Memoirs MCZ 5403

/niemoirs of

tlje

/iDuseum of Comparative Zoology

AT HARVARD COLLEGE
Vol. LIV. No.

3.

THE
PLACENTATION OF THE MANATEE
(Trichechus latirostris)

BY

GEORGE

B.

WISLOCKI

WITH SEVEN PLATES

CAMBRIDGE,

U.S.A.

IPrtnteD for tbe /iDuseum

December, 1935



THE PLACENTATION OF THE MANATEE
INTRODUCTORY REMARKS
Less

is

known about

mammals. Only two

the placentation of the Sirenia than of any group of

papers,

now some

fifty

years old, exist to the writer's know-

These, by Harting (1878) and Turner (1889),

ledge, regarding this subject.

describe the nature of the fetal inembranes in

mens

of Halicore dugong.

Consequently

receive a well-preserved, intact uterus

chus latirosiris)

of this

Study

.

it

and

two rather poorly preserved

was

of considerable interest to

fetus of the Florida

speci-

me

to

manatee {Triche-

specimen revises and extends to a large degree

the previous knowledge of placentation in the order Sirenia.
of the salient features of the placentation of the

A

summary

brief

manatee, as observed in this speci-

men, has been recently published (Wislocki, 1933). I wish to express
gratitude to Mr. George Nelson of the Museum of Comparative Zoology
i

my
of

deep
Harv-

ard University for securing this valuable and well-preserved pregnant uterus.

GROSS DESCRIPTION
The specimen
preserved fetus in

an entire gravid uterus containing an excellently
The length of the fetus is 44 cm. from snout to tip of tail.

consists of

situ.

a male, possesses the well-developed outer form of a manatee.

The

fetus,

The

skin at this stage

which

is

character of the fetus

The

uterus

is

is

is

set

with scattered short hairs or

well depicted in figure

bristles.

The

outer

1.

a bilobed object consisting of two short, stout cornua, one of

much

The

ovaries

had been

which, containing the fetus,

is

moved from the specimen;

the Fallopian tubes and cervix are present.

very

relationships of the uterus to the fetus

diagrammatically in figure

1.

The

enlarged.

and the

fetus

and

fetal
its

re-

The

adnexa are shown semi-

membranes including the

placenta are located entirely in the right horn of the uterus, no opportunity being
in the lowermost uterine
given, by virtue of the narrowness of the uterine lumen
for
segment, as well as by the fact that the two cornua join almost at the cervix,

the fetal

membranes

The most

to extend into the opposite horn.

striking thing

upon opening the uterus

is

the appearance of the

placenta. It surrounds the fetus as a thick, sharply dehmited purple belt or gir'
In this note I designated my specimen of the Florida manatee as Manatus latirosiris, basing my terI have
minology upon the classification given in the second edition of Max Weber's well-known book.
now changed the designation to Trichechus latirosiris, following the advice of Dr. Glover M. Allen.


PLACENTATION OF THE MANATEE

160

no sense be construed as being

die of the typical zonary type. Its appearance can in

topography and relationships are presented in figures 1, 2, 3 and 5.
The umbiUcal cord is a relatively short, stout mass which radiates Uke a

diffuse. Its gross

collapsed tent from the umbilical ring towards the placenta.

which there are two

sels, of

and one vein

arteries

The

umbilical ves-

at the umbiUcus, divide, within

a centimeter or two from the ring, into four sets of paired vessels which proceed
as four pedicles towards the placenta

The nature

divisions.

umbihcal cord

of these leashes of diverging vessels

shown

is

ceeds, unlike the others,

vessel, a small artery, is given off singly

and pro-

amnion

to reach

around the whole circumference

the placenta at a place remote from the umbiUcal cord

is

chorionic pole

smaller pole

is

is

more extensive than the other

oriented towards the uterine outlet.

completely membranous. The placenta

made up

is

(figs. 1

and

2).

placed to one side of the equator of the entire blastocyst, so that one

membranous

and

of the

placenta constitutes a broad girdle or zone of sharply defined tissue

The
which

which constitute the

In addition to the four major sets of paired

in figure 2.

one seemingly aberrant

vessels,

upon reaching which they undergo further

is

and 2). The

(figs. 1

Both chorionic

poles are

grossly of the type described as zonary

of a series of rather intimately

cemented lobes

of variable size

and contour ranging from four to eight centimeters in diameters (figs. 2 and 3).
The tendency to form lobes is best discerned along the periphery of the placenta.

On

cross section the placenta

is

found to consist

about one centimeter in thickness

(fig. 5).

of a rather firm plate of tissue,

The outer

red or purple, whereas the basal half, constituting

endometrium, is whitish, containing the cut aspects
ies

and

and a

The border

veins.

slightly

its

of

half of the placenta

(fig. 5).

deep

zone of junction with the

numerous endometrial

of the placenta is elevated, possessing

undercut edge

is

From this border the

arter-

a smooth contour

chorion leaves the pla-

centa as a stout, whitish membrane. In the placental zone the fetal tissues cannot

be stripped
intimate.

off

from the maternal, because the interlocking

is

two

is

much

too

Outside the area of the zonary placenta the chorion separates easily

from the uterus,
brane.

of the

The

its

outer surface presenting the appearance of a smooth

uterine surface which

is

mem-

uncovered by stripping away the chorion,

almost identically smooth. There are, however, scattered near the placental

border some half dozen small, round areas no larger than a half of a centimeter
in width where the chorion cUngs tenaciously to the endometrium.

discoidal patches are reddish.

On

These minute

microscopic section they prove to be, as their

gross appearance suggests, minute areas of chorionic attachment structurally

resembling the placenta.

They

are true accessory placental areolae, but their


GROSS DESCRIPTION
total area

is

be practically
3 and

and accordingly

quite negligible,
nil.

The

gross appearance

must

their functional significance

of these areolae

is

shown

in figures 2,

6.

The

membranous chorion

fetal surface of the

abundant blood-vessels, readily
the placental vessels

The

(fig. 2)

and

is

fused throughout

its

entire

suppUed by
naked eye, which are derived from
is

.

semidiagrammatically in figures
extensive,

visible to the

amnion and

relationships of

is

This chorio-allantoic membrane

extent with the allantois.

and

1

allantois are complex.

2.

The

allantois

is

They

shown

are

a lobulated sac which

is

fused everywhere with the chorion from pole to pole, excepting

and

where the amnion succeeds in appl>dng
to the chorion. Thus the allantoic sac is much more extensive than the

for a small triangular area
itself

161

(figs. 1

amniotic sac, and surrounds

it

2)

with the exception of the small triangular area of

amnio-chorionic fusion.

The

allantois consists essentially of four saccular diverticula,

median and two

larger lateral ones.

umbilical pedicle.

The

latter, as

two small

These sacculations are related to the curious
has been said above, consists of four stout

diverging pairs of blood-vessels which can be Ukened approximately to the four

The space within the pyramid is a
antrum from which commodious sacculations lead off through

edges of a hollow quadrilateral pyramid.

common

allantoic

the four sides of the pyramid between the marginal leashes of blood-vessels.

attempt tg show these complicated relationships has been made in figure

membranous
allantois,

form mesenteries

walls of the bulging sacculations

which ensheath the respective leashes

chorionic sac, lying side
surface.

It

is

by

lesser sacculations

side,

area of amnio-chorionic fusion

is

2) .

(fig.

triangular with

its

this point a curious, shallow vortex is

placenta into which the amnion apparently dips

The

It will be

The

vessels at the

noted that this

base near the umbilicus and
lesser allantoic saccu-

formed on the surface

(figs. 1

blood-vessels supplying the placenta and fetal

description.

of the placental

two sacculations that the triangular
where the amnion achieves a restricted

apex on the placenta contiguous to the apices of the two

At

of the

distal to the apices of these

fusion with the chorion overlying the placenta

lations.

and completely

occupy the equator

and fused with the chorion

area not occupied by the allantois exists

its

of reduplicated

and give them a
The two major saccu-

lations extend into the poles of the chorion, fusing with the latter

The two

The

of blood-vessels

mesentery-like attachment along their outer borders.

enclosing the amnion.

2.

An

and

of the

2) .

membranes merit a

umbihcal ring are three in number: two

brief

arteries


PLACENTATION OF THE MANATEE

162

and one

vein.

About two centimeters from the umbilical

ring these di\ade giving

four sets of divergent paired vessels which proceed to the surface of the

rise to

placenta.

In addition to these a pecuUar artery of

medium

size,

without ac-

companying vein, branches off from one of the umbilical arteries and courses
between the amnion and allantois to a distant point on the opposite side of the
placenta

given

Moreover, a number

2).

of

minute blood-vessels are

from the above enumerated paired vessels, which
the amniotic and allantoic sacs with a few fine branches. Thus

off at irregular intervals

supply the walls of
the

and

1

{art., figs.

membranous

walls of these sacs are not totally devoid of blood supply.

approaching the surface

of the placenta the four

the umbilical pedicle give off
surface

major pairs of vessels constituting
large branches which pass to the adjacent placental

The main stems

(fig. 3).

Upon

of the original vessels,

however, upon reaching

the surface of the placenta, course for long distances diminishing ultimately in
size

by giving

off

numerous subsidiary

These subsidiary branches, while

vessels.

traversing the surfaces of the placental lobes, give off a multitude of finer branches
(the ultimate ones visible to the

naked eye) which run from the centrally placed

vessels to the periphery of the lobes, lending to the surface of the latter a finely

streaked appearance

(fig. 3).

At the periphery of the zonary placenta numerous medium-sized and small
arteries and veins enter the membranous chorion supplying it to its utmost poles
with an abundance of small vessels
tois is
is

amply

much

vascularized.

The

(fig. 2).

Thus the membranous

vascularity of the

membranous

chorio-allan-

chorio-allantois

membranous redupUcavessels. The latter are rela-

greater than that of the amnio-allantois or of the

tions of allantois covering the leashes of umbilical

umbiUcal cord, but become

tively vascular in the neighborhood of the

one leaves the vicinity of the large
tered, as one retreats

from the

vessels.

\'icinity of

Areas

of

less

so as

amnio-chorion are encoun-

the cord, in which the slender vessels

supplying them appear to have become occluded. This observation suggests that
the walls of the amniotic and allantoic sacs are destined at later stages to lose

much

of their present blood suppl3^

Nothing has been said yet

The

cental vessels.

of the curious

morphology

of the walls of the pla-

four pairs of vessels constituting the umbiUcal pedicle reach

the placental surface, whereupon they give off branches which extend to
of the placenta.

of

them

parts

These vessels are not buried in the placenta but are raised for the

most part from the

Some

all

embossed upon it.
possessing small mesenteries. The most

surface, giving the appearance of being

are free to the extent of

characteristic thing regarding these vessels

is

the nature of their adventitial


GROSS DESCRIPTION
These are thickened

sheaths.

163

in a multitude of places to

protuberances projecting into the allantoic cavity

produce a variety of

3 and 4). These bodies

(figs. 2,

are white with a

waxy lustre. They occur about equally along arteries and veins,
uneven in number and distribution in different parts of the placenta.

but are

Moreover, a small percentage

of

them protrude from the

placental surface with-

out any distinct relationship to recognizable placental vessels. These bodies are

of three general types

mon

is

with

all

transitions

between them

(fig. 4)

.

The most com-

undoubtedly a protuberance on the vessel wall, seemingly Uke a drop of

wax. In a few instances these drops follow one another so closely as to give a

beaded appearance. Again for short distances vessels may appear as though
they had been coated with wax. Next in order of frequency come protuberances
that have surfaces which, instead of being smooth, are cauhflower-like. Finally,
in frequency

rectly

or in

come

similar cauliflower-Uke masses which, instead of resting di-

upon the placenta,* are attached to the placental surface by short stalks
some instances by long threads. The cauUflower-Uke terminal expansions

of these

pendulous structures are often flattened. None of the structures enumer-

ated are large, their greatest size being two to four milUmeters in diameter,

although the threads by which the longest pedunculated ones are attached
attain in

some instances a length

of

one to three centimeters.

appendages are irregularly distributed over the entire surface
including that small triangular area to which

amnion instead

may

These various
of the placenta,

of allantois is at-

They accompany the blood-vessels which leave the placental border to
vascularize the membranous chorion for only one to three centimeters at most.
tached.

Thus the inner
of

surface of the

membranous

chorio-allantois

is

practically devoid

them. Moreover, there are but occasional ones on the remaining membranous

walls of the allantoic sacculations. Similarly there are none visible to the

naked

eye on the umbiUcal cord. The amnion, excepting for a few excrescences Umited
to that small area of the

amnion which

is

fused with the placenta,

is

otherwise

devoid of these structures. The amnion possesses, nevertheless, a curious texture.

Running

one's finger over the wall of the amniotic sac gives the sensation of

cloth on which fine grains of sand have been sprinkled
it

can readily be seen that, instead

with the smallest

visible,

of

and on

being smooth, the surface

is

close inspection

closely

studded

whitish particles constituting minute elevations from

the surface. In contrast to the amnion the interior surface of the allantoic cavity
is

smooth, Uke the surface of

chorion and placenta

is

glass,

affected

excepting where

its

texture in the region of the

by the above described appendages,


PL AGENT ATION OF THE MANATEE

164

MICROSCOPIC DESCRIPTION
The most

interesting part of the microscopic examination of this specimen

concerns the nature of the zonary placenta. Both of the pre\aous investigators

(Harting and Turner) examined the placental area of their alcohoUc specimens
resorting mostly to studying small teased bits or

by rather primitive means,

Their pictures of these preparations show the inadequacy

free-hand sections.
of the technique.

However, from

their observations they

clusion that placentation in Halicore dugong
of simple interdigitation of intact fetal

is

diffuse

and maternal

both came to the con-

and adeciduate consisting
This finding

vilU.

The

trary to the present observations of the Florida manatee.

is

con-

sections of the

present specimen, which are fixed and stained by

modern technique, show beyond

a doubt that the zonary placenta of the manatee

is

That

one of deciduate character.
related

dugong

is

a highly complex labyrinthine

this observation holds also for the closely

extremely probable in view of the fact that grossly in numerous

major particulars, in so

Harting and Turner go, the morph-

far as the accounts of

ology of the placenta and fetal membranes in our several specimens

tallies

completely.

Following these anticipatory remarks,

I shall pass to a detailed description

The zonary

of the microscopic structure of the placenta in the present specimen.

placenta

is

band varying from one

a lobulated, thick

meters in thickness

(fig.

5)

.

It is

composed

of

to one

and a

half centi-

an irregularly thickened, relatively

pale-staining layer of tissue on the fetal surface of the placenta in which the fetal

Beneath

vessels are distributed.
five

milUmeters thick constituting the placental labyrinth in which the fetal and

maternal circulations become intimately united
deeply. Beneath this
of

lamina some four to

this outer covering is a

is

placental labyrinth

pletely deciduate in that

maternal and

upon microscopic examination proves

(figs.

cells.

12, 13, 14 and 15).

The endotheUum

accompanying the sUghtly larger

mesenchyma. The

com-

composed of a fine-meshed trelHs-work of fused
which separation of the two is impossible and in

are recognizable because the blood within

red blood

to be

it is

fetal tissues in

endometrium

This zone stains very

rests.

which there has been a loss on the maternal part
of the

7).

a Ught-staining zone of about equal thickness composed

maternal tissue upon which the labyrinth

The

(fig.

of

The

most of the

cellular

them contains here and

lining the capillaries

vessels there

components

fetal capillaries in the labyrinth

is

an

fetal capillaries are oriented for the

is

there nucleated

distinguishable,

and

additioiaal sheath of fetal

most part

in

rows from the


MICROSCOPIC DESCRIPTION

165

surface to the base of the placenta, but there are besides

numerous anastomoses

between them so that they are to a considerable degree plexiform. The maternal
blood spaces are narrow, tortuous channels, for the most part not injected with
blood, lying in the meshes between the fetal plexus.
is

In places, however, blood

recognizable within them, distinguishable from that in the fetal capillaries

the relative abundance of leucocytes in

and the absence

it

by

of nucleated erj^thro-

cytes.

Separating the maternal from the fetal vessels are narrow laminae of

an interpretation

of the nature of

placental labyrinth which

same character and
visible.

They have

and constitute

in

we have

is

important in determining the type

before us. These cells appear to be

to be syncytial in that boundaries

large, oval nuclei

pale-staining cytoplasm.
fetal capillaries.

which

They

cells,

all

of

of the

between them are not

surrounded by a relatively abundant, rather

These syncytial sheets

of cells invest the walls of the

enclose on their opposite faces the maternal capillaries

my estimation the Umiting walls of the maternal blood channels.

If this interpretation

be correct, the syncytiimi in question

is

trophoblastic and

of fetal origin. It constitutes, moreover, the sole enclosure for the

the latter circulating in labyrinthine spaces lined
then, the maternal blood-vessels must have

by

maternal blood,

trophoblast.

Evidently,

lost all of their tunics including the

endothelium, making of the labyrinth a hemochorial one according to the concept
of Grosser.

This decision has not been simple to make, because of the complexity

of the tenuous layer of cells

between the two

circulations.

The

that the syncytium intervening between the two circulations

and that some

possibihty remains

may not

be uniform

of the

homogeneous cells making up
the lamina may be swollen and altered maternal endotheUum. However, after
much study of the sections I believe that the interpretation that there is a hemo-

in character or derivation,

chorial type of labyrinth before us appears to be justified.

mitted would be that
of other

it is

in whole or part

The

an endotheUochorial labyrinth. Study

specimens of the placenta when further stages are obtainable

more complete answer to

this question.

the endometrium having been invaded
tion of the maternal epitheUum

may

give a

There remains, however, absolutely no

doubt whatsoever about the essential fact that the labyrinth

is

truly deciduate,

by trophoblast with the complete destruc-

and connective

tissue with the ultimate intimate

fusion of the trophoblast with eroded maternal blood channels.
are,

alternative per-

These findings

moreover, fully substantiated by studying the peculiar morphology of the

surface as well as the base of the placenta.

At the base

of the placenta tongue-like

masses

of fetal tissue,

resembUng


PLACENTATION OF THE MANATEE

166
chorionic
latter is

villi,

can be seen penetrating the mucosa

(figs. 15, 17,

The

18 and 21).

undergoing wide-spread erosion in the neighborhood of the advancing

trophoblast. These processes of fetal tissue are covered externally

trophoblast of the placental labyrinth which

is

by trophoblast;

mesoderm. Unlike the

in their interior they contain cores of vascularized fetal

syncytial and pale staining, the

trophoblast covering the growing tips of the villous processes, which are invading

composed of cells which are small, with deeply staining nuclei,

and which are for the most part rather regularly set. Indeed in many places the

the mucosa,

cells

is

appear to constitute cytotrophoblast instead of being syncytial. Between

the tongues of the chorionic

villi

are narrow bands of pale, rather acellular,

degenerating maternal connective tissue.

At

where large maternal

intervals

blood vessels reach the neighborhood of the placenta, the chorionic

have

villi

penetrated more actively into the mucosa, sending out long sprouts which
exhibit a tendency to follow the walls of the blood-vessels
(figs. 17,

A

18 and 21).

of the chorionic process

completely.

The darkly

curious observation

is

that the trophoblast on the side

apphed to the maternal
staining trophoblast

and to ensheath them

vessel changes its character

composed

which

of small cells,

characteristic of these basal prolongations of the chorion, changes

where

it

is

comes

in contact with the wall of the maternal vessel into syncytial trophoblast

the trophoblastic

cells

cytoplasm and nuclei

whereby
in
reactions
of both
become
immediately
paler
staining
(figs. 17, 19 and 21). This enclosing of the maternal ves-

accompanied by degeneration of the two outermost vascular tunics, advenand media, so that the maternal blood comes to flow in a confining channel

sels is
titia

of trophoblast.

To what

remain intact within

some
(fig.

vessels the
17),

this sheath is difficult to

endotheUum can be seen

but in other

19 and 21).

(figs.

extent the endotheUal elements of the maternal vessel

say with absolute certainty. In

definitely as a thin, nuclear

vessels, in places along their walls,

The endothelium being exceedingly

the fact that the specimen, although well fixed,

may

fixed for the complete preservation of so delicate a

sume that

it

was completely present during Ufe

it is

membrane

not discernible

deUcate, coupled with

not have been perfectly

membrane,

leads

me

in these larger afferent

to pre-

and

effer-

ent maternal trunks.

The

Some

uterine glands play no conspicuous role in the formation of the placenta.

distance below the basal layer of the labyrinth, in a less compact zone of

the mucosa, there are groups of glands scattered at irregular intervals

(fig.

16).

These glands are conspicuous neither by virtue of size nor by evidence of being
markedly secreting. They are small, with walls composed of a single layer of


MICROSCOPIC DESCRIPTION
low

which are not unusually

cells

active.

167

Their ducts pass outward toward the

base of the placenta where they are evidently sealed

Rarely, one of the

off.

glands in close proximity to the placental base appears to be somewhat dilated,

and

in

one section

into the

lumen

I

have come across a place where the trophoblast has erupted

such a dilated gland

of

(fig.

20).

Passing from a description of the basal portion of the placenta,
sary to turn our attention to the fetal surface of the organ

Here some

rather extraordinary features are present.

nal vessels, endotheUal-hned but otherwise ensheathed

The

(figs. 12,

by a tunic

which run

parallel to the surface

wall adjacent to the labyrinth,

(fig.

23).

(fig.

many

of their

numerous openings leading into the ultimate

from larger afferent

sinusoids that the maternal

In

22).

These possess, in that side

intervillous or intertrabecular spaces of the fine-meshed labyrinth.

transition points

,

of trophoblast,

zone of the labyrinth the vessels divide into short branches

this external

moment on

22 and 23)

larger afferent mater-

penetrate the placenta to reach the fetal surface of the labyrinth

of

neces-

it is

It is at these

vessels to the labyrinthine capillaries or

endotheUum

is lost,

the maternal blood from this

The

circulating in the interstices of the labyrinthine trophoblast.

opposite sides of the vessels bear a curious relationship to the trophoblast at the
surface of the placenta.

Between these

at the surface of the labyrinth

nant maternal blood which
cells (figs.

12 and 22).

is

is

vessels

and the limiting trophoblast

a series of recesses or lacunae containing stag-

being actively phagocytized by trophoblastic

These recesses containing extravasated maternal blood

constitute a narrow zone covering the entire placenta.
this region for histiotrophic

Thus provision is made

nourishment of the fetus by the destruction and

milation of stagnated maternal blood. This formation

hematomata (green and brown borders

of carnivores)

is

tures which I

and other

fig.

1)

giving

besides a

and

my

number

attempting to describe,

I

devices, mostly

mammalian

my readers may understand more fully the

am

assi-

the equivalent of the

paraplacental structures, for the histiotrophic nourishment of

In order that

in

fetuses.

nature of the struc-

have constructed a diagram

(text-

interpretation of the morphology of the zone under discussion,
of

photographs of the actual histological sections

(figs. 12,

22

23).
It

is

evident beyond doubt from the sections that there

is

a series of small

controphoblastic lacunae over the whole surface of the placenta. These pockets

tain stagnated maternal blood.

The

trophoblastic cells Uning the pockets are

unlike the trophoblastic cells seen in the form of syncytium in the bulk of the placental labyrinth or as small-celled cytotropho-blast described at the growing base


PLACENTATION OF THE MANATEE

168
of the placenta.

broad columnar

The
cells

trophoblastic cells in these recesses are separate, discreet,

with somewhat basally situated nuclei and a large amount

of distally placed vacuolated cytoplasm.
of

In the cytoplasm are large numbers

whole or fragmented erythrocytes, as well as a quantity

of

golden pigment,

the latter usually in the neighborhood of the nucleus.

FetV.

/TA/es.

Hist.

Tr.

-F^f. V.

Endo

Plac-

Lab.

Text-fig. 1. Diagram illustrating the author's interpretation of the structure and nature of the surface
of the placental labyrinth in the manatee. F. mes., Fetal mesoderm clothing the surface of the placenta
and accompanying the fetal vessels entering the labyrinth. Fet. v., Fetal vessels entering the labyrinth.

M.

Maternal vessel lined by endothelium (Endo.) communicating above with trophoblastic lacunae
which contain stagnant maternal blood (Hisl.) undergoing absorption by the trophoblast; and

below by a series of openings into the maternal blood channels of the placental labyrinth {Plac. lab.).
Note that neither the lacunae on the one side of the maternal vessel nor the channels leading into the
labyrinth on the opposite side are lined by endothelium.
v.,

(Tr. lac.)

The

question arises as to

Their source
lined

is

how

to be sought in the subjacent afferent maternal vessels

by endothelium ensheathed

apparently give

endothehum

these extravasations of maternal blood occur.

way

in trophoblast.

The endotheUal

which are

walls of these

in places, allowing maternal blood to escape through the

into adjacent pockets of trophoblast in which no free circulation

is

possible, so that stagnation follows.

One could conceive that such an extravasation, once having escaped
of the maternal vessel

might by

its

the limits

mere pressure lead to the formation

pocket-like indentation of the surrounding trophoblast.

reasoning to explain matters. However,

I offer

This

may

be

of a

sufficient

a further suggestion from a clue


MICROSCOPIC DESCRIPTION

169

given by examination of the extreme border of the placenta.

Here, as one ap-

proaches the edge of the placenta, the blood-containing lacunae dwindle in
size

and amount

of contained blood

(fig.

on the ultimate placental margin by
vacuolated, degenerating centers.

mass

in all likeUhood to be a

23).

The pockets

are finally replaced

clusters of syncytial trophoblast with

Thus the precursor

of the

redundant trophoblastic syncytium which has

of

accumulated between the maternal vessels and the overlying

The

the chorio-allantois.

lacunae appears

stroma

fetal

of

cores of these trophoblastic accumulations undergo

vacuolar degeneration, whereby the wall of an adjacent maternal vessel becomes

weakened, so that maternal blood extravasates into the degenerated core of the
adjacent trophoblast.

Rearrangement

of the cells takes place in the structure,

eventuating in the trophoblast becoming columnar and actively phagocytic.

Moreover
larger.

in the course of time the pockets, initially small,

This

is

a reasonable explanation,

I

become considerably

beheve, of the formation of the pockets

from the observations. Naturally the relationships in
zone are complex, and it will doubtlessly require study of further stages to

and follows

logically

this
elu-

cidate the problem fully.

Leaving the placenta proper,
important structures.
seen grossly on

The

its walls,

Uned throughout by a

I shall

allantois,

pass to the description of several other

and more particularly the excrescences

arouse curiosity as to their nature.

The

allantois

is

Without any seeming

single layer of small epitheUal cells.

may be flat and button-Hke, or, on the other
cells may be elevated Uke small clubs, with the

regularity these

hand, for a certain

distance the

small dark-stained

nucleus at the attached end, and a large vacuole at the clubbed, distal end
(fig.

27).

Nowhere, where sectioas have been taken,

layering of the epithehal

The waxy

is

there

any e^^dence

of

cells.

numerous along the walls of the allantoic vessels
supplying the placenta, are found on microscopic examination to be due merely
to a prohferative growth of the mesodermal stroma of the allantois. The minute
excrescences, so

character of these structures

is

shown

in figs. 25

between them and the ordinary mesodermal

membranes,
fibrillar

lies

and

embryonic

more

easily perceived interlacing

minute blood

cell outlines

cells as

are

more

irre-

seen in rapidly growing

These prohferative growths, as well as the
the chorio-allantoic connective tissues, are suppUed with

tissue or tissue cultures.

remaining bulk of

difference

seen elsewhere in the fetal

matrix, that the cells are fewer, and that the

mesenchymal

The main

tissue,

in the facts that the tissue has a

gular than ordinary, resembUng

26.

vessels.


PLACENTATION OF THE MANATEE

170
Leaving the

few descriptive remarks concerning

allantois, I shall pass to a

the paraplacental border and uterine mucosa. At

down

to a wedge, without changing

(figs.

5 and

From

8).

Fused with the

allantois

the latter presents on
situated nuclei

its

(fig.

its

24).

latter, a millimeter

its

its

border the placenta tapers

character to any extent, and disappears

edge arises a thick sheet, the membranous chorion.

by

a heavy sheet of well-vascularized connective tissue,

uterine surface a paUsade of columnar cells with basally

The chorion

is

from the border

not fused with the uterine mucosa.

The

shows the character

of a

of the placenta,

completely intact mucous surface provided with a complete epitheUal covering
(figs.

The

8 and 11).

cells closely

uterine epitheUum
It

packed.

is

is

composed

as a rule no thicker than the epithelium
of modified

columnar

of the vesicle

columnar

worth noting that minute, endo-epitheUal cysts occur
These are small vesicular structures,

at short intervals in the uterine epithelium.

composed
the lumen

of slender, high,

(fig.

11).

cells

itself, filled

with secretion and with walls

which have become flattened out around

These structures have a configuration

of their

walls, resembling strikingly the figures of so-called endo-epitheUal glands,

in

no instance in

interpret

them

my

sections

have

I

down

surface, so that I

as being cystic instead of glandular.

Beneath the uterine epithelium
reaches

them open onto the

seen

but

is

a narrow layer of loose stroma which

In this layer one encounters at intervals

to the musculature.

small nests of uterine glands, simple in architecture, with small, low epithehal
cells lining

them and presenting no evidence

Near the placental margin,

of

marked

activity

(fig.

16).

as described in the gross description, there are

about a dozen minute, scattered areas, some two to four milUmeters in diameter,
in which chorion and uterine epithelium are fused, leading to the formation of

A

minute, accessory, placental areas.
these accessory placental areolae

is

photograph

shown

of a section

through one of

in figure 10.

The umbiUcal cord on low power examination, about two centimeters from
the umbiUcal ring, shows three blood vessels

an extensive

cleft,

the allantoic duct

(fig. 9).

:

— two arteries and a vein, besides

Grossly the surface of the umbilical

cord appears smooth without apparent carunculae.

On

section, however, one

encounters scattered patches of thickened umbiUcal (amniotic) epitheUum.
section

is

The

taken from the short cord about one and one-half centimeters distant

from the point, within a few milUmeters

of the umbilical ring,

where the black,

pigmented skin of the fetus gives way to the white, unpigmented tissue of the
cord. Another observation of some interest is that the connective tissue stroma
of the cord

is

well vascularized

by small

arterial

and venous branches

of the


CERVIX AND VAGINA

171

The stroma thus has

a plentiful capillary blood

umbilical arteries and veins.

Noteworthy

supply.

the fact that in some areas the venulea are almost

is

The presence

cavernous in character.

mammals

cord of

is

of vascularized

stroma

in the umbilical

rather the rule than the exception, as I have discussed in a

recent paper on the placentation of the porpoise (Wislocki, 1933).

exception of the Primates,
the majority of

mammals

have found the stroma

I

of the

With the

umbiUcal cords

of

well vascularized during the whole course of gestation.

This vascularization cannot be attributed

solely,

as explained there, to

the

presence of persistent vitelline vessels. In the present specimen, for example, no
trace of a vitelline duct or vessels can be found in sections of the umbilical cord.

The minute

elevations discovered in the gross

upon the surface

of the

amnion

prove upon section to be composed of a deUcate core of stroma clothed by
epithelial cells. The latter differ from the ordinary epithelium covering the

amnion

in that they are larger

and sometimes vacuolated.

I

have noted in some

minute appendages cystic transformation of the epithelium, as well as
degenerative changes involving both epitheUum and stroma. The usual character

of these

of

one of the appendages

is

shown

in figure 28.

THE CERVIX AND VAGINA
A

brief description is

appended

of the rarity of the present material.

of the cervix

The

and

its

relationships because

external genitalia do not

accompany

the specimen.

The lumens
form a

of the right

relatively short,

and

left

common,

uterine cornua unite as

mately nine centimeters long, terminates at what

The lumen

of the uterine

mucosa thrown
outlet

is

The

uterine cavity.
I

latter,

What

in figure

which

is

1

to

approxi-

judge to be the cervical outlet.

body, as well as of the cornua,

into low, longitudinal folds.

shown

is

is

circular with the

presumed to be the uterine

a dense, rubbery mass perforated in the center by the transversely

flattened canal of the cervix

(fig.

This mass, about eight centimeters in

la).

diameter, protrudes quite definitely into the cavity of the vagina running at

almost right angles to

from the

it.

cervical outlet.

The protruding
Its

margin

is

cervix

is cleft

delineated

much undercut, so as to constitute a deep fornix.
The cavity into which the cervix protrudes
flattened anteroposteriorly.

Its lateral

by a

lies

by deep furrows

radiating

circular furrow, caudally

at right angles to

it

and

is

margins have the outUne of a pear, the

bulbous part surrounding the cervix, the constricted portion extending toward the


PLACENTATION OF THE MANATEE

172

rubbery folds

of

The

composed of a number of heavy,
mucosa which converge toward the somewhat constricted vaginal

genital vestibule.

walls of the vagina are

This vaginal segment

outlet.

is

about twelve centimeters long. The bladder wall,

partly intact, attaches to the ventral surface of the lower uterine segment, and

the urethra leaves the neck of the bladder to join the genital passage at the point

where the specimen has been amputated. The point
with the genitaUa passage

is

of junction of the urethra

well external to the cervical orifice,

assume that the recess into which the cervix opens

ible to

is

making

it

plaus-

homologous to the

vagina of other mammals, the urogenital sinus or vestibule being in that case the
outlet

beyond and external

of the

topography

of

to the urethral meatus.

my specimen because

give this brief description

I

the interpretation of the presence of a

vaginal segment differs from the observations by Freund (1930) of a virginal
uterus in which cervix and urethra opened so close together that the recess

which formed a

common

outlet for

them was

interpreted as the vestibule, so that

a vagina seemed to be totally lacking. I present

my

observations merely to call

attention to the need of examination of other specimens.

DISCUSSION
The present observations upon the placenta of the manatee place the place ntation of the Sirenia in an entirely new light. The only previous accounts of
placentation in this order of

each of

whom

mammals

are

by Harting

(1878)

described a fetus and placenta of the dugong.

and Turner (1889),
Their rather brief

accounts of the gross topography of the fetal membranes in the dugong bear a
striking resemblance to the gross findings in the present specimen of the manatee.

Thus the configuration and

relationships of allantois

and anmion are in the main

about the same. The curious structure of the umbilical cord coincides in both
genera.

The placenta

in Turner's specimen (length of fetus, 163 cm.) is zonary

as in the manatee, whereas in Harting's

much younger specimen

(length of

fetus, 27.8 cm.) the placenta is quite diffuse, excepting bare spots at the chorionic

poles.

This dissimilarity between the two dugongs Turner ascribes to the

ing ages of the specimens, with which I agree. In
in

which the fetus

is

my own

differ-

specimen of manatee,

considerably longer than Harting's, the placenta is completely

zonary coinciding with Turner's specimen. Thus grossly the placental topography

manatee and dugong is manifestly aUke.
When it comes to the microscopic examination

of the

findings diverge radically.

Careful examination of

of the placenta,

my

however, our

specimen reveals

it

to be


DISCUSSION
a deciduate, hemochorial placenta of

173

marked complexity. Harting's and Turner's

dugong placentae, on the other hand, are described as consisting of an interlocking of intact fetal and maternal villi in the manner characteristic of the ungulates and designated as diffuse. Against their findings are the facts that their

examinations were carried out on crude histological preparations (free-hand
sections

and teased preparations) and

their material

was poorly preserved

for

imcroscopic work. In view of the great similarity of our several specimens upon
gross examination, I
will
is

I

am

inclined to believe that microscopically the placentae

be found in the main to be identical as soon as modern histological technique
to a placenta of the dugong.

appUed

am

hood

From

careful consideration of the matter,

forced to the conclusion that placentation in the manatee, and in
in the Sirenia in general,

is

of the place of the Sirenia in

In this regard the Sirenia must be removed from the

Ungulata and Cetacea with their totally
If this is

the case, to what groups of

different placentation.

mammals do

The placenta being zonary and deciduate

affinities?

Ukeli-

deciduate and hemochorial.

These findings necessitate a reconsideration
placental classification.

all

the Sirenia bear placental

naturally invites comparison

with other zonary and deciduate placentae: the carnivores, Hyrax and the elephant. Aside from its zonary shape, which is of no great importance in deciding
placental affinities, the placenta of the manatee bears no great structural affinities

to the dog or cat.

have characteristically
exhibits during the
reaction.

None

The placentae

of the latter are endotheliochorial;

they

speciaUzed placental borders, and the endometrium

first

part of gestation a characteristic profuse glandular

of these features of the carnivores is present or

marked

in the

manatee. Aside from the external form, the two types of placentae are dissimilar.

mammals, the Hyracoidea and the Proboscidea,
whose placentae are zonary and deciduate, the resemblances are more far-reachof study in recent years by
ing. The placenta of Hyrax has been the subject

With the two other groups

of

Assheton (1906), D. Thursby-Pelham (1924), and Wislocki (1930). On comparing their accounts of the placentation of the hyracoids with the present description of the placenta of the manatee, one

becoming

later distinctly

struck by the great similarity in the

Hyrax is grossly in the beginning almost
zonular. The labyrinth is, moreover, hemo-

major characteristics. The placenta
diffuse,

is

of

from the zonular placenta of the carnivores.
surrounded completely by the allantois which is voluminous.

chorial,

differing therein

amnion

is

umbiUcal cord branches into four pedicles
the placenta.

The
The

of paired blood-vessels wliich reach

These pedicles constitute the hmiting borders

of four sac-hke


PLACENTATION OF THE MANATEE

174

and Thursby-Pelham, two
the blastocyst, while two smaller sacculations are

dilatations of the allantois, according to Assheton
of

which occupy the poles

apposed to the surface

of

of the

zonary placenta. The striking similarity in

major points between the placentation
apparent. It
to

may

it

many

manatee and the hyracoids

be stated with certainty that the resemblance

any other known form, unless

The

of the

is

is

greater than

be the elephant.

placentation of the elephant

very incompletely known, even for a

is

However, on reading over the papers by Owen (1857), Chapman
(1881, 1899), .\ssheton and Stevens (1905), Assheton (1906), and Boecker (1907),

single stage.

it is

apparent that the placenta

is

zonary and deciduate. The gross topography

and membranes

is

sufficiently clear in the text

of the placenta

by Owen (1857) and Chapman (1881)

in the papers

major characteristics
I

of its placentation.

On studying

and

illustrations

to acquaint one with the
their accounts

and

figures,

am impressed by the striking resemblances between the placenta in the elephant

and

The shape

in the manatee.

of the chorion, the character of the

zonary

placenta, the division of the umbihcal cord into four sets of paired vessels, the

extensive allantois which

is

sacculated and surrounds the amnion, the presence

of allantoic bodies attached to the placental vessels all contribute to

resemblances very striking.

On

making the

the basis of the gross configuration of the pla-

centa and membranes, the manatee, Hyrax and the elephant easily

fall

into a

natural grouping.

The

finer structure of the elephant's placenta is

badly in need of further

However, from the studies of Turner (1876), Assheton and Stevens
(1905), Assheton (1906), and Boecker (1907), it is accepted as being deciduate.

study.

From

the poorly illustrated and rather incomplete account of Boecker

likely, moreover, that the intricate placental labyrinth

(1927) accepts

it

as being hemochorial.

is

it

hemochorial.

This evidence regarding

its

appears
Grosser

microscopic

larity

some additional support to my thesis of the simibetween the placenta of the manatee, Hyrax and the elephant. It seems

most

likely for the present that the closest affinities of the elephant's placenta

nature, scanty as

it is,

lends

are to the type of zonary, deciduate, hemochorial placentation which characterizes

both the manatee and Hyrax.

In view

close affinities of
tation, I

upon the manatee and the suggested
the Hyracoidea, Proboscidea and Sirenia in regard to placen-

of the present observations

have undertaken a revision

of a

diagram used in a previous paper to

illustrate graphically the types of placentation occurring in
fig. 2).

The diagram

is

borrowed

for this

mammals

(text-

purpose from one originally presented


DISCUSSION
by W. K. Gregory
of mammals.

The

(1910) to

show

175

concept of the relationships of the orders

his

monotremes and marsupials. The broken
mammals in which the trophoblast exhibits little

solid disks represent the

circles represent the orders of

or no invasive tendencies, hence placentation in these has been termed diffuse
Cetaceo
J

\

{

')Arhodocfy/o

/

.'

Pjnniped Corni^oreS

( ''\PerissodQcfy/a

lores

TorSluS

/

Lemurs \

Tupoioidii

Craleopithecus

lo/yprofodon/ fiorsup'o/s

^^i

Qiprotodont Morsup'o/s

^^^

The author's schematic representation of the types of placentation in mammals, revised
accordance with the considerations derived from the present study. The original diagram is borrowed
from the work of W. K. Gregory (1910) representing his conception of the probable relationships of the
orders of mammals. For a discussion of the diagram see text.
Text-fig. 2.

in

or

adeciduate

Cetacea, Artiodactyla, Perissodactyla and Manidae constitute

unbroken

The lemurs,
this class. The

(epithehochorial or partially syndesmochorial).

circles represent categories of

mammals

extensively invasive, hence placentation

is

which the trophoblast is
deciduate (endotheliochorial and
in

The endothehochorial type of placentation is represented
and Bradypodidae. The remaining large bulk of mammals

hemochorial types).

by the carnivores
possess so-called

sundry groups
indicating that

of
it

hemochorial placentae.

mammals shows

Hemochorial placentation in the

a considerable morphological diversification

has followed several evolutionary patlis from the primitive


PLACENTATION OF THE MANATEE

176

type or types from which

it

The marked

arose.

similarity of placentation in the

Hyracoidea, Proboscidea and Sirema indicates that we are deahng in these
orders of

mammals with

a well-defined placental type which differs in

The

standing ways from other hemochorial types.

similarity in

many outthe mode of

placentation in these three orders coincides well with the generally accepted

view that they are in other respects
lessly the

most primitive

The Hyracoidea, doubtthought by some to bear resemblances,

fairly closely alUed.

of the three, are

on the other hand, to a primitive proto-ungulate stock. How the ungulates
derived their diffuse placentation on the one hand, and the Hyracoidea, Proboscidea and Sirenia their hemochorial placentation on the other hand, must remain
for further study to

open

attempt to elucidate.

SUMMARY
An excellently preserved fetus

manatee {Trichechus

(44 cm.

latirostris) in situ

basis of the present account.

from snout to

tip of tail) of the Florida

with membranes and placenta forms the

The only other

descriptions of placentation in the

by Harting (1878) and Turner (1889) on two rather inadequately
preserved specimens of Halicore dugong (fetuses 28 and 163 cm.). Their hisSirenia are

tological examinations
is

were necessarily

brief.

According to them, the placenta

at first diffuse, later zonary, while limited microscopic examination

to be non-deciduate with simple interlocking of intact endometrial

shows

it

and chorionic

vim.

In the present specimen the membranes and placenta occupy solely the
right uterine cornu.
tois is

voluminous

The placenta

filling

is

zonary and sharply delimited. The allan-

the chorion from pole to pole, leaving only a small

The

angular area for amniochorionic fusion.

allantois

is

tri-

subdivided into four

compartments which communicate between the pedicles of four leashes of
blood vessels constituting the umbilical cord. Thus the allantoic vessels form

large

the septal margins of the four allantoic sacculations. There

is

no yolk sac at this

stage.

The placenta on microscopic examination
entirety of intimately fused chorionic

meshed labyrinth

is

found to be composed in

and uterine

tissues,

of a hemochorial, deciduate variety.

producing a

There

is

its

fine-

provision for

histiotrophic nourishment of the fetus through the formation at the fetal sur-

face of the labyrinth of lacunae containing stagnant maternal blood which

phagocytized by specialized trophoblastic

cells.

is

SUMMARY
The membranous chorion
endometrium outside the

by

epithelial cells.

The

site of

covered by paHsade-hke, columnar

the zonary placenta at this stage

in the ranks of the

removes

it

into

it;

the amnion

Deciduata with a placenta

in regard to placentation

from any

From

of the

provided with ex-

of the placenta of the latter

animal

hemochorial type, and

close association with the Cetacea,

various considerations

closely alUed in regard to placentation to the

Accounts

is

numerous

of the placenta of Trichechus latirostris places this

Artiodactyla, or Perissodactyla.

most

The

fully clothed

allantoic sac has over the placental area

mesenchymal appendages protruding
tremely minute carunculae.

The organization

is

cells.

uterine glands are not very conspicuous, playing no great

The

role in placentation.

is

177

it

appears to be

Hyracoidea and Proboscidea.

forms describe them as being zonary and

hemochorial and hence distinctly urdike the endotheliochorial placentae of
carnivores which they resemble only in regard to outer form.

The evidence

adduced from the present study supports the conclusion that placentation in the
manatee, Hyrax and the elephant
chorial type.

is

of a closely related

and

distinctive

hemo-


PLACENTATION OF THE MANATEE

178

LITERATURE
ASSHETON, R.

The morphology

1906.

elephant and hyrax.

of the ungulate placenta,

Phil. Trans.

Roy. Soc. London,

and notes upon the placenta

of the

Ser. B, 198, pp. 143-220.

AsSHETON, R. AND Th. G. StEVENS
1905. Notes on the structure and the development

of the elephant's placenta.

Quart.

Jour. Micr. Sci., 49, pp. 1-37.

Boecker, E.
1907. Zur Kenntnis des Baues der Placenta von Elephas indicus

L. Arch.

f.

mikr. Anat.,

71, pp. 297-323.

Chapman, H. C.
1881. The placenta and generative apparatus

of the elephant.

Jour. Acad. Nat. Sci.

Phil., 8, pp. 413-422.

1899. La gestation et
pp. 525-526.

le

placenta de I'elephant {Elephas asiaticm).

C. R. Soc. Biol.,

1,

Freitnd, L.
1930. Beitrage zur Morphologic des Urogenitalsystems der Saugetiere. IL Der weibliche
Urogenitalapparat von Manahis. Zeitsch. f. Morph. u. Okol., 17, pp. 424-440.

Gregory, W. K.
1910. The orders

of

mammals.

Bull.

Amer. Mus. Nat.

Hist., 27, pp. 1-524.

New York.

Grosser, O.
1909. Vergleichende Anatomie and Entwicklungsgeschichte der Eihaute und der Placenta
mit besonderer Beriicksichtigung des Menschen. 314 pp. Wien.

Harting, p.
1878. Het

ei

en de placenta van Halicore dugong. Diss. Utrecht, pp. 1-65.

Owen, R.
1857. Description of the foetal

membranes and placenta

of the elephant {Elephas indicus,

Cuv.) with remarks on the value of placentary characters
i-f^-

Lip

in the classification of the

mammalia., Trans. Roy. Soc. London, pp. 347-353.

Thursby-Pelham, D.
1924. I. The placentation

of

Hyrax

capensis.

Phil. Trans.

Roy. Soc. London,

Ser. B,

213, pp. 1-20.

Turner, W,
Lectures on the comparative anatomy of the placenta, p. 27.
On the placentation of Halicore dugong. Trans. Roy. Soc. Edinburgh, 35, pp.
644-662.
1876.
1889.

WiSLOCKI, G. B.
1930. On an unusual placental form

in the Hyracoidea. Carnegie Contrib. to Embryol.,
83-95.
21, pp.
1933. On the placentation of the manatee {Manatus latirostris)
Anat. Rec, 55, p. 84
.

(abstract).

1933.

On

the placentation of the harbour porpoise {Pliocacna phocoena L.)

66, pp. 80-98.

Biol. Bull


EXPLAiNATION OF THE PLATES


ABBREVIATIONS USED IN PLATES
Ace.

pi.

1

AND

2


PLATE

1