Morphological and ecological features of some nematodes of the genus Rhabdochona in marinka obtained from Fergana Valley, Uzbekistan

Abstract

The aim is to study the morphological and ecological features of some nematode species of the genus Rhabdochona parasites of marinka fish in the Fergana Valley, Uzbekistan. Rhabdochona gnedini, Rhabdochona denudata and Rhabdochona hellichi turkestanica were detected as 5.3%, 7.9% and 3.7%, respectively. According to the Authors’ knowledge, Rh. hellichi turkestanica was recorded in Uzbekistan and Central Asian republics for the first time. Rhabdochona spp. were only detected in the intestine of marinkas lived in the mountain rivers Rezaksay, Chodaksay and small tributaries of the Syrdarya river in western Fergana. The prevalence of Rhabdochona spp. in the marinka can be associated with a wide range of nutrition in the mountain rivers and small tributaries of the Syrdarya river, where it could eat large numbers of mayfly and caddis larvae that act as intermediate hosts of rhabdochona.

Introduction

Among the 87 fish species currently registered in the ichthyofauna of Uzbekistan, more than 26 species are of commercial importance, of which the common marinka is of particular interest (Mukhamediev 1982). As a typical representative of the Mountainous Asian complex of ichthyofauna, marinka is widespread in the mountain rivers of the upper reaches of the Syrdarya (Mukhamediev 1982). The results of recent studies have established that the common marinka (Schizothorax intermedius) living in the mountain rivers of the Fergana Valley is genetically identical to the morphology of Schizothorax eurystomus which regularly mentioned by scientists since 1872, but there is need a still considerable amount of identification works to prove this similarity. Among the river forms of the marinka fished from the Isfairamsay river, there are also individuals with traits of lake fish living in places with more diverse feeding conditions, which indicates a high morpho-ecological variability of the species (Mukhamediev 1982). In this regard, it should be noted that as a result of anthropogenic impact, the river flow of the region decreased somewhat, which in turn caused negative changes in aquatic ecosystems, primarily expressed in an unfavourable epizootic situation and significant economic damage from the effects of parasites and fish diseases, as well as in a dangerous factor for human health (Karimov 2007).

Some authors previously studied the parasite fauna of reservoirs in the middle reaches and the lower reaches of the Syrdarya river and reported 35 to 128 species of parasites in fish (Osmanov 1971; Karaev 1994; Karimov 2007; Safarova 2017). Karimov (2007) reported 36 species of parasites, of which 10 species belong to myxosporidia, 7 to ciliates, 11 to trematodes, 4 to nematodes, 2 to cestodes, and 2 to acanthocephalans in marinka sampled in the water bodies of the Fergana Valley. The other researcher found 13 helminth species in common marinka lived in various types of water bodies in the northeast of Uzbekistan (Safarova 2017).

The genus Rhabdochona belong to the order Spirurida, Nematoda (Anderson 2000). The genus Rhabdochona includes a large number of species that parasitize freshwater fish in the world (Moravec 2010; González Solís and Chavan 2014). Eight species of this genus were detected previously in freshwater fish that lived in Uzbekistan (Akramova et al. 2019). These parasites have been reported from marinka (Safarova 2017; Karimov 2007). Rhabdochona denudata and Rhabdocona gnedini are recorded from common marinka in the middle reaches of the Syrdarya river in Uzbekistan (Safarova 2017). Rhabdocona denudata and Rhabdocona heillichi are also reported from the waterbodies of Northern Tajikistan (Karimov 2007).

Marinka is a very popular species for local fishing in Uzbekistan. The helminth fauna of marinka that lived in the Fergana Valley has been studied extremely insufficiently. The available data is fragmentary. The study aims to examine the prevalence of nematode species of the genus Rhabdochona in common marinkas lived in the Fergana Valley of Uzbekistan. Moreover morphological and ecological features were studied.

Material and methods

Marinka (n:185) was sampled a period between April 2018 and October 2020 from three different regions including the mountain rivers and small tributaries of the Syrdarya (40° 17′ 85″ north latitude, 71° 58′ 44″ east longitude), the mountain rivers Isfairamsay, Sokh, Shakhimardansay located in the south of the Fergana Valley (former tributaries of the Syrdarya) and the mountain rivers Chodaksay and Rezaksay located in the north of the valley (Fig. 1). The sampling period was intensive post-spawning feeding time of the marinka, which characterized by the highest probability of infection fish helminths.

Fig. 1.

Map of the water reservoirs of the Fergana Valley. Mountain rivers: I—Chodaksay, Rezaksay; III—Sokh; IV—Isfayramsay; V—Shohimardansay; II—Western Fergana: Syrdarya river and adjacent reservoirs

The fish necropsy was performed according to Bykhovskaya-Pavlovskaya (1985). Simultaneously with the examination of the intestinal tract, a thorough examination of the body cavity and other organs and systems of fish were carried out. The nematodes were obtained from the intestines and then fixed in 2% formalin solution and hot ethyl alcohol (70%). They were examined using a light microscope (ML 2000, Meiji Techno Japan). The parasite pictures were drawn with a drawing apparatus RA-5 in the Laboratory of General Parasitology of the Institute of Zoology of the Academy of Sciences of the Republic of Uzbekistan. The monographs were used to determine the species of parasites (Agapova 1962; Chubb 1982; Vismanis et al. 1987).

Results

Three species of the genus Rhabdochona (Rhabdochona gnedini Skrjabin, 1946, Rh. denudata Dujardin, 1845, and Rh. hellichi turkestanica Skrjabin, 1917) were only observed in the intestine of the marinkas (n:8) sampled from the mountain rivers Rezaksay, Chodaksay and small tributaries of the Syrdarya river in western Fergana.

Rhabdochona gnedini was found in marinkas sampled from the small tributaries of the Syrdarya of western of Fergana (5.3%) and the river of Rezaksay (3.0%) for the first time in the present study (Table 1). The number of Rh. gnedini per fish was higher in Syrdarya than that of Rezeksay (8 ± 0.4 vs. 2 ± 0.1). The ratio of females to males is 1:2 on average. Rhabdochona denudata was observed in small tributaries of the Syrdarya of western Fergana (7.9%). The number of Rh. denudata per fish was 16 ± 0.8. The ratio of infected males to females fish averages 1:3. Rhabdochona hellichi turkestanica was detected in fish sampled from the tributaries of the Syrdarya in the western of Fergana (3.7%) and the mountain river Chodaksay in the northern part of the valley (2.0%). The number of Rh. hellichi turkestanica per fish was closer in Syrdarya with the Chodaksay river (3 ± 0.2 vs. 3 ± 01). The ratio of females to males is 1:2 on average. The total infection of marinkas by Rhabdochona species is a ranged from 3.0 to 7.9%, and the nematode intensity in fish ranged from 1 to 21 individuals, respectively (Table 1). The prevalence of Rhabdochona spp. associated with a wide range of nutrition of the marinkas in the mountain rivers and small tributaries of the Syrdarya River. Marinkas can easily eat large numbers of mayfly and caddis larvae that act as intermediate hosts of Rhabdochona spp. in these rivers.

Table 1.

Prevalence of Rhabdochona nematodes collected from Schizothorax eurystomus in the upper of the Syrdarya river, Fergana Valley

Species	Number	Prevalence (%)	Intensity (mean)	Location
Rhabdochona gnedini	38	2 (5.3)	1–15 (8)	Small tributaries*
	33	1 (3.0)	1–4 (2)	Rezaksay
Rhabdochona denudata	38	3 (7.9)	5–21 (16)	Small tributaries
Rhabdochona hellichi turkestanica	27	1 (3.7)	1–5 (3)	Small tributaries
	49	1 (2.0)	1–3 (2)	Chodaksay
Total	185	8 (4.8)	1–21 (6.2)	–

^*Small tributaries—the map indicate as Western Fergana: Syrdarya river and adjacent reservoirs

Some morphological characteristics and measurements of the Rhabdochona species shown in below and in Table 1.

The morphological characters of Rhabdochona gnedini Skrjabin, 1946 as follows: the body was small and covered with a smooth cuticle. The tail was ended conical in shape either with a sharp point or rounded. The cervical papillae were medium in size. The parasite possess one pair lateral preanal papillae. The distal end of the long spicula was bluntly ended (Fig. 2).

Fig. 2.

Rhabdochona gnedini: a anterior end of the male; b posterior end of the female; c posterior end of the male (original)

The morphological characters of Rhabdochona denudata Dujardin, 1845 as follows: The body was tapered at both ends. The cuticle was smooth. The distal end of the spicule possess a tooth-like extension. The number of pairs of preanal papillae was between 9 and 13 (Table 2; Fig. 3).

Table 2.

Morphological characters of Rhabdochona species

Morphological criteria (mm)	Rhabdochona gnedini (n = 6)		Rhabdochona denudata (n = 6)		Rhabdochona hellichi turkestanica (n = 3)
	♂	♀	♂	♀	♂	♀
Body length	7.8 ± 1.1	16.8 ± 1.2	4 ± 0.2	13.5 ± 0.5	10.45 ± 0.4	13.3 ± 0.4
	5.8–9.8	12.2–21.4	3–5	12–15	9.4–11.5	11.2–15.4
Body width	0.1 ± 0.01	0.24 ± 0.04	0.11 ± 0.02	0.22 ± 0.03	0.15 ± 0.02	0.24 ± 0.03
	0.08–0.12	0.18–0.30	0.1–0.12	0.20–0.25	0.14–0.16	0.21–0.28
Prostom length	0.025 ± 0.002	0.035 ± 0.003	0.016 ± 0.001	0.025 ± 0.002	0.024 ± 0.002	0.028 ± 0.002
	0.02–0.03	0.03–0.04	0.015–0.018	0.02–0.03	0.021–0.027	0.026–0.035
Prostom wide	0.016 ± 0.001	0.025 ± 0.002	0.011 ± 0.001	0.015 ± 0.001	0.016 ± 0.001	0.021 ± 0.002
	0.015–0.018	0.02–0.03	0.01–0.012	0.01–0.02	0.015–0.018	0.018–0.024
Esophagus length (muscular)	0.36 ± 0.02	0.43 ± 0.02	0.21 ± 0.01	0.30 ± 0.02	0.33 ± 0.01	0.40 ± 0.03
	0.30–0.42	0.38–0.48	0.16–0.26	0.20–0.40	0.33–0.34	0.34–0.47
Esophagus length (granular)	3.5 ± 06	5.2 ± 0.5	1.8 ± 0.3	2.8 ± 0.3	3.3 ± 0.3	3.4 ± 0.3
	2.8–4.2	4.2–6.2	1.5–2.0	2.2–3.4	3.1–3.5	3.1–3.8
Nerve ring*	0.24 ± 0.03	0.22 ± 0.02	0.18 ± 0.03	0.18 ± 0.03	0.19 ± 0.03	0.21 ± 0.02
	0.20–0.28	0.20–0.24	0.16–0.21	0.16–0.21	0.18–0.21	0.20–0.23
Excretory pore*	0.3 ± 0.02	0.28 ± 0.01	0.22 ± 0.02	0.2 ± 0.03	0.27 ± 0.02	0.33 ± 0.01
	0.26–0.34	.26–0.30	0.16–0.28	0.13–0.27	0.22–0.32	0.32–0.34
Preanal papillae	8 ± 0.2		11 ± 0.3		9 ± 0.2
	7–9	–	9–13	–	7–9	–
Spicule length (left)	0.58 ± 0.02		0.28 ± 0.04		0.52 ± 0.02
	0.48–0.68	–	0.19–0.38	–	0.50–0.54	–
Spicule length (right)	0.012 ± 0.001		0.1 ± 0.02		0.13 ± 0.02
	0.010–0.015	–	0.09–0.11	–	0.13–0.14	–
Vulva length*		8.1 ± 0.8		7.8 ± 0.7		7.0 ± 0.4
	–	5.20–11.0	–	5.10–10.6	–	6.3–7.8
Tail length	0.36 ± 0.04	0.29 ± 0.03	0.26 ± 0.04	0.21 ± 0.02	0.41 ± 0.03	0.28 ± 0.04
	0.32–0.40	0.26–0.32	0.32–0.40	0.20–0.22	0.39–0.43	0.24–0.32

^*Measurements are from anterior extremity

Fig. 3.

Rhabdochona denudata: a anterior end of the male; b posterior end of the female; c posterior end of the male (original)

The morphological characters of Rhabdochona hellichi turkestanica Skrjabin, 1917 as follows: they were medium-sized nematodes. Prostom funnel-shaped and small basal prostomal teeth were visible in lateral view. The tail of both sexes was ended with a sharply pointed tip (Fig. 4).

Fig. 4.

Rhabdochona hellichi turkestanica: a anterior end of the male; b posterior end of the female; c posterior end of the male (original)

Discussion

The marinka is a polyphage fish that consumes both plant and some animals (among which there is small trash fish) as food in different seasons of the year. This feeding activity contributes to high infection of the fish with helminth species, especially during the period of post-spawning fish feeding (Najmiddinov et al. 2020). The marinka as a typical representative of the Mountainous Asian complex of ichthyofauna lives in a considerably wide area from the extreme western border of the mountains in northern Iran, the Alay-Turkestan mountains in the Fergana Valley to the Western Tien Shan, which stretches quite far to the east and is directly interconnected with the Himalayas, Tibet (Osmanov 1971). At the same time, these fish species is accepted as the main carrier of the parazitofauna of fish (Osmanov 1971).

In our study, Rh. gnedini, Rh denudata and Rh. hellichi turkestanica were observed in the intestine of the common marinkas sampled in Vergana Valley. The results of the present study were similar to Karimov (2007), who noted a significantly high infection rate of marinka with Rabdochona denudata, Rh. gnedini and Rh. chellichi in the river Isfara, Tajikistan. Rhabdochona hellichi occurs in mountain rivers, lakes and some foothill reservoirs in the Central Asia region (Karimov 2007). At the same time, it should be noted the presence of some morphs and geographical races of the indicated helminth, the distribution area of which is much wider. Rh. hellichi turkestanica reported from fish lived in Indian water bodies, as well as the morphologically close subspecies Rh. hellichi kurdistanensis is found in the local subspecies of the barbel in Iraq (Moravec et al. 2010, 2012).

Moravec et al. (2010) reported that Rh. hellichi turkestanica were found in Schizothorax spp. (Cyprinidae, Cypriniformes), Rh. hospeti in Tor spp. (Cyprinidae) and Rh. mazeedi in Clupisoma garua in India. They are carried out light and electron microscopic analysis made it possible to reveal new, previously unknown morphological and taxonomic characters and made it possible to describe this species again in more detail (Moravec et al. 2010). Rh.hellichi turkestanica (synonym R. denudata filamentosa, R. kashmirensis, R. schizothoracis) was considered as a subspecies different from another typical subspecies R. hellichi hellichi mainly in the shape of the distal end of the left spicule, in molecular characteristics and geographic distribution. The morphology of the aforementioned form of Rhabdochona hardly differs from those of the original subspecies Rhabdochona hellichi Raillet 1916. In the present study, Rh.hellichi turkestanica was observed as a medium-sizes nematode, the body of the parasite was narrowed at both ends. The cuticle was smooth. At the caudal end, the female parasites have a ring-shaped formation, the edges of which were dotted with spines. The lips were poorly developed, barely visible. The oral capsule was funnel-shaped. Very small cervical papillae were normal in shape. The tail of both sexes was conical in shape with a sharply pointed tip. Thus, the Rhabdochona species we have characterized differ from each other in several morphologic characters, including the size of the body and spicule, the shape of the tail and eggs (Table 2).

Marinka lives in all surveyed mountain rivers and the Syrdarya river and adjacent water bodies of Western Fergana. However, the parasites were observed only sampled in the mountain rivers Rezaksay, Chodaksay and small tributaries of the Syrdarya river in western Fergana in the present study. The main factors of fish infectivity with a parasite in the upper reaches of the Syrdarya river are the rich hydrofauna and a wide range of fish nutrition. The marinka can infect parasites by eating small trash fish and mayfly larvae that act as intermediate host of these parasites (Karimov 2007). This is supported by the results of Stein (1959), who claimed a relationship between the increase in the content of dissolved oxygen in the water and a strong infestation of mayfly larvae with larvae of Rhabdochona spp. The development of Rhabdochona spp. is similar to each other. Mayflies of the genera Heptagenia, Ephemerella (Stein 1959) or larvae of Hydropsyche (Trichoptera) play a role as intermediate hosts in the life cycle of Rhabdochona denudata (Vojtkova 1971). Further, considering the reasons why marinkas are infected with parasites, it is suggested some opinion such as the adaptation of Rhabdochona spp. to the fast flow and low temperature of the water of mountain rivers that included the relatively poor composition of animal species as food, for this reason, marinkas switches to feeding benthic, thus they can easily swallow larvae of Rhabdochona spp. (Karimov 2007). The flow rate is the leading factor in the formation of ichthyofauna and ichthyoparasite fauna of mountain rivers (Mukhamediev 1982). For example, the first noted subspecies Rhadochona hellichi turkestanica was detected in the common marinka Schizothorax eurystomus (family Cyprinidae) lived in the mountain rivers of the Fergana Valley in the present while, Rhadocona chodukini is reported in Aral and Turkestan barbels sampled from the Aral Sea basin (Osmanov 1971). Rhadochona hellichi Sramek is common in barbels (Cyprinidae) in the rivers of the Czech Republic (Scholz 1995). Rhadochona hellichi turkestanica is recorded from marinkas sampled in rivers, streams, lakes and ponds of the plains and foothills of Asia, in particular in India and from some local catfish species (Siluridae) in Pakistan (Moravec et al. 2010). Rhabdochona kurdistanensis parasitizes local subspecies of the barbel, as well as the Mesopotamian sucker catfish in northern Iraq (Moravec et al. 2012). Consequently, Rhabdochona spp prefer mainly rheophilic species (like as Cyprinidae) and habitat is the determining factor of the host selection. As noted above, numerous mayflies and larvae of the other aquatic insects are the intermediate hosts of rhabdochon in the water bodies of the Fergana Valley, which are intensively consumed by the marinkas during the post-spawning feeding period. In late spring-early summer (the sampled season of this study), the water temperature (+ 16–21 °C) becomes favourable for the reproduction of large numbers of aquatic insects in the water bodies of the Fergana Valley. Many insect species and their larvae can often be infected with nematode larvae in the water bodies in the Valley. The marinka, as a euryphagous species, with its characteristic mobility, actively searches for food. In the present study, more than 85% of the intestinal contents of the marinkas (total body size between 19.8 and 29.5 cm), necropsied during the above-mentioned period, were consisted of fragments of insects and small fish, the remaining part consisted of the pieces of plants eaten by the fish. The prevalence of Rhabdochona spp. in the marinka can be associated with a wide range of nutrition in the mountain rivers and small tributaries of the Syrdarya River, where it could eat large numbers of mayfly and caddis larvae that act as intermediate hosts of rhabdochon biology. The prevalence of Rhabdochona spp. in the marinka is associated with the presence or absence of mayfly and caddis larvae in the river. In the present study, it was pointed out that some abiotic factors such as the flow rate, water temperature and high content of dissolved oxygen in it, as well as the nutritional characteristics of the common marinka can be the most important factors to the distribution of Rh.denudata, Rh. gnedini, Rh. hellichi turkestanica in marinkas from mountain rivers of the Fergana Valley.

In conclusion, the marinka population sampled from the mountain rivers Rezaksay, Chodaksay and small tributaries of the Syrdarya river in western Fergana were infected with Rh.denudata, Rh. gnedini and Rh. hellichi turkestanica. According to the Authors’ knowledge, Rh. hellichi turkestanica was recorded in Uzbekistan and Central Asian republics for the first time. The prevalence of Rhabdochona spp. in the marinka can be associated with a wide range of nutrition in the mountain rivers and small tributaries of the Syrdarya River, where it could eat large numbers of mayfly and caddis larvae that act as intermediate hosts of rhabdochon biology. The flow rate, water temperature and high content of dissolved oxygen in rivers, and the nutritional characteristics of the marinka can be responsible for the infection. The ecological properties of marinkas in Fergana Valley and abiotic factors affecting the distribution of fish nematodes should be clarified in the future.

Authors contributions

The study was designed by AEK. Materials was collected by EKhN and RRK. Original draft was written by AEK, AMM and KY. EKhN performed statistical analysis of data. All authors read and approved the final manuscript.

Declarations

Conflict of interest

There are no conflicts of interest in our present study.