ISSN 00220930, Journal of Evolutionary Biochemistry and Physiology, 2009, Vol. 45, No. 6, pp. 717723.

Pleiades Publishing, Ltd., 2009.

Original Russian Text M. V. Nechaeva, 2009, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2009, Vol. 45, No. 6, pp. 592597.

PROBLEM PAPERS

Rhythmical Contractile Activity of Amnion in Embryogenesis

of Reptiles and Birds
M. V. Nechaeva
Koltsov Institute of Developmental Biology, Russian Academy of Sciences, Moscow, Russia
Received April 06, 2009

AbstractRhythmical contractile activity of amnion accompanies development of reptiles and birds

in the course of a large part of embryogenesis. These rhythmical contractions are myogenic and
spontaneous. The strength, frequency, and character of the amnion contractions change in em
bryogenesis in a regular way. This type of rhythmical activity is sensitive to many neurotransmitters
and external factors. Features of similarity and difference of the amnion rhythmical contractile ac
tivity in the reptile and bird embryogenesis are considered. There are discussed a possible functional
significance of this rhythmical activity and its participation in response of embryo to external ac
tions, such as temperature fluctuations and acute hypoxia.
DOI: 10.1134/S002209300906009X
Key words: amnion, rhythmical contractions, birds, reptiles, temperature, hypoxia.

INTRODUCTION
In works of A.V. VoinoYasenetskii, a great at
tention was paid to study of origin, mechanisms, and
functional role of rhythmical processes in ontogen
esis (see [1]). A special consideration in these works
was given to study of embryonic motor activity. The
motor activity is known to be an integral epigenetic
characteristics of embryonic development of verte
brate animals. It accompanies development from
early stages of embryogenesis and affects essentially
development of the supportmotor system as well
as formation of the CNS nervous connections (see,
for example, the review [2]). Disturbances of motor
activity in embryogenesis and the embryonic aki
nesia can lead to abnormalities of development and
functional disturbances that are often preserved at
the postnatal period [35].
In the higher vertebrate animals (amniotes) the

motor activity in embryogenesis consists of rhyth

mic somatic movements of the fetus itself and of
the extrafetal motor activity. The latter can be of
various nature in different classes of amniotes [6].
Thus, in birds it is represented by rhythmic con
tractions of extrafetal membranesamnion and
yolk sac, in reptilesby rhythmic contractions of
amnion, while in mammals, except for egglaying
mammals,by rhythmic contractions of uterus.
This rhythmic activity changes regularly in em
bryogenesis by facilitating formation of optimal
conditions for fetus development.
The goal of the present work was to consider
peculiarity of the amnion rhythmical contractile
activity in embryogenesis of birds and reptiles, of
mechanisms of regulation of this rhythmical ac
tivity and its changes in response to action of ex
ternal factors, such as brief temperature oscillations
and acute hypoxia.

717

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NECHAEVA

RHYTHMICAL CONTRACTILE ACTIVITY

OF CHICK EMBRYO AMNION
Rhythmical contractions of amnion have been
described in ontogenesis of many bird species [7
9]. Amnion is the extrafetal membrane that di
rectly surrounds the embryo by forming amnion
cavity filled with amniotic fluid. The rhythmical
contractions of amnion lead to rhythmical passive
swinging movements of fetus inside the amniotic
cavity. This type of rhythmic activity was studied
in the greatest detail by the example of chick em
bryo. It was shown that the frequency, strength,
and periodicity of amniotic contractions changed
regularly during embryonic development. It is to
be noted that such type of rhythmical activity was
studied with great attention in the works of A.V.
VoinoYasenetskii and of a researcher of his Lab
oratory L.A. Polyakova [10, 11]. By summing up
results of these studies and of works of other au
thors [7, 8, 1216], the rhythmic contractile ac
tivity of the chick embryo amnion in embryogen
esis can be described as follows: the contractile ac
tivity can be continuous or packed; the duration
of contractions is 27 s, and their frequency varies
from 6 to 20 per 1 min; the amnion contractions
appear at the 35th day of incubation, the frequen
cy of contractions gradually increases by reaching
maximum at the 79th day, then it decreases to a
certain level by the 1314th day of incubation and
is preserved almost unchanged until the 1819th
days. Structure of the chick embryo amnion is stud
ied in detail. It has been shown that amnion con
sists of epithelial and smooth muscle layers divid
ed by basal membrane [8, 13, 1719]; amnion is
not innervated and has no blood vessels [8, 13, 20];
the rhythmic contractions of amnion are of myo
genic nature and occur due to spontaneous con
tractions of smooth muscle cells. In the process of
development, there are observed changes in struc
ture of the amnion smooth muscle layer, which to
a certain degree correlate with dynamics of changes
in its contractile activity. Thus, starting from the
5th day of incubation, the amnion smooth muscle
structure gradually becomes multilayered, and the
typical starlike structures appear in them; from
the 10th day of incubation the number of these
structures begin to decrease, what coincides with
the beginning of a decrease of frequency of amnion

contractions. Then, by the 14th day, only single

muscle figures are observed, and by the 17th day
the amnion muscles become intensively loosen and
the large spaces filled with connective tissue ap
pear between the cells [13, 18, 21].
It is to be noted that isolated amnion retains the
capability for spontaneous rhythmical contractions
and is sensitive to many neurotransmitters [7, 8,
2226]. Our previous studies [15] have shown the
presence of reciprocal humoral regulation of con
tractile activity of the chick embryo amnion, which
occurs due to changes in the amniotic fluid of con
centration of inhibitory (noradrenaline) and stim
ulatory (serotonin) neurotransmitters, to which the
amnion is sensitive. Changes in concentrations of
these two hormones alongside with morphologi
cal alterations of amnion structure determine the
level of contractile activity of the chick embryo
amnion, characteristic of each stage of develop
ment.
It is also to be noted that external factors, such
as temperature and changes in the gas composi
tion of environmental air (hypoxia, hyperoxia, and
hypercapnia), affect to significant degree the con
tractile activity of the chick embryo amnion [8, 13,
24, 2729].
The main function of amnion is considered to
be protection of embryo from drying and mechan
ical damage [8]. But the role of rhythmical con
tractions of amnion in embryogenesis is still un
clear. It was suggested that amnion contractions
in embryogenesis were necessary for mixing the
amniotic fluid to prevent adhesion of fetal surface
to the amniotic membrane [6, 8, 16]. This is espe
cially important during the first half of embryogen
esis, when the skin covers of fetus are not yet de
veloped and it is just at this period that the amnion
contractile activity is the highest. Another sugges
tion is compensation of deficit of the fetal somatic
motor activity at early stages of development [6,
16]. Thus, these works have established that in
embryogenesis the levels of embryonic somatic
motor activity and contractile activity of amnion
have opposite dynamics: the early stages are char
acterized by low somatic motor activity with high
level of amniotic contractile activity, whereas at the
end of embryogenesis, on the contrary, a high lev
el of somatic motor activity is observed, while the
amnion contractile activity is decreased. One more

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RHYTHMICAL CONTRACTILE ACTIVITY OF AMNION IN EMBRYOGENESIS

suggestion about the significance of amniotic

rhythmical contractions consists in the periodic
changes in the pressure of amniotic fluid inside the
amniotic cavity, which occurs as a result of am
nion contractions: such smoothing of embryo
due to amnion contractions can be important for
normal development of skin covers and receptors,
as well as of muscles of fetus [1, 30]. Besides, we
have put forward a suggestion that change in the
amnion rhythmical activity under effect of various
environmental factors participates in the fetus
complex response to the changing conditions of
environment and thus can be involved in the pre
natal adaptation [6]. Such suggestion has appeared
on the basis of that the fetus own regulatory sys
tems at the embryonic period are not yet developed
or developed insufficiently, and the extrafetal
membranes including amnion, participating in the
embryo response to external actions, can either
promote compensation of these actions or provide
development of embryo under new changed con
ditions.
AMNION RHYTHMICAL CONTRACTIONS
IN EMBRYOGENESIS OF REPTILES
Rhythmical contractions of amnion in reptile
embryogenesis were studied to the lesser degree.
These were mainly visual observations of this type
of motor activity in the developing egg and histo
logical studies of the amnion structure in some rep
tile species. Thus, the smooth muscle cells, similar
to those in the amnion chick embryo, were found
in amnion of several species of lizards Gecko verti
cillarius, Tiliqua nigrolutea, Egernia whitei, Mabuia
multifasciata, snakes Vipera berus and Tropidono
tus natrix, and alligator [31, 32]. As to the amnion
rhythmical contractions, they were described in
lizards Lacetra vivipara and Anguis fragilis [33, 34],
in snakes Vipera berus and Natrix natrix [32, 33]
and in the turtle Testudo horsfieldi [35]. However,
in other turtle speciesTerrapere carolina and
Caretta carettathe rhythmical contractions of
amnion were not found [36]. We have performed
a comparative study of the amnion rhythmical con
tractile activity in ovo in embryogenesis of sand liz
ard Lacerta agilis [37], Yemenia veiled chameleon
Chamaeleo calyptratus [38], African house snake
Lamprophis fuliginosus and Elaphe radiata [39] and

719

swamp turtle Emys orbicularis [40]. The results

obtained in these studies have allowed us to iden
tify the main peculiarities of the amnion contrac
tile activity in reptiles.
1. Contractions of reptile amnion are very
slow (duration of one contraction varies from 0.8
to 3.5 min, and frequency of contractions varies
from 2 to 10 per 10 min).
2. Amnion contractions appear at the early
embryonic development stages comparable in dif
ferent species and continue until the stages close
to hatching. Thus, the greatest part of the reptile
embryonic development occurs under effect of
amnion rhythmical contractions.
3. The dynamics of changes in frequency and
strength of amnion contractions in the process of
embryonic development can differ in different rep
tile species. Thus, in chameleon there is observed
their significant increase at the end of embryogen
esis, in turtle and lizard the significant changes in
frequency were not found, but in the snake there
was observed only a tendency for an increase of fre
quency of amnion contractions at the end of em
bryogenesis.
4. The described changes in frequency and
strength of amnion contractions in reptile embryo
genesis correlate with changes in structure of its
smooth muscle elements. Morphological studies
have shown that, for example, the chameleon am
nion performs changes from the single smooth
muscle cells in the beginning of development to the
complex system of crosslike muscle structures
with welldeveloped network of actin filaments at
the end of embryogenesis, i.e., at the period of most
intensive contractile activity of amnion in chame
leon. In the turtle, similar morphological changes
in amnion are absent, and so are significant chang
es in contraction frequency in embryogenesis.
5. The amnion rhythmical contractions in
reptiles are spontaneous, as an isolated amnion in
vitro preserves the capability for rhythmical spon
taneous contractions in all studied species.
6. Neurotransmitters affect the amnion con
tractile activity in reptiles. Thus, for lizard, snake,
and turtle, it was shown that noradrenaline was the
suppressive agent with the dosedependent inhib
itory effect on the amnion contraction frequency
in experiments in vitro and in ovo; this effect is ter
minated under action of propranolol. Acetylcho

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NECHAEVA

line produces the dosedependent stimulatory ef

fect, while serotonin does not change the amnion
contractile frequency. These data give ground to
suggest the existence of humoral regulation of the
amnion contractile activity with participation of
neurotransmitters in amniotic fluid by analogy with
the chick embryo amnion. To confirm this sugges
tion, additional studies are necessary.
7. Temperature affects significantly the con
tractile activity of the reptile amnion at various
stages of development. At brief temperature fluc
tuations in the diapason that can take place during
development of reptile eggs under natural condi
tions, the frequency and duration of amnion con
tractions are changed.
8. At the same time, studies of effect of acute
hypoxia on contractile activity of reptile amnion,
performed by the example of turtle embryo, did not
reveal statistically significant changes in the am
nion contractile frequency.
AMNION RHYTHMICAL CONTRACTIONS
AND PRENATAL ADAPTATION
Since the rhythmical contractile activity of am
nion in reptiles and birds is sensitive to changes in
environmental factors, of interest is its possible
participation in the complex response of the de
veloping organism to changes of environment and
its role in adaptation.
At present, a great attention has been paid to
study of effect of conditions of embryonic devel
opment on formation of the main functional sys
tems in vertebrate animals. It is shown that action
during the prenatal period of such external factors
as temperature and changes in the content of oxy
gen (hypoxia and hyperoxia) and carbon dioxide
(hypercarnia) in environmental air can induce sig
nificant morphofunctional alterations appearing in
the course of embryonic development and pre
served at the postembryonic period [2, 4144].
However, there remains poorly studied the ques
tion how exactly the effects of these environmen
tal factors on embryonic development are realized,
which functional systems are participated in such
response, as well as what is the contribution of in
dividual functional systems to the total reaction to
action.
Effect of external factors on endogenous rhyth

mical processes in embryogenesis was extensively

studied in works of A.V. VoinoYasenetskii.
Among his studies and those of associates of his
Laboratory was effect of such factors as light,
sound, and vibration on embryonic motor activity
of the chick embryo [1, 4547]. Subsequently, an
action of light on contractile activity of chick em
bryo amnion was shown [16].
In the present work, we have focused our atten
tion on effect of brief temperature fluctuations and
acute hypoxia on the rhythmical contractile activ
ity of amnion in embryogenesis of birds and rep
tiles and on interaction of changes in this activity
with response of cardiovascular and respiratory
systems.
In the chick embryo, the optimal temperature
for amnion spontaneous contractile activity is
38C, which coincides with temperature of incu
bation of chick eggs. The frequency of amnion con
traction decreases as the temperature falls by 0.7C;
a decrease of temperature to 3633C as well as an
increase of temperature to 43C results in arrest of
amnion contractions [13, 24, 27, 29]. In reptiles,
the comparable by value temperature fluctuations
affect the amnion contraction frequency to the
lesser degree: the frequency of amnion contrac
tions changes but, unlike the chick embryo, the
contractile activity of amnion does not stop. Thus,
in the sand lizard the heating of egg by 3C and
cooling by 5C relative to the incubation tempera
ture (25C) induced an increase and a decrease of
the amnion contraction frequency by 44 and 56%,
respectively, as compared with the initial values
[37]. In the swamp turtle, change in incubation
temperature by 3 relative to the incubation tem
perature of 8C led to an increase of the amnion
contraction frequency, on average, by 40% or to a
decrease by 50% [40]. In the house snake, an in
crease of temperature by 4C relative to the incu
bation temperature increased the amnion contrac
tion frequency by 40%, whereas a decrease of tem
perature by 4 and 8C resulted in a decrease of the
amnion contractions frequency by 15 and 40%,
respectively [32]. In chameleon, an increase of the
temperature by 2.5C did not change the amnion
contraction frequency, but a decrease of the tem
perature by the same value decreased the amnion
contraction frequency, on average, by 35% [38].
It can be suggested that since development of rep

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RHYTHMICAL CONTRACTILE ACTIVITY OF AMNION IN EMBRYOGENESIS

tile eggs under natural conditions occurs during

temperature fluctuating in the wider diapason that
in birds, the lower sensitivity of their amnion con
tractile activity to temperature might reflect adap
tation of reptiles to these conditions of develop
ment. Still it is not clear so far why in some cases
the reptile amnion reactions to the temperature
increase or decrease differ considerably.
Comparison of responses of the amnion contrac
tile activity and the heart rhythm to the tempera
ture fluctuation in reptile embryogenesis has re
vealed an essential difference in the value of coef
ficient Q10 [40]. Thus, Q10 for the amnion con
tractile activity in the studied species of reptiles is
within the diapason from 3 to 7 by exceeding Q10
for the heart contraction frequency, the value of
which is from 1.9 to 3. As to the oxygen consump
tion rate at temperature changes, in the swamp tur
tle embryogenesis, Q10 varied from 3 to 1 at tem
perature changes, i.e., it was comparable with heart
rhythm. It can be suggested that the high Q10 for
the amnion contractile activity in reptile embryo
genesis can be due to peculiarities of amnion con
tractile elements or to the presence of additional
factors affecting the amnion rhythmic contrac
tions, such as, for example, neurotransmitters
present in amniotic liquid and able to affect the
amnion contractile activity in addition to the di
rect effect of temperature.
The responses of the amnion rhythmic contrac
tile activity to acute hypoxia also differ in embryo
genesis of reptiles and birds. Thus, in chick em
bryo, a decrease in the air oxygen content to 10%
reduces frequency of the amnion contractions or
completely ceases them [28]. The same decrease
in the air oxygen content did not change the am
nion contraction frequency in the swamp turtle
[40]. These differences can reflect adaptation of the
turtle embryo to possible periods of hypoxic action
in the nature, as development of reptiles occurs in
the depth of soil, in which episodes of hypoxia of
different duration are often observed [48].

reptiles and birds, the amnion rhythmic contrac

tions are observed during the comparable period
of development, the contractions are myogenic
and spontaneous, have similar sensitivity to neu
rotransmitters, and are sensitive to temperature
changes. Significantly different are the time char
acteristics of the amnion contractile activity: du
ration of the reptile amnion contractions is about
2090 times longer and the frequency of contrac
tions, respectively, is lower. There are also differ
ences in dynamics of changes in the amnion con
traction frequency in embryogenesis: in reptiles
there was not observed a peak of activity charac
teristic of the bird amnion in the first half of em
bryogenesis; the frequency of their amnion con
tractions either does not change in embryogenesis
or increases by the end of embryonic development.
The sensitivity to the temperature changes is high
er in the bird amnion: a similar temperature de
crease relative to the temperature of incubation
induces cessation of amnion contractions in chick
embryo and only decreases its frequency in reptiles.
The bird amnion also is more sensitive to acute
hypoxia: at a comparable level of hypoxia the fre
quency of chick embryo contractions decreases or
they are ceased, whereas the amnion contraction
frequency in the turtle is not changed. Thus, the
amnion of chick embryo is more sensitive to chang
es in external factors (temperature, hypoxia) than
the amnion of the studied reptile species.
ACKNOWLEDGMENTS
The work was partly supported by the Russian
Foundation for Basic Research (project no. 0804
01063).
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721

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