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БИОЛОГИЧЕСКИЕ НАУКИ КАЗАХСТАНА №1, 2013
to the intermediate hosts; 5) feeding of
definitive hosts by these insect species.
Every from called conditions is the limiting
factor for the nematodes. But in the same
time for such parasites the relative aridity
of biotope is not dangerous. To this group
nematode Abreviata abbreviata from sand
lizard is belonged.
3. Geo-helminthes with the active free-
living stages for the surviving of which
are necessary: 1) optimal conditions
of temperature, salty and moisture; 2)
substrate for the migration of active larval
stages (grass or suitable soil structure); 3)
minimum of predators and competitors
among free-living stages of other parasites
and/or soil invertebrates. For nematodes
from Trichostrongylidae family (which is
represented by Oswaldocruzia filiformis
all these requires may be satisfied with the
presence of grass by next causes:
- grass (especially bush and rootstock
cereals) causes the especial micro-climate,
protecting the eggs and larvae from drying,
over-heating and direct sun radiation;
- protecting the larval stages from over-
salty of the soil solution at the expense of
keeping of fresh dew and moisture from
the plant guttation;
- decreasing of acute competition and
probability of consummation of predatory
soil invertebrates at the expense of
migration, because a lot of nematodes can
rise on the plants;
- acceleration and increasing of
probability of penetration to definitive host
at the expense of seizing by frogs the insects
from grass (that decreases the probability of
annihilation and infecting larvae of 3 stage
from unfavorable environment conditions).
Moreover, on our observations, larvae of
O.filiformis often penetrate with the grass
in the digestive tract of herbivorous insects
and than hit into the frog’s intestine with
the insects.
4. Nematodes developing with
heterogony – with availability in the life
cycle separately-sex generation, living in
the soil. The condition of their surviving
– the same, as for active free-living stages
of geo-helminthes: a) optimum of non-
biotic conditions (temperature, moisture,
salty, structure of soil, absence of high
concentrations of toxic substances); b)
minimum of predators and competitors.
However Rhabdias bufonis spending in
the environment more time than other
geo-helminthes (with account of free-
living generation) are more steady to the
unfavorable environment conditions, about
which widespread in all biotopes and high
indexes of frogs’ infection testify. Probably
long-term stay in the environment leads
to the forming of correspondent worms’
adaptations on ontogenetic and filogenetic
levels.
5. Geo-helminthes with passive
stages in the environment. In this
group nematodes of suborder Oxyurata
were belonged – with larvae moulting
in the eggs. But in studied widespread
cold-blooded vertebrates of Pavlodar
region this group of helminthes is not
registered.
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БИОЛОГИЧЕСКИЕ НАУКИ КАЗАХСТАНА №1, 2013
The analysis of biotope arrange of
moor frog and sand lizard helminthes
show their dependence on the
landscape conditions connected with
the development of parasites in the
environment and intermediate hosts.
O.ranae. This trematode were revealed
in all researched water-bodies, but
with different intensity of infection and
spreading. It relatively rarely recorded in
the flood-lands of Irtysh and Usolka rivers
and rather often, with high intensity of
infection – in low ground near country
«Yablonka», derelict sand pit and lake on
the outskirts of Pavlodar near Children
railway. In these water-bodies of
anthropogenic landscape there are many
faint-flowing good warmed shallows
causing the favorable conditions for the
living of gastropods from Lymnaeidae
family. The same arrange of trematodes
with wide list of intermediate hosts
(including O.ranae) to the anthropogenic
water-bodies was recorded in Kostroma
region [17]. A little salty of biotope in
low ground near country «Yablonka» and
especially near Children railway isn’t
prevent to trematode’s dissemination,
what may be caused as the forming
parasites’ adaptations (during several
generations), as the periodic decreasing
of salty – seasonal (with melting of
ice and snow) and years (different
quantity of precipitations and level of
ground water). Individual finding of
O.ranae in researched biotope of Kazak
Melkosopochnik were caused by small
quantity of gastropods in Birzhankol lake
(that can be caused by the lake’s origin,
far distance from the flood-lands of large
rivers or chemical compound of water).
H.cylindracea were revealed in
Usolka river flood-land and near
“Yablonka” country. It’s life cycle and
requires to the biotope conditions are the
same as for O.ranae: in is necessary faint-
flowing good shallows with numerous
first intermediate hosts – gastropods; the
second intermediate hosts of worm may
be as gastropods, as tadpoles. The absence
of H.cylindracea in the biotopes, where
high quantity of O.ranae was recorded,
at first sight may seem a strange, but we
may presume several probability causes.
In the first place it may be the competition
of trematodes’ parthenites in the first
intermediate hosts – snails of Lymnaeidae
family (this phenomena was showed by
T.M.Budalova [18] on the example of
Haplometra cylindracea and Fasciola
hepatica in Lymnaea truncatula); in the
second place, this may be the appearance
of anticipating effect from O.ranae, which
has the adaptations as to the landscape, as
to the intermediate hosts (because species
occupying ecological niche in first place
has several advantages and difficulty
superseded by competitors). In the third
place O.ranae may be more adapted to the
salty of landscapes than H.cylindracea,
what is demonstrated by the fact of living
this trematode species only in Irtysh and
Usolka flood-land with fresh water and
soil and absence of halophyte plants. In
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БИОЛОГИЧЕСКИЕ НАУКИ КАЗАХСТАНА №1, 2013
the forth place trematodes with long life
and fluctuated indexes of infection (by
the long-term observation of V.G.Vakker
and N.E.Tarassovskaya, H.cylindracea
is from such parasites) may penetrate
not in all distance from flood-land water-
bodies in comparison with numerous
helminthes. In the fifth place, in different
years the quantity of different parasites’
species may substantially exchange,
that is to say trematodes species may
have certain time niche on the level with
space niche. Absence of H.cylindracea in
Kazak Melkosopochnik (Birzhankol lake)
may be caused the same reasons that for
O.ranae: almost full absence of fresh-
water gastropods and small probability of
the penetration to the lakes distance from
large rivers.
O.filiformis had high infection indexes
in the neighbourhood of Birzhankol lake,
flood-lands of Irtysh and Usolka rivers,
more low – near “Yablonka” country,
relatively rarely met near the sand pit (in
1993 year), near Children railway from
the small autopsied frogs’ group the single
find took place. Basic limited factors for
the distribution of O.filiformis may be:
1) small area of grass (sand pit); 2) salt
soil solution (in low ground near country
«Yablonka» - cumulating of mineral and
organic fertilizing, near Children railway
– presence of soil salts), which indirectly
confirmed by the presence among herbal
cover obligate and facultative halophytes.
We mustn’t exclude third possible cause
– competitor interaction with trematode
O.ranae also parasitizing in the small
intestine and usually locating in the low
half of intestine. Quantity of O.filiformis
was low just in that biotopes where
O.ranae was remarkable of high quantity
and extensity of hosts’ infection.
R.bufonis. As by data of V.G.Vakker
and N.E.Tarassovskaja [5], as by results
of consider of our today material this
nematode had stability high quantity
and infection indexes in all biotopes,
independently on herbal cover, chemical
compound of soil and water, degree of
anthropogenic influence, agricultural and
technical pollutions. We proposed, that
such resistance of R.bufonis to wide specter
of biotope conditions is connected with
the existence of obligate free-living stage
in the environment, that is to say long-
term dwelling in the certain environment
conditions leads to the adaptations on the
ontogenetic and species levels.
Temporary increasing of formal
infection indexes (extensity of infection
and abundance index) of R.bufonis in the
middle of the summer, observed every
year in our material recorded by many
researchers, were connected with the
metamorphose and mass birth of first-
years frogs for which the certain time
for the contact with infection elements
is necessary, because the infection by
nematodes may take place only on the
land and only on post-embryonic stage of
amphibians.
More low in comparison of other
landscapes infection indexes of frogs by
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БИОЛОГИЧЕСКИЕ НАУКИ КАЗАХСТАНА №1, 2013
R.bufonis in 2005 near Usolka river may
be connected not only with young age and
small sizes of caught amphibians (because
infection indexes by R.bufonis, as most
other helminthes, increase with frogs’
age), but partly with the distribution in this
biotope of H.cylindracea also parasitizing
in the lungs.
Sex and age of host are very important
factors influencing to the quantitative and
qualitative composition of helminthes’
fauna. This ruler of ecological parasitology,
postulated by V.A.Dogel [19], was
corroborated by many researchers for
different hosts’ groups, and most important
results were generalized in monograph of
C.Kennedy [20]. Such works were made
on the anural amphibians, moreover the
arrange of different helminthes’ species
to sex and age of hosts, by result of
different researches, may be different and
non-simple. This is the consequence of
many-sides influences of hosts’ sex and
age on the parasites, because these factors
are the system of different or hierarchy
subordinated factors, vectors with different
directions, sum of which is the general
result, which can see the researcher.
Consequently, subsequent studies in this
aspect (as on the field, as on experimental
data), including generalized works with
analysis of all ecological and physiological
factors, connected with sex and age of
animals, are necessary.
Our results on sex and age arrange
of three helminthes species – O.ranae,
R.bufonis, O.filiformis – in moor frog
populations in the town’s outskirt show,
that in common groups of frogs there
are no diversity of infection between
males and females. Trematode O.ranae
is distributed between young and mature
frogs evenly, two nematodes species –
R.bufonis and O.filiformis – are mainly
arranged to older frogs in comparison with
young amphibians (tables 1-4).
However helminthes’ distribution
between males and females in every age
group is non-even. Quantity of trematode
O.ranae is distributed between males and
females of immature frogs evenly, and
among adult frogs it is concentrated mainly
in males. Both nematodes species are for
certain arranged to females in immature
and in males – in adult frogs.
Near Birzhankol lake, where in 2004-
2005 years exclusively or prevalence
large frogs of older age, distribution
of O.filiformis between different sex
frogs was almost even, the abundance
of R.bufonis gravitated to females – but
without statistical authentic differences
(even by Pearson criterion).
We can reasonable interpret described
sex and age dynamics of helminthes’
quantity with the attraction of known
facts about physiological, ecological and
behavior peculiarities of amphibians of
different sex and age. Mature males are
the mobile and actively removing part
of the population (that were noted by
many researchers in regard to many so
different groups of animals – as worm-
blooded, as cold-blooded), that may
59
БИОЛОГИЧЕСКИЕ НАУКИ КАЗАХСТАНА №1, 2013
rise the probability of their contact with
propagate stages of helminthes, moreover
this is true for parasites with oral and
subcutaneous infection of host. But in the
same time it is probably, that most mobile
population elements have high risk of
annihilation – accidental or selective (from
predators, non-biotic factors, pathological
agents). We can propose several causes
for annihilation of most mobile specimens
connected with parasites: 1) death caused
by high parasitic energetic loading and/
or pathologic influence of parasites in the
cases of high intensity of infection; 2)
influence of parasites to the physiological
state, mobility, movement co-ordination
of host, what can play main role in the
safety from predators; 3) organism of
intensively infected animal worse survives
in unfavorable environmental conditions
in comparison of non-infected animal or
host with moderately intensity of infection
– in view of addition energetic load at
the expense of parasites. Moreover in
literature it is known that the resistance
of adult animals of different sex group
is diversity in consequence of hormonal
influences: androgens and corticosteroids
have the catabolic influence to thymus,
causing in the organism of mature males
the deficiency of T-lymphocytes, whereas
women hormones have the protection
importance [21]; however this problem was
better investigated in regard to worm-blooded
animals with their more reactive immune
system. But we can’t lose sight of this factor
for cold-blooded animals, especially taking
into consideration of election high infection
by helminthes of adult males of frogs.
Age factor in the distribution of helminthes
in the populations of land cold-blooded
vertebrates is compound. Age of animal – is
singular super-factor, which can influence on
the parasites’ quantity at the expense of the
next factors:
1. Probability of the contact with
propagate stages which caused, in the first
place, with more mobility of adult animals in
comparison of young animals, in the second
place, with the time of life, which leads to the
accumulation of parasites even with small
length of life.
2. Stage of life cycle on which
infection exclusively or mainly take place.
Land animals with external fertilization
(amphibians) infect by some helminthes’
species exclusively on the tadpole stage
(Tetracotyle), by other species – as on the
larval stage (penetration of cercaria with the
next migration of trematodes to digestive
tract of young frog), as on the adult stage – at
the expense of feeding the snails (trematodes
of Plagiorchidae family – for example,
O.ranae); by third species (most nematodes
species) – exclusively on the land after
metamorphose.
3. Age resistance which can manifest
itself in two ways: a) increasing of
reactivity and resistance of organism with
the age which will decrease the probability
of penetration and surviving the parasites
and other pathologic agents; b) during
long time organism contacts with many
parasites species and accumulates them
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БИОЛОГИЧЕСКИЕ НАУКИ КАЗАХСТАНА №1, 2013
in the organism, and in result of antigens’
competition the decreasing of immune
response to every pathologic agent and
immune fatigue may take place. This
is actually not only for worm-blooded
animals with their reactive immune system,
but in regard to cold-blooded vertebrates.
4. Growth of cold-blooded vertebrates
continues all their life, and increasing of
body sizes of host signifies the increasing
of potential feed sources for all parasites
with any locations. Absolute quantity of
consumed food (most imported for the
parasite of digestive tract) also will be large
in the organism of big older amphibians.
5. Large amphibians and reptilians of
older ages have most sizes of lung and
intestine – potential space niches for the
parasites, which is most important for
large helminthes.
In our materials on moor frog the arrange
of two nematodes species – R.bufonis and
O.filiformis – to the older frogs may be
caused by all of called reasons, including
the activity of large adult amphibians,
considerable feed sources and sizes of
organs of parasites’ location. The absence
of reliable diversities in the infection by
trematode O.ranae between young and
older frogs may be connected with the same
probability of infection on the larval stage
(the infection of tadpoles by cercaria with
the next migration of parasite to the digestive
tract and forming there of mature trematode)
and on the stage of metamorphosed frogs –
with the feeding of snails (mainly older large
frogs’ specimens consume snails).
We must pay attention to the fact, that
different age groups of amphibians often
choose different places of dwelling (that was
recorded in the neighbourhoods of Pavlodar
and in Bajanaul national park). Such
separation of space niches and sub-spaces
by the amphibians of different generations
has ecological importance, decreasing or
including feed competition, increasing the
probability of surviving of every generation
at the expense of different pressing of enemies
and competitors, contributing to the settling
of population and species and assimilation of
new biotopes. And also it is not included, that
the separation of different frogs’ generation
provides the rational exploitation of host’s
population by the populations of different
parasites’ species, arranged to the certain
biotopes (and not only connected with the
possibility of surviving for larval stages of
parasites in the certain landscapes). On our
observations, young moor frogs often dwell
on the open plots, whereas old specimens
prefer the areas with grass (which are most
favourable for the dissemination of nematode
O.filiformis from Trichostrongylidae
family).
And we can bring up else one hypothesis
which doesn’t include earlier voiced
suppositions about the causes of sex and
age distribution of parasites. “Chess”
sex and age dynamics of the distribution
of abundance of 2 worm species, when
among immature frogs females were higher
infected in comparison with males, but
among adult amphibians males were more
infected in comparison of females, may
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БИОЛОГИЧЕСКИЕ НАУКИ КАЗАХСТАНА №1, 2013
be connected with competitor interactions
between the parasites, using the certain
sex and age groups as the ecological
niches or with the age change of energetic
expenditure caused with reproductive
functions. The arrange of all 3 mature
helminthes’ species to the males and whole
poor species composition of worms enable
to propose the second from described
explanation. Adult females expend for the
forming of roe more quantity of substances
and energy, than males for the forming
of milt, and excessive parasite loading
to the females will be expedient for the
populations as the host as the parasites:
mass annihilation of certain part of
host’s population will lead to the sudden
decreasing of the parasites’ quantity.
Thus, the arrange of most helminthes
species to the older frogs may be caused
by higher probability of the contact with
propagate parasites’ stages (long time of
life, activity and mobility, dwelling in the
most favorable for parasites biotopes), and
also larger feed sources of the organism
and sizes of organs of location, which are
especially actual for the large helminthes.
Distribution of the same helminthes species
between males and females of amphibians
may change in the different years, in the
diverse biotopes and among the various
hosts’ species, which may be caused by the
fact, that the cold-blooded animals have
poorer immune reactivity and resistance of
organism, than worm-blooded vertebrates,
consequently, the influence of hormones to
the immune system is not so considerable.
From ecological factors the different
activity and mobility of males and females
can play certain role, that can lead, on the
one hand, to the increasing of contacts
with propagate parasites’ stages and, on the
other hand – to the selective annihilation of
most infected specimens.
LITERATURE
1 Соболева Т.Н. К гельминтофауне водных
амфибий и рептилий Казахстана // Экология па-
разитов водных животных. – Алма-Ата, 1975. –
С. 186-192.
2 Аралханова А.Е. Гельминтофауна ам-
фибий и рептилий северо-востока Казах-
стана: автореф. дис. … канд. биол.наук /
А.Е.Аралханова. – Алматы: ТОО «Казахский
научно-исследовательский ветеринарный ин-
ститут» АО «КазАгроИнновация», 2010. – 26 с.
3 Ваккер В.Г. Паразитофауна рептилий юга
Казахстана и их роль в циркуляции некоторых
гельминтов человека и животных: дис. … канд.
биол. Наук / В.Г.Ваккер. – Алма-Ата: Институт
зоологии АН КазССР, 1971. – 365 с.
4 Ваккер В.Г. Популяционные особенности
гельминтов прыткой ящерицы в Среднем При-
иртышье: тез. докл. 8 Всесоюз. сов. зоологов пе-
динститутов / В.Г.Ваккер. - Витебск, 1984. – С.
56-58.
5 Ваккер В.Г. Биология Rhabdias bufonis
в Среднем Прииртышье / В.Г.Ваккер,
Н.Е.Тарасовская. – М., 1988. – 17 с. – Деп. в ВИ-
НИТИ, №4146-В88.
6 Ваккер В.Г Биология Oswaldocruzia
filiformis В Среднем Прииртышье / В.Г.Ваккер,
Н.Е.Тарасовская. – М., 1988. – 27 с. – Деп. в ВИ-
НИТИ, № 4147-В88.
7 Ваккер В.Г. Биология Opisthioglyphe
ranae в Среднем Прииртышье / В.Г.Ваккер,
Н.Е.Тарасовская. – М., 1988. – 21 с. – Деп. в ВИ-
НИТИ, №4148-В88.
8 Ваккер В.Г. Зараженность гельминтами
остромордой лягушки Rana arvalis в Казахском
Мелкосопочнике / В.Г.Ваккер, Н.Е.Тарасовская.
– Деп. в КазгосИНТИ 12.08.93 г., № 3971-Ка93.
9 Ваккер В.Г. Гельминты амфибий в степной
и лесостепной зонах Казахстана / В.Г.Ваккер,
Н.Е.Тарасовская. – Деп. в КазгосИНТИ 12.08.93
г.,
№ 3969-Ка93.
10 Котельников Г.А. Гельминтологические
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