Analysis of Parasitofauna and Endosymbionts of Lissotriton vulgaris L., 1758 (Caudata, Salamandridae) in Natural and Urban Gradients of the Environment

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ISSN 1062-3590, Biology Bulletin, 2024, Vol. 51, No. 1, pp. 131–138. © Pleiades Publishing, Inc., 2024.
Analysis of Parasitofauna and Endosymbionts of Lissotriton vulgaris L.,
1758 (Caudata, Salamandridae) in Natural and Urban
Gradients of the Environment
A. V. Burakovaa, *, D. L. Berzina, and V. L. Ve rsh inina, b
a Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences, Yekaterinburg, 620144 Russia
b Ural Federal University, Institute of Natural Sciences and Mathematics, Yekaterinburg, 620002 Russia
*e-mail: annabios@list.ru
Received November 16, 2022; revised February 1, 2023; accepted February 6, 2023
Abstract—The analysis of the parasitic and endosymbiontofauna of the common newt (Lissotriton vulgaris L.,
1758) in the natural and urban landscapes of the Middle Urals is presented for the first time. Four species of
helminths belonging to the Nematoda type were found, including one taxon indeterminate to the species
(Nematoda sp.) and one species of endosymbionts (phylum Chromista). The works devoted to the species
composition of L. vulgaris parasites on the territory of Eurasia are analyzed. The fauna of the helminths of the
common newt on the eastern slope of the Urals is depleted, which is probably determined by the limited dis-
tribution of the species outside Europe, the temperature regime in the north, and the availability of moisture
in the south.
Keywords: common newt, helminths, urbocenosis, natural gradient of the environment
DOI: 10.1134/S1062359023602732
The common newt (Lissotriton vulgaris L., 1758) is
a widespread and ecologically flexible species of tailed
amphibians (Vershinin, 2007), inhabiting the forest
zone of the European part and second in number only
to brown frogs. This species is found in anthropogenic
landscapes (mainly in forested and suburban areas)
(Vershinin, 2007; Kuzmin, 2012). Threat of extinction
of local populations L. vulgaris relatively small com-
pared to Triturus cristatus (Laurenti, 1768) (Kinne,
2006). However, in the landscapes of megacities,
L. vulgaris may have the status of a rare and even
endangered species (Fayzulin and Kuzovenko, 2015;
Kidov et al., 2021).
The number and distribution of many species of
amphibians have been declining globally in recent
decades for various reasons: chemical pollution,
destruction and transformation of habitats, various
infections, and the emergence of invasive species of
fish and amphibians (Berger et al., 1998; Houlahan
et al., 2000; Reshetnikov, 2001; Blaustein and
Kiesecker, 2002; Kinne, 2006; Wake and Vredenburg,
2008).
One of the significant biotic factors that regulate
the number of hosts, and therefore affect the survival
of animals, is parasitic invasions. Amphibians can be
biological reservoirs of parasites and distributors of
helminth infections in natural ecosystems and can
serve as definitive, intermediate, facultative, and res-
ervoir hosts for helminths. Some types of trematodes
can accelerate puberty in newts and cause a reduction
in life expectancy (Sinsch et al., 2018a) and various
anomalies (Sessions and Ruth, 1990), making them
most vulnerable to predators (Caffara et al., 2014), and
thereby reduce the survival rate of amphibians and
lead to population decline.
Within Russia, the parasitic fauna L. vulgaris has
been described for Vologda oblast (Shabunov and
Radchenko, 2012) and the Republic of Mordovia
(Ruchin and Chikhlyaev, 2016). The most complete
study of the helminth fauna of L. vulgaris was under-
taken in Samara oblast (Chikhlyaev, 2007; Chikhlyaev
et al., 2018).
For the Ural region, information on the parasites
L. vulgaris is absent. In this regard, the purpose of this
work is a comparative analysis of the parasitic fauna
L. vulgaris in the European part of the range and in
natural and urban landscapes of the Middle Urals.
MATERIALS AND METHODS
This study was carried out in May 2020 and 2021 in
natural and urban areas of the Middle Urals (Fig. 1).
The study of parasitic fauna along an urbanization gra-
dient was carried out using the example of the city of
Yekaterinburg, located on the eastern slope of the
Middle Urals.
ZOOLOGY

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BURAKOVA et al.
Fig. 1. Map-scheme of collecting material (1, residential
part of the city of Yekaterinburg; 2, forest–park part of the
city of Yekaterinburg; 3, village of Mramorskoye; 4, village
of Bolshoye Koshaevo).
60q
60q
56q
57q
Yekaterinburg
2
3
1
4
Within the urban agglomeration, a residential part
and a forest park zone were distinguished (Vershinin
et al., 2015). Suburban populations were used as con-
trols for L. vulgaris (Fig. 1).
191 individuals of the common newt were studied,
of which 119 specimens lived within the urban agglom-
eration (residential zone, 34 specimens; forest park
zone, 85), and 72 specimens were from rural areas.
Identification of parasites was carried out accord-
ing to standard methods (Ivashkin et al., 1971; Ryzhi-
kov et al., 1980). The infestation of amphibians is
assessed according to the following indicators: P
(extensiveness of invasion), the proportion of infected
host individuals in the studied sample (%); A (abun-
dance index), the average number of parasites of a cer-
tain species or group of parasites in all individuals of
the host, specimen/individual of the host (Breev,
1976). The assessment of the dominance structure was
carried out using the approach of A.A. Kirillov
(Kirillov, 2011). Statistical data processing was carried
out using the Quantitative Parasitology program
(Rozsa et al., 2000) and Statistica 7.0.
RESULTS
In the intestines of the common newts studied,
four species of nematodes were found (one taxon was
not identified to the species) and one species of endo-
symbiotic protozoa. The species composition and
infestation rates are presented in Tables 1 and 2.
In natural areas L. vulgaris nematodes are repre-
sented by three species of the order Rhabditida; spec-
imens of unknown species were also noted (Nema-
toda sp.). In urban communities of L. vulgaris, two
types of nematodes were identified (Table 1). Along
with the presence of common species (Oswaldocruzia
filiformis and Megalobatrachonema terdentatum) on
the studied territories of the Middle Urals, for L. vul-
garis only on the eastern slope was a nematode larva of
Neoxysomatium brevicaudatum noted, and specimens
of Nematoda sp. were found on the western slope. The
endosymbiotic protozoa Cepedea dimidiata was identi-
fied in L. vulgaris from the eastern slope of the Middle
Urals and in urban communities.
In Central Ural populations of L. vulgaris, on the
eastern slope, in terms of the share in the component
community, the dominant species is M. terdentatum
(97%), compared with the western slope (25%) (Fig. 2).
In natural populations of L. vulgaris on the western
slope, a bidominant structure is noted—O. filiformis
(40%) and Nematoda sp. (35%) (Fig. 2). The exten-
siveness of invasion of M. terdentatum is also signifi-
cantly higher for amphibians on the eastern slope
compared to the western slope (Table 1).
For amphibians of the urban agglomeration (resi-
dential and forest–park zones) and natural areas, two
general types of parasites have been noted—O. fili-
formis and M. terdentatum (Table 2). On the territory
of the urban community and natural areas of the east-
ern slope, M. terdentatum dominates; its share in the
urbanization gradient remains at a high level (from
96.67% for amphibians in suburban areas to 97.44%
for animals in residential areas). The share of O. fili-
formis is low and increases along the urbanization gra-
dient (from 1.67% in suburban areas to 2.56% in resi-
dential areas) (Fig. 3).
Nematode larvae of N. brevicaudatum were noted
in animals in natural populations; the proportion was
1.67% (Table 2, Fig. 3).
Fig. 2. The ratio of parasite species in L. vulgaris on the
western and eastern slopes of the Middle Urals (W, West-
ern slope; E, Eastern slope).
O. filiformis M. terdentatum
N. brevicaudatum, larvae Nematoda sp.
97%
25%
2%
1%
35%
40%
WE

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ANALYSIS OF PARASITOFAUNA AND ENDOSYMBIONTS 133
Endosymbiotic protozoa have been observed both
in residential areas and in natural landscapes. The
extensiveness of invasion for C. dimidiata is signifi-
cantly higher in L. vulgaris in the residential area, in
comparison with the forest park area and natural area
(Table 2).
An analysis of the literature data regarding the
fauna of parasites of the common newt on the territory
of Eurasia showed that the most diverse in the species
composition of helminths is the Republic of Belarus
(eight species, including five species of trematodes and
three species of nematodes) and the Samara region
(eight species, including six species of trematodes and
two types of nematodes). The fewest helminth species
were observed in populations from Italy (Sesto
Fiorentino, Tuscany region), Northern Greece, and
the Republic of Mordovia (one species). Moreover,
trematodes were detected in the first two European
regions, and nematodes were detected in newts on the
territory of the Republic of Mordovia (Table 3).
For most of the regions of Europe and the Russian
Federation considered, the two most common nema-
todes are O. filiformis, marked in L. vulgaris in Europe
in the southwestern part of Germany (Rhineland-
Palatinate), in Northern Greece, in the Republic of
Belarus, and in the regions of the Russian Federation
(Vologda and Samara oblasts, Republic of Mordovia),
and the nematode M. terdentatum identified in L. vul-
garis in Germany, in the southwestern part of England
(Somerset County), and in Vologda and Samara
oblasts.
A number of species are known only for certain
areas: larval forms of trematodes: Paralepoderma
cloacicola (Luhe, 1909), met., Pharyngostomum cor-
datum (Diesing,1850), met., Strigea sp., met., marked
in L. vulgaris from the territory of Samara oblast;
trematodes: Strigea sphaerula (Rudolphi, 1803) Szi-
dat, 1928 and Opisthioglyphe ranae (Frohlich, 1791);
nematodes: Cosmocerca ornata (Dujardin, 1845) Dies-
in g, 1861 and Agamospirura Henry, Sisoff 1913 sp., lar-
vae, found for common newts from the territory of the
Republic of Belarus. The fluke Clinostomum spp.
Leidy, 1856 was identified in L. vulgaris, in Italy (Tus-
cany region); the fluke Parastrigea robusta Szidat,
1928 and the nematode Cosmocerca longicauda (Lin-
stow, 1885) were found in a common newt from Ger-
many. Skreben Acanthocephalus anthuris (Dujardin,
1845) was found in L. vulgaris inhabiting the south-
western part of England (Table 3).
Table 1. Species composition and occupancy rates by parasites and endosymbionts in L. vulgaris in ecosystems of the Mid-
dle Urals
Above the line, P, extent of invasion, %; below the line, A, abundance index, host specimen/individual; SE, mathematical error; in the
column “Total species,” the number of species of parasites and endosymbionts is indicated through a fraction; A is significantly higher
compared to the western slope (P < 0.05); “–” means no data.
Parasite/Endosymbiont
P ± SE/A ± SE
Middle Urals
(n = 191)
natural areas (n = 72)
Urban cenosis
(n = 119)
Western slope
(n = 37)
Eastern slope
(n = 35)
Phylum Nematoda Cobb, 1932
Class Chromadorea Inglis, 1983
Order Rhabditida Chitwood, 1933
Oswaldocruzia filiformis (Goeze, 1782)
Megalobatrachonema terdentatum (Linstow, 1890)
Neoxysomatium brevicaudatum, larvae Zeder, 1800 ‒ ‒
Nematoda sp.‒‒
Phylum Chromista Cavalier-Smith, 1987
Class Opalinea Wenyon, 1926
Cepedea dimidiata (Metcalf, 1923) ‒
Total species 3/0 3/1 2/1
±
±
24.30 7.05
0.54 0.21
±
±
40.0 8.28
1.71 0.60
±
±
29.40 4.18
1.04 0.23
±
±
8.10 4.46
0.22 0.16
±
±
2.90 2.84
0.03 0.02
±
±
1.70 1.19
0.03 0.02
±
±
5.40 3.72
0.14 0.11
±
±
34.3 8.03
1.66 0.60
A
±
±
28.60 4.14
1.02 0.21
±
±
2.90 2.84
0.03 0.02
±
±
24.30 7.05
0.19 0.09
±
±
17.10 6.36
9.06 4.37
±
±
31.1 4.24
17.33 2.93

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BURAKOVA et al.
DISCUSSION
The parasitic fauna of common newts in the study
areas is characterized by both widespread species and
specialized helminths of tailed amphibians.
The nematode M. terdentatum is a European spe-
cies, a highly specific parasite, characteristic of the
common newt in the western regions of Ukraine,
Belarus, and Czechoslovakia, noted in L. vulgaris on
the territory of Vologda oblast (Shabunov and Rad-
chenko, 2012) and the Volga region (Samara) (Kirillov
et al., 2018). Infection by M. terdentatum occurs orally
in water or through reservoir hosts (Petter and Cha-
baud, 1971). There is the opinion that the presence of
some species of nematodes may be associated with the
isolation of the ecological niche of caudates, which
influenced the independent formation of the helminth
fauna of this group of hosts during evolution (Ryzhi-
kov et al., 1980).
According to A.A. Kirillov et al. (Kirillov et al.,
2018), the nematode M. terdentatum in the common
newt living in the city of Samara was noted for the first
time. Infection of animals with this species was also
low and amounted to 25% and 0.5 helminths per indi-
vidual. Similar data are shown for L. vulgaris from the
territory of Vologda oblast (infestation is two speci-
mens per individual) (Shabunov and Radchenko,
2012).
Domination of M. terdentatum in common newts
on the Eastern slope of the Middle Urals in natural
ecosystems and urban communities is probably due to
the specific ecology of the host itself (L. vulgaris), as
well as the biology of this helminth. Infection with
M. terdentatum occurs orally during the aquatic phase
of life of the common newt during active feeding when
the reservoir hosts eaten are gastropods and oligo-
chaetes (Petter and Chabaud, 1971). It was established
(Petter and Chabaud, 1971) that the third invasive
stage of M. terdentatum develops in an aquatic envi-
Table 2. Population by parasites and endosymbionts in L. vulgaris in the urbanization gradient
Above the line, P, extent of invasion, %; below the line, A, abundance index, host specimen/individual; SE, mathematical error; a, significantly
higher compared to forest–park area (P < 0.05); b, significantly higher compared to natural territory (P < 0.05); “–” means no data.
Parasite/Endosymbiont
P ± SE/A ± SE
Residential territory
(n = 34)
Forest–park area
(n = 85)
Natural areas
(n = 72)
Phylum Nematoda Cobb, 1932
Class Chromadorea Inglis, 1983
Oswaldocruzia filiformis (Goeze, 1782)
Megalobatrachonema terdentatum (Linstow, 1890)
Neoxysomatium brevicaudatum, larvae Zeder, 1800 ‒ ‒
Phylum Chromista Cavalier-Smith, 1987
Class Opalinea Wenyon, 1926
Cepedea dimidiata (Stein, 1860) (Metcalf, 1923)
±
±
26.50 7.57
1.15 0.42
±
±
31.80 5.05
1.40 0.26
±
±
42.90 5.83
1.89 0.59
±
±
5.30 3.84
0.05 0.03
±
±
2.50 1.69
0.05 0.03
±
±
2.90 1.98
0.03 0.02
±
±
23.50 7.27
1.12 0.42
±
±
31.80 5.05
0.98 0.25
±
±
34.30 5.59
1.66 0.60
±
±
2.90 1.98
0.03 0.02
±
±
47.10 8.56
18.82 4.99
ab
±
±
24.70 4.68
16.73 3.59
±
±
17.10 4.43
9.06 4.37
Fig. 3. The ratio of parasite species for L. vulgaris in urban-
ized and natural areas of the eastern slope of the Middle
Urals (III, residential area of the city of Yekaterinburg; IV,
forest park zone of the city of Yekaterinburg; С, natural
areas).
O. filiformis M. terdentatum
N. brevicaudatum, larvae
97.65%
97.44%
96.67%
2.35%
2.56%
1.67% 1.67%
C IIIIV

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ANALYSIS OF PARASITOFAUNA AND ENDOSYMBIONTS 135
ronment at a temperature of about 20°C. It has been
shown (Berzin and Burakova, 2022) that infection of
sexually mature animals of Triturus cristatus (Laurenti,
1768) by the nematode M. terdentatum begins already
at a water temperature of 16.9°C and above. Unlike the
crested newt, L. vulgaris is a less stenotopic species and
its reproduction begins earlier at lower temperatures
(t=+8°C) (Vershinin, 2007). In urban communities,
spawning reservoirs warm up faster (Vershinin, 2007),
which creates optimal conditions for the development
of both newts and the nematodes M. terdentatum.
Thus, most likely, favorable temperature conditions,
as well as the presence of active nutrition in the aquatic
phase of the life cycle, affect the likelihood of infec-
tion by L. vulgaris of this species.
Another type of helminth is the nematode O. fili-
formis, which is widespread in the Palearctic, parasit-
izing a wide range of amphibians and reptiles (Ryzhi-
Table 3. Species composition of parasites in L. vulgaris according to the literature data
Parasite
Region
England
Germany
Italy
Northern Greece
Republic of Belarus
Vologda oblast
Republic of Mordovia
Samara oblast
Phylum Plathelminthes Gegenbaur, 1859
Diplodiscus subclavatus (Pallas, 1760) + +
Para lepoderma cloacicola (Luhe, 1909), met. +
Pharyngostomum cordatum (Diesing, 1850), met. +
Strigea sp., met. Abildgaard, 1790 +
Strigea sphaerula (Rudolphi, 1803) Szidat, 1928 +
Clinostomum spp. Leidy, 1856 +
Opisthioglyphe ranae (Frohlich, 1791) +
Pleurogenoides medians (Olsson, 1876) + +
Alaria alata (Schrank, 1788) Krause, 1914 + +
Parastrigea robusta Szidat, 1928 +
Phylum Nematoda Cobb, 1932
Oswaldocruzia filiformis Goeze, 1782 + +++++
Megalobatrachonema terdentatum (Linstow, 1890) + + + +
Cosmocerca ornata (Du jardi n, 1845 ) Dies in g, 1861 +
Agamospirura Henry, Sisoff 1913 sp., larvae +
Cosmocerca longicauda (Linstow, 1885) +
Phylum Acanthocephala Kölr., 1771
Acanthocephalus anthuris (Dujardin, 1845) +
Author
Aver y, 1971
Sinsch et al., 2018a,
Sinsch et al., 2018b
Caffara, 2014
Sattmann, 1990
Shimalov, 2009
Shabunov and Radchenko, 2012
Ruchin and Chikhlyaev, 2016
Faizulin et al., 2011,
Chikhlyaev et al., 2018,
Kirillov et al., 2018

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BURAKOVA et al.
kov et al., 1980; Wacker, 2018). Common newts
become infected by O. filiformis orally through acci-
dental contact with infective larvae on land (Hen-
drikx, 1983).
Infestation of L. vulgaris by the nematode O. fili-
formis is low, but this type of helminth is in second
place in terms of its share in the component commu-
nity. It has been shown (Kirillova et al., 2021) that the
greatest infestation was noted for the common toad
(Bufo bufo Linnaeus, 1758), as a species of large size
and leading a predominantly terrestrial lifestyle. Most
likely one of the reasons for the low infestation rates is
the small size of the common newt and the relatively
long duration of the aqueous phase.
Infection by O. filiformis in common newts occurs
during the terrestrial phase of the life cycle, through
accidental ingestion of food items. The most favorable
conditions for the existence of common newts on land
are special microclimatic conditions provided by the
height and density of the grass stand (Vershinin,
2007). It has been shown (Wakker, 2018) that for the
development of eggs of the nematode O. filiformis,
optimal conditions are needed: these are biotopes with
sufficient soil moisture, air temperature about
+14…+15°C, dense vegetation cover on it, free-stand-
ing trees that create shade, and shrubs and reeds nec-
essary for the movement of the larvae of this nema-
tode. Thus, another reason for the infection of com-
mon newts by the nematode O. filiformis, in addition
to the size of the animal, is the height of the grass stand
along which the nematode larvae migrate.
N. brevicaudatum, larvae Zeder, 1800 is one of the
parasites found in representatives of the herpetofauna
of Europe (Borkovcová and Kopriva, 2005; Yildirim-
han et al., 2005; Saglam and Arikan, 2006; Jones et al.,
2012), noted in amphibians of the genera Bombina
Oken, 1816; Bufo Laurenti, 1768; Hyla Laurenti, 1768;
Rana Linne, 1758; and Triturus Raf ine squ e, 1815 and
sometimes reptiles of the genera Anguis Linnaeus, 1758
and Natrix Laurenti, 1768 (Shimalov and Shimalov,
2000; Jones et al., 2012). A nematode that has a direct
life cycle (first-stage larvae hatch from eggs outside
the host and then develop and molt twice until the
third stage of infection). The final host becomes
infected orally, and larvae can be found in the tissues
(Vashetko and Siddikov, 1999; Saeed et al., 2007).
Infestation with larvae of N. brevicaudatum is
small, which is probably related, as in the case of the
nematode O. filiformis, with the small size of the host
itself.
One of the simplest amphibians that inhabits the
digestive tract is C. dimidiata (Wahab et al., 2008). It is
believed that this species has an endosymbiotic rela-
tionship with its hosts, without exerting any negative
effects, despite their detection in large numbers (Poy-
nton and Whitaker, 2001 cited in Mohammad et al.,
2013).
It was shown (McConnachie, 1960) that the colo-
nization of amphibians by representatives of the class
Opalinea occurs during the breeding season and
depends on the secretion of host hormones. After
emerging from hibernation, amphibians begin to feed
actively; with increasing daylight hours, the produc-
tion of gonadotropin increases. Another factor influ-
encing the activity of the pituitary gland, which
secretes gonadotropin, in sexually mature individuals
is an increase in the environmental temperature in the
spring (McConnachie, 1960).
The temperature of the environment, as well as of
the hosts themselves, influences the morphological
and physiological characteristics of protozoa (Mikhal-
chenko, 1958; Sukhanova, 1953, 1963, quoted from
Sukhanova, 1968).
For example, Opalina ranarum (Purkinje et Valen-
tin, 1835) showed that in tadpoles, young of the year,
and mature frogs, the average survival time of proto-
zoan cysts is higher in a reservoir with a higher water
temperature (Sukhanova, 1968).
High rates of invasion by the endosymbiotic proto-
zoa C. dimidiata are probably associated with the syn-
chronization of the life cycles of the host and protozoa
during the period of reproduction, including the tem-
perature regime of the reservoir; in May the water
begins to warm up, which affects the reproduction and
survival of protozoan cysts.
There is a trend towards an increase in the rates of
invasion by endosymbionts in common newts in the
urbanization gradient (toward zone III), which may be
due to the thermal pollution characteristic of urban
communities. In urban areas, approximately 1–2°C
higher than outside the city, accordingly, in the resi-
dential area, the May average monthly temperatures of
water bodies are approximately 3°C higher than in the
forest park zone and natural areas (Vershinin, 2014).
The specificity of the species composition of the
parasitic complex of the common newt on the eastern
slope of the Urals is determined by the limited distri-
bution of the species outside of Europe (Skorinov
et al., 2008), the temperature regime in the north, and
moisture supply in the south (Terentyev and Chernov,
1949; Kuzmin, 2012).
CONCLUSIONS
As the range of the common newt moves eastward,
climatic zones and plant communities change, and the
temperature and moisture supply of the territories
change. The eastern slope of the Urals in this sense is
characterized by an increasingly continental climate,
which affects the species composition and diversity of
the parasitic fauna of the common newt. Anthropo-
genic modifications of communities differ from natu-
ral ones in their greater thermal supply, but insuffi-
cient humidity, which affects the survival of helminths
with a direct life cycle (O. filiformis, N. brevicaudatum,

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ANALYSIS OF PARASITOFAUNA AND ENDOSYMBIONTS 137
larvae) compared to M. terdentatum, the development
of which occurs with a change in reservoir hosts.
ACKNOWLEDGMENTS
The authors are grateful to I.V. Bratseva for help in pre-
paring the list of references.
FUNDING
This work was carried out within the framework of a
State Assignment of the Institute of Plant and Animal Ecol-
ogy, Ural Branch, Russian Academy of Sciences (state reg-
istration no. 122021000082-0).
ETHICS APPROVAL AND CONSENT
TO PARTICIPATE
Permission to collection of this species in Russia is not
required. Animals were collected, handled and euthanized
in accordance with Russian Federation national rules from
1977 and the second part of Working Party Report DGXT
of the EU (1997).
CONFLICT OF INTEREST
The authors of this work declare that they have no con-
flicts of interest.
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