Hostname: page-component-6bf8c574d5-n2sc8 Total loading time: 0 Render date: 2025-03-06T12:12:25.776Z Has data issue: false hasContentIssue false
  • English
  • Français

Helminths of the rock lizards Darevskia dahli and D. armeniaca in their invaded range in Ukraine

Published online by Cambridge University Press:  27 February 2025

R. Svitin Open the ORCID record for R. Svitin [Opens in a new window] ,
O. Marushchak ,
I. Dmytriieva ,
V. Dupak ,
O. Greben ,
A. Nechai  and
Y. Syrota
R. Svitin*
Affiliation:
I. I. Schmalhausen Institute of Zoology of National Academy of Sciences of Ukraine, Kyiv, Ukraine North-West University, Potchefstroom Campus, South Africa Taras Shevchenko National University of Kyiv, Ukraine
O. Marushchak
Affiliation:
I. I. Schmalhausen Institute of Zoology of National Academy of Sciences of Ukraine, Kyiv, Ukraine Université de Strasbourg, CNRS, IPHC, UMR 7178, F-67000 Strasbourg, France
I. Dmytriieva
Affiliation:
I. I. Schmalhausen Institute of Zoology of National Academy of Sciences of Ukraine, Kyiv, Ukraine
V. Dupak
Affiliation:
I. I. Schmalhausen Institute of Zoology of National Academy of Sciences of Ukraine, Kyiv, Ukraine
O. Greben
Affiliation:
I. I. Schmalhausen Institute of Zoology of National Academy of Sciences of Ukraine, Kyiv, Ukraine
A. Nechai
Affiliation:
I. I. Schmalhausen Institute of Zoology of National Academy of Sciences of Ukraine, Kyiv, Ukraine State Research Institution ‘Kyiv Academic University’, Ukraine
Y. Syrota
Affiliation:
I. I. Schmalhausen Institute of Zoology of National Academy of Sciences of Ukraine, Kyiv, Ukraine Institute of Parasitology, Slovak Academy of Sciences, Košice, Slovakia
*
Corresponding author: R. Svitin; Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This study investigated the helminths of the mixed invasive population of Darevskia armeniaca and D. dahli, collected during two field trips in Denyshy, Zhytomyr region, Ukraine, in 2023. In total, 67 adult lizards (35 D. armeniaca and 32 D. dahli) were examined. Molecular and morphological approaches were used to identify the parasites. The analyses revealed six helminth species, including four nematodes (Toxocara cati, Strongyloides darevskyi, Oswaldocruzia sp., and Spirurida gen. sp.), one trematode (Pleurogenes claviger), and one cestode (Mesocestoides litteratus). Toxocara cati had the highest prevalence, found in cysts located primarily on the liver and in the body cavity of the hosts. The qualitative and quantitative comparative assessment of the helminth community suggests that, due to the introduction of these lizards, most helminth species from their native range have been lost. Additionally, most local helminth species have not yet adapted to parasitising these lizards as normal hosts of their life cycle.

Keywords

ParasitesReptiliainvasive populationsenemy release
Type
Research Paper
Information
Journal of Helminthology , Volume 99 , 2025 , e38
Copyright
© The Author(s), 2025. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amundsen, P, Lafferty, K, Knudsen, R, Primicerio, R, Kristoffersen, R, Klemetsen, A and Kuris, AM (2013) New parasites and predators follow the introduction of two fish species to a subarctic lake: implications for food-web structure and functioning. Oecologia 171, 993–1002.CrossRefGoogle ScholarPubMed
Balzani, P, Vizzini, S, Santini, G, Masoni, A, Ciofi, C, Ricevuto, E and Chelazzi, G (2016) Stable isotope analysis of trophic niche in two co-occurring native and invasive terrapins, Emys orbicularis and Trachemys scripta elegans. Biological Invasions 18, 3611–3621. https://doi.org/10.1007/s10530-016-1251-x.CrossRefGoogle Scholar
Bellard, C, Genovesi, P and Jeschke, J (2016) Global patterns in threats to vertebrates by biological invasions. Proceedings of Biological Sciences 283, 20152454.Google ScholarPubMed
Blackburn, T and Ewen, J (2017) Parasites as drivers and passengers of human-mediated biological invasions. EcoHealth 14, 61–73.CrossRefGoogle ScholarPubMed
Capinha, C, Essl, F, Seebens, H, Moser, D and Pereira, HM (2015) The dispersal of alien species redefines biogeography in the Anthropocene. Science 348, 1248–1251.CrossRefGoogle ScholarPubMed
Cogălniceanu, D, Rozylowicz, L, Székely, P, Samoilă, C, Stănescu, F, Tudor, M, Székely, D and Iosif, R (2013) Diversity and distribution of reptiles in Romania. ZooKeys 341, 49–76.Google Scholar
Darevsky, I (2006) Consequences of a failed attempt of introduction of bisexual species of rock lizards Darevskia mixta (Mehely, 1909) (Sauria, Lacertidae) from Georgia to Zhitomir region of Ukraine. Vestnik Zoologii 40(4), 370.Google Scholar
Darevskiy, I and Shcherbak, N (1968) Acclimatisation of parthenogenetic lizards in Ukraine Priroda 5, 1–93. [Даревский И.С., Щербак Н.Н. Акклиматизация партеногенетических ящериц на Украине // При, Щербак Н.Н. Акклиматизация партеногенетических ящериц на Украине. Природа 5:1–93].Google Scholar
Duz, S, Kukushkin, O and Nazarov, R (2012) A record of the Turkestan naked-toed gecko, Tenuidactylus fedtschenkoi (Sauria: Gekkonidae) in the south-western Ukraine Sovremennaya herpetologia 12(3/4), 123–133. [Дузь С. Л., Кукушкин О. В., Назаров Р. А. О находке туркестанского геккона, Tenuidactylus fedtschenkoi (Sauria, Gekkonidae), в юго-западной Украине. Современная герпетология 12(3/4):123–133].Google Scholar
Ellis, EC, Antill, EC and Kreft, H (2012) All is not loss: Plant biodiversity in the Anthropocene. PLoS ONE 7, e30535.CrossRefGoogle Scholar
Fong, JJ and Chen, TH (2010) DNA evidence for the hybridization of wild turtles in Taiwan: Possible genetic pollution from trade animals. Conservation Genetics 11, 2061–2066. https://doi.org/10.1007/s10592-010-0066-z.CrossRefGoogle Scholar
Garcia-Diaz, P, Ross, JV, Woolnough, AP and Cassey, P (2016) The illegal wildlife trade is a likely source of alien species. Conservation Letters 10(6), 690–698. https://doi.org/10.1111/conl.12301.CrossRefGoogle Scholar
Georgiev, B, Biserkov, V and Genov, T (1986) In toto staining method for cestodes with iron acetocarmine. Helminthologia 23(4), 279–281.Google Scholar
Heger, T, Jeschke, JM, Bernard-Verdier, M, Musseau, CL and Mietchen, D (2024) Hypothesis description: Enemy release hypothesis. Research Ideas and Outcomes 10, e107393. https://doi.org/10.3897/rio.10.e107393.CrossRefGoogle Scholar
Hidalgo-Vila, J, Martínez-Silvestre, A, Pérez-Santigosa, N, León-Vizcaíno, L and Díaz-Paniagua, C (2020) High prevalence of diseases in two invasive populations of red-eared sliders (Trachemys scripta elegans) in southwestern Spain. Amphibia-Reptilia 41(4), 509–518. https://doi.org/10.1163/15685381-bja10021.CrossRefGoogle Scholar
Krasylenko, Y and Kukushkin, O (2017) An update of thin-toed gecko Tenuidactylus bogdanovi (Reptilia, Gekkonidae) population status in Odessa City, Ukraine. Zbirnyk prats’ Zoologichnogo museyu 48, 3–12.Google Scholar
Li, Y, Niu, L, Wang, Q, Zhang, Z, Chen, Z, Gu, X, Xie, Y, Yan, N, Wang, S, Peng, X and Yang, G (2012) Molecular characterization and phylogenetic analysis of ascarid nematodes from twenty-one species of captive wild mammals based on mitochondrial and nuclear sequences. Parasitology 139(10), 1329–38. https://doi.org/10.1017/S003118201200056X.CrossRefGoogle ScholarPubMed
Literák, I, Tenora, F, Letková, V, Goldova, M, Torres, J and Olson, P (2006) Mesocestoides litteratus (Batsch, 1786) (Cestoda: Cyclophyllidea: Mesocestoididae) from the red fox: Morphological and 18S rDNA characterization of European isolates. Helminthologia 43, 191–195. https://doi.org/10.2478/s11687-006-0036-7.CrossRefGoogle Scholar
Manchester, SJ and Bullock, JM (2000) The impacts of non-native species on UK biodiversity and the effectiveness of control. Journal of Applied Ecology 37, 845–864. https://doi.org/10.1046/j.1365-2664.2000.00538.x.CrossRefGoogle Scholar
Marushchak, O, Syrota, Y, Dmytrieva, I, Kuzmin, Y, Nechai, A, Lisitsina, O and Svitin, R (2024) Helminths found in common species of the herpetofauna in Ukraine. Biodiversity Data Journal 12, e113770. doi: 10.3897/BDJ.12.e113770.CrossRefGoogle ScholarPubMed
Matveev, AS, Kukushkin, OV and Sokolov, LV (2013) On the record of a new for Ukrainian fauna lizard species. Vestnik Zoologii 47(5), 394. [Матвеев А. С., Соколов Л. В., Кукушкин О. В. 2013 а. О находке нового для фауны Украины вида ящериц – Podarcis muralis (Sauria, Lacertidae). Вестник зоологии 47(5):394].Google Scholar
Meyer, L, Du Preez, L, Bonneau, E, Heritier, L, Quintana, M, Valdeon, A, Sadaoui, A, Kechemir-Issad, N, Palacios, C and Verneau, O (2015) Parasite host-switching from the invasive American red-eared slider, Trachemys scripta elegans, to the native Mediterranean pond turtle, Mauremys leprosa, in natural environments. Aquatic Invasions 10(1), 79–91. doi: http://doi.org/10.3391/ai.2015.10.1.08.CrossRefGoogle Scholar
Nadler, S, Carreno, R, Mejía-Madrid, H, Ullberg, J, Pagan, C, Houston, R and Hugot, J (2007) Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism. Parasitology 134(Pt 10), 1421–1442. https://doi.org/10.1017/S0031182007002880.CrossRefGoogle ScholarPubMed
Nekrasova, O and Kostiushyn, V (2016) Current distribution of the introduced rock lizards of the Darevskia (saxicola) complex (Sauria, Lacertidae, Darevskia) in Zhytomyr Region (Ukraine). Vestnik zoologii 50(3), 225–230.CrossRefGoogle Scholar
Nekrasova, O, Tytar, V, Pupins, M and Ceirans, A (2022) Range expansion of the alien red-eared slider Trachemys scripta (Thunberg in Schoepff, 1792) (Reptilia, Testudines) in Eastern Europe, with special reference to Latvia and Ukraine. BioInvasions Records 11(1), 287–295. https://doi.org/10.3391/bir.2022.11.1.29,CrossRefGoogle Scholar
Nekrasova, O, Marushchak, O, Pupins, M, Skute, A, Tytar, V and Čeirāns, A (2021) Distribution and potential limiting factors of the European pond turtle (Emys orbicularis) in Eastern Europe. Diversity 13(280), 1–11. https://doi.org/10.3390/d13070280.CrossRefGoogle Scholar
Nekrasova, O, Pupins, M, Marushchak, O, Tytar, V, Martinez-Silvestre, A, Škute, A, Čeirāns, A, Theissinger, K and Georges, J-Y (2024) Present and future distribution of the European pond turtle versus seven exotic freshwater turtles, with a focus on Eastern Europe. Scientific Reports 14(21149), 1–15. https://doi.org/10.1038/s41598-024-71911-4.CrossRefGoogle ScholarPubMed
Oskyrko, O, Laakkonen, H, Silva-Rocha, I, Uller, T, Carretero, M, Nekrasova, O and Marushchak, O (2019) Inferring the origin and pathway of the allochthonous populations of common wall lizards, Podarcis muralis, in Ukraine. XX European Congress of Herpetology, Milan. P. 282.Google Scholar
Pimentel, D, Zuniga, R and Morrison, D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52, 273−288.CrossRefGoogle Scholar
Pupina, A, Pupins, M, Nekrasova, O, Tytar, V, Kozynenko, I and Marushchak, O (2018) Species distribution modelling: Bombina bombina (Linnaeus, 1761) and its important invasive threat Perccottus glenii (Dybowski, 1877) in Latvia under global climate change. Environmental Research, Engineering and Management 749(4), 79–86. https://doi.org/10.5755/j01.erem.74.4.21093.Google Scholar
Roca, V, Jorge, F, Ilgaz, Ç, Kumlutaş, Y, Durmuş, SH and Carretero, MA (2015) The intestinal helminth community of the spiny-tailed lizard Darevskia rudis (Squamata, Lacertidae) from northern Turkey. Journal of Helminthology 90(2), 144–51. https://doi.org/10.1017/S0022149X14000911. PMID: 26821706.CrossRefGoogle Scholar
Ryzhikov, KM, Sharpilo, VP and Shevchenko, NN (1980) Helminths of Amphibians of the Fauna of the USSR. Moscow: Nauka. [Гельминты амфибий фауны СССР].Google Scholar
Sargsyan, N, Aralelyan, M, Danielyan, F and Vartanyan, F (2014) Helminthes of some species of reptiles from the Republic of Armenia. Electronic Journal of Natural Sciences 1(22), c50.Google Scholar
Schoeman, A, Kruger, N, Secondi, J and Du Preez, L (2019) Repeated reduction in parasite diversity in invasive populations of Xenopus laevis: A global experiment in enemy release. Biological Invasions 21, 1323–1338. https://doi.org/10.1007/s10530-018-1902-1.CrossRefGoogle Scholar
Sharpilo, VP (1976) Parasitic Worms of Reptiles of the USSR Fauna. Kyiv: Naukova Dumka. [Паразитические черви пресмыкающихся фауны СССР].Google Scholar
Simberloff, D (2011) How common are invasion-induced ecosystem impacts? Biological Invasions 13, 1255–1268.CrossRefGoogle Scholar
Smit, N, Malherbe, W and Hadfield, K (2017) Alien freshwater fish parasites from South Africa: Diversity, distribution, status and the way forward. International Journal for Parasitology: Parasites and Wildlife 6, 386e401.Google ScholarPubMed
Sprent, J (1956) The life history and development of Toxocara cati (Schrank 1788) in the domestic cat. Parasitology 46, 54–78.CrossRefGoogle ScholarPubMed
Suzuki, N, Hoshino, K, Murakami, K, Takeyama, H and Chow, S (2008) Molecular diet analysis of Phyllosoma larvae of the Japanese spiny lobster Palinurus japonicus (Decapoda: Crustacea). Marine Biotechnology 10, 49–55.CrossRefGoogle Scholar
Tarkhnishvili, D, Murtskhvaladze, M and Anderson, C (2017) Coincidence of genotypes at two loci in two parthenogenetic rock lizards: How backcrosses might trigger adaptive speciation, Biological Journal of the Linnean Society 121(2), 365–378. https://doi.org/10.1093/biolinnean/blw046.CrossRefGoogle Scholar
Zaleśny, G, Hildebrand, J and Popiołek, M (2010) Molecular identification of Heterakis spumosa Schneider, 1866 (Nematoda: Ascaridida: Heterakidae) with comparative analysis of its occurrence in two mice species. Annales Zoologici 60, 647–655. https://doi.org/10.3161/000345410X550517.CrossRefGoogle Scholar