trematoda 5 1 4 3 4 2
Acanthocephala 1 0 0 0 0 1
Nematoda 20 2 1 1 1 3
Total 41 5 6 6 6 11
367 Helminth Fauna in Carnivoran Mammals from Uzbekistan
Nematodes (15 species) and cestodes (8 species) are the most widely represented. Of the
total number of species (26), all cestodes (8 species), acanthocephalans (2 species) and acan-
thocephalans (1 species) develop with the participation of intermediate hosts, belong to het-
eroxenic parasites. Nematodes are represented by both heteroxenic and monoxenic species.
Helminths of wolf (Canis lupus L innaeus , 1758)
Of the 62 studied wolves, 50 were infected with parasitic worms (80.6 %) (table 2).
26 helminth species belonging to cestodes (11 species), trematodes (2 species), acantho-
cephalans (2 species) and nematodes (11 species) were identified: Diphyllobothrium latum
(Linnaeus, 1758), Dipylidium caninum (Linnaeus, 1758), Diplopylidium nölleri (Skrjabin,
1924), Taenia hydatigena Pallas, 1766, Taenia ovis (Cobbold, 1869), Multiceps multiceps
(Leske, 1780), Multiceps skrjabini Popow, 1937, Tetratirotaenia polyacantha (Leuckart,
1856), Echinococcus multilocularis (Leuckart, 1863), Echinococcus granulosus (Batsch,
1786), Mesocestoides lineatus (Goeze, 1782), Plagiorchis elegans (Rudolphi, 1802), Alaria
alata (Goeze, 1792), Macrocanthorynchus catulinus Kostylew, 1927, Moniliformis monil-
iformis (Bremser, 1811), Capillaria plica (Rudolphi, 1819), Capillaria putorii (Rudolphi,
1819), Trichocephalus vulpis Froelich, 1789, Dioctophyma renale (Goeze, 1782), Ancylosto-
ma caninum (Ercolani, 1859), Toxascaris leonina (Linstow, 1902), Toxocara canis (Werner,
1782), Spirocerca lupi (Rudolphi, 1809), Physoloptera sibirica Petrow et Gorbunov, 1931,
Dirofilaria immits (Leidy, 1856), and Dirofilaria repens Railliet et Henry, 1911.
The basis of the helminth fauna of wolves was cestodes and nematodes, most of which
are parasites of domestic and game animals and humans.
Helminths of corsac (Vulpes corsac L innaeus , 1768)
The total infection of corsacs with helminths was 80.3 %, 49 individuals out of 61
studied were found infected (table 2). The helminth fauna consists of 23 species: Dipy-
lidium caninum (Linnaeus, 1758), Diplopylidium nőlleri (Skrjabin, 1924), Taenia crassi-
ceps (Zeder, 1800), Hydatigera taeniaeformis (Batsch, 1786), Tetratirotaenia polyacantha
(Leuckart, 1856), Echinococcus multilocularis (Leuckart, 1863), Echinococcus granulosus
(Batsch, 1786), Plagiorchis elegans (Rudolphi, 1802), Alaria alata (Goeze, 1792), Macrocan-
thorynchus catulinus Kostylew, 1927, Moniliformis moniliformis (Bremser, 1811), Thominx
aerophilus (Creplin, 1839), Ancylostoma caninum (Ercolani, 1859), Uncinaria stenocephala
(Railliet, 1884), Toxascaris leonina (Linstow, 1902), Toxocara canis (Werner, 1782), Toxo-
cara mystax (Leder, 1800), Oxynema numidica Linstow, 1899, Spirocerca arctica (Petrow,
1927), Spirocerca lupi (Rudolphi, 1809), Physoloptera praeputialis Linstow, 1888, Physolop-
tera sibirica Petrow et Gorbunov, 1931, and Rictullaria affinus Jägerskiold, 1904.
The helminth communities found in carnivorous animals were composed of 12 spe-
cies of nematodes, seven species of cestodes, two species of trematodes, and two species
of acanthocephalans. These species are considered typical for carnivorous animals. By the
nature of the life cycle, the noted helminth species are representatives of heteroxenic and
monoxenic forms, in the circulation of which corsac populations participate in the biogeo-
cenoses of Uzbekistan.
Helminths of the fox (Vulpes vulpes (Linnaeus , 1768))
A helminthological study of 68 individuals of foxes from Uzbekistan revealed parasitic
worms in 63. The prevalence of infection was very high (92.6 %) (table 2). The intensity of
infection varied considerably ranging from a single to several dozens of specimens.
368 A. Safarov, A. Khan, D. Azimov, F. Akramova, K. Saparov & M. Ben Said
The fauna of fox helminths consisted of 42 species: Diphyllobothrium latum (Linnaeus,
1758), Spirometra erinaceieuropaei (Rudolphi, 1819), Dipylidium caninum (Linnaeus, 1758),
Diplopylidium nőlleri (Skrjabin, 1924), Joyeuxiella echinorhynchoides (Sonsino, 1884), Joyeuxiella
pasqualei (Diamara, 1893), Joyeuxiella rossicum (Skrjabin, 1923), Taenia hydatigena Pallas, 1766,
Taenia macrocystis (Diesing, 1850), Taenia pisiformis (Bloch, 1780), Hydatigera krepkogorski
(Schulz et Landa, 1934), Hydatigera taeniae formis (Batsch, 1786), Tetratirotaenia polyacantha
(Leuckart, 1856), Echinococcus multilocularis (Leuckart, 1863), Echinococcus granulosus (Batsch,
1786), Mesocestoides lineatus (Goeze, 1782), Dicrocoelium dendriticum (Rudolphi, 1819), Plagior-
chis elegans (Rudolphi, 1802), Echinochasmus perfoliatus (Ratz, 1908), Alaria alata (Goeze, 1792),
Macrocanthorynchus catulinus Kostylew, 1927, Moniliformis moniliformis (Bremser, 1811), Cap-
illaria plica (Rudolphi, 1819), Capillaria putorii (Rudolphi, 1819), Thominx aerophilus (Creplin,
1839), Trichocephalus vulpis Froelich, 1789, Dioctophyma renale (Goeze, 1782), Strongyloides
vulpis Petrow, 1941, Ancylostoma caninum (Ercolani, 1859), Uncinaria stenocephala (Railliet,
1884), Crenosoma vulpis (Rudolphi, 1819), Toxascaris leonina (Linstow, 1902), Toxocara canis
(Werner, 1782), Toxocara mystax (Leder, 1800), Oxynema numidica Linstow, 1899, Spirura ry-
tipleurites (Deslongchamps, 1824), Spirocerca lupi (Rudolphi, 1809), Physoloptera praeputialis
Linstow, 1888, Physoloptera sibirica Petrow et Gorbunov, 1931, Gongylonema pulchrum Molin,
1857, Dirofilaria immits (Leidy, 1856), and Dirofilaria repens Railliet et Henry, 1911. Some domi-
nant helminth species are presented in figure 2.
Of the total number of species (n = 42) of fox helminths, approximately 50 % can para-
sitize domestic, commercial animals and humans.
Helminth fauna of Mustelidae
In total, 5 species of mustelids (stone marten, American mink, badger, weasel and river
otter) infected with parasitic worms were investigated. The features of the helminth fauna
of the studied species of martens are presented below.
Fig. 2. Carnivorans of Uzbekistan and some of their helminths: a — Vulpes vulpes; b — Canis familiaris; c —
C. aureus; d — Felis lybica; e — F. catus; g — F. chaus; 1 — Dioctophyma renale; 2 — Taenia hydatigena; 3 —
Dirofi laria immits; 4 — Toxocara canis.
369 Helminth Fauna in Carnivoran Mammals from Uzbekistan
Helminths of the s tone marten (Martes fo ina (Erxleben, 1777))
In the study of 43 marten individuals, helminths were detected in 21. The infection
rate was 49.0 % (table 2). The collected parasites were representatives of 17 species be-
longing to cestodes (6 species), trematodes (1 species) and nematodes (10 species): Taenia
crassiceps (Zeder, 1800), Taenia hydatigena Pallas, 1766, Taenia martis (Zeder, 1803), Tae-
nia mustelae Gmelin, 1790, Hydatigera taeniaeformis (Batsch, 1786), Mesocestoides lineatus
(Goeze, 1782), Alaria alata (Goeze, 1792), Capillaria mucronata (Molin, 1858), Capillaria
plica Rudolphi, 1819, Capillaria putorii Zeder, 1800, Thominx aerophilus (Creplin, 1839),
Dioctophyma renale (Goeze, 1782), Uncinaria stenocephala (Railliet, 1884), Crenosoma vul-
pis (Rudolphi, 1819), Filaroides martis (Werner, 1782), Spirocerca lupi (Rudolphi, 1809),
and Filaria martis Gmelin, 1790.
Helminths of the American mink (Muste la v i son Schreber , 1777)
As shown in table 2, 11 out of 26 individuals were found infected with 18 species of
helminths reported for the first time in Uzbekistan. These species are Diphyllobothrium
latum (Linnaeus, 1758), Taenia crassiceps (Zeder, 1800), Taenia martis (Zeder, 1803), Tae-
nia mustelae Gmelin, 1790, Taenia pisiformis (Bloch, 1780), Mesocestoides lineatus (Goeze,
1782), Plagiorchis elegans (Rudolphi, 1802), Euparyphium melis (Schrank, 1788), Alaria
alata (Goeze, 1792), Corynosoma strumosum (Rudolphi, 1802), Capillaria plica Rudolphi,
1819, Capillaria putorii Zeder, 1800, Thominx aerophilus (Creplin, 1839), Dioctophyma
renale (Goeze, 1782), Strongyloides martis Petrow, 1940, Uncinaria stenocephala (Railliet,
1884), Crenosoma petrowi Morosov, 1939, and Filaroides osleri (Cobbold, 1879).
Mink helminths are represented by cestodes (6 species), trematodes (2 species), acan-
thocephalans (1 species) and nematodes (11 species). By the nature of the life most hel-
minths found, except for nematodes Strongyloides martis and Uncinaria stenocephala, de-
velop with the participation of intermediate and paratenic hosts.
Helminths of badger (Meles meles (Linnaeus , 1758))
Out 57 individuals, 23 were found infected with helminths belonging to 19 species
(table 2). Cestodes were represented by 5 species, trematodes — by 1 species, acanthoceph-
alans — by 2 species, nematodes — by 11 species. The core of the helminth fauna of bad-
ger in Uzbekistan was comprised by cestodes and nematodes characteristic of predatory
mammals: Spirometra erinaceieuropaei (Rudolphi, 1819), Dipylidium caninum (Linnaeus,
1758), Taenia crassiceps (Zeder, 1800), Taenia martis (Zeder, 1803), Mesocestoides lineatus
(Goeze, 1782), Alaria alata (Goeze, 1792), Macrocanthorynchus catulinus Kostylew, 1927,
Moniliformis moniliformis (Bremser, 1811), Capillaria plica Rudolphi, 1819, Capillaria
putorii Zeder, 1800, Thominx aerophilus (Creplin, 1839), Ancylostoma caninum (Ercolani,
1859), Uncinaria stenocephala (Railliet, 1884), Crenosoma vulpis (Rudolphi, 1819), Vigiso-
spirura potekhini (Petrow et potekhina, 1953), Physoloptera sibirica Petrow et Gorbunov,
1931, Gnathostoma spinigerum Owen, 1836, Pneumospirura capsulata Gerichter, 1948, Fi-
laria martis Gmelin, 1790.
The collected species were localized mainly in the organs of the digestive system (16
species), as well as the respiratory system (2 species) and subcutaneous tissue (1 species).
Helminths of weasel (Muste la nival i s (Linnaeus , 1766))
In 35 weasels from the desert zones of Northwestern (Karakalpakstan, Ustyurt, Ky-
zylkum), Eastern and Northeastern Uzbekistan, helminths were found in 16 individuals.
The infection rate was 46.2 % (table 2). A total of 9 species of parasites were identified as
following: cestodes — 2 species, trematodes — 2 species, acanthocephalans — 1 species
370 A. Safarov, A. Khan, D. Azimov, F. Akramova, K. Saparov & M. Ben Said
and nematodes — 4 species: Taenia mustelae Gmelin, 1790, Mesocestoides lineatus (Goeze,
1782), Euparyphium melis (Schrank, 1788), Alaria alata (Goeze, 1792), Macrocanthoryn-
chus catulinus Kostylew, 1927, Capillaria putorii Zeder, 1800, Strongyloides martis Petrow,
1940, Filaria martis Gmelin, 1790, Gnathostoma spinigerum Owen, 1836.
Helminths of the r iver ot ter (Lutra lutra (Linnaeus , 1758))
Of 6 specimens of river otter seized from poachers on December 5, 2022 in the reser-
voirs of the Hissar district of Surkhandarya region, 4 animals were found infected with hel-
minths belonging to cestodes, trematodes and nematodes: Diphyllobothrium latum, Spiro-
metra erinaceieuropaei, Mesocestoides lineatus, Fasciola hepatica, Alaria alata, Plagiorchis
lutrae, Dioctophyma renale, Physoloptera sibirica, Rictullaria affinis, Strongyloides martis.
In total, 10 specis of helminths have been identified for the first time in Uzbekistan. The
intensity of infection of the detected trematodes varied from 2 to 13 specimens. D. latum,
M. lineatus, F. hepatica, A. alata and D. renale are parasites of farm animals and humans.
Helminthofauna of Fel idae
In this study, 4 species of wild and domestic cats from Uzbekistan were surveyed for
helminths’ infection. Of the total number of 125 dissected individuals, 82 (65.6 %) were
found infected with helminth parasites.
Helminths of jungle cat (Fel i s chaus Guldenstaedt , 1776)
Out of 43 studied individuals of the jungle cat, helminth were found in 31 with an
infection rate of 74.4 % (table 2). 23 species were identified, namely: Spirometra erinaceieu-
ropaei (Rudolphi, 1819), Dipylidium caninum (L., 1758), Diplopylidium nőlleri (Skrjabin,
1924), Joyeuxiella rossicum (Skrjabin, 1923), Taenia hydatigena Pallas, 1766, Taenia macro-
cystis (Diesing, 1850), Hydatigera krepkogorski (Schulz et Landa, 1934), Hydatigera taeniae-
formis (Batsch, 1786), Mesocestoides lineatus (Goeze, 1782), Macrocanthorynchus catulinus
Kostylew, 1927, Moniliformis moniliformis (Bremser, 1811), Thominx aerophilus (Creplin,
1839), Dioctophyma renale (Goeze, 1782), Ancylostoma caninum (Ercolani, 1859), Tro-
glostrongylus badanini Muminov, 1964, Toxascaris leonina (Linstow, 1902), Vigisospirura
potekhini (Petrow et potekhina, 1953), Physoloptera sibirica Petrow et Gorbunov, 1931,
Gnathostoma spinigerum Owen, 1836, Rictularia cahirensis Jägerskiold, 1904, Dirofilaria
immits (Leidy, 1856), Dirofilaria repens Railliet et Henry, 1911.
Cestodes were represented by 9 species, acanthocephalans by 2 species and nematodes
by 11 species. The noted helminth species are characteristic of predatory mammals, with
the exception of Troglostrongylus badanini Muminov, 1964, which was not found in other
carnivorans.
Helminths of the s teppe cat (Fel i s lybica Forster , 1780)
Of 11 studied individuals, helminths were detected in 7 (63.6 %) (table 2). In total, 15 hel-
minth species, cestodes and nematodes, were identified: Spirometra erinaceieuropaei (Rudol-
phi, 1819), Dipylidium caninum (L., 1758), Diplopylidium nőlleri (Skrjabin, 1924), Joyeuxiella
rossicum (Skrjabin, 1923), Taenia macrocystis (Diesing, 1850), Taenia pisiformis (Bloch, 1780),
Echinococcus multilocularis (Leuckart, 1863), Mesocestoides lineatus (Goeze, 1782), Uncinaria
stenocephala (Railliet, 1884), Toxascaris leoninа (Linstow, 1902), Toxocara mystax (Leder, 1800),
Oxynema numidica Linstow, 1899, Vigisospirura potekhini (Petrow et Potekhina, 1953), Physo-
loptera sibirica Petrow et Gorbunov, 1931, Rictullaria affinus Jägerskiold, 1904.
Helminths of domest ic cat (Fel i s catus L innaeus , 1758)
Out of 65 domestic cats, helminths belonging to Cestoda, Acanthocephala and Nema-
toda were found in 40 individuals. The total infection rate was 60.5 % (table 2). The inten-
371 Helminth Fauna in Carnivoran Mammals from Uzbekistan
sity of the infection was low, ranging from a single to several dozen specimens. In total,
23 species were revealed including 12 species of cestodes and 11 species of nematodes. All
recorded species were heteroxenous helminths: Dipylidium caninum (Linnaeus, 1758), Dip-
lopylidium acanthotetra (Parona, 1886), Joyeuxiella pasqualei (Diamara, 1893), Joyeuxiella
rossicum (Skrjabin, 1923), Taenia hydatigena Pallas, 1766, Taenia crassiceps (Zeder, 1800),
Taenia laticollis Rudolphi, 1819, Taenia macrocystis (Diesing, 1850), Taenia pisiformis
(Bloch, 1780), Hydatigera taeniaeformis (Batsch, 1786), Echinococcus granulosus (Batsch,
1786), Mesocestoides lineatus (Goeze, 1782), Capillaria putorii Zeder, 1800, Ancylostoma
caninum (Ercolani, 1859), Uncinaria stenocephala (Railliet, 1884), Toxascaris leonina (Lin-
stow, 1902), Toxocara canis (Werner, 1782), Spirura rytipleurites (Deslongchamps, 1824),
Physoloptera praeputialis Linstow, 1888, Physoloptera sibirica Petrow et Gorbunov, 1931,
Rictullaria affinus Jägerskiold, 1904, Dirofilaria immits (Leidy, 1856), Dirofilaria repens
Railliet et Henry, 1911.
Helminths of lynx (Lynx lynx (Linnaeus , 1758))
In this study, 5 individuals killed by poachers in the South and Northeast of Uzbekistan
in 2020–2022 were investigated and two species of cestodes (Taenia mystax and T. macra-
cystis) were reported for the first time. Four individuals were infected with helminths, of
which 16 species belonging to Cestoda (7 species) and Nematoda (9 species) were identi-
fied: Spirometra erinaceieuropaei (Rudolphi, 1819), Taenia hydatigena Pallas, 1766, Tae-
nia laticollis Rudolphi, 1819, Taenia pisiformis (Bloch, 1780), Hydatigera taeniaeformis
(Batsch, 1786), Echinococcus granulosus (Batsch, 1786), Mesocestoides lineatus (Goeze,
1782), Capillaria plica Rudolphi, 1819, Capillaria putorii Zeder, 1800, Thominx aerophilus
(Creplin, 1839), Ancylostoma caninum (Ercolani, 1859), Ancylostoma tubaeforme (Zeder,
1800), Uncinaria stenocephala (Railliet, 1884), Toxocara canis (Werner, 1782), Toxocara
mystax (Leder, 1800), Petrowospirura lynxi Matschulsky, 1952.
Features of l i fe cycle of helminth fauna of carnivorous mammals of Uz-
bekistan
Parasites registered in predatory mammals, with the exception of a few species (Fas-
ciola hepatica, and Dirocoelium dendriticum) belong to obligate helminths of the studied
animals.
According to the nature of the biological cycle, the helminths of carnivorous mammals
recorded by us can be divided into two groups: monoxenous species (development without
the participation of an intermediate host) and heteroxenous species (development with
the participation of an intermediate host). Heteroxenous parasites in our material were
represented by 61 species (85.9 %) of the total helminth fauna. These included all cestodes
(23 species), trematodes (9 species), acanthocephalans (3 species) and nematodes (26 spe-
cies).
Discussion
Several studies on the helminth fauna of carnivorous animals were carried out in Uz-
bekistan between 1950 and 1975 (Delyanova, 1958; Irgashev, 1958; Matchanov, 1959; Mur-
tazayev, 1964; Matchanov, 1967; Sadykov, 1967; Sultanov, 1969; Baratov, 1971; Reimov,
1972; Sultanov et al., 1975). The authors registered 32 species of helminths belonging to
Cestoda, Trematoda, Acanthocephala, and Nematoda in dogs from Northeastern, Eastern,
Central and Northwestern Uzbekistan. Total helminth infection in dogs ranged from 83.5
to 94.5 %. The species composition of helminths in rural dog populations in the studied
372 A. Safarov, A. Khan, D. Azimov, F. Akramova, K. Saparov & M. Ben Said
regions of Uzbekistan varied from 18 to 28 species. In the urban dog populations of the cit-
ies of Samarkand, Bukhara, Navoi, Ferghana and the metropolis of Tashkent, the parasitic
worm fauna ranged from 8 to 20 species (Safarov, 2020).
Information on the helminth fauna of wild carnivores in Uzbekistan is currently lim-
ited. The first studies focusing on the helminth fauna of predatory mammals in Uzbekistan
were conducted by the renowned Russian zoologist Professor A. P. Fedchenko. He led a
scientific expedition that worked in the territory of former Turkestan between 1868 and
1871. Fedchenko, together with G. Krabbe and Linstov, conducted research on Turkestan
dogs and identified five species of parasitic worms present in their intestines: Taenia hy-
datigena, Multiceps multiceps, Dipylidium caninum, Toxocara canis, and Spirocerca lupi
(Safarov et al., 2022).
Despite this early work, there has been little additional research on the helminth fauna
of wild carnivores in Uzbekistan. Our study therefore aims to build on this earlier work
and provide a more comprehensive understanding of the parasitic worms present in the
intestines of wild carnivores in the region.
Additionally, the list of works on helminths’ distribution and ecology is relatively small
(Irgashev, 1958; Muminov, 1963; Kairov, 1965; Koschanov, 1972; Matchanov et al., 1973;
Taryannikov, 1983). The authors’ research was devoted to the study of the helminthfauna
of individual species of carnivorous mammals from the Samarkand, Syrdarya regions and
Karakalpakstan, where about 26 species of parasitic worms (cestodes, trematodes, acantho-
cephalans and nematodes) were recorded. The data of previous studies have become no-
ticeably outdated, which is confirmed by data of the study of helminthfauna of carnivorous
animals of Karakalpakstan (Berdibaev, 2021).
In this study, 53 helminth species were detected in 278 individuals of carnivorous
mammals (jackal, wolf, fox, badger and jungle cat). The total infection rate of the studied
animals was 50.4 %. The diversity of helminth species is not the same among the studied
wild carnivore species. The highest number of species was found in the fox population (n =
40), with a total of 27, 25 and 22 helminth species reported in the jungle cat, jackal and wolf,
respectively. The lowest number of species was found in the badger (16 species).
Taking into account the known literature data and the results of our research, it is pos-
sible to state that the helminth fauna of dogs in Uzbekistan comprises 41 species. Of these,
cestodes are represented by 15 species, trematodes by 5 species, acanthocephalans by 1 spe-
cies, and nematodes by 20 species (table 7).
All recorded helminth species (41) belong to common parasites of carnivorous mam-
mals, including domestic dogs of Uzbekistan, from both rural (41) and urban (21) popu-
lations. There is a noticeable depletion of the helminth fauna of urban dog populations,
due to the characteristics of the urban environment. The helminth communities that we
observed in rural dog populations are uneven across the different natural areas of Uzbeki-
stan (table 7). Helminth species diversity is highest in the Northeastern (33 species) and
Northwestern (32 species) regions. The poorest helminth fauna (18 species) was found in
the territory of the Eastern region.
The results we obtained on the helminth fauna of dogs of rural populations partly
confirm the data of previous studies (Delyanova, 1958; Matchanov, 1959; Baratov, 1971),
summarized by Sultanov et al. (1975) in the monograph “Helminths of domestic mammals
of Uzbekistan”, where 32 species of parasitic worms were reported. Previously discovered
parasitic worm species in Uzbekistan dogs (Delyanova, 1958; Matchanov, 1959) were not
included. The present study identified five species of trematodes in these dogs, which are
Plagiorchis elegans (Rudolphi, 1802), Mesorchis denticulatus (Rudolphi, 1802), Alaria alata
373 Helminth Fauna in Carnivoran Mammals from Uzbekistan
Table 7. Summary data on helminthfauna of dogs in Uzbekistan according to the literature
Higher
taxon Species Helminths of dogs
Rural Urban
Cestoda Diphyllobothrium latum (Linnaeus, 1758) + –
Spirometra erinaceieuropaei (Rudolphi, 1819) + +
Dipylidium caninum (Linnaeus., 1758) + +
Joyeuxiella rossicum (Skrjabin, 1923) + +
Diplopylidium nőlleri (Skrjabin, 1924) + +
Mesocestoides lineatus (Goeze, 1782) + +
Taenia hydatigena Pallas, 1766 + +
Taenia ovis (Cobbold, 1896) + –
Taenia pisiformis (Bloch, 1780) + –
Taenia macrocystis (Diesing, 1850) + –
Multiceps multiceps (Leske, 1780) + +
Multiceps serialis (Gervais, 1847) + –
Multiceps skrjabini Popow, 1937 + –
Echinococcus granulosus (Batsch, 1786) + +
Echinococcus multilocularis (Leuckart, 1863) + –
Trematoda Dicrocoelium dendriticum (Rudolphi, 1819) + –
Plagiorchis elegans (Rudolphi, 1802) + –
Echinochasmus perfoliatus (Ratz, 1908) + –
Mesorchis denticulatus (Rud, 1802) + –
Alaria alata (Goeze, 1792) + –
Acanthocephala Macrocanthorynchus catulinus (Kostylew, 1927) + +
Nematoda Capillaria plica (Rudolphi, 1819) + –
Capillaria putorii (Zeder, 1800) + –
Thominx aerophilus (Creplin, 1839) + –
Trichocephalus vulpis Froelich, 1789 + +
Dioctophyma renale (Goeze, 1782) + +
Ancylostoma caninum (Ercolani, 1859) + +
Uncinaria stenocephala (Railliet, 1884) + +
Filaroides osleri (Cobbold, 1879) + –
Toxascaris leonina (Linstow, 1902) + +
Toxocara canis (Werner, 1782) + +
Toxocara mystax (Leder, 1800) + –
Spirocerca lupi (Rudolphi, 1809) + +
Spirocerca arctica (Petrow, 1927) + –
Physoloptera praeputialis (Linstow, 1899) + +
Gongylonema pulchrum (Molin, 1857) + +
Rictullaria affi nus (Jagerskiold, 1904) + +
Rictullaris cahirensis (Jagerskiold, 1904) + –
Dirofi laria immits (Leidy, 1856) + +
Dirofi laria repens (Railliet et Henry, 1911) + +
Dracunculus medinensis (Linnaeus, 1758) + –
Total number 41 21
Abbrev ia t ions . +/– — presence or absence of the helminths of dogs in rural or urban areas.
374 A. Safarov, A. Khan, D. Azimov, F. Akramova, K. Saparov & M. Ben Said
(Goeze, 1792), Echinochasmus perfoliatus Ratz, 1908 and Brachylaemus sp.; 1 species of
cestodes — Spirometra erinaceieuropaei ( Rudolphi, 1819) and 3 species of nematodes —
Thominx aerophilus (Creplin, 1839), Filaroides osleri (Cobbold, 1879) and Rictularia cahi-
rensis Jägerskiold, 1904.
The distribution of these species in the biogeocenoses of Uzbekistan is characterized
by a limited nature. They are found in a small number of dogs studied on the territory of
Karakalpakstan and the Tashkent region. It is characteristic that during the entire research
period (2018-2022), we did not identify these species.
Relatively, the helminth fauna of dogs in the studied cities (Nukus, Samarkand, and
Tashkent) is similar and includes from 20 to 22 species.
The species of helminths found in dogs can be divided into 2 groups: those of medical
and sanitary importance (Cestodes — Diphyllobothrium latum, Dipylidium caninum, Tae-
nia hydatigena, Multiceps multiceps, Echinococcus granulosus, Echinococcus multilocularis;
Nematodes — Dioctophyma renale, Toxocara canis, Gongylonema pulchrum, Dirofilaria
repens, Dracunculus medinensis); of economic importance.
The distribution of parasite communities depends on the peculiar ecological charac-
teristics of natural and urbanized territories.
The role of dogs in the spread of zoonoses has long held the attention of biologists
and parasitologists with medical and veterinary profiles. Numerous publications bear wit-
ness to this in particular generalized work on dog endo- and ectoparasites in both natural
and urbanized territories (Arkhipovа, 2004; Arkhipov & Arkhipovа, 2004; Morgan, 2013;
Dantas-Torres & Domenico Otranto, 2016). Dog populations, as an integral part of societal
life, have been found to be infected with a general group of helminths, most of which can
parasitize in the larval or mature stage in the human body and domestic animals. The most
widely known of them are echinococcosis, cenurosis, hymenolepidosis, diphyllobothriosis,
ancylostomosis, toxacarosis, toxascariasis, dirofilariasis and dioctophimosis.
Any adverse events or factors in the life of society are always accompanied by epidem-
ics of the aforementioned animal and human helminthiasis, causing enormous economic
damage. Given the actual infection of dogs with zoonotic pathogens, it should be assumed
that in modern conditions the problems of improving dog populations against parasitic
diseases and protecting pets and humans have not lost their relevance. All this requires
controlling the number of dog populations in urbanized territories - megacities and other
settlements (Chomel, 2014; Idikaa et al., 2017; Norkobilov et al., 2020; Safarov et al., 2018,
2021, Wu et al., 2021; Safarov et al., 2022; Deak et al., 2022).
According to the literature data (Anderson, 2000; Azimov et al., 2015; Safarov, 2020;
Safarov et al., 2021), the biological cycle was studied in 13 species of cestodes, five species
of trematodes, one species of acanthocephalans, and ten species of nematodes. The de-
velopment of 29 species of helminths of the studied dogs occurs with the participation of
intermediate hosts and 12 species in a direct way. The transmission of helminth larvae into
the final host is carried out in different ways, which are considered when describing the
biocenotic relationships of predatory mammals and their parasites.
Martens in Uzbekistan are represented by 11 species and subspecies belonging to 6
genera — Mustela Linnaeus, 1785; Vormela Blasius, 1844; Martes Pinel, 1792; Mellivora
Storr, 1780; Meles Brisson, 1762; and Lutra Brisson, 1762 (Shernazarov et al., 2006). The
representatives of these genera were found to be hosts for helminths, as reported in cases
of infestation of some species of martens (such as bandages, stone martens, and badgers)
in Uzbekistan (Kontrimavichus, 1969; Koshanov, 1972). The author recorded 5 species of
helminths (2 species of cestodes and 3 of nematodes).
375 Helminth Fauna in Carnivoran Mammals from Uzbekistan
The feline family in Uzbekistan is represented by 10 species and 4 subspecies that live
in diverse biocenoses and are important components of biodiversity. In helminthological
terms, the cats of Uzbekistan belong to poorly studied objects. The available information
on the helminth fauna of certain species is fragmentary (Muminov & Alloyarov, 1963; Kos-
chanov, 1972) and rather outdated.
Cestodes and nematodes are the core of the helminth faunal complexes of carnivorans
of Uzbekistan.
As mentioned earlier, the total helminth infection of carnivoran mammals was 79.8 %.
The intensity of infection varied considerably from a single to several dozen specimens. In
the vast majority of cases, mixed infections of several types of parasites were recorded in
infected animals with 3 to 9 species of helminths, which, it should be assumed, have a seri-
ous effect on the body, leading to the death of intensely infected animals.
When discussing the presented material, it should be noted that the registered para-
sites of dogs in other vertebrates belong to different stages of development. Fishes, amphib-
ians, reptiles, birds and some orders of mammals act as intermediate or reservoir hosts,
corresponding species or groups of canine parasites in natural and urbanized areas.
Thus, the relationship of the parasitofauna of domestic dogs with representatives of
other classes of vertebrates is very close, of the 41 species of dog parasites in Uzbekistan,
34 use in their transmission representatives of other classes: fishes — 12.2 %, amphibians,
reptiles and birds — 14.6 %, and other orders of mammals — 26.8 %. As it should be, a large
percentage of dog helminths is recorded in mammals of other orders.
The results of our research conducted in all regions of Uzbekistan covering a large
number of species of predatory mammals also showed a rather rich fauna of helminths
consisting of representatives of the classes Cestoda, Trematoda, Acanthocephala and
Nematoda. In total, we have registered 71 species of helminths. It is characteristic that the
species diversity of the parasite community of domestic and wild predatory mammals is
associated with the parasite’s fauna of many species and groups of animals in Uzbekistan.
In this respect, the helminthfauna of predatory animals is unique and plays an impor-
tant role in the formation of helminthic faunal complexes of other vertebrates, including
humans. Carnivorous animals serve as reservoir to a number of species that infect rep-
resentatives of other orders of mammals and classes of vertebrates. The role of almost all
species of cestodes, several species of nematodes of the genera Dirofilaria, Ancylostoma,
Toxocara, Spirocerca in the occurrence of zoonotic helminthiasis is particularly signifi-
cant (Bronstein & Tokmalaev, 2004; Safarov et al., 2021, 2022). In this case, predatory
mammals participate as obligate hosts of helminths, dispersing the invasive elements in
diverse landscapes.
Interest in the study of the helminthfauna of carnivorous carnivores does not wane
at present. Numerous publications reflect the results of research on various issues of the
helminth community of both domestic and wild carnivores (Vieria et al., 2008; Shulyak &
Arkhipov, 2010; Subotin, 2011; Tulov, 2013; Romashova et al., 2014; Yakubovsky, 2015;
Ibragimov, Fataliev, 2015; McAllister et al., 2019). This is explained by two reasons. On
the one hand, among the helminthis of carnivorous mammals, there are a significant
number of agents of dangerous helminthiasis of both domestic animals and humans. On
the other hand, all cestodes, trematodes, acanthocephalans and two types of nematodes
with their unique life cycles are research objects with a general zoological and general
biological orientation. These circumstances, as we believe, are also relevant at the present
time.
376 A. Safarov, A. Khan, D. Azimov, F. Akramova, K. Saparov & M. Ben Said
The information presented by us on the helminthfauna of carnivorous mammals of
Uzbekistan, one of the important regions of Central Asia, will serve as a basis for further
long-term monitoring of the helminthological situation and conducting anti-helminthic
measures for agricultural and commercial animals and humans.
Conclusion
Our research has shown that the helminth fauna of carnivorous mammals in Uzbekistan
consists of 71 species belonging to cestodes, trematodes, acanthocephalans and nematodes. The
distribution of helminth species in individual carnivore groups is very uneven. The greatest di-
versity of species was recorded in canids (51 species), slightly fewer helminth species were found
in felids (40 species), while the helminth fauna of mustelids is markedly depleted (35 species).
The complex of species that make up the fauna of parasitic worms of predatory mam-
mals in Uzbekistan significantly complements previous literature data on the diversity of
helminth species and their role in the occurrence of zoonotic helminthiasis. In this regard,
predators deserve special attention as a source of helminthiasis pathogens that are very
dangerous for humans and livestock, such as diphyllobatriosis, dipylidiosis, echinococco-
sis, cenurosis, cysticercosis, mesocystoidosis, dioctophimosis, toxocarosis, dirofilariasis. In
the spread of these helminthiases in the natural and urbanized areas of Uzbekistan, we
believe that the main source of invasion is domestic dogs, due to their large numbers.
Knowledge of the helminth fauna of carnivorous mammals, the distribution of domi-
nant species and groups of parasitic worms, is extremely important for the justification and
implementation of anti-helminthic measures. The control of helminthiases in dogs is an
important link in the prevention of zoonotic diseases in humans and livestock.
Acknowledgements
We would like to thank all veterinarians of Uzbekistan for helping in sample collection.
Funding
Th is research was carried out on the basis of the research program of the Institute of Zoology of the
Academy of Sciences of the Republic of Uzbekistan for 2020–2025 on “Improvement of ways of formation,
taxonomy and control measures of vertebrate helminth fauna” and on the basis of the economic contract
“Parasitological monitoring of foreign objects (pastries and reservoirs) in Karakalpakistan” which is planned
for implementation in 2021–2022 (No. /4/2021 of April 13, 2021).
Data availability. All relevant data is enclosed within the manuscript.
Code availability. Not applicable.
Declarations
Ethics approval and consent to participate the study was reviewed and approved by the center’s ethics
committee (approval code: No. 7 protocol on 31 March 2022).
Consent for publication. Not applicable.
Confl icts of interest. Th e authors declare no confl icts interests.
Author contributions. Alisher Safarov (AS) designed this study, collected samples and epidemiological
data, wrote the manuscript; Firuza Akramova (FA) performed the identifi cation of helminths; Mourad Ben
Said (MBS) performed the statistical analysis. Mourad Ben Said (MBS), Adil Khan (AK), Djalaliddin Azimov
(DA) and Kalandar Saparov (KS) edited and fi nalized it. All these authors approved the fi nal version of the
manuscript.
377 Helminth Fauna in Carnivoran Mammals from Uzbekistan
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Received 24 February 2023
Accepted 22 August 2023
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/NLD (Gebruik deze instellingen om Adobe PDF-documenten te maken die zijn geoptimaliseerd voor prepress-afdrukken van hoge kwaliteit. De gemaakte PDF-documenten kunnen worden geopend met Acrobat en Adobe Reader 5.0 en hoger.)
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| id | oai:ojs.akademperiodyka.org.ua:article-467 |
| institution | Zoodiversity |
| issn | 2707-7268 |
| keywords_txt_mv | |
| language | English |
| last_indexed | 2026-08-21T01:01:32Z |
| publishDate | 2023 |
| publisher | Publishing House "Akademperiodyka" of the National Academy of Sciences of Ukraine |
| record_format | ojs |
| resource_txt_mv | ojsakademperiodykaorgua/e0/b98b0ce000655a8acf1eda1db0cc68e0.pdf |
| spelling | oai:ojs.akademperiodyka.org.ua:article-4672026-08-20T12:37:14Z Helminth Fauna in Carnivoran Mammals from Uzbekistan Safarov, A. Khan, A. Azimov, D. Akramova, F. Saparov, K. Ben Said, M. helminths Carnivora Canidae Felidae Mustelidae Uzbekistan Helminths, or parasitic worms, are a group of organisms that can infect various animal species, including humans. In Uzbekistan, previous studies on the helminth fauna of mammals have mainly focused on domestic animals and some wildlife species, with little attention given to carnivoran mammals. This survey aims to conduct a comprehensive study for the first time in Uzbekistan on the helminth fauna of Carnivora. In this study, helminths were collected from 1002 carnivorans (Canidae, n = 710; Mustelidae, n = 167; and Felidae, n = 125) from five locations in Uzbekistan (Northeastern, Eastern, Central, Southern and Northwestern). A total of 71 species of helminths were identified in domestic and wild carnivores by necropsy and faecal examination, of which 36, 23, 9, and 3 species belonged to the higher taxon Nematoda, Cestoda, Trematoda and Acanthocephala respectively. The highest number of helminth species was recorded in studied Canidae (51 species), followed by Felidae (40 species) and Mustelidae (35 species). The overall infection rate of carnivorans was 79.8 %. Infection intensity ranged from a single to dozens of specimens. The statistical analysis indicated that the diversity of helminth species is significant among members of Canidae, with foxes having 42 species and dogs having 41 species (P &lt; 0.05). Our study proves that the parasitic worm species that inhabit predatory mammals in Uzbekistan are a diverse and complex group that can cause helminthiases, which may be dangerous to livestock and humans. Publishing House "Akademperiodyka" of the National Academy of Sciences of Ukraine 2023-07-05 Article Article application/pdf https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/467 10.15407/zoo2023.04.359 Zoodiversity; Vol. 57 No. 4 (2023): Zoodiversity Zoodiversity (Vestnik Zoologii); Том 57 № 4 (2023): Zoodiversity 2707-7268 2707-725X 10.15407/zoo2023.04 en https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/467/225 Copyright (c) 2023 Zoodiversity |
| spellingShingle | Safarov, A. Khan, A. Azimov, D. Akramova, F. Saparov, K. Ben Said, M. Helminth Fauna in Carnivoran Mammals from Uzbekistan |
| title | Helminth Fauna in Carnivoran Mammals from Uzbekistan |
| title_full | Helminth Fauna in Carnivoran Mammals from Uzbekistan |
| title_fullStr | Helminth Fauna in Carnivoran Mammals from Uzbekistan |
| title_full_unstemmed | Helminth Fauna in Carnivoran Mammals from Uzbekistan |
| title_short | Helminth Fauna in Carnivoran Mammals from Uzbekistan |
| title_sort | helminth fauna in carnivoran mammals from uzbekistan |
| topic_facet | helminths Carnivora Canidae Felidae Mustelidae Uzbekistan |
| url | https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/467 |
| work_keys_str_mv | AT safarova helminthfaunaincarnivoranmammalsfromuzbekistan AT khana helminthfaunaincarnivoranmammalsfromuzbekistan AT azimovd helminthfaunaincarnivoranmammalsfromuzbekistan AT akramovaf helminthfaunaincarnivoranmammalsfromuzbekistan AT saparovk helminthfaunaincarnivoranmammalsfromuzbekistan AT bensaidm helminthfaunaincarnivoranmammalsfromuzbekistan |