Research Article |
Corresponding author: Tsitsino Lomidze ( tsitsino.lomidze@iliauni.edu.ge ) Academic editor: Anna Faltynkova
© 2024 Ketevan Nikolaishvili, Tsitsino Lomidze, Lela Arabuli, Ketevan Asatiani, Lali Murvanidze.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Nikolaishvili K, Lomidze T, Arabuli L, Asatiani K, Murvanidze L (2024) Gastrointestinal helminths of small mammals (Rodentia and Carnivora) in the vicinity of Usholta, Georgia. Caucasiana 3: 245-256. https://doi.org/10.3897/caucasiana.3.e132243
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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.
Caucasus, Cestoda, host, life cycle, Nematoda, parasite
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 (
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.
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 (
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
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
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
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 |
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 (
The infection rate of Apodemus uralensis was 5/8. Similarly,
Mouse-like rodents, usually voles, serve as the main intermediate hosts of E. multiloсularis larvae (
Nematodes in A. uralensis are presented with three species: Heligmosomoides polygyrus (Dujardin, 1845), Trichuris muris (Schrank, 1788), and Syphacia obvelata (Rudolphi, 1802) (Tables
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;
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. (
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;
According to the literature data, M. patens is a very specific parasite of Carnivora and is widespread in Mustelidae (
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;
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.
The authors have declared that no competing interests exist.
No ethical statement was reported.
No funding was reported.
All authors have contributed equally.
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
All of the data that support the findings of this study are available in the main text or Supplementary Information.