ISSN 1062!3590, Biology Bulletin, 2016, Vol. 43, No. 4, pp. 344349. Pleiades Publishing, Inc., 2016.

Original Russian Text E.V. Kuznetsova, N.Y. Feoktistova, S.V. Naidenko, A.V. Surov, N.B. Tikhonova, Ju.E. Kozlovskii, 2016, published in Izvestiya Akademii Nauk,
Seriya Biologicheskaya, 2016, No. 4, pp. 405411.

ZOOLOGY

Seasonal Changes in Blood Cells and Biochemical Parameters

in the Mongolian Hamster (Allocricetulus curtatus)
E. V. Kuznetsovaa, N. Y. Feoktistovaa, S. V. Naidenkoa, A. V. Surova,
N. B. Tikhonovab, and Ju. E. Kozlovskiib
a Severtsov
Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii pr. 33, Moscow, 119071 Russia
b
Research Institute of Human Morphology, Russian Academy of Medical Sciences, ul. Tsuryupa 3, Moscow, 117418 Russia
e!mail: feoktistova@sevin.ru
Received July 8, 2015

AbstractIt was shown previously that the Mongolian hamster (Allocricetulus curtatus) is a mammalian spe!
cies with irregular short hibernation. The purpose of the present study was to determine how this status affects
seasonal changes in the biochemical and hematological parameters in A. curtatus males under a natural tem!
perature and light regime. It was found that a reduction in circulating white blood cells, specifically lympho!
cytes, neutrophils, eosinophils, basophils, and monocytes, occurred in winter and bilirubin levels increased
in spring. These characteristics make Mongolian hamsters closer to the true hibernating species. At the same
time, the character of seasonal changes in the number of red blood cells, glucose, total protein, creatinine,
and albumin is closer to species with torpor.
DOI: 10.1134/S1062359016040087

INTRODUCTION and chipmunks, may consume feed during awaken!

The autumnwinter season is the most critical
period for animals. It requires substantial physiologi!
cal and habitual rearrangements. Physiological hypo!
thermia is one of the most effective mechanisms for
the economy of energetic resources of an organism. It
is related to modification of biological functions
(Carey et al., 2003). Hypothermia is stimulated by a
complex of external factors, such as shortening of the
length of the day, a decrease in the environment tem!
perature, a deficiency of feed, and others, through
endogenic circadian changes in the neuroendocrine
system of the animal (Schmidt!Nielsen, 1982).
One of the possible types of hypothermia is hiber!
nation, which occurs in different groups of mammals,
such as monotremes, marsupials, insectivores,
rodents, and cheiropteras. During hibernation, the
body temperature of the animal decreases down to
nearly environmental temperature values, the total
metabolic rate becomes depressed, the heart rate
drops, and activity of the neurons and many other sys!
tems of the organism is inhibited (Lyman et al., 1982;
Wang, 1988). The body mass increases in winter!
hibernating animals in autumn before the hibernation.
It reaches a minimum value in spring. Hibernation
may last from 3 to 9 months, but it is interrupted for 6
10 h by periodic short awakenings. The maximum lon!
gevity of hypothermia can last for up to 22 days in the
black!capped marmot Marmota camtschatica, 17 days
in the long!tailed ground squirrel Spermophilus undu!
lates, and 9 days in the Siberian chipmunk Tamias
sibiricus. Some hibernating species, such as hamsters
ings, while others, for example ground squirrels, mar!
mots, and hedgehogs can dispense with feed. Urine
and excrement or urine alone are removed from the
organism in this case (Anufriev, 2008). The blood for!
mula and its biochemical parameters change in the
preparation period and during hibernation: blood
clotting time increases, the volume and the number of
leukocytes and erythrocytes also increase, and the rel!
ative numbers of peripheral blood cells change
(Yasuma et al., 1997; Anufriev, 2008). At the same
time, the lifetime of the erythrocytes increases during
hibernation (Alekseeva and Yunker, 1979). Bilirubin
and glucose concentrations decrease during winter as
compared to autumn almost 2!fold and 3!fold,
respectively. Both parameters increase significantly
and reach their annual maximums by spring (Anufriev,
2008). Violent oscillations of the physiological param!
eters in the organisms of hibernating animals are not
pathological, given the minimal consumption of the
energy resources at a low body temperature; the integ!
rity of all vital functions is preserved. This allows the
animals to come back to the active state (Kramarova et
al., 2009).
Some mammalian species demonstrate another
type of hypothermia than the winter hibernation type
during the autumn and winter period. This type is
manifested by short periods of slowing down in the
metabolism and lowering the body temperature. Such
periods are called the torpors. This phenomenon is
described in several mammal orders, such as night
bats, insectivores (common shrews), rodents

344
 SEASONAL CHANGES IN BLOOD CELLS AND BIOCHEMICAL PARAMETERS
(Muridae, Cricetidae, Gliridae, and Citellidae), pri!
mates (lemurs), marsupials (several orders), and
monotremes (anteaters) (Nikol and Andersen, 2000).
Torpor is well studied in the Cricetinae subfamily such
as the Phodopus order (Figala et al., 1973; Heldmaier
and Steinlechner, 1981; Feoktistova, 2008; Ushakova
et al., 2012). It is usually observed in the early morn!
ings and lasts for 25 h. During torpor, the body tem!
perature is 1518C, and the energy saving reaches
67% (Heldmaier and Klingenspor, 2003). The torpor
ends by spontaneous awakening with a body tempera!
ture rise to 3738C due to internal heat production.
The animals can start foraging, nest building, or other
activity immediately after awakening. There are lim!
ited data on seasonal changes in the biochemical and
hematological parameters in torpid animals. Leuko!
cyte numbers increase, while erythrocyte numbers stay
unchanged in the autumn and winter season in the
Australian brush!tailed possum Trichosurus vulpecula
as opposed to hibernating in winter mammalian spe!
cies (Hallam et al., 1995). The majority of biochemi!
cal blood parameters drastically decrease during tor!
por, but they quickly recover during active periods
between bouts in the South African torpid marsupial
Chiloe opossum Dromiciops gliroides. In general, sea!
sonal changes in the blood biochemical parameters are
profound in members of this species: the glucose con!
centration is minimal in winter, and the total protein
has the lowest values in summer (Franco et al., 2013).
Thus, truly winter!hibernating and torpid species
substantially differ in some physiological, hematolog!
ical, and biochemical parameters. However, there are
species that cannot be assigned to either hibernating or
torporing. For example, nonstandard short hiberna!
tion with irregular periods of normothermia was
described in Mongolian hamster Allocricetulus curta!
tus and Eversman hamster A. eversmanni (Ushakova
et al., 2010; Feoktistova et al., 2013; Klevezal et al.,
2015). The observations were made by using intraperi!
toneally transplanted Petrovskys temperature!sensi!
tive loggers. Unlike truly hibernating animals, which
gain maximum weight before falling into hibernation,
Eversman hamsters gain weight by the middle of the
summer and afterwards begin to reduce it by Novem!
ber and December, when the first bouts of hypother!
mia happen. This is also characteristic for the animals
demonstrating daily torpors. The plot of body weight
dynamics of the Mongolian hamster is located during
the course of the year between common hamster
(Cricetus cricetus) hibernated in the winter and torpid
Djungarian hamster (Phodopus sungorus) (figure).
Both Allocricetulus species hamsters are able to lower
their body temperature down to 4.55C. Such hypo!
thermia may last from several hours to 2 days. The
body temperature increases to normal values during
periodic spontaneous interbout arousals like in true
hibernating animals. During the awakenings, the ani!
mals eat and remove metabolic products actively
(Feoktistova et al., 2013).
BIOLOGY BULLETIN Vol. 43 No. 4 2016
345
%
160 1
2
3
120
80
40
0
IV V VI VII VIII IX X XI XII I II III
Month
Body weight seasonal dynamics of three hamster species
with different hypothermia strategies. Body weight in April
is taken to be 100%. 1, Mongolian hamster (Kuznetsova
et al., 2014); 2, common hamster (Masson!Pvet et al.,
1994); 3, Djungarian hamster Phodopus sungorus.
Such hypothermia holds an intermediate position
in terms of the character of enamel recordings
between true hibernation, which gives a clear sight of
alternate narrow and broad bands (Klevezal et al.,
2012), and torpor, which leaves no recordings on the
enamel of incisor teeth. In the case of Eversman ham!
sters, a recording of short hibernation can be seen on
the incisor teeth (Klevezal et al., 2015). So, Eversman
hamsters hold an intermediate position based on the
character of hypothermia and the body weight dynam!
ics between torpid and truly hibernating species, but it
is not clear how this is reflected in the levels of bio!
chemical response and hematological parameters.
The aim of this study is to reveal seasonal features of
the blood biochemical parameters, the characteristics
of changes in leukocyte and erythrocyte numbers, and
also the leukogram in Mongolian hamsters under nat!
ural temperature and light regime.
MATERIALS AND METHODS
Ten mature male Mongolian hamsters, which were
bred from animals caught near Tere!Khol Lake
(Republic of Tyva), were used in the experiment in
2012 and 2013. The animals were kept under a natural
light and temperature regimen in a facility (located in
Moscow) that was protected from rain and snow. Cot!
ton wool and excelsior were used as nesting material.
Feed was given to the animals ad libitum and included
grain mix, raw or boiled meet, curd cheese, eggs, and
fresh vegetables. The hamsters were kept in single
cages per 26 20 13 cm. Hypothermia manifesta!
tions were assessed daily by the absence of a reaction to
tactile stimuli by contacts. The blood was taken from
346 KUZNETSOVA et al.

Seasonal changes in leukocytic and biochemical blood parameters in male Mongolian hamsters (Xav SE; N = 10)

Units
Parameter Winter Spring Summer Autumn F(3, 116) P
of measure

Erythrocytes 106 cells/L 9.96 0.23a 10.73 0.31ab 9.7 0.36ac 9.75 0.34ac 3.72 0.013
Leukocytes (all forms 103 cells/L 3.85 0.39a 5.38 0.43b 5.78 0.39b 6.2 0.52b 8.7 0.00003
of them)
Neutrophils
segmented Same 1.45 0.16a 2.14 0.19ab 2.48 0.19b 2.28 0.31b 6.5 0.0004
banded '' 0.12 0.02a 0.29 0.05b 0.24 0.03ab 0.16 0.03ab 4.85 0.003
a b abc b
Lymphocytes '' 2.01 0.19 2.45 0.18 2.33 0.19 3.19 0.25 7.03 0.0002
Basophils cells/L 13.70 5.33 43.13 11.49 30.42 5.16 45.87 12.07 2.2 0.09
a b b b
Eosinophils Same 56.63 16.08 165.33 27.59 189.21 34.15 179.76 46.42 6.47 0.0004
Monocytes '' 185.44 26.7a 294.73 33.2ab 557.5 64.4c 369.0 47.4b 24.6 0.00001
a a ab b
Glucose mg/dL 124.6 7.4 126.3 4.7 117.0 3.7 98.8 5.1 4.58 0.005
Bilirubin '' 1.64 0.09a 2.46 0.23b 1.42 0.11a 1.03 0.26a 9.79 0.00001
Total protein g/L 72.68 1.91 72.27 1.83 80.23 2.63 74.9 2.12 2.41 0.07
Albumin '' 39.74 0.8a 42.69 0.73ab 42.93 0.55ab 38.7 0.78ac 4.92 0.003
Creatinine mg/dL 0.35 0.02 0.43 0.04 0.38 0.02 0.36 0.02 1.72 0.167
Xav means average values; SE is the error of the average value; N is the number of animals; F(3, 116) is the number of the degrees of freedom;
P is the significance; a, b, and c are the same letters designating nonsignificant differences between the seasons.

active animals from the sublingual vein in the amount
of 0.70.9 mL once a month from 9:00 to 11:00 a.m.
This procedure lasts less than 30 s, so it does not affect
plasma cortisol and glucose levels (Graievskaya et al.,
1986). The blood was collected into two plastic tubes.
One was with K2 EDTA for counting blood cells and
preparing smears; the other contained clotting activa!
tor and separating gel for obtaining blood serum
(Microvette, Sarstedt, Germany), which was then centri!
fuged 10 min at 5000 g for separation of serum and
transferred into clean tubes for measuring the bio!
chemical parameters.
Glucose, bilirubin, creatinine, total protein, and
albumin concentration in blood serum of the experi!
mental animals was measured by a ChemWell 400 bio!
chemical analyzer using standard methods described
in the appendices to Spinreact kits (Girona, Spain).
Leukocyte and erythrocyte blood counts were
measured in Goryaev chambers by a unified method
(Lyubina, 1984). The leukogram was determined in
dry fixed and stained blood smears. Methanol was
used for smears fixation, and Diff!Quik (Medion
Diagnostics AG, Switzerland) was used as a staining
agent. The staining was performed according to the
manufacturers protocol. The proportion of different
types of white blood cells was assessed on the basis of
an examination of total 100 leucocytes in blood smear
under oil immersion. Different leucocyte counts were
obtained by multiplying their proportions with blood
cells (Lyubina et al., 1984).
Statistical analysis was performed with the Statis!
tica software kit (StatSoft, ver. 8.0). The seasonal
dynamics of the biochemical and hematological
parameters was assessed by one!way analysis of vari!
ance (ANOVA) with a Tukey post!hoctest.
RESULTS
Short irregular periods of hypothermia, which
lasted no longer than 48 h, were observed in experi!
mental animals from January to April. All the data
regarding biochemical parameters and blood formulas
are presented in the table. A significant decrease in in
the number of leukocytes was observed in winter in
male Mongolian hamsters; the increase in the number
of leukocytes took place in spring. This dependency
was seen for all leukocytes subtypes, specifically lym!
phocytes, neutrophils, eosinophils, basophils, and
monocytes. The number of erythrocytes did not differ
significantly in the blood of experimental animals in
autumn compared to winter; however, this parameter
was significantly higher in spring compared to summer
and autumn.
The glucose concentration in the peripheral blood
changed significantly depending on the season. It was

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 SEASONAL CHANGES IN BLOOD CELLS AND BIOCHEMICAL PARAMETERS
higher in winter and spring, decreased in summer, and
reached a minimum in autumn.
The bilirubin concentration did not change during
the year except for spring.
Significant seasonal changes in total protein and
creatinine were not revealed. However, the albumin
concentration was higher in summer and spring com!
pared to autumn and winter.
DISCUSSION
We revealed leukocytopenia in Mongolian ham!
sters, which is characteristic for all hibernating ani!
mals studied so far, including prominent representa!
tives of hibernating species, such as ground squirrels
(Spurrier and Dawe, 1973; Frerichs et al., 1994; Toien
et al., 2001; Anufriev, 2008; Bouma et al., 2010b,
2011), hedgehogs (Suomalainen and Rosokivi, 1973),
and some hamster species, specifically the common
hamster and the Syrian hamster Mesocricetus auratus
(Reznik et al., 1975; Schalms 2010). Leukocytope!
nia affects granulocytes, namely neutrophils, eosino!
phils, and basophils, lymphocytes, and monocytes. It
is also observed in truly hibernating species (Bouma et
al., 2010a). A decrease in the number of blood leuko!
cytes is primarily related to their ability to deposit in
some organs, for example in the intestine, bone mar!
row, spleen, and lungs (Bouma et al., 2010a; Franco et
al., 2013). Moreover, leukocytopenia could be par!
tially stipulated by the formation of thrombocyte/leu!
cocyte!aggregates. These aggregates are formed as a
result of a decrease in the body temperature (Bouma
et al., 2010b). The most important consequence of
this leukocytopenia for the organism may be immune
depression and, consequently, increased susceptibility
to infections (Franco et al., 2013).
A pronounced decrease in the numbers of circulat!
ing neutrophils and monocytes may result in signifi!
cantly reduce acute inflammatory responses and non!
sufficient phagocytosis, and the reduction in leuco!
cytes will strongly affect immune surveillance, leading
to impaired cellular and humoral immune responses
(Bouma et al., 2010a). A constant value of the number
of erythrocytes observed in the blood of Mongolian
hamsters during a year is characteristic for regularly
torpid animals, but this parameter differs in animals
with a prominent hibernation, in which this parameter
increases. For example, it is known for the Syrian and
the common hamsters that red blood cell counts and
hemoglobin concentration are higher in hibernating
animals. Red blood cell senescence is delayed and
RBC destruction is virtually absent during hiberna!
tion, with an observed increase in RBC lifespan of up
to 160 days, as compared with the normal erythrocyte
lifespan of 5070 days in non!hibernating hamsters
(Brock, 1960; Reznik et al., 1975). Seemingly, aging is
slowed down and the lifespan of erythrocytes is
increased also in Mongolian hamsters during hiberna!
tion. This is supported by the data on the seasonal
BIOLOGY BULLETIN Vol. 43 No. 4 2016
347
dynamics of the bilirubin concentration in the blood:
its concentration was increased in spring after hiber!
nation. Our data on bilirubin changes in Mongolian
hamsters during the course of a year confirm only
partly the data for animals with true hibernation. This
could be related to more frequent and longer awaken!
ings. For example, according to the data obtained in
long!tailed ground squirrels, the bilirubin concentra!
tion decreases almost 2!fold during deep hibernation
(which takes place from January to March) as com!
pared to the autumn period, and it increases before the
end of the hibernation, when spontaneous awakenings
become more frequent. The bilirubin concentration is
at a maximum in the animals that just left hibernation.
This is stipulated by the initiation of synthetic pro!
cesses, specifically red blood cell renewal (Anufriev,
2008). The bilirubin concentration was almost con!
stant in Mongolian hamsters during the autumn and
winter months.
The data obtained on the seasonal dynamics of the
glucose concentration in the blood of Mongolian
hamsters differ from the data registered in either truly
hibernating or torpid animals. A profound hypoglyce!
mia is observed in winter in the animals with true
hibernation and in torpid ones (Al!Badry and Taha,
1983; Anufriev, 2008; Franco et al., 2013). However,
the concentration of glucose, which is consumed dur!
ing hypothermia, is largely compensated for during
interbout arousals: it rises to the values registered in
the same animals in the active state (Al!Badry and
Taha, 1983). The glucose concentration increases sig!
nificantly after full awakening. This indicates main!
taining of a certain level of gluconeogenesis in the ani!
mals and its hypercompensation by spring (Anufriev,
2008).
Proteins contribute to gluconeogenesis during
spontaneous interbout arousals (Klain and Whitten,
1968; Al!Badry and Taha, 1982). It was shown, for
example, for hedgehogs that the total protein concen!
tration in plasma increased during hibernation; how!
ever, this increase was interrupted by intervals of its
obvious drops during periodic awakenings. The albu!
min concentration in blood changed in the same way:
it decreased slightly in autumn and increased promi!
nently in winter. A decline in the plasma albumin con!
centration was observed in fully awake animals (Al!
Badry and Taha, 1982). The absence of similar
changes in the total protein and albumin in blood
serum of Mongolian hamster males during the year is
probably related to less deep and shorter hibernation
compared to true winter!hibernating animals.
During hibernation, the kidneys are in a hypother!
mic conditions, renal blood flow is minimal, and
uropoiesis is substantially reduced. Periodic awaken!
ings are associated with kidneys reperfusion and the
recovery of intensity of uropoiesis (Zatzmann, 1984;
Zancanaro et al., 1999). According to the data
obtained in the eared hedgehog Hemiechinus auritus
aegyptius (Al!Badry and Taha, 1982) and the Chiloe
348 KUZNETSOVA et al.
opossum (Franco et al., 2013), the creatinine concen!
tration in the blood is decreased during hibernation.
As sleeping animals are starving, endogenous reserves
for creatinine synthesis are limited, which leads to a
slow speed of its generation. These data along with
reduced glomerular filtration in kidneys could explain
the decreased creatinine concentration in the blood
during hibernation (Al!Badry and Taha, 1982). Sea!
sonal changes in the creatinine level are absent in the
Mongolian hamster, while in the animals with true
hibernation they approach the changes seen in torpid
species.
The Mongolian hamster holds an intermediate
position with its short unusual hibernation according
to the character of the seasonal changes in the body
weight and also hematological and biochemical blood
parameters between actively hibernating gnawing ani!
mals and the animals being active year round or having
torpor. In general, one could say that Eversman ham!
sters, and specifically the Mongolian hamster, are
characterized by high plasticity showing nonstandard
short hypothermia periods with subtle seasonal
changes in the biochemical parameters of the blood.
The animals may not demonstrate hypothermia of any
type when in mild climate conditions. In the case of a
cold winter, they demonstrate hypothermia up to 2
days long helping to save valuable amounts of energy.
ACKNOWLEDGMENTS
This work was supported by the Presidium of the
Russian Academy of Sciences, grant Live Nature,
and the Russian Foundation for Basic Research,
project 14!04!31325_mol_a and 16!34!
01071_mol_a.
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