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Theriogenology 69 (2
Early embryo development in the elephant assessed by serial
a,*, R. Hermes
, F. Göritz
, C. Gray
, J. Kurz
, T.B. Hildebrandt
Leibniz Institute for Zoo- and Wildlife Research, PF 601 103, 10252 Berlin, Germany
African Lion Safari, Cambridge, ON, Canada N1R 5S2
Jürgen Kurz Römerstr. 12, 4800 Attnang-Puchheim, Austria
Received 17 September 2007; received in revised form 21 December 2007; accepted 29 January 2008
The elephant has an extraordinary long pregnancy, lasting 21 months. However, knowledge on embryo development is limited.
To date, only single morphological observations of elephant embryo development associated with placentation are available, all
lacking correlation to gestational age. The present study describes morphological characteristics of early embryo development in
the elephant with exact biometric staging. Six pregnancies in five Asian and one African elephants with known conception dates
were followed by 2D and 3D ultrasound, covering the embryonic period from ovulation to day 116 post-ovulation. The embryonic
vesicle was earliest observed was on day 50 p.o. The proper embryo was not detected until day 62 p.o. Embryonic heartbeat was first
observed on day 71 p.o. The allantois, which became visible as a single sacculation on day 71 p.o. was subdivided in four
compartments on day 76 p.o. By day 95 p.o., head, rump, front and hind legs were clearly distinguished. Between days 95 and 103
p.o. the choriovitelline placenta was replaced by the chorioallantoic placenta. A physiological midgut herniation was transiently
present between days 95 and 116 p.o. On the basis of the late appearance of the embryonic vesicle, delayed implantation in the
elephant is discussed. The study provides a coherent description of elephant embryonic development, formation of the
extraembryonic organs and their role in placenta formation, all of which are of interest for both comparative evolutionary studies
and the improvement of assisted reproduction techniques.
# 2008 Elsevier Inc. All rights reserved.
Keywords: Elephant; Reproduction; Embryogenesis; Ultrasound; Extraembryonic organs
The situation of the African (Loxodonta africana) and
Asian elephant (Elephas maximus) in their respective
native countries is quite different. In Asia, the ever-
growing human population repels the wild-elephant
population to restricted areas. To ensure their survival,
* Corresponding author at: Leibniz Institute for Zoo- and Wildlife
Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany.
Tel.: +49 30 5168246; fax: +49 305126104.
E-mail address: firstname.lastname@example.org (B. Drews).
0093-691X/$ – see front matter # 2008 Elsevier Inc. All rights reserved.
wild-elephant herds are thus forced to raid crops, causing
severe conflict with man. Furthermore, natural habitats
are more and more fragmented, separating subpopula-
tions and impeding genetic exchange .
From historical reports it is known that the African
elephant once inhabited the whole continent .
Extensive ivory trade dating back as far as in Roman
times , expanding human settlements  and civil
wars  are associated with a decline of the African
elephant population. Elephants have long vanished from
North Africa and populations are greatly diminished in
West, Central and East Africa .
B. Drews et al. / Theriogenology 69 (2008) 1120–1128 1121
In Southern Africa, where the elephant population
had almost gone extinct due to ivory poaching in the
19th century, numerous National parks have been
founded to save the species. Here, elephant numbers in
protected areas continuously build up and lead to local
overpopulations. In the Kruger National Park, an
estimated population of 10 individuals in 1908
augmented to approximately 6500 elephants 60 years
later . According to the South African National
Parks Board, this number overstrained the natural
capacities of the park. In 1965 it was decided to limit
the elephant population to 7000 animals. In the
following 18 years, about 16,200 elephants were
culled. Due to political and public pressure, the culling
policy was abandoned in 1994. Since then, elephant
numbers in the park increase by 7% per annum and
culling is reconsidered .
In captivity, breeding success is still insufficient to
come by Wiese reported that without imports from the
wild or dramatically improved fecundity, the captive
Asian elephant population in North America will
decline to 10 individuals in 50 years . The prospect
for the captive North American African elephant
population, with a decline of 2% per year, is almost
equally alarming . Reasons for poor reproduction in
captivity are numerous. Proven breeder bulls are rare
and the majority of captive females that were once
imported from the wild are now post reproductive age.
To improve captive breeding, ultrasound guided
artificial insemination was developed [11–13].
In light of the elephant situation in the wild and in
captivity it is obvious that more knowledge about its
reproductive biology is needed. Our understanding of its
embryogenesis in particular will enhance our abilities to
manage in situ and ex situ populations appropriately.
Foetal specimens collected during culls provided for
our knowledge on elephant prenatal development 
and placentation [15–18]. However, the age of the
specimens described was not known and the develop-
ment of the embryo could not be correlated to the
Pregnant elephants examined by 2D and 3D ultrasound
Scanned elephant Species Studbook # Institution
Elephant 1 La
143 Indianapolis Zoo, In
Elephant 2 Em
356 African Lion Safari,
Elephant 3 Em 264 African Lion Safari,
Elephant 4 Em 347 African Lion Safari,
Elephant 5 Em 8403 Whipsnade Wild An
Elephant 6 Em 424 African Lion Safari,
African elephant (Loxodonta africana).
Asian elephant (Elephas maximus).
development of its extraembryonic organs and placenta
formation. Since gestational age was not known,
specimens were classified according to their body mass
[19,20]. Growth curves derived from newly published
data showed a systematic error in previously published
growths graphs of up to 60 days .
Transrectal ultrasound was already employed in field
contraception studies conducted between 1996 and
1998 in the Kruger National Park in South Africa .
Using ultrasound, the reproductive status of the
elephant was determined prior subcutaneous implanta-
tion of contraceptive hormones to avoid hormone
treatment of pregnant animals. However, 3 of 57
animals that were diagnosed as non-pregnant and
treated with contraceptives turned out to be pregnant
when a second ultrasound exam was performed 1 year
later. These preliminary findings suggested a delayed
implantation in the elephant and prompted us to conduct
further study of elephant embryo development pre-
sented here. This study aimed to describe the early
embryonic development in elephants as seen by
transrectal 2D and 3D ultrasound in correlation with
gestational age with a special focus on depicting the
topographic relationship of the
and their function in placental formation.
2. Materials and methods
Five Asian elephants (E. maximus) and one African
elephant (L. africana) were examined (Table 1). All
elephants were kept in free contact management setting.
Gestational age in the six females was known from
artificial insemination (n = 1) or observed mating
(n = 5) and corresponded with LH and progesterone
measurements [23,24]. In addition to hormonal data, the
rupture of the leading follicle was monitored by
ultrasound. The day of ovulation was defined as day
0 of gestation.
No. of exams Gestational age (days p.o.)
dianapolis, USA 4 37, 44, 58, 62
Cambridge, CA 12 67–112
Cambridge, CA 17 12–115
Cambridge, CA 28 38–116
imal Park, GB 3 74, 89, 116
Cambridge, CA 46 52–116
B. Drews et al. / Theriogenology 69 (2008) 1120–11281122
2.2. Ultrasound examination
Transrectal ultrasound examinations were performed
as described by Hildebrandt et al. . The number of
ultrasound examinations during the embryonic period
(days 0–116 post-ovulation, p.o.) ranged from 3 to 37
per animal (Table 1). The ultrasound systems used in
this study included the stationary Voluson 530 and
Voluson 730 and the portable Voluson ‘‘i’’ (GE
Using 3D ultrasound, the structure of interest was
first located with conventional 2D ultrasound before
switching to volume mode. While the hand of the
examiner did not move, the transducer was automati-
cally pivoted over the predefined area by a probe
internal motor. The volume was acquired by scanning a
set of consecutive 2D planes and continuously storing
the images. The pixel were interpolated into voxel.
Seconds after acquisition, the scanned region was
displayed on the screen. It was then checked if the
volume contained the structure of interest and if
necessary, the scan was repeated.
All ultrasound examinations were recorded on
miniDV tapes (GV 100P, Sony Inc., Japan) for
retrospective analysis. 3D scans were stored on
magneto-optical-discs or CD. Each ultrasound exam-
ination took between 30 and 90 min.
2.3. Retrospective analysis
For retrospective analysis, every ultrasound record-
ing was carefully viewed with a video recorder
connected to a monitor. Video sequences were
digitalized (Adobe Premiere Pro 1.5, Adobe
Inc., USA) and characteristic sonograms were gener-
ated and stored as jpeg-files. For the measurement of
biometric parameters (analySIS
Soft Imaging System
GmbH, Germany), the optimal plane showing the
structure in full extent was selected. For the evaluation
of the 3D scans, the volume data could be displayed in
Fig. 1. bar = 10 mm (A) Sonogram of free fluid (arrows) within the lumen
vesicle (Ev) at day 52 p.o. (C) Sonogram of the embryonic vesicle with the em
day 63 p.o.
three different modes: multiplanar mode, render mode
and inverse render mode (4DView, GE Healthcare,
Austria). In multiplanar mode, the object of interest is
displayed simultaneously in three perpendicular planes
(sagittal, transverse and frontal). In this way the
structure to be measured was depicted in its optimal
plane and measurements were taken without prior
calibration. The free rotation of the object and the
choice of different section planes permitted the
topographic analysis of the scanned volume. In render
mode the embryo was depicted in a 3D view, giving an
impression of its surface structure. In contrast, the
algorithms of the inverse render mode visualize those
parts of the data set which are anechoic, such as fluid
filled cavities. Thus the size, location and changes in
formation of the yolk sac, the amnion and the allantois
could be visualized.
3.1. Embryonic vesicle
In weeks 1–4 p.o., the endometrium appeared
hyperechogenic and was barely distinguishable from
the myometrium. In week 5 p.o., the endometrium
increased in thickness and appeared hypochechogenic
compared to the myometrium. Between days 36 and
45 p.o., free fluid within the uterus was observed. On
day 46 p.o., the fluid accumulation became more
distinct (Fig. 1A). A definitive embryonic vesicle
could not yet be visualized. An embryonic vesicle,
clearly defined by two hyperechoic lines, was
depicted for the first time on day 50 p.o. (Fig. 1B).
It was found in the lower section of the uterine horn
(pseudouterine body), ipsilateral to the ovary where
ovulation had occurred. The diameter of the round-
shaped vesicle was 8 mm. The endometrium sur-
rounding the embryonic vesicle appeared darker than
the rest of the endometrium, indicative for the
decidual reaction of the implantation site.
of the uterine horn (dashed arrows). (B) Sonogram of the embryonic
bryonic disc (Ed) at day 59 p.o. (D) Sonogram of the embryo proper at
B. Drews et al. / Theriogenology 69 (2008) 1120–1128 1123
3.2. Choriovitelline placenta and formation of the
A faint hyperechoic dot close to the endometrium on
day 59 p.o. indicated evidence of embryonic tissue
(Fig. 1C). The still round shaped embryonic vesicle had
increased to 30 � 0.2 mm. A definite embryonic
structure of 5 mm became visible on day 62 p.o. when
the embryonic vesicle was 35 mm in diameter (Fig. 1D).
Embryonic heartbeat was detected as flickering motion
on day 71 p.o. The embryonic heart was also identified
by colour Doppler. On day 76 p.o., a thin membrane
divided the embryonic vesicle into two compartments of
unequal size. The larger compartment, ventral to the
now 7-mm embryo, was identified as yolk sac and the
smaller compartment dorsal to the embryo as not yet
divided allantois. For identification of the different
cavities the structures were traced back from later stages
where they were unambiguous. The yolk sac was large
and filled the greatest part of the embryonic vesicle. At
the abembryonic pole it was flattened and in full contact
with the underlying endometrium, providing evidence
for a functional choriovitelline placenta. The amniotic
cavity could not be depicted at that stage.
3.3. Chorioallantoic placenta
On day 73 p.o., a subdivision of the allantois in four
compartments became visible. In close proximity to the
embryo (15 mm), the endometrium protruded into the
chorioallantoic cavity. This part of the endometrium
appeared slightly hyperechoic and denoted the begin-
ning development of the chorioallantoic placenta.
With the progressing pregnancy, the embryo showed
a dorsoconvex flexure and head and rump could be
distinguished from day 83 p.o. onwards. The allantoic
compartments increased in size, embracing the yolk sac
from its lateral sides. The yolk sac was oval in shape and
still formed a choriovitelline placenta at the abem-
bryonic pole. At the transition of the allantoic
compartments to the choriovitelline placenta sac, the
adjacent endometrium was slightly hyperechoic,
demonstrating endometrial activation. A small hypoe-
choic cavity around the embryo was identified as
amniotic fluid limited by a fine allantoamniotic
membrane. On day 85 p.o., the architecture of the
allantoic compartments was clearly depicted (Fig. 2A)
and individual differences in the topography became
evident. In 2D mode, the allantochorionic placenta was
seen as protrusion into the embryonic vesicle. In inverse
render mode, the indentation of the allantoic sacculation
alluded to the allantochorionic placenta (Fig. 2B). The
embryo itself could not be outlined in inverse render
mode. Its position was indicated by the oval shaped
impression of the yolk sac (Fig. 2B).
Beginning on day 95 p.o., fore and hind limb buds of
the embryo were observed and the triangular nose
clearly characterised the embryo as an elephant
(Fig. 2C). A widening of the umbilical cord was
identified as physiological midgut herniation. The
allantoic compartments had increased in size and
reached the abembryonic pole, almost separating the
yolk sac from the endometrium (Fig. 2C and D). Further
development of the allantochorionic placenta resulted
in the formation of a placental band, which was not yet
completed. The form and volumes of the allantoic
compartments and the yolk sac greatly varied between
the different elephants as well as between the different
examination days of the same elephant. This phenom-
enon can be explained by the fact that the chorioal-
lantoic membrane, which is not involved in
placentation, is not attached to the endometrium. The
filling of the guts, the positioning of the pregnant
elephant during the exam and the position of the uterus
therefore influence the topography of the allantoic
compartments. The double membranes which are
formed by the adjacent allantoic sacculations were
also free, so that the embryo itself was not bound to a
constant position in relation to the placenta, either. It
was found in parallel as well as in perpendicular
position to the placental band. Between days 95 and 102
p.o., front and hind limb buds of the embryo had grown
to proper feet and movements of the latter were
observed. The nose had elongated in a short trunk and
the ears appeared as roundish structures lateral of the
head. The ring formation of the chorioallantoic placenta
was completed between days 97 and 103 p.o. However,
in two females, the principle placental ring formation
remained interrupted in one and two sections, respec-
tively. These sonographic findings were confirmed in
one elephant by the examination of the afterbirth. The
yolk sac became pedunculated beginning on day 97 p.o.
Due to its long stalk, it could be observed ventral or
dorsal to the embryo. Beginning on day 100 p.o., the
different embryonic compartments were better distin-
guished as their fluid quality changed: the quality of the
allantoic fluid became more echo dense in contrast to
the yolk sac fluid which remained hypoechoic and clear.
With advancing gestation, the embryo increased in
size and filled the greater part of the chorioallantoic
cavity, so that it was frequently found in perpendicular
position to the placental band from day 110 p.o.
onwards. With the elongated and slightly curved trunk,
the big ears and the feet with their characteristic flat
B. Drews et al. / Theriogenology 69 (2008) 1120–11281124
Fig. 2. bar = 10 mm (A) Sonogram of elephant conceptus at day 83 p.o. with embryo (Em), chorioallantoic placenta (Pl), allantoic sacculations (Al)
and Yolk sac (Ys). (B) 3D sonograms of the same conceptus at day 83 p.o. in inverse render mode depicting the topography of allantoic sacculations
(Al) and yolk sac (Ys). The position of the embryo can be deduced from the impression of the yolk sac. (C) Sonogram of elephant conceptus at day 95
p.o. The allantoic sacculations (Al) have enlarged and begin to displace the yolk sac (Ys) from the endometrium. The trunk (Tr) and forelimb buds
(Fl) of the embryo are recognizable. The amnion is a fine membrane surrounding the embryo. The allantochorionic placenta (Pl) protrudes into the
allantochorionic cavity. (D) 3D sonogram of elephant conceptus at day 95 p.o. in inverse render mode, illustrating the volumes of allantois (Al) and
yolk sac (Ys). The allantoic sacculations embrace the embryo from lateral and dorsal. (E) 3D sonogram in render mode of elephant conceptus at day
116 p.o. The embryo has developed into a foetus, which displays the typical elephant shaped trunk (Tr), ear (Ea), front (Fl) and hind legs (Hl). On its
ventral side, the paired allantoic vessels (Av) that travel to the placenta (Pl) can be seen. (F) 3D sonogram in inverse render mode of the same
conceptus at day 116 p.o. The ring shaped impression of the allantois (Al) marks the fully established chorioallantoic placenta. The pedunculated
yolk (Ys) sac has greatly diminished in size. (G) Sonogram of an embryo at day 73 p.o. (H) Corresponding drawing of an early conceptus according
to Perry depicting free uterine lumen (Ul), the different germ layers and extraembryonic organs (Am—amnion, Al—allantois, Ys—yolk sac).
Mesoderm is indicated as red-hatched line, trophoblast as blue line and the surrounding endometrial layer as black line.
B. Drews et al. / Theriogenology 69 (2008) 1120–1128 1125
sole, the outer shape of the embryo showed a great
alikeness to its adult counterpart (Fig. 2E), indicating
the end of the embryonic period. Close to the abdomen,
the subdivision of the umbilical vessels became visible
(Fig. 2E). The yolk sac was still present, but had shrunk
considerably until day 116 p.o. (Fig. 2F).
In literature, description of early embryonic devel-
opment in the elephant in association with the formation
of the extraembryonic organs was hampered by lack of
adequate age determination and scarce availability of
early specimens. Since the age of the specimens was not
known to the authors, a direct comparison with the
images obtained by ultrasound was not possible.
However, the 3D ultrasound technique provided the
free selection of plane within the 3D volume data sets.
With this method it was possible to depict ultrasound
sections which corresponded to the histological sections
published in literature . The comparison of the
conceptus of known age as seen by ultrasound allowed
the reliable age determination of the previously
published embryo data [16–18].
4.1. Early blastocyst
Embryonic development in general begins with the
fertilization of the oocyte within the oviduct. Fertiliza-
tion triggers cleavage of the fertilized oocyte to the
morula and eventually to the blastocyst stage while it
travels down the oviduct to the uterus. Before it attaches
to the uterine wall, the blastocyst moves freely within
the uterine lumen. The time period between ovulation
and implantation differs greatly between species
(human: 20 days , dog: 12 days , sheep: 16
days ). In our study, an embryonic vesicle or
blastocyst with a diameter of 8 mm could first be
detected by ultrasound on day 50 p.o. Perry described a
bilaminar blastocyst in the pre-attachment phase with a
diameter of 10 mm after fixation . Allen and co-
workers rescued two specimens that consisted of a
choriovitelline membrane containing several millilitres
of fluid [17,18]. These specimens were obviously in a
later developmental stage since the trophoblast was
already attached to the endometrium [17,18]. From the
comparison of the ultrasound data with the available
histological data we conclude that the blastocyst
observed by ultrasound was still in an early stage of
implantation. The time period between ovulation and
implantation is therefore extended, suggesting that the
elephant exhibits delayed implantation.
Delayed implantation or diapause is a typical feature
of marsupials , enabling the lactating mother to
store an unimplanted blastocyst in an arrested stage of
development in the uterus. If the newborn is removed
from the pouch, the quiescent blastocyst reassumes its
development. Other mammalian species that exhibit
delayed implantation independent from lactation
include bears , mustelids , and the European
roe deer as the so far only member of the artiodactyls
described . In the European roe deer, the hatched
blastocyst exhibits reduced mitotic activity for 5 months
and only reassumes its normal development shortly
before implantation [33,34]. During implantation,
serum progesterone levels are elevated [35,36]. Inter-
estingly, the period of implantation in the elephant also
coincides with a first rise in serum progesterone in
weeks 6–8 p.o. .
4.2. Development of the embryo proper and the
Before the conceptus establishes its placenta, it
forms its extraembryonic organs such as amnion, yolk
sac and allantois. The amniotic membrane directly
envelops the embryo with its fluid representing the
water environment where the life of vertebrates started.
Yolk sac and allantois play an important role in placenta
formation since their mesoderm provides the vascular
supply of the placenta. Whereas the choriovitelline
placenta is the definitive placenta of marsupials, it is
only transiently present in some eutherians and replaced
by the chorioallantoic placenta early in ontogenesis
. A choriovitelline placenta was also described in
the elephant [16–18].
An embryonic disc was first observed by ultrasound
on day 59 p.o., when the blastocyst had a diameter of
30 mm. The respective developmental stage described
by Perry was a blastocyst consisting mainly of a large
primitive yolk sac where mesoderm formation had just
started and an embryonic disc was present .
By ultrasound, the embryonic disc formed into a
definite embryonic structure on day 62 p.o. and the yolk
sac was in contact with the surrounding endometrium. A
conceptus described by Perry contained an embryo of
5 mm which was folded off and closely invested in its
amnion . A mesoderm covered yolk sac was
present. Perry assumed that the yolk sac in this
specimen was near its maximum size. The uncomparted
allantois had just reached the chorion at one place and
exocoel was described . By sonography, an allantoic
vesicle was observed on day 71 p.o., when the embryo
had a size of 7 mm. By that time, the flattened yolk sac
B. Drews et al. / Theriogenology 69 (2008) 1120–11281126
at the abembryonic pole, closely applied to the
underlying endometrium, demonstrated a functional
When the sonogram of the embryo on day 71 p.o.
(Fig. 2G) is compared to Perry’s drawing of a 5-mm
embryo (Fig. 2H) the similarity of the two images is
striking. Although the embryo observed by ultrasono-
graphy on day 71 measured already 7 mm, the size
difference can be neglected due to the morphological
alikeness. In the ultrasound image, no free uterine lumen
can be observed. The free uterine lumen described by
Perry suggests that attachment is only superficial and that
the trophoblast was detached during processing.
On day 76 p.o. the allantois became comparted and
the chorioallantoic placenta began to develop. The yolk
sac was still large and in contact with the endometrium.
A subdivision of the allantois was described by Perry in
an embryo of 20 mm . The architecture of the
allantoic compartments could not be reconstructed
owing to fragmentation during fixation. The yolk sac in
this specimen had considerably reduced. Perry’s
embryo of 20 mm in length corresponds to an age of
Fig. 3. Depiction of the embryonic and foetal period of the elephant. The dif
are shown on an explosion of the time axis. The time window for transrectal
depicted by a violet line, the yolk sac by an orange line. The allantoic comp
allantoic compartments are outlined although the typical subdivision in four
approximately 83 days . In contrast to the
observation of Perry, our ultrasound data show that
the yolk sac at this stage is prominent and forms a
choriovitelline placenta. The choriovitelline placenta is
replaced by the chorioallantoic placenta between days
95 and 103, when the embryo has formed fore and hind
limbs and the trunk begins to develop. On day 116,
when the embryonic period has reached its end and the
foetus displays its typical elephant shape, the yolk sac is
still visible but considerably diminished in size. The
embryonic development of the elephant as described in
this study is illustrated in Fig. 3
The shift of the allantoic fluid quality from clear to
cloudy around day 100 p.o. indicates the production of
urine by the well developed and functionally active
mesonephros of the elephant . The amniotic cavity
was found to be very small compared to the allantoic
sacculations. From this observation we conclude that
the allantois provides for the greatest part of the foetal
fluids. The rupture of the allantoic sacculations during
the birthing process facilitates easy down gliding of the
foetus through the long-urogenital tract of its mother.
ferent morphological stages of the embryonic period (days 0–116 p.o.)
ultrasonography is from days 0 to 240 p.o. The trophoblast/chorion is
artments are shown as a green line. Owing to the 2D graph, only two
compartments was observed. The chorioallantoic placenta is indicated
B. Drews et al. / Theriogenology 69 (2008) 1120–1128 1127
In conclusion the longitudinal ultrasound monitoring
provides not only exact staging of the embryo but also
contributes to morphological description of early
implantation stages, extraembryonic organs and the
development of the elephant embryo.
The authors thank the staff at the African Lion Safari,
CA and at Whipsnade Zoo, GB, for their great elephant
expertise and support. The work at the African Lion
Safari has been funded by a grant of the German
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- Early embryo development in the elephant assessed by serial ultrasound examinations
Materials and methods
Choriovitelline placenta and formation of the embryo
Development of the embryo proper and the extraembryonic organs
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