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Research Article
Gastrointestinal helminths of small mammals (Rodentia and Carnivora) in the vicinity of Usholta, Georgia
expand article infoKetevan Nikolaishvili, Tsitsino Lomidze, Lela Arabuli, Ketevan Asatiani, Lali Murvanidze
‡ Ilia State University, Tbilisi, Georgia
Open Access

Abstract

In this study, we investigated the gastrointestinal helminth fauna of small mammals in the highland region of Usholta (Racha, Western Georgia). In total, 19 specimens of small mammals were examined, of which 10 gastrointestinal helminth species were detected. Five out of eight specimens of Apodemus uralensis were infected with three nematode species: Heligmosomoides polygyrus, Syphacia obvelata, and Trichuris muris. Notably, the liver of a single individual of A. uralensis was also infected with cestode—Echinococcus multilocularis, (larvocysts) —a novel host record for this parasite in Georgia. All eight exeminated Microtus daghestanicus specimens were infected with both cestode (Paranoplocephala omphalodes and Rodentolepis asymmetrica) and nematode (Heligmosomum costellatum and Syphacia sp.) parasites. Similarly, all three exeminied specimens of Mustela nivalis were infected with cestodes (Versteria mustelae) and nematodes (Molineus patens, Syphacia sp.). For Syphacia sp., M. nivalis is a new host record in Georgia. Only one specimen of A. uralensis was simultaneously infected by two species of nematodes (Syphacia sp., T. muris) and also a single individual of M. nivalis was infected with three species of helminths (V. mustelae, M. patens, Syphacia sp.). This study provides valuable insights into the helminth diversity and host-parasite relationships in the region, highlighting the importance of continued research on wildlife parasites.

Key words

Caucasus, Cestoda, host, life cycle, Nematoda, parasite

Introduction

Gastrointestinal helminths (GH) are one of the main groups of parasites found in small mammals and represent a significant economic concern, causing parasitic diseases in humans and animals (Han et al. 2015; Ranjbar et al. 2017). Good knowledge on the distribution and diversity of GH, their hosts, host-parasite interactions, and the possible ways of transmission to humans and livestock is crucially important for the prevention of parasitic diseases (Hamzavi et al. 2024). Additionally, GH represent a significant part of biodiversity, and their role in ecosystem functioning cannot be underestimated. Thus, acquiring the primary data on GH diversity and their hosts at a local to global scale is of primary importance (Aloyan 1956; Shakhtakhtinskaya et al. 1970; Manasyan 1985; Shimalov and Shimalov 2001; Nakao et al. 2010; Miller et al. 2016; Lucio et al. 2021; Khan et al. 2022; Haukisalmi et al. 2024; Kirillova et al. 2024). In Georgia, the study on the GH of small mammals was conducted in the second half of the last century by Kirshenblat (1948), Rodonaia (1951, 1966, 1971), Matsaberidze (1966a, 1976), and Kurashvili et al. (1989). In the recent years, only a single paper was published reporting the infestation of mole-rat Nannospalax xanthodon by a cestode — Paranoplocephala (Nikolaishvili et al. 2022). Thus, the data on the diversity of GH of small mammals in Georgia is scarce.

The vicinity of Usholta (Racha-Lechkhumi-Lower Svaneti region) is one of the unexplored parts of the Georgian highlands in terms of GH. The aim of this research is to study the GH fauna of small mammals and find out possible ecological connections between the identified parasites and their hosts in a given geographical locality.

Materials and methods

Study area

Usholta (N42°29'59", E43°24'07") and its surroundings are located within the Oni Municipality in Western Georgia on the border of forest and subalpine landscape zones (Ukleba 1981) (Fig. 1 A, B). The region is rich with fauna, with records of around 42 species of mammals (Bukhnikashvili et al. 2023).

Figure 1. 

Map (A) and the view (B) of Usholta area, Georgia.

Examination of small mammals for helminthes

A total of 19 specimens of small mammals were collected in 2022, including eight specimens of lesser wood mice Apodemus uralensis (family Muridae), eight specimens of Daghestan voles Microtus daghestanicus (family Cricetidae), and three specimens of common weasels Mustela nivalis (family Mustelidae). For each specimen, the gastrointestinal tract and related organs were examined for GH. To assess the species diversity of the host helminth fauna and their infestation rates, wherever possible, the following parasitological indicators (the prevalence; mI—mean intensity of infestation (specimen); the R—parasitation range; mA—mean abundance) were calculated according to Bush et al. (1997), Anikanova et al. (2007), and Dege et al. (2019). The cestodes were washed in water and fixed in 70° alcohol; a glycerin and lactic acid equal mixture was used to achieve the temporary transparency of the samples. Permanent preparations were stained in aceto-carmine, dehydrated in an ascending alcohol series, and mounted in Canada balsam (Fried and Manger 1992). The nematodes were washed in water and fixed in 70° alcohol, and lactic acid and glycerin in equal volumes were used for transparency. A morphological and morphometric study of the material was carried out using a stereomicroscope (Omax AC 100-240 V) with dual lights and a 10 MP USB digital camera. Helminths were identified according to key features (Abuladze 1964; Matsaberidze 1976; Ryzhikov et al. 1978, 1979; Kurashvili et al. 1989). The material is stored in the collection of the Institute of Zoology, Ilia State University.

Results

Five out of eight specimens of Apodemus uralensis were infected with one or more helmints, while maximum infestation was observed in Microtus daghestanicus (all eight specimens) and three Mustela nivalis (all three specimens). Ten species of GH (Cestoda and Nematoda) were recorded. There were 4 species of cestodes: Paranoplocephala omphalodes (Hermann, 1783) (Anoplocephalidae), Versteria mustelae (Gmelin, 1790) = (Taenia tenuicollis = Taenia mustelae), Echinococcus (=Alveococcus) multilocularis, larvae (Leuckart, 1863) (Taeniidae), and Rodentolepis asymmetrica (Janicki, 1904) (Hymenolepididae); six species of nematodes: Heligmosomoides polygyrus (Dujardin, 1845), Heligmosomum costellatum (Dujardin, 1845) (Heligmosomidae), Syphacia obvelata (Rudolphi, 1802), Syphacia sp. (Oxyuridae), Trichuris muris (Schrank, 1788) (Trichuridae), Molineus patens (Dujardin, 1845) (Molineidae) (Table 1).

Table 1.

Distribution of cestodes and nematodes in small mammals in the vicinity of Usholta.

Gastrointestinal helmints Hosts
Apodemus uralensis Microtus daghestanicus Mustela nivalis
Cestoda
Paranoplocephala omphalodes +
Versteria mustelae +
Rodentolepis asymmetrica +
Echinococcus multilocularis , larvae +
Nematoda
Heligmosomoides polygyrus +
Heligmosomum costellatum +
Syphacia obvelata +
Syphacia sp. + +
Trichuris muris +
Molineus patens +

The prevalence, infestation intensity, infestation ranges, and mean abundance of parasites are given in Table 2. Noteworthy, Syphacia sp. and M. patens have the highest prevalence in M. nivalis (both with prevalence 2/3), followed by H. polygyrus in A. uralensis and R. asymmetrica in M. daghestanicus, both with prevalence 3/8. The rest of the helminths have been detected only in single-host specimens. It was noted that one A. uralensis had numerous larvocysts of E. multilocularis on the liver (around 60 vesicles 1-3 mm in size) (Fig. 2; Table 2). Only one specimen of A. uralensis was simultaneously infected by two species of nematodes (Syphacia sp., T. muris), and also a single individual of M. nivalis was infected with three species of helminths (V. mustelae, M. patens, and Syphacia sp.).

Figure 2. 

Echinococcus multilocularis , larvocysts in Apodemus uralensis collected in Usholta, Georgia.

Table 2.

Qualitative and quantitative helminths structure of the small mammals (Rodentia and Carnivora) in the vicinity of Usholta (Georgia). N – number of parasitized hosts; P – prevalence; R – parasititation range; mI – mean intensity; mA – mean abundance.

Helminths Hosts
Apodemus uralensis (n=8) Microtus daghestanicus (n=8) Mustela nivalis (n=3)
N P R mI mA N P R mI mA N P R mI mA
Cestoda
Paranoplocephala omphalodes 1 1/8 1 1 0.125
Versteria mustelae 1 1/3 3 3 1
Rodentolepis asymmetrica 3 3/8 1–4 2.0 0.75
Alveococcus multilocularis , larvae 1
Nematoda
Heligmosomoides polygyrus 3 3/8 3–39 18 6.75
Heligmosomum costellatum 1 1/8 2.0 2.0 0.25
Syphacia obvelata 1 1/8 66 66 8.25
Syphacia sp. 1 1/8 158 158 19.75 2 2/3 10–17 13.5 9
Trichuris muris 1 1/8 2.0 2.0 0.25
Molineus patens 2 2/3 1–18 9.5 6.33

Discussion

The overall infection rate with gastrointestinal helminths in 19 examined animals was quite high – 84.2%, despite the fact that in the vicinity of Usholta, the summer period (July 2022) was characterized by a low number of rodents and a limited species composition (personal note by A. Bukhnikashvili). Microtus daghestanicus and Mustela nivalis stood out with a higher infestation rate. Ten species of helminths were identified in the examined small mammals. Various environmental factors (type of food, soil-related lifestyle, and others) are supposedly involved in the formation of the helminth fauna of rodents, which act as definitive, intermediate, and reservoir hosts of helminths and are vectors of a number of zoonotic diseases (Kurashvili 1961; Matsaberidze 1966a, 1976; Kennedy 1978; Kirillova and Kirillov 2008; Ranjbar et al. 2017; Lucio et al. 2021; Khan et al. 2022; Jouet et al., 2023).

The infection rate of Apodemus uralensis was 5/8. Similarly, Matsaberidze (1966a) indicates the infestation of wood mice in eastern Georgia at 57%. In the vicinity of Usholta, A. uralensis was not distinguished by the species diversity of helminths, especially cestodes. Manasyan (1985) explains the presence of a small number of cestode species in wood mice A. sylvaticus in Armenia by the predominance of green food in nutrition. This limits the possibility of eating intermediate hosts of cestodes. We agree with the conclusion of Manasyan (1985), and the presence of Echinococcus multiloсularis larvae in the liver of A. uralensis as an intermediate host is most probably due to local environmental conditions and food sources. It should be noted that the larval stage of Echinococcus differs from the strobilar stage in its wide distribution and exceptional pathogenicity (Ginetsinskaya and Dobrovolsky 1978).

Mouse-like rodents, usually voles, serve as the main intermediate hosts of E. multiloсularis larvae (Kirillova and Kirillov 2008; Nakao et al. 2010; Miller et al. 2016). In Georgia, the first occurrence of the larval form of Echinococcus in the social vole Microtus socialis was registered by Kurashvili (1961). Then Matsaberidze (1966, 1966a, 1976) discovered it in the liver of the mountain voles M. roberti in the forest, subalpine, and alpine zones of Eastern Georgia. There is data in the literature where, along with voles, different species of wood mice were studied on E. multiloсularis (Stieger et al. 2002; Barabási et al. 2011; Miller et al. 2016). Kirillova and Kirillov (2008) found E. multiloсularis larvae in the liver of both the common vole M. arvalis and the field mouse A. agrarius on the territory of the Mordovinsk floodplain of Samarskaya Luka (Russia). The infestation rate was 1.3% for M. arvalis and 1.2% for A. agrarius (Kirillov and Kirillova 2017). Larvocysts of E. multilocularis have not been found in the genus Apodemus in Georgia. According to our data, A. uralensis in the vicinity of Usholta turned out to be a new host of E. multilocularis in Georgia. This fact deserves attention; it allows us to predict the spread of such a dangerous helminth, both among the known intermediate hosts inhabiting this zone – from Rodentia, and for its final hosts – Canidae.

Nematodes in A. uralensis are presented with three species: Heligmosomoides polygyrus (Dujardin, 1845), Trichuris muris (Schrank, 1788), and Syphacia obvelata (Rudolphi, 1802) (Tables 1 and 2). They are obligate widespread parasites of rodents and were recorded in different regions of Georgia by Kirshenblat (1938, 1948), Matsaberidze (1966, 1966a), and in the adjacent republics of the South Caucasus (Aloyan 1956; Shakhtakhtinskaya et al. 1970; Manasyan 1985). According to Matsaberidze (1976), H. polygyrus in Georgia was found in wood mice (4.2%) in the zone of steppes and semi-desert vegetation. In the vicinity of Usholta, H. polygyrus turned out to be the dominant nematode with a prevalence of 3/8. T. muris is a rather widespread parasite. Infestation varies in a wide range. It most often infected wood mice in Georgia (Kirshenblat 1938, 1948; Rodonaia 1956, 1966; Matsaberidze 1966, 1966a, 1976; Kurashvili et al. 1989). Matsaberidze (1966) recorded it in forest, subalpine, and alpine zones. In our study area, two specimens of T. muris were found in only one A. uralensis and had the lowest mA (0.25) compared to H. polygyrus (mA = 6.75) and S. obvelata (mA = 8.25) (Table 2). Sixty-six specimens of the latter were found in the cecum of one individual of A. uralensis. A similar abundance (1-300) of S. obvelata in the gastrointestinal tract of rodents was recorded by Matsaberidze (1966a) in the forest, subalpine, and alpine zones of Eastern Georgia, to which our data fits well.

From cestodes, Paranoplocephala omphalodes and Rodentolepis asymmetrica were detected in M. daghestanicus, with much higher prevalence of the latter. These species of cestodes were discovered by Kirshenblat (1948) in the Daghestan vole in the forest zone at 1040 m a.s.l. (village Ermani, Dzhava region). Both cestodes are obligate parasites of rodents (Kurashvili et al. 1989) and were recorded several times in Transcaucasia (Kirshenblat 1948; Akhumyan 1956; Matsaberidze 1966a, 1976; Tarzhimanova 1970). In Georgia, these helminths are revealed in Microtus arvalis, M. socialis goriensis, Pitymys majori, and Chionomys roberti on the northern slopes of the Trialeti Range. According to Kirshenblat (1938, 1948), P. omphalodes is distributed mainly in alpine meadows, in the high-mountain steppe, and in forest zones. Matsaberidze (1966a) found P. omphalodes both in the zone of steppes and semi-desert vegetation and in forest, subalpine, and alpine zones, where armored and thyroglyphoid mites (participating in the biological cycle of helminth development) are widely represented. As noted by Kirillova and Kirillov (2008), infection with most adult forms of cestodes, including P. omphalodes, occurs through accidental eating, along with grassy food or digging holes, of small invertebrates (soil mites, springtails) – intermediate hosts of helminths. We discovered P. omphalodes at the border of the forest and subalps in the vicinity of Usholta. Since M. daghestanicus is an herbivore that mainly eats any part of the plants above the soil, we believe that a similar process of feeding and invasion occurs in the case of P. omphalodes.

A single species of cestode, Versteria mustelae, was found in M. nivalis in the area around Usholta. M. nivalis is widely distributed in the forest and subalpine landscape zones of Georgia, reaching a height of up to 3000 m a.s.l. (Janashvili 1963; Shidlovsky 1964). In M. nivalis studied in various regions of Georgia, Rodonaia (1951) discovered the cestode Taenia sp. in M. nivalis, and based on the descriptions of Petrov (1941) and Abuladze (1964), it was classified by her as a species – Taenia tenuicollis (now a synonym of V. mustelae) (Rodonaia 1971). Bagnato et al. (2022) believe that all new species of the genus Versteria are potential “zoonotics”. We also consider that the cestode V. mustelae, which we found in M. nivalis in the vicinity of Usholta, can also become a source of zoonotic invasion in the wild.

Nematodes Syphacia sp. and Molineus patens were also represented in M. nivalis. Syphacia sp. in the intestinal tract of M. nivalis was discovered for the first time in Georgia. It is noteworthy that in each group of studied animals, including the M. nivalis, nematodes of the genus Syphacia were found with a high mean intensity of invasion and in an abundance. Nematodes of this genus often parasitize different species of rodents in various parts of the intestinal tract (Kirshenblat 1948; Matsaberidze 1976). Syphacia sp. are strict-specific parasites’, most of them host-specific at the genus level (Vlasov et al. 2015). An explanation for the fact revealed above was found in the work of Varodi et al. (2017), in which the presence of rodent nematodes Syphacia arvicola and Heligmosomoides sp. in the intestinal tract of mustelids was usually observed in studies of this host group. The authors discovered a fairly diverse community of nematode species acquired by weasels from rodents and considered post-cyclic parasitism. Helminthological examinations of mustelid carcasses (ermine and weasels) conducted in Belarus (Shimalov and Shimalov 2001) revealed a high total (78.7%) infestation of these animals with 20 species of helminths.

According to the literature data, M. patens is a very specific parasite of Carnivora and is widespread in Mustelidae (Varodi et al. 2017; Pavlović et al. 2021), which is also commonly detected in M. nivalis in Georgia (Rodonaia 1951, 1956, 1966, and 1971).

Despite the low number and species composition of studied small mammals in the vicinity of Usholta, we identified a noticeably high overall infestation of GH. At the same time, the mean intensity of invasion was relatively small. Such a ratio of these parameters indicates that in this parasitologically unexplored region, the basic conditions for the functioning of the “parasite-host” system are preserved, and this data agrees with the findings previously obtained in different regions of Georgia (Kirshenblat 1948; Matsaberidze 1976; Rodonaia 1971). The formation of micromammal helminth fauna in the vicinity of Usholta is connected with the local ecosystem, which includes a complex of biotic and abiotic factors. New data on the study of GH of small mammals in the vicinity of Usholta will supplement the existing material on the biodiversity of helminth fauna and expand the knowledge on their distribution and host specificity in Georgia.

Acknowledgements

We express their gratitude to the staff of the Institute of Zoology at the Ilia State University, Dr. Aleхandеr Bukhnikashvili, for the identification of hosts and photos, as well as laboratory assistant Giorgi Sheklashvili for collecting small mammals and Ani Bikashvili for map design. We are also indebted to the reviewers, Anna Faltynkova and Levan Mumladze (editors), for their extensive help in the improvement of the manuscript.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

No funding was reported.

Author contributions

All authors have contributed equally.

Author ORCIDs

Ketevan Nikolaishvili https://orcid.org/0000-0001-9627-3916

Tsitsino Lomidze https://orcid.org/0000-0002-3321-1088

Lela Arabuli https://orcid.org/0000-0001-9921-6343

Ketevan Asatiani https://orcid.org/0000-0002-7357-9434

Lali Murvanidze https://orcid.org/0000-0001-6516-2762

Data availability

All of the data that support the findings of this study are available in the main text or Supplementary Information.

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