ll B R.AR.Y
OF THE
UNIVERSITY
OF ILLINOIS
590.5
FI
v. 35
cop. 3
NATURAL HISTORY
SURVEV
PLACENTATION OF THE PIGMY
TREESHREW
TUPAIA MINOR
WALDEMAR MEISTER
AND
D. DWIGHT DAVIS
FIELDIANA: ZOOLOGY
VOLUME 35, NUMBER 4
Published by
CHICAGO NATURAL HISTORY MUSEUM
:PTEMBER H, 1955
PLACENTATION OF THE PIGMY
TREESHREW
TUPAIA MINOR
WALDEMAR MEISTER
Associate, Division of Vertebrate Anatomy
AND
D. DWIGHT DAVIS
Curator, Division of Vertebrate Anatomy
FIELDIANA: ZOOLOGY
VOLUME 35, NUMBER 4
Published by
CHICAGO NATURAL HISTORY MUSEUM
SEPTEMBER 14, 1956
THEllBRWnrOFTHF
OCT 2 1966
PRINTED IN THE UNITED STATES OF AMERICA
BY CHICAGO NATURAL HISTORY MUSEUM PRESS
FI
Placentation of the Pigmy Treeshrew
& /
Tupaia minor
The Bornean Zoological Expedition of Chicago Natural History
Museum collected three pregnant uteri of the pigmy treeshrew,
Tupaia minor. In view of the important position of the Tupaiidae
at, or at least near, the base of the primate line, information on the
several species composing this family is extremely desirable. The
fetal adnexa of the treeshrews are very inadequately known, and
have not hitherto been examined from the standpoint of modern
concepts.
The pigmy treeshrew is the smallest of the treeshrews. The
average head and body length is about 130 mm., and adult animals
weigh about 50 grams. The species occurs in Borneo, Sumatra, and
the southern part of the Malay Peninsula. Its relationships to other
species of the genus Tupaia are unknown.
Amniogenesis and the morphogenesis of the placenta in Tupaia
javanica, a small long-tailed Javanese species, were described and
figured many years ago by Hubrecht (1895, 1899). De Lange
and Nierstrasz (1932) reviewed the placentation of Tupaia javanica
very briefly, adding little to Hubrecht's data. Recently van der
Horst (1949) redescribed the placentation of Tupaia javanica, partly
from a re-examination of Hubrecht's slides and partly from newly
sectioned material from the Hubrecht collection. Van der Horst
challenged many of Hubrecht's interpretations, replacing them with
unique and most extraordinary interpretations of his own. Van der
Horst's views differ not only from those of Hubrecht, but from
those of all other students of the mammalian placenta.
MATERIAL AND METHODS
The material on which this study is based was collected in the
vicinity of Sandakan, North Borneo, in 1950. Two uteri represent
pre-implantation and early blastocyst stages of pregnancy, re-
spectively, while a third was near term (C-R length of fetus 29 mm.).
The intact uteri were preserved in 10 per cent formalin in the field,
73
74 FIELDIANA: ZOOLOGY, VOLUME 35
and were transferred some months later to 68 per cent alcohol.
The reproductive tract of the advanced pregnancy was preserved
in situ.
Each specimen was first dissected, using a 9X binocular micro-
scope where necessary. Tissues for histological study were removed,
embedded in paraffin, and serially sectioned at 8-10 micra. All sec-
tions were stained with hematoxylin-eosin.
OBSERVATIONS
Morphology of Reproductive Organs
Gross structure. The female reproductive organs of Tupaia
ferruginea (=T. glis) were described very briefly by Jones (1917),
and except for brief notes by earlier workers this is the only descrip-
tion of these organs in the Tupaiidae. Tupaia glis is a much larger
species than T. minor.
The uterus is bicornuate in Tupaia and very similar to that of
the Insectivora in gross form. In the early stages of pregnancy
it consists of a short median corpus and two elongate horns (pi. 10,
fig. 1), and bears only a general resemblance to the figures given by
Jones. The corpus consists largely of an elongate massive cervix,
which projects prominently into the vagina, leaving deep fornices
at the proximal end of the vagina. The corpus measures about
7 mm. in length (to the distal end of the cervix).
The lining of the cervical canal is thrown up into longitudinal
rugae, while the lining of the uterine part of the corpus is smooth.
The cornua are short and stout, measuring about 7 mm. in length
by 4 mm. in diameter.
The oviduct is a relatively long, slightly contorted tube enclosed
between the two layers of the broad ligament. It measures about
15 mm. in length by about 1 mm. in diameter and is curved in a loop
that almost completely encircles the ovary. The infundibulum lies
at the proximal pole of the ovary. It has a funnel shape, is provided
with short fimbriae, and is attached to the ligament near the en-
trance to the bursa ovarica.
The ovary is a flattened triangular body about 2 mm. in greatest
diameter, the apex lying adjacent to the infundibulum. The ovary
is enclosed in a peritoneal recess (the ovarian bursa) that encloses
both ovary and oviduct. The bursa communicates with the peri-
toneal cavity through a wide slit-like opening near the tip of the
uterine horn.
MEISTER AND DAVIS: PIGMY TREESHREW 75
The broad ligament is a triangular fold of peritoneum extending
between the uterine horn and the ventro-lateral wall of the pelvis.
The round ligament is a narrow fibro-muscular band lying in the
lateral edge of the broad ligament. It reaches the pelvic wall in the
region of the inguinal canal. The two round ligaments form an
angle of about 60 when stretched. Beyond the round ligament
the peritoneal fold is continued dorsad and mesad as a recto-uterine
fold, to pass dorsal to the rectum where it continues as the short
mesorectum. The two recto-uterine folds form a deep recto-uterine
pouch.
In late pregnancy (pi. 10, fig. 2) the cornua are much enlarged
and are thin-walled throughout their entire length. There are two
fetuses, one in each horn, apparently near term; the crown-rump
length is 29 mm. Each fetus lies with the head toward the uterine
body, the belly directed toward the maternal midline. The head is
flexed, the limbs are tightly pressed against the belly, and the tail is
curved forward along the side of the body. The two parts of the
placenta embrace the fetus on either side of its ventral midline. The
fetuses are unpigmented; there are short dark vibrissae and a few
long hairs are scattered over the body.
Histology. A complete set of transverse serial sections of one
uterine horn was cut, representing a very early stage of pregnancy.
No trace of the blastocyst was found in the uterine cavity, indicat-
ing that the cleaving egg had not yet reached the uterus. The
following description is based on this specimen (pi. 13, figs. 11, 12).
The myometrium is composed of a relatively thin outer layer of
longitudinal muscle fibers and a much thicker inner layer of circular
fibers. The uterine vessels are situated in the outer part of the
circular muscular layer, where they form a relatively regular vas-
cular sheet from which branches are sent to the endometrium.
The endometrium is as thick as the whole myometrial layer and
is slightly furrowed. On opposite sides of the uterine cavity it con-
tains the two cushion-like trophospongia (Hubrecht's terminology),
the pre-implantation placental structures characteristic of Tupaia.
The epithelial lining of the uterus consists of tall simple columnar
cells that show no trace of cilia. Uterine glands penetrate the whole
thickness of the endometrium and are sectioned in all directions.
The uterine glands are cylindrical, not dilated at the fundus, and
with no constriction at the neck. The glandular epithelium is of
columnar or low cuboidal type; no cilia are present. There is no
evidence of active secretion at either early or late stages of gestation.
The glands are densely and evenly distributed through all parts of
76 FIELDIANA: ZOOLOGY, VOLUME 35
the endometrium except in the trophospongia, which consists of
dense endometrial stroma in which glands are wanting. There is
a thin layer of uterine glands, flattened between the trophospongia
and the myometrium, beneath the trophospongia; in some places
the trophospongia is in direct contact with the myometrium, and
in such places there are no glands and many vessels pass from the
myometrium into the trophospongia.
The bursa ovarica enclosing the ovary is composed of a double
layer of peritoneum containing blood vessels for the ovary. Its
structure is similar to that of the uterine ligaments. The germinal
epithelium on the surface of the ovary is of a tall simple columnar
type. The cortex is densely packed with primary follicles. More
mature follicles are situated deeper, protruding into the medullary
zone. The medullary zone is composed of dense ovarian stroma
with vessels; it contains a large corpus luteum of pregnancy and
a relatively small corpus albicans (pi. 14, fig. 15).
The oviduct (pi. 14, fig. 17) has a muscular wall with a mostly
circular arrangement of the fibers. The mucosa is thrown up into
numerous folds that protrude into the lumen. The lining of the
oviduct consists of tall simple columnar epithelium, which is ciliated.
Placenta and Fetal Membranes
The placenta is double discoidal, consisting of two sharply
circumscribed kidney-shaped structures, approximately equal in
size, each measuring about 18 X 8 mm. along the inner curvature.
The two structures are attached to the dorsal and ventral walls,
respectively, of the uterus. Implantation is bilateral, the two
placental structures attaching on either side of the mesometrial
line; their adjacent borders are only about 7 mm. apart. There
is no macroscopically visible yolk sac. The umbilical cord is long,
measuring about 20 mm. in length. It is untwisted and is flattened
in cross section (pi. 14, fig. 18). A few millimeters before reaching
the placentas the cord divides into two subequal funnel-shaped groups
of umbilical vessels, one for each of the two placental structures.
The vessels enter each placental structure from its anti-mesometrial
side. No vessels pass across from one placental structure to the
other.
The Blastocyst Stage
One uterine horn containing a pregnancy in the blastocyst stage
was serially sectioned. The blastocyst was probably at an early
MEISTER AND DAVIS: PIGMY TREESHREW 77
stage of implantation. It is in the uterine cavity, detached from the
endometrium and partly destroyed by maceration (pi. 13, figs. 13,
14). The site of implantation may be identified by the presence
of the developing syntrophoblast, eroding the uterine epithelium
and penetrating into the uterine stroma at the site of the tropho-
spongia.
The uterine wall is only slightly distended, compared with the
earlier pregnancy shown in plate 13, fig. 11. The blastocyst is at the
trilaminar stage of development. The trophoblast has both cyto-
and syntrophoblastic proliferations. The two placental primordia
are interconnected by a thin trophoblastic layer underlain by
loosely arranged extra-embryonic coelomic mesoderm (pi. 13, fig.
14). The trophospongia, forming the decidua basalis of the develop-
ing placenta, consists of a dense, well-vascularized proliferation of
the endometrial stroma. On the surface of the trophospongia the
uterine epithelium is lost and the superficial layer of the stroma
eroded, an obvious indication of the activity of the syntrophoblast
at the site of implantation.
The yolk sac is a small bilaminar vesicle lying beneath the
embryonic plate. In the embryonic hemisphere the embryonic
plate is surrounded by undifferentiated extra-embryonic mesoderm;
it is impossible to tell how far this mesoderm extended into the
abembryonic hemisphere. There is no indication of amniogenesis.
The Late Fetal Stage
The chorio-allantoic placenta is of the hemochorial labyrinthine
type. It is composed of a thin endometrial part, the decidua
basalis (maternal), and a thick chorio-allantoic part (embryonic).
The decidua basalis is moderately thick, about one-seventh of
the thickness of the entire placenta at its thickest part. It is com-
posed of endometrial stroma, through which pass the endometrial
arteries communicating with the maternal feeder channels. A trophic
uterine glands are scattered through the tissue of the decidua
basalis and the decidua parietalis. The glandular epithelium is low,
and there is no evidence of secretory activity. The uterine epithe-
lium is completely lost on the surface of the decidua basalis but
remains intact on the decidua parietalis, where it lies against the
chorion.
The trophoblast is about five times as thick as the decidua. It is
composed of a thin basal syntrophoblastic layer in contact with the
decidua basalis, and a much thicker labyrinthine part. In several
78 FIELDIANA: ZOOLOGY, VOLUME 35
places the placenta exhibits degenerative changes, consisting of
localized deposits of fibrin in the trophoblastic tissue (pi. 11, fig. 5).
The thickness of the basal layer varies, and in some places it is even
interrupted.
The labyrinthine part of the trophoblast consists of a heavy
meshwork of syncytium enclosing relatively narrow maternal
sinuses. The sinuses are in wide communication with one another.
Toward the margin of the placenta the meshwork becomes coarser,
and isolated scattered lacunae appear. The fetal capillaries are
enclosed in crude finger-like structures, not quite villi but certainly
villus-like. Each villous structure is composed of a core of chorionic
mesenchyme containing fetal capillaries, surrounded by a layer of
syntrophoblastic tissue of varying thickness, and separated from
adjacent villi by spaces filled with maternal blood. The spaces
between the villi form a maze of irregular trophoblastic channels.
Thus the actual barrier to fetal-maternal interchange consists of
three fetal tissues: the syn trophoblast, the chorionic mesenchyme,
and the endothelium of the capillary, and Tupaia clearly shows
the labyrinthine hemochorial relationship between maternal and fetal
circulations.
The large branches of the umbilical vessels on the fetal surface
of the placenta ramify to and from the villi. The vessels penetrate
into the depth of the placenta before breaking up into capillaries.
No giant cells were observed in this placenta.
There is no evidence that the allantoic vesicle reaches the fetal
surface of the placenta.
The yolk sac consists of a large thin-walled bilaminar omphalo-
pleure, provided with small vitelline vessels in its mesenchyme layer
(pi. 12, fig. 6). The cavity of the yolk sac is lined with a single layer
of flattened endodermal cells, which are taller where the omphalo-
pleure is adjacent to the margin of the placenta. The mesenchymal
layer of the yolk sac fuses with that of the chorion. It is impossible
to determine on this specimen whether the yolk sac is inverted or not.
The chorion is in direct contact with the endometrial stroma
beneath the placenta, but beyond the placental margin the uterine
epithelium is intact (pi. 12, fig. 6). Thus, over the whole decidua
parietalis the chorionic epithelium is in contact with the uterine
epithelium, a primitive condition.
The amnion covers the fetal surface of the placenta as a part of
the inner surface of the gestation sac (pi. 11, fig. 3; pi. 12, fig. 6).
MEISTER AND DAVIS: PIGMY TREESHREW 79
Maternal Circulation in the Placenta
Maternal blood is delivered to the trophoblastic labyrinth
through large feeder channels (pi. 11, fig. 4), which are connected
with the endometrial arteries of the decidua basalis. These channels
have relatively thick trophoblastic walls, and their lumens are lined
with the same trophoblastic elements. They are located at one side
of the placenta, in the region between the middle and outer thirds
of the placental diameter. The channels penetrate the thickness of
the placenta to about its center, where they break up into smaller
inter-villous trophoblastic channels. Numerous trophoblastic la-
cunae of various sizes, in the marginal part of the placenta opposite
to the feeder channels, collect de-oxygenated maternal blood from
the inter-villous trophoblastic channels and return it to the general
maternal circulation via the uterine veins. These venous lacunae
have thin trophoblastic walls, often composed of a single layer of
cells (pi. 11, fig. 5).
DISCUSSION
Our data agree completely with the early work of Hubrecht
(1895, 1899) on Tupaia javanica. Unfortunately Hubrecht's interest
in his material was very specialized (amniogenesis, morphogenesis
of the placenta) and covered only a fraction of the broad area used
in modern studies of placentation.
Recently van der Horst (1949) attempted to describe the placenta
of Tupaia javanica and to classify it on the basis of the characteristics
of the maternal circulation alone. He states that the maternal
channels are lined with endothelium, and therefore refers to these
structures as "maternal arteries" surrounded by trophoblast, and
interprets the placenta of Tupaia as endotheliochorial ! The relation
between maternal and fetal circulations is nowhere discussed in
relation to classification of placental type. Van der Horst concluded
that in Tupaia "the decaying trophospongia is the main source of
food for the developing embryo" and that "the uterine glands also
feed the embryo"! This author obviously misunderstood Grosser's
classical studies and has contributed nothing to our understanding
of placentation in the treeshrews.
The treeshrews (family Tupaiidae) have often been allied with
the elephant shrews (family Macroscelididae) in a group usually
called the Menotyphla. Most recent students (cf. Simpson, 1945)
have denied this relationship, referring the treeshrews to the primates
and the elephant shrews to the Insectivora. The only description
80 FIELDIANA: ZOOLOGY, VOLUME 35
of placentation in an elephant shrew is a recent study of Elephantulus
myurus by van der Horst (1950). We find van der Horst's paper
extremely difficult to understand and have relied mainly on his
drawings in interpreting his data. The accompanying table sum-
marizes the available data for Tupaia and Elephantulus. It is
evident from the table that the placenta and fetal membranes in
these two forms differ in almost every respect except placental type.
The labyrinthine hemochorial placental type appears to characterize
all insectivores 1 and at least the early stages of rodents; it probably
represents a shared primitive feature rather than indicating affinities.
Data from the placenta and fetal membranes support the view that
the treeshrews and elephant shrews are not closely related.
The fetal adnexa of Tupaia are significantly different from those
of the Insectivora. In detail the conditions in Tupaia represent
stages interpreted by students of placentation as more advanced
than the corresponding stages represented by the Insectivora. Ex-
amples are the vestigial nature of the yolk-sac placenta, the vestigial
allantoic vesicle, and the incipient development of villi in the
trophoblast. Morphologically, these are differences of degree, and
the Tupaia condition is easily derivable from the insectivore con-
dition.
What of the supposed relationship of the treeshrews to the
primates? The diffuse, non-deciduate, epitheliochorial placenta of
the lemurs (both Lemuriformes and Lorisiformes) differs dramati-
cally from that of other primates and closely resembles that of
ungulates. This circumstance has been variously interpreted.
Some authors (e.g. Hill, 1932) have argued that this is an essentially
primitive placental type from which the discoidal, deciduate, hemo-
chorial placenta of the higher primates can be derived. Others
(e.g. Wislocki, 1929) have regarded it as a secondarily simplified
placenta and therefore useless either as an indicator of the affinities
of the lemurs or as representative of a stage in the evolution of the
primate placenta. Still others (e.g. Mossman, 1937) have interpreted
the placental data literally, maintaining that the lemurs are not
primates at all. To us Wislocki's interpretation is the only reason-
able one in the light of existing knowledge, which means that the
lemurine placenta may be omitted from consideration in the present
connection.
On the other hand, the placenta and fetal membranes of Tupaia
are extraordinarily similar to those of the more generalized members
1 Except our term specimen of Echinosorex, described elsewhere.
"3
c
^* O ^
C _fr
"* o O
fl S S
III
-is
c:*
O) co
tructure
o
0>
'">> "
Sog
oT-c ~
C.ti >_
1i
CO
Cebidae 1
antimesorr
superficial
GL* ^ ^
c
2
none
o>
o
c
13
CO
o>
w^: 01
^ o co
22 S"~
^ OJ3
I s w
1^2
B^ ^
labyrinthi
chorial, wi
advanced
structures'
. O
IE
CO >>
>-s
ar placenta
1
^S i
O co
(
1
ed
fl Ss
C 3
C
S
i
j= rt g
>8
C ^
to "
3
"Z^ ti
_w
O >Q
J3 'S
O) "co
C3
o
o>
o"^
Si- 8 .
^2 * >>
3-i: u
o>
0)
03"3
3 -M
. o>
i I-.
S-s3
J3 >
-*J 3
Eik
.Sj
Is s'S
-2 |e
.5
CD
c- eu K
CO ; - et O>
Q. CO m -4J
Hfri
cfl go .,
O e b -S
c^:^ c
bo
c
2
O)
o
c
none
PN
"3
CO
-o"
d> el)
'co co
||i
111
11
CO
<D
O>
C
13
Tupaia
bilateral
superficial
i "3
3 >v ^
g-^'f.S
111!
CO M 'O ^^
^3 tO C
o>
3
ffi
bo
small; no data on
persistence
marginal remnants
persist to term
incomplete inversio:
small and without
villi
two kidney-shaped
structures, unstalke
labyrinthine, hemo-
chorial, with villus-
like structures
small, not reaching
placental surface
CO
C
'
rt
CO
co
is is a misleading tei
E
3a
o
c" 1
a"
CD !
Cl>
A
t,
" . "~-
Elephanlulus 1
mesometrial
eccentric
capsularis incompl
disappears early;
thick basalis; basa
glands large early,
degenerate later
cavitation
large; no data on
persistence
!l
... ot co
CD m
bO T3
* *j 3
inverted, large,
without villi
single, cup-shaped
stalked
labyrinthine, hemi
chorial
medium, reaches
placental surface
"33
bo
J2
o>
ctf
"rt
various authors.
^3 '-i
^i .
11
I*!
E
|
.^
U
a
M
O ^
g
Q^
1
|
oj
o>
r:
Cf}
M
"H.
"a.
"c
c
I
15 *3
03
ti
""*
/
"3
"H,
c
at
>
r
CO ^
jr
OJ
w
"3.
-
<*,
s .
o.
c
4>
o
0) m
P
~*
a
Si
:>,
^ Pi
nplantation:
Orientation
Depth . .
ed
o
'G
o>
mniogenesis .
oik sac:
Bilaminar 01
Chorio-vitel
Vascular spl
horio-allanto
Shape
1
llantoic vesic
1 Authorit;
c.
ri
id
P
3 Wislocki
a former pa
HH
Q
<1
>*
O
<J
c
81
82 FIELDIANA: ZOOLOGY, VOLUME 35
of the Cebidae and Cercopithecidae. In almost every detail they
represent a condition nearly ideally intermediate between such
generalized insectivores as the Tenrecoidea and Erinaceoidea on the
one hand, and the more generalized members of the Anthropoidea
on the other. The placenta is single in insectivores, double in Tupaia,
typically double with one element of the pair secondary in the lower
monkeys, and single again in the higher anthropoids and man. In
Tupaia the villous nature of the trophoblast, with villus-like chori-
onic structures formed around the fetal capillaries, foreshadows the
true villous placenta with the wide, open inter-villous spaces and
true villi of the higher primates. The size and persistence until the
end of gestation of the uterine glands in the decidua basalis seen in
Tupaia appear to differ only in degree from the conditions seen in
the Ceboidea and more primitive cercopithecids. Finally, the other
fetal membranes in Tupaia are intermediate between the insectivores
and the non-lemurine primates. Morphologically the placenta and
other fetal membranes of Tupaia are almost an ideal starting point
from which to derive the corresponding structures of the primates.
These facts are difficult to interpret, whatever significance is
assigned to differences in the fetal adnexa, because of the anomalous
placenta and fetal membranes of the lemurs. Obviously, placental
structures must have evolved, either parallel with or independently
of the rest of the organism. Similarities must be due to genetic
relationship, to parallelism, or to convergence. The agreement
among Tupaia, Tarsius, and the lower Anthropoidea is so broadly
based and detailed that it is unlikely to be due to parallelism or
convergence. The alternative requires the assumption that the
placenta and fetal membranes of the Lemuriformes (exclusive of the
Tupaiidae) and Lorisiformes underwent extensive and radical
change after these stocks arose, whereas the fetal structures of the
Tupaiidae and Tarsiidae have remained relatively unchanged and
to this day differ little from those of the most primitive monkeys.
We see no alternative conclusion that does not involve far greater
improbabilities.
If the lemurs are omitted, the comparative morphology of the
fetal adnexa of the insectivores and primates appears to us to
parallel the comparative morphology of the adult organisms as
closely as could be wished.
MEISTER AND DAVIS: PIGMY TREESHREW 83
SUMMARY
1. The female reproductive organs of Tupaia minor are de-
scribed.
2. The blastocyst and the fetal membranes in a near-term stage
of pregnancy are described.
3. Placentation is labyrinthine hemochorial, but with villus-like
chorionic structures.
4. The allantois is vestigial and the yolk sac small.
5. The fetal adnexa of Tupaia are very different from those of
Elephantulus.
6. The fetal adnexa of Tupaia are in almost every respect inter-
mediate between those of generalized insectivores and those of the
more generalized Anthropoidea.
REFERENCES
HILL, J. P.
1932. The developmental history of the primates. Phil. Trans. Roy. Soc.
London, (B), 221: 45-178, 17 figs.
HUBRECHT, A. A. W.
1895. Die Phylogenese des Amnions und die Bedeutung des Trophoblastes.
Verh. K. Akad. Wetenschappen Amsterdam, 4, no. 5, pp. 1-66, 4 pis.
1899. tlber die Entwicklung der Placenta von Tarsius und Tupaja, nebst
Bemerkungen iiber deren Bedeutung als haematopoietische Organe. Proc.
4th Internat. Congr. Zool., Cambridge, pp. 343-411, pis. 4-15.
JONES, F. W.
1917. The genitalia of Tupaia. Jour. Anat., (London), 51: 118-126, 7 figs.
LANGE, DAN. DE, and NIERSTRASZ, H. F.
1932. Tabellarische Ubersicht der Entwicklung von Tupaia javanica Horsf.
Ontog. der Wirbeltiere in Ubersichten, 1 : 1-87, 29 figs., 4 pis.
MEISTER, WALDEMAR, and DAVIS, D. D.
1953. Placentation of a primitive insectivore, Echinosorex gymnura. Fieldi-
ana: Zool., 35: 11-26, 1 fig., pis. 4-9.
MOSSMAN, H. W.
1937. Comparative morphogenesis of the fetal membranes and accessory
uterine structures. Carnegie Inst. Washington, Contr. Embryol., 26: 128-
246, 12 figs., 24 pis.
SIMPSON, G. G.
1945. The principles of classification and a classification of mammals. Bull.
Amer. Mus. Nat. Hist., 85, xvi + 350 pp.
VAN DER HORST, C. J.
1949. The placentation of Tupaia javanica. Proc. K. Akad. Wetenschappen
Amsterdam, 52: 1205-1213, 6 figs.
84 FIELDIANA: ZOOLOGY, VOLUME 35
1950. The placentation of Elephantulus. Trans. Roy. Soc. S. Africa, 32:
435-629, 71 figs.
WISLOCKI, G. B.
1929. On the placentation of primates, with a consideration of the phylogeny
of the placenta. Carnegie Inst. Washington, Contr. Embryol., 20: 51-80,
1 fig., 7 pis.
EXPLANATION OF PLATE 10
FIG. 1. Female urogenital system of Tupaia minor in early pregnancy.
The left oviduct has been detached from the bursa and extended. Dorsal view.
X 3.5.
FIG. 2. Pregnant uterus in situ; left horn opened to show placenta. Ventral
view. X 1.
Fieldiana: Zoology, Volume 35
Plate 10
Ovarium
Tuba uterina
Vagina
Cornu dextrum
uteri
Ovarium in
bursa ovarica
Corpus uteri
Lig. latum
Ovarium
Vesica urinaria
Placenta
EXPLANATION OF PLATE 11
FIG. 3. Section through entire placenta in late fetal stage (see pi. 10, fig. 2).
Maternal surface at top, fetal at bottom. The numbered rectangles indicate the
approximate sites at which photographs at higher magnification were taken.
X 15.
FIG. 4. Maternal arterial feeder channel breaking up into inter-villous
trophoblastic channels. The surrounding trophoblast contains numerous villous
structures containing fetal capillaries. The thin dark layer of the basal tropho-
blast is seen at the top. X 100.
FIG. 5. Trophoblastic lacunae collecting venous maternal blood. X 100.
diana: Zoology, Volume 35
Plate 11
EXPLANATION OF PLATE 12
FIG. 6. Fetal membranes at margin of placenta, a, intact uterine epi-
thelium; b, chorion; c, yolk sac; d, amnion. X 112.
FIG. 7. Umbilical vessels at margin of placenta. Artery to the left, vein
to the right. X 67.
FIG. 8. Villous structures, composed of fetal capillaries surrounded by
chorionic mesenchyme covered with trophoblastic layer; trophoblastic channels
filled with maternal blood. X 720.
diana: Zoology, Volume 35
Plate 12
EXPLANATION OF PLATE 13
FIG. 9. Maternal arterial feeder channel in connection with an endometrial
artery. Atrophic uterine glands are present in the decidua basalis. X 100.
FIG. 10. Umbilical arteriole (center) penetrating placenta and breaking up
to form the fetal capillaries of the villous structures. X 100.
FIG. 11. Section through uterine horn in pre-implantation stage. Visible
are the two trophospongial cushions, one on either side of the uterine lumen, the
flattening of the endometrial glands between the trophospongia and the myo-
metrium, and in the myometrium the uterine vessels supplying the trophospongia.
X 36.
FIG. 12. The same specimen as in figure 11, showing an endometrial artery
penetrating into the trophospongia (lower left). X 100.
FIG. 13. Remnants of blastocyst in trilaminar stage of development. Two
placental primordia (detached) at top. Embryonic plate at center, with bilaminar
yolk sac beneath. Portions of extra-embryonic mesoderm, undifferentiated into
splanchnopleure and somatopleure, are shown. X 36.
FIG. 14. Same as figure 13, showing chorionic membrane connecting the two
placental primordia. X 36.
eldiana: Zoology, Volume 35
Plate 13
EXPLANATION OF PLATE 14
FIG. 15. Section through ovary at initial stage of pregnancy. The large
corpus luteum of pregnancy at the top, and the corpus albicans of a previous
pregnancy at the bottom. X 60.
FIG. 16. Tertiary follicle with maturating egg. Two polar bodies are present
in the zona pellucida. X 545.
FIG. 17. Section through oviduct enclosed in bursa ovarica, and part of
ovary containing corpus luteum of pregnancy. X 75.
FIG. 18. Cross section through umbilical cord. Shown are two arteries (top)
and one vein (bottom) and the allantoic duct between the two arteries. X 60.
eld i ana: Zoology, Volume 35
Plate 14
Publication 803
UNIVERSITY OF ILLINOIS-URBANA
