Research Article

Ecological and Faunistic Analysis of Helminths of Wild Mammals from the Order Carnivora in Karakalpakstan

Erkinjon B. Shakarboev1*, Abat S. Berdibaev2

1Institute of Zoology, Academy of Sciences of Uzbekistan, Bogishamol st., 232b,Tashkent,100053, Uzbekistan; 2Nukus State Pedagogical Institute, Nukus, Uzbekistan.

Received | February 15, 2023; Accepted | April 07, 2023; Published | November 06, 2023

*Correspondence | Erkinjon B. Shakarboev, Institute of Zoology, Academy of Sciences of Uzbekistan, Bogishamol st., 232b,Tashkent,100053, Uzbekistan; Email: shakarboev@rambler.ru

Citation | Shakarboev EB, Berdibaev AS (2023). Ecological and faunistic analysis of helminths of wild mammals from the order carnivora in Karakalpakstan. Adv. Anim. Vet. Sci., 11(11):1801-1809.

DOI | https://dx.doi.org/10.17582/journal.aavs/2023/11.11.1801.1809

ISSN (Online) | 2307-8316

Copyright: 2023 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

INTRODUCTION

Carnivorous animals are known to be a source of dangerous parasitic diseases in humans and agricultural animals. Therefore, to identify pathogens of zooanthropozoonoses in wild carnivores and to develop measures to combat parasitic diseases is highly important from the scientific and practical aspects.

In Uzbekistan, the species composition, biology and ecology of helminths of carnivores have been studied by Tarannikov (1983), Azimov et al. (1991), Shakarboev (2009), Safarov et al. (2018), Azimov et al. (2019), Akramova et al. (2019) and other researchers. As a result, the species composition of helminths in some domestic and wild predatory animals in Uzbekistan has been specified. However, the fauna of helminths of predatory mammals in Karakalpakstan with specific natural environment has been studied very insufficiently.

26 species of wild mammals from the order Carnivora have been registered in the wildlife of Karakalpakstan (Ishunin, 1961; Palvaniyazov, 1974). They represent the families Canidae, Mustelidae, Hyanidae and Felidae (Shernazarov et al., 2006). In addition, 2 species of domestic predators – the Dog (Canidae) and the Cat (Felidae) – are recorded in Karakalpakstan in human settlements and natural areas adjoining them. For different ecological and ethological reasons, various trophic and chorological relations are established between wild and domestic (dog and cat) predators, which also actively exchange parasites. Domestic carnivores are components of and important links in the ecological circulation of parasitic worms.

These carnivores successfully adapt to anthropogenic ecosystems and actively participate in the circulation of zoonotic helminthiases. In the contemporary environment, helminthiases of predatory mammals, on the one hand, are becoming increasingly widespread and, on the other hand, are showing a local increase in the epizootological tension (Gorokhov et al., 2011). The information provided above shows that studying helminths and helminthiases in wild carnivores in Karakalpakstan is important.

The purpose of the work is to study the fauna and some aspects of the ecology of helminths parasitising wild predators and to assess the current situation with zoonotic helminthiases in the territory of northwestern Uzbekistan (Karakalpakstan).

MATERIALS AND METHODS

The studies were conducted between 2017 and 2022. The research was carried out between 2017 and 2022 on the territory of the Republic of Karakalpakstan (Figure 1). 258 individuals of wild predatory mammals and 15 individuals of the Domestic Dog were studied using the method of complete and partial helminthological dissection developed by Skryabin (1928). Most of the wild carnivores were provided by hunters (on verbal agreement with them). 19 of the animals died on roads, hit by vehicles. 10 carnivores were killed for research purposes on the basis of a permit. Domestic dogs were examined after they were killed by dog catchers. The predatory mammals were represented by 6 species the Wolf, Golden Jackal, Fox, Badger, Jungle Cat and Domestic Dog from the families Canidae, Felidae and Mustelidae. The collected Trematoda, Cestoda and Acanthocephala were preserved in 70o alcohol, and Nematoda in Barbagallo fluid.

In addition, 42 samples of jackal excrement, 18 samples of wolve excrement, 38 samples of fox excrement, 56 sample of badger excrement and 11 samples of jungle cat excrement were collected. A total of 165 faecal samples were examined using known methods (Kotelnikov, 1974). The material was collected in February and March 2021. The faeces of domestic dogs were collected from the rectum, those of wild predators were taken from the ground within the Lower Amudarya Biosphere Reserve and on the Ustyurt Plateau. The faecal samples collected from each animal were put in plastic containers, labelled and stored in a refrigerator. Zoologists from the Karakalpak State University and Nukus State Pedagogical Institute helped identify in situ the species to which the excrement belonged. The eggs were measured and their images and descriptions in a guide were used to carry out a differential diagnosis of the eggs (Cherepanov et al., 1999). The eggs of Uncinaria stenocephala and Ancylostoma caninum differed in size (Cherepanov et al., 1999).

 

The preparations were made following generally accepted methods (Khotenovsky, 1966; Sudarikov and Shigin, 1965). Microscopes MBI-6, MBS-10, LOMO and a range of binocular microscopes were used to study the morphology of the parasitic worms. To identify Trematoda, Cestoda and Acanthocephala species, the parasites were stained with carmine alum and used to make permanent and temporary preparations. To identify Nematoda species, the worms were treated with a 1:1 mixture of lactic acid and glycerol. The helminths were measured using a graduated eyepiece ruler.

A number of identifiers and monographs were used to identify helminth eggs and larvae in the faeces (Kotelnikov, 1974; Tokobaev, 1976; Kozlov, 1977).

Prevalence and infection intensity were used as indicators to evaluate the presence of parasites in the hosts organisms and their distribution across population.

The infection intensity data were statistically processed (Lakin, 1990).

RESULTS AND DISCUSSION

In the biocoenoses of Karakalpakstan, 5 species of wild carnivores and the domestic dog were examined for helminths. The total prevalence was 49.8%. 53 species of helminths were identified, representing 39 genera, 25 families, 13 orders, 4 classes and 3 phyla, with 17 species (32%) from the class Cestoda, 4 (8%) from Trematoda, 3 (6%) from Acanthocephala and 29 (55%) from Nematoda (Table 1).

Analysis of the material shows that Nematoda are represented by the largest number of species (29), followed by Cestoda (17) and Trematoda (4). Acanthocephala account for the smallest number of helminth species (3). The highest diversity of helminth species among the studied predators was recorded in the Fox–40 species, which was followed by the Jungle Cat (27 species), Golden Jackal (25), Wolf (22), Domestic Dog (20) and Badger (16 species) (Table 2).

 

Table 1: Species composition of the studied animals and helminth prevalence.

Animals species1	Number of studied individuals	Infected %
Canis aureus (Linnaeus, 1758)	91	52.7
Canis lupus (Linnaeus, 1758)	41	41.5
Vulpes vulpes subsp. karagan (Erxleben, 1777)	62	59.7
Meles meles subsp. leucurus Hodgson, 1847	25	36.0
Felis chaus Guldenstaedt, 1776	39	48.7
Canis familiaris (Canis lupus familiaris Linnaeus, 1758)	15	40.0

 

1Scientific names of species of carnivores and helminths were checked against information from https://fauna-eu.org/, https://itis.gov/

 

According to the research, 4 species from the class Cestoda – J. pasqualei, T. ovis, H. krepkogorski and M.skrjabini, and 7 species from the class Nematoda – C. putorii, U. stenocephala, C. vulpis, O.numidica, C. subaequalis P. capsulata and Dipetalonema sp., were recorded in the fauna of Karakalpakstan for the first time. The last nematode in the list is reported to be a new species for the fauna of the CIS countries.

A brief description of the nematode (according to the original material) newly discovered in the territory of CIS countries. The body is white, thread-like and elegant (delicate). The cuticle is smooth. The tail is blunt. The male is 62 mm long and 0.32 mm wide. The general appearance is similar to that of Dipetalonema dracunculoides (Cabbold, 1870), but the localisation was different. We recorded Dipetalonema sp. in the right ventricle of a jackal’s heart.

Due to the insufficiency of the material, we referred this nematode as Dipetalonema sp. The material is stored in the zoological collection of the Institute of Zoology, Academy of Sciences of the Republic of Uzbekistan, under No. 24 (Figure 2).

 

Table 2: Diversity of the helminth fauna of carnivorous animals in Karakalpakstan.

Helminth species	Host species
	Wolf	Golden Jackal	Fox	Badger	Jungle Cat	Dog
Trematoda Rudolphi, 1808
Plagiorchis elegans Rudolphi, 1802	-	+	+	-	-	-
Echinochasmus perfoliatus Ratz, 1908	-	-	+	-	-	-
Mesorchis denticulatus Rud., 1802	-	-	+	-	-	-
Alaria alata Krause, 1914	+	+	+	+	+	+
Cestoda Rudolphi, 1808
Spirometra erinacei-europei Rudolphi, 1819	-	+	+	+	+	+
Dipylidium caninum Linnaeus, 1758	+	+	-	+	+	+
Diplopylidium nőlleri Skrjabin, 1924	+	-	+	-	+	-
Joyeuxiella echinorhynchoides Sonsino, 1889	-	+	+	-	-	-
Joyeuxiella pasqualei Diamare, 1893	-	-	+	-	-	-
			Tables continued on next pages............
Helminth species	Host species
	Wolf	Golden Jackal	Fox	Badger	Jungle Cat	Dog
Joyeuxiella rossicum Skrjabin. 1923	-	-	-	-	+	-
Taenia hydatigena Pallas, 1766	+	+	+	-	-	+
Taenia macrocystis Diesing, 1850	-	-	+	-	+
Taenia ovis Cobbold, 1869	-	+	-	-	-	+
Taenia pisiformis Bloch, 1780	+	-	+	-	-	-
Hydatigera krepkogorski Schulz et Landa, 1934	-	-	+	-	+	-
Hydatigera taeniaformis Batsch, 1786	-	+	-	-	-	-
Multiceps multiceps Leske, 1780	+	+	+	-	-	+
Multiceps skrjabini Popov, 1937	+	-	-	-	-	-
Echinococcus multilocularis Leuckart, 1863	-	+	+	-	-	-
Echinococcus granulosus Batsch, 1786	+	+	+	-	-	+
Mesocestoides lineatus Goeze, 1782	+	+	+	+	+	+
Nematoda Rudolphi, 1808
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, 1854	+	-	+	+	+	+
Crenosoma vulpis Rudolphi, 1819	+	-	+	+	-	+
Troglostrongylus bаdanini Muminov, 1964	-	-	-	-	+	-
Toxascaris leonina Linstow, 1902	+	+	+	-	+	+
Toxocara canis Werner. 1782	+	+	+	+	+	+
Toxocara mystax Zeder, 1800	+	+	+	-	+	+
Oxynema numidica Seurat, 1915	-	-	-	-	+	-
Spirura rytipleurites Deslongchamps, 1824	-	-	+	-	-	-
Cylicospirura subaequalis Molin, 1860	-	-	+	-	-	-
Spirocerca arctica Petrow, 1927	-	-	+	-	-	-
Spirocerca lupi Rudolphi, 1809	+	-	-	-	-	-
Vigisospirura potekhini Petrow et Potekhina, 1953	-	-	-	+	+	-
Vigisospirura skrjabini Tschernikowa, 1934	-	-	+	-	-	-
Physaloptera praeputiale Linstow, 1888	-	-	+	-	+	-
Physaloptera sibirica Petrow et Gorbunow, 1931	-	+	+	+	+	+
Gongylonema pulchrum Molin, 1857	-	-	+	-	-	-
Pneumospirura capsulata Gerichter, 1948	-	-	-	+	-	-
Rictularia affinis Jagerskiold, 1904	+	+	+	-	+	+
Rictularia cahirensis Jagerskiold, 1904	+	-	+	-	+	-
Dipetalonema sp.	-	+	-	-	-	-
Dirofilaria immitis Leidy, 1856	+	+	+	-	+	+
Dirofilaria repens Railliet et Henry, 1911	+	+	+	-	+	+
Dracunculus medinensis L., 1758	-	+	-	-	+
Acanthocephala Rudolphi, 1801
Macracanthorynchus hirudinaceus Pallas, 1781	+	-	+	+	-	-
Macracanthorhynchus catulinus Kostylew, 1927	-	+	+	+	+	+
Moniliformis moniliformis Bremser, 1811	+	-	+	+	+	-

 

Table 3: Distribution of helminths of foxes by their dominance in Karakalpakstan.

Helminth category	Helminth species	Infection indicators
		Prevalence, %	Infection intensity, individuals
Dominant	Strongyloides vulpis	42.0	4.9 ± 0.92
	Toxocara canis	40.3	20.4 ± 1.81
	Crenosoma vulpis	40.3	4.0 ± 0.63
	Multiceps multiceps	38.7	6.4 ± 0.41
	Toxascaris leonina	37.0	14.8 ± 1.32
	Rictularia cahirensis	35.4	4.4 ± 0.54
	Trichocephalus vulpis	33.8	4.2 ± 0.52
	Mesocestoides lineatus	32.2	2.7 ± 0.24
	Taenia hydatigena	30.6	3.4 ± 0.30
	Toxocara mystax	30.6	8.6 ± 0.72
	Spirura rytipleurites	30.6	3.0 ± 0.31
Subdominant	Echinochasmus perfoliatus	24.1	1.7 ± 0.13
	Cylicospirura subaequalis	24.1	1.5 ± 0.21
	Rictularia affinis	24.1	1.8 ± 0.41
	Alaria alata	22.5	1.3 ± 0.09
	Echinococcus multilocularis	21.0	2.8 ± 0.24
	Uncinaria stenocephala	21.0	2.2 ± 0.13
Intermediate	Physaloptera sibirica	19.3	1.9 ± 0.16
	Dirofilaria immitis	19.3	1.2 ± 0.09
	Taenia pisiformis	17.7	1.7 ± 0.64
	Plagiorchis elegans	17.7	0.9 ± 0.05
	Hydatigera krepkogorski	17.7	1.1 ± 0.08
	Thominx aerophilus	17.7	0.8 ± 0.05
	Spirocerca arctica	17.7	1.6 ± 0.24
	Vigisospirura skrjabini	17.7	2.0 ± 0.15
	Physaloptera praeputiale	17.7	1.7 ± 0.21
	Macracanthorynchus hirudinaceus	16.1	0.8 ± 0.15
	Mesorchis denticulatus	14.5	0.9 ± 0.24
	Joyeuxiella echinorhynchoides	14.5	1.5 ± 0.31
	Echinococcus granulosus	14.5	1.7 ± 0.42
	Capillaria putorii	14.5	0.9 ± 0.05
	Ancylostoma caninum	14.5	1.1 ± 0.08
	Gongylonema pulchrum	14.5	1.7 ± 0.17
	Spirometra erinacei-europei	13.0	1.0 ± 0.08
Rare	Joyeuxiella pasqualei	8.0	0.9 ± 0.05
	Diplopylidium nőlleri	8.0	0.8 ± 0.05
	Dirofilaria repens	8.0	0.4 ± 0.12
	Moniliformis moniliformis	6.4	0.4 ± 0.22
	Taenia macrocystis	6.4	0.9 ± 0.05
	Macracanthorhynchus catulinus	4.8	0.8 ± 0.05

 

The relatively small number of helminths found in wolves, badgers and dogs is apparently associated with the composition of the food consumed by the predators and the individual characteristics of their organisms.

According to the studies, the number of helminth species varies from host to host. 75.5% of the helminth species were found in foxes, 51.0% in jungle cats, 48.0% in golden jackals, 41.5% in wolves, 38.0% in domestic dogs and 30.2% in badgers. As we can see, the largest number of species was observed in foxes, which is associated with their ecology and distribution (Table 3).

The ecological and faunistic analysis of the helminthofauna of predatory mammals was based on the helminth distribution principle proposed by Romashova et al. (2014). According to the classification of Fedorov (1986), taking into account the indicators such as prevalence and infection intensity, two groups of helminths were identified: primary and secondary species (Table 3). Primary helminth species include dominant, subdominant and intermediate species; secondary species are rare and casual ones (Romashova et al., 2014).

The helminths recorded in foxes are so diverse that, in our opinion, they are characterised by two main environmental factors: relatively large populations and ecological flexibility. The helminths found in foxes are characterised by high species diversity, high infection intensity and a wide range of trophic relations with the host.

Compared to other wild mammals, foxes in Karakalpakstan are quite numerous in either natural ecosystems or recreational and agricultural areas. Consequently, they play an important role in the circulation of infection in a number of natural foci and in ensuring the functional stability of these foci. Therefore, we have analysed helminthological material reflecting quantitative indicators of the circulation of zoonotic helminthiases. The fox is an active and vital link in this process. A significant part of the helminth species found in foxes in the study area should be considered as potential pathogens of helminthiases (T. hydatigena, T. canis, T. leonina, D. immitis, M. multiceps, E. granulosus and D. repens). The most significant of the listed helminths from the medical and veterinary aspects are E. granulosus, E. multilocularis, Toxocara canis, Toxascaris leonina Dirofilaria immitis, Dirofilaria repens and Dracunculus medinensis. Our data are consistent with the data of other researchers (María Soledad Moleón et al., 2015; Fiocchi et al., 2016; Jacek et al., 2020).

The highest prevalence was shown by 8 Nematoda species: Strongyloides vulpis (42.0%), Crenosoma vulpis (40.3%), Toxocara canis (40.3%), Toxascaris leonina (37.0%), Rictularia cahirensis (35.4%), Trichocephalus vulpis (33.8%), Spirura rytipleurites (30.6%), Toxocara mystax (30.6%). They were followed by other 12 nematode species: Rictularia affinis (24.1%), Cylicospirura subaequalis (24.1%), Uncinaria stenocephala (21.0%), Physoloptera sibirica (19.3%), Dirofilaria imittis (19.3%), Physoloptera praeputiale (17.7%), Vigisospirura skrjabini (17.7%), Thominx aerophilus (17.7%), Spirocerca arctica (17.7%), Gongylonema pulchrum (14.5%), Ancylostoma caninum (14.5%) and Capillaria putori (14.5%). Only one species – Dirofilaria repens – showed a prevalence of less than 10%.

 

Table 4: Distribution of helminths of the Jungle Cat in Karakalpakstan by dominance.

Helminth category	Helminth species	Infection indicators
		Prevalence, %	Infection intensity, individuals
Dominant	Taenia macrocystis	41.0	5.5 ± 0.62
	Joyeuxiella rossicum	38.4	3.8 ± 0.52
	Toxocara canis	38.4	24.1±1.63
	Toxascaris leonina	35.8	12.6±0.74
	Physaloptera praeputiale	33.3	3.4 ± 0.31
	Rictularia affinis	30.7	4.3 ± 0.42
Subdominant	Physaloptera sibirica	28.2	4.1 ± 0.73
	Alaria alata	28.2	2.7 ± 0.33
	Uncinaria stenocephala	28.2	4.7 ± 0.76
	Oxynema numidica	28.2	2.8 ± 0.54
	Rictularia cahirensis	28.2	4.5 ± 0.65
	Hydatigera krepkogorski	23.0	2.4 ± 0.36
	Mesocestoides lineatus	23.0	3.5 ± 0.73
	Macracanthorhynchus catulinus	23.0	2.1 ± 0.34
	Moniliformis moniliformis	23.0	1.8 ± 0.23
	Thominx aerophilus	23.0	1.6 ± 0.54
	Dioctophyma renale	23.0	2.3 ± 0.62
	Troglostrongylus bodanini	23.0	2.5 ± 0.41
	Toxocara mystax	23.0	7.8 ± 0.83
	Vigisospirura potekhini	23.0	3.7 ± 0.52
Intermediate	Diplopylidium nőlleri	20.5	3.4 ± 0.43
	Ancylostoma caninum	20.5	2.6 ± 0.34
	Spirometra _rinaceid-europei	18.4	1.6 ± 0.15
	Dipylidium caninum	18.0	4.2 ± 0.64
	Dirofilaria immitis	18.0	1.7 ± 0.26
	Dirofilaria repens	10.2	0.6 ± 0.052
Rare	Dracunculus medinensis	7.6	0.3 ± 0.043

 

Currently, the epidemiological and epizootological crisis associated with diseases caused by this group of nematodes is increasing. In particular, dirofilariasis, toxocariasis and toxocaridosis of wild animals in the coming years may form natural foci of infection in Karakalpakstan.

Trematoda showed the following prevalence: Echinochasmus perfoliatus 24.1% and Alaria alata 22.5%. Currently, the range of definitive hosts for the trematode Alaria alata is growing. The prevalence of Cestoda in wild animals varies greatly (Korol et al., 2106). High values (20-40%) were recorded in 4 species Taenia hydatigena, Multiceps multiceps, Alveococcus multilocularis and Mesocestoides lineatus. Somewhat lower prevalence (10-20%) was registered in other 5 species: Spirometra erinacei-europei, Joyeuxiella echinorhynchoides, Taena pisiformis, Hydatigera krepkogorski and Echinococcus granulosus. The Cestoda species Diplopylidium nölleri, Joyeuxiella pasqualei and Taenia macrocystis showed a prevalence of less than 10%. 3 species of Acanthocephala were recorded in wild animals. Macracanthorynchus hirudinaceus showed a prevalence of 16.1%. The prevalence of Macracanthorhynchus catulinus and Moniliformis moniliformis was 4.8% and 6.4%, respectively. The research into the helminthofauna of the Fox resulted in some completely new information complementing that in previously published works (Koshanov, 1970; Shakarboev, 2009).

 

Table 5: Distribution of helminths of the Golden Jackal in Karakalpakstan by dominance.

Helminth category	Helminth species	Infection indicators
		Prevalence, %	Infection intensity, individuals
Dominant	Toxocara canis	51.6	12.6 ± 1.1
	Toxascaris leonina	50.5	8.3 ± 0.5
	Multiceps multiceps	31.8	3.5 ± 0.4
	Toxocara mystax	30.7	4.6 ± 0.6
Subdominant	Trichocephalus vulpis	26.3	3.5 ± 0.4
	Taenia hydatigena	25.2	2.6 ± 0.2
	Mesocestoides lineatus	23.0	2.0 ± 0.1
	Rictularia affinis	23.0	1.5 ± 0.1
	Dirofilaria immitis	23.0	1.1 ± 0.08
Intermediate	Echinococcus multilocularis	20.8	2.0 ± 0.1
	Physaloptera sibirica	18.6	1.4 ± 0.08
	Dipylidium caninum	18.6	2.0 ± 0.1
	Spirometra erinacei-europei	17.5	2.1 ± 0.6
	Hydatigera taeniaformis	15.3	3.0 ± 0.18
	Taenia ovis	14.2	1.8 ± 0.04
	Echinococcus granulosus	14.2	2.3 ± 0.15
	Ancylostoma caninum	14.2	2.7 ± 0.17
	Dioctophyma renale	13.1	1.6 ± 0.54
	Joyeuxiella echinorhynchoides	12.0	1.1 ± 0.8
Rare	Plagiorchis elegans	9.8	1.4 ± 0.16
	Macracanthorhynchus catulinus	9.8	0.5 ± 0.7
	Alaria alata	8.7	1.9 ± 0.04
	Dirofilaria repens	8.7	0.3 ± 0.13
	Dracunculus medinensis	5.4	1.2 ± 0.18
	Dipetalonema sp.	1.0	0.01 ± 0.05

 

2 Cestoda species (Joyeuxiella pasqualei and Taenia ovis) and 3 Nematoda species (Capillaria putorii, Cylicospirura subaequalis and Dipetalonema sp.) were recorded for the first time in wild animals in the study area.

Thus, in anthropogenic ecosystems, zoonotic helminthiasis of foxes can play the role of an additional ecological link in the circulation of helminthiases. Only 4 dominant helminth species were recorded in the Jungle Cat (Table 4).

In the natural ecosystems of Karakalpakstan, jackals form quite a large group of predators (Palvaniyazov, 1974). Our research identified 25 helminth species in this predator (Table 5). The infection rate in the Golden Jackal in our studies is much higher compared to the data of other researchers, either in Uzbekistan (Koshanov, 1970) or in other countries (Ćirović et al., 2013).

22 helminth species were identified in wolves, of which 2 are dominant, 5 subdominant, 14 intermediate and 1 rare (Table 6). Intermediate species comprise most of the helminthofauna of wolves (63.6%). The portion of dominant and subdominant species is 31.8%.

 

Table 6: Distribution of helminths of the Wolf in Karakalpakstan by dominance.

Helminth category	Helminth species	Infection indicators
		Prevalence, %	Infection intensity, individuals
Dominant	Toxascaris leonina	34.1	8.0±1.1
	Multiceps multiceps	31.7	4.0±0.4
Subdominant	Taenia hydatigena	26.8	3.2±0.3
	Diplopylidium nőlleri	22.0	2.1±0.1
	Crenosoma vulpis	22.0	1.1±0.08
	Toxocara canis	22.0	9.8±0.9
	Rictularia cahirensis	22.0	2.1±0.1
Intermediate	Dipylidium caninum	19.5	2.6±0.2
	Taenia pisiformis	19.5	1.2±0.08
	Multiceps skrjabini	19.5	1.2±0.08
	Mesocestoides lineatus	17.0	2.0±0.1
	Macracanthorynchus hirudinaceus	17.0	1.3±0.08
	Moniliformis moniliformis	17.0	1.0±0.04
	Toxocara mystax	17.0	4.4±0.6
	Spirocerca lupi	17.0	2.3±0.1
	Echinococcus granulosus	14.6	1.7±0.1
	Uncinaria stenocephala	14.6	1.4±0.09
	Rictularia affinis	14.6	1.5±0.1
	Alaria alata	12.2	0.8±0.05
	Ancylostoma caninum	12.2	1.2±0.08
	Dirofilaria immitis	12.1	0.7±0.05
Rare	Dirofilaria repens	7.3	0.4±0.002

 

It was established that the helminthofauna of the Badger included 1 dominant, 2 subdominant, 7 intermediate and 6 rare species (Table 7). Most of the parasites in the helminthofauna of the Badger are intermediate and rare species.

Among five corsacs investigated in Samarkand region of Uzbekistan, species A. alata, T. hydatigena, T. leonina, U. stenocephala and D. caninum were found with similar levels of the infection (Young et al., 2019). All the carnivorous mammals are parasitiыed by A. alata, whose intermediate hosts are molluscs from the family Planorbidae and amphibians; their reservoir hosts are amphibians, reptiles, birds and mammals.

 

Table 7: Distribution of helminths of the Badger in Karakalpakstan by dominance.

Helminth category	Helminth species	Infection indicators
		Prevalence, %	Infection intensity, individuals
Dominant	Alaria alata	20.0	1.4 ± 0.09
Subdominant	Macracanthorhynchus catulinus	16.0	1.0 ± 0.08
	Toxocara canis	16.0	8.3 ± 0.5
Intermediate	Dipylidium caninum	12.0	2.3 ± 0.1
	Mesocestoides lineatus	12.0	1.7 ± 0.6
	Macracanthorynchus hirudinaceus	12.0	1.0 ± 0.08
	Moniliformis moniliformis	12.0	0.9 ± 0.05
	Crenosoma vulpis	12.0	1.2 ± 0.09
	Vigisospirura potekhini	12.0	1.5 ± 0.1
	Pneumospirura capsulata	12.0	1.1 ± 0.08
Rare	Spirometra erinacei-europei	8.0	0.8 ± 0.05
	Capillaria putorii	8.0	0.7 ± 0.05
	Thominx aerophilus	8.0	0.6 ± 0.05
	Ancylostoma caninum	8.0	1.1 ± 0.08
	Uncinaria stenocephala	8.0	1.0 ± 0.08
	Physaloptera sibirica	8.0	1.3 ± 0.09

 

CONCLUSIONs and Recommendations

Our studies identified 53 species of helminths in the predatory mammals of Karakalpakstan. Their distribution across the studied mammal species is the following: 16 species of parasitic worms were recorded in badgers, 22 in wolves, 25 in jackals, 27 in jungle cats and 40 in foxes. Most species and groups parasitise in the digestive system and occur as mixed infections.

A number of species (A. alata, M. lineatus and T. canis) were found to be common in all the studied host predators. The species S. lupi and M. skrjabini were recorded only in wolves, G. pulchrum, V. skrjabini, S. arctica, C. subaequalis, S. rytipleurites, M. denticulatus, Ech. perfoliatus and J. pasqualei only in foxes, Dipetalonema sp. and H. taeniaformis only in jackals, O. numidica, T. bodanini and J. rossicum only in jungle cats, and P. capsulata was found only in badgers.

The helminth fauna of foxes is very diverse in species composition (40 species). This is probably associated with the animal’s ecology, population stability and trophic relationships.

Among the helminth species we have identified, some are important from the epidemiological and epizootological aspects. It is quite probable that wild and domestic predators exchange helminths. The overall helminthological situation in predatory mammals indicates the need for systematic monitoring and a complex of anti-helminthic measures.

ACKNOWLEDGEMENTS

The work was carried out within the framework of the program “Ways of the Development of Helminth Fauna in Vertebrates, Taxonomy and Improvement of Control Measures” implemented by the Academy of Sciences of the Republic of Uzbekistan. We express our gratitude to Academician D. A. Azimov and Professor F. D. Akramova for their help in the morphological identification of helminth species.

Novelty Statement

For the first time, the current state of wild animal helminths on the territory of Karakalpakstan was analyzed, 53 species were registered, belonging to 3 types, 4 classes, 13 genera, 25 families, 39 genera, of which 44 species belong to biohelminths and 9 species geohelminths;

Author’s Contribution

Materials was collected, morphological study and performed statistical analysis of data by Abat Berdibaev. Identification of species, analysis of collected materials and preparation of manuscripts of articles was carried out by Erkinjon Shakarboev. Both author read and approved the manuscript.

Conflict of interest

The authors have declared no conflict of interest.

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