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Placenta 29 (2008) 484e491

Female Reproductive Tract and Placentation in Sucker-Footed Bats

(Chiroptera: Myzopodidae) Endemic to Madagascar
A.M. Carter a,*, S.M. Goodman b,c, A.C. Enders d
a
Department of Physiology and Pharmacology, University of Southern Denmark, Odense DK-5000, Denmark
b
Field Museum of Natural History, Chicago, IL, USA
c
Vahatra, Antananarivo, Madagascar
d
Department of Cell Biology and Human Anatomy, University of California, Davis, CA 95616, USA
Accepted 20 February 2008

Abstract

The reproductive tract was examined in four non-pregnant and two gravid specimens of Myzopoda. The ovaries had little interstitial tissue.
The uterus was bicornuate and the lenticular placental disk was situated mesometrially in one horn. The interhaemal barrier of the placental
labyrinth was of the endotheliomonochorial type. There was a single layer of trophoblast cells. The cells of the maternal endothelium were large
and basophilic, contained abundant rough endoplasmic reticulum, and rested on an irregular basement membrane. Blunt projections of endo-
metrium extended into the placental disk and clusters of large cells occurred between the endometrial stroma and labyrinth. At the margins
of the disk folds of trophoblast occurred and at the cranial end they formed an haemophagous region. The folds lateral to the disk included
some peculiar tubular-appearing structures. There was a persistent yolk sac containing large endodermal cells around a largely collapsed lumen.
Several features of placentation, such as the interhaemal barrier and the haemophagous region, are consistent with an association of Myzopo-
didae with Emballonuridae. No support was found for alternative hypotheses that include Myzopodidae in the noctilionoid or vespertilionoid
lineages.
Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: Comparative placentation; Fetal membranes; Haemochorial placentation; Haemophagous region; Trophoblast

1. Introduction
Next to Rodentia, Chiroptera is the mammalian order with
the greatest number of species. The fossil record of bats is in-
complete, but they seem to have undergone a rapid radiation in
the early Eocene coincident with an increase in plant diversity
and a peak in insect abundance [1]. Perhaps this explains the
great diversity in their placentation, which has been remarked
upon by several authors [2e4]. Currently 18 families of bats
are recognized in molecular and morphological studies [5e8].
The sucker-footed bats, genus Myzopoda (Myzopodidae),
are endemic to Madagascar. Their name is derived from
adhesive pads borne on the thumb and hind foot. Structures
with a similar function but different morphology are found
in the disc-winged bats, genus Thyroptera (Thyropteridae),
a remarkable instance of convergent evolution [9]. Two spe-
cies of Myzopoda are now recognized [10]. Myzopoda aurita
occurs in the humid eastern forests of Madagascar, whilst M.
schliemanni occurs in the dry western forests of the island. Al-
most nothing is known of reproduction in either species. We
here present information on the female reproductive tract
and definitive placentation of both species.
2. Materials and methods

The reproductive tract was studied in situ and the external genitalia exam-
* Corresponding author. Tel.: þ45 6550 3716; fax: þ45 6613 3479. ined in four non-pregnant females, one of M. aurita and three of M. schlie-
E-mail address: acarter@health.sdu.dk (A.M. Carter). manni (Table 1). A pregnant uterus and both ovaries were taken from

0143-4004/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.placenta.2008.02.009
 A.M. Carter et al. / Placenta 29 (2008) 484e491 485

Table 1
Specimens of Myzopoda spp. examined
Species Museum Collection No. Description
Myzopoda aurita FMNH 184490 Pregnant female
FMNH 92832 Non-pregnant female
Myzopoda schliemanni FMNH 185791 Subadult female
FMNH 185792 Non-pregnant female
FMNH 185794 Non-pregnant female
FMNH 187610 Pregnant female
Abbreviation: FMNH, Field Museum of Natural History, Chicago.

a specimen of M. aurita that had been fixed and then stored in 70% alcohol. A
pregnant uterus and both ovaries of M. schliemanni were removed in the field
and fixed in Karnovsky’s fixative, i.e. 2.5% paraformaldehyde and 2.5% glu-
taraldehyde in 0.1 M phosphate buffer.
After dissection to establish the gross morphology, the ovaries and portions
of the placenta and fetal membranes were removed and embedded in Araldite
epoxy resin for semi-thin sectioning. Tissues from M. schliemanni were first
processed for transmission electron microscopy (TEM) by postfixation in
2% osmium tetroxide prior to dehydration and embedding in plastic. A total
of 1 mm sections were stained with Azure B and examined by light micros-
copy, after which selected regions were thin-sectioned and examined by TEM.

3. Results

The external genitalia were characterized by a small clitoral

pad and transverse orientation of the vulval opening. The
uterus was bicornuate. Pubic nipples were not present.
In both pregnant animals, the fetus and placenta were situ-
ated in one horn of the bicornuate uterus, which was greatly
enlarged in the cranial direction. The corpus luteum was in
the ovary from the same side in one animal and in the ovary
of the opposite side in the other. None of the four ovaries
had more than a small amount of interstitial tissue, and the tis-
sue present was confined to the hilus, suggesting that it was of
embryonic origin.
The placental disk was situated mesometrially and a col-
lapsed yolk sac was situated beside the disk. In one specimen
the yolk sac was rod shaped and slightly longer than the disk
(Fig. 1A); in the other it was flattened and substantially longer
than the disk of the chorioallantoic placenta. Except for the
relatively poor fixation of the specimen of M. aurita, and
a more compact yolk sac, the two placentae were similar
and will be described together.
The discoidal placenta was approximately 7  9 mm, being
elongated in the cranio-caudal direction. The umbilical cord
was situated closer to the caudal end than the centre of the
disk. There were two umbilical arteries and a single vein.
The more cranial aspect of the disk had a pinkish area which
proved to be a small haemophagous region. A yolk sac duct
joined the umbilical cord close to the surface of the placental
disk.
The placental disk was a lenticular structure, superficially
lobulated on the fetal surface where allantoic arteries accom-
panied by a small amount of connective tissue extended into
the labyrinth (Figs. 1B and 2A). The junctional zone between
the labyrinth and the endometrium underlay most of the pla-
cental disk, with the margins of the disk extending laterally
over the surface of the uterine luminal epithelium.
Fig. 1. A. General view of the placental disk, elongated yolk sac and fetus. B.
Section through the placental disk to show the endometrial projections (endo
proj), labyrinth, and marginal folds. The fetal surface is lined by chorionic
mesenchyme containing some prominent allantoic blood vessels. A segment
of the chorioallantoic membrane appears at far left. Much of the space be-
tween the placenta and uterine wall is artefactual. Scale bars ¼ 2 mm (A),
0.85 mm (B). M. aurita (A); M. schliemanni (B).
The underlying endometrium was irregular, with blunt pro-
jections extending into the placental disk (Figs. 1B and 2B).
Between the less modified stroma of the endometrium and
the labyrinthine portion of the disk was a region of large cells.
Some of these cells were clustered and others intercalated be-
tween the clusters (Fig. 2C,D). In a few regions, clearly decid-
ualized stromal cells could be found towards the less
decidualized endometrium.
The fetal side of the placental disk had numerous arteries
and venous sinuses. Extending down into the disk from this
surface were branches of the arteries, giving rise to the abun-
dant small capillaries seen throughout the labyrinth (Fig. 2A).
Maternal vessels appeared to extend into the labyrinth from
some of the endometrial projections (Fig. 2B). Areas of con-
fluence of maternal placental capillaries into endometrial veins
were found near the junctional region (Fig. 3A).
Within the labyrinth, the endothelial cells of the maternal
capillaries were cuboidal and strongly basophilic (Fig. 3A).
They were typically surrounded by a single layer of large
pale cytotrophoblast cells (Fig. 3B,C). The intercalated fetal
vessels were unremarkable with normal squamous
endothelium.
486 A.M. Carter et al. / Placenta 29 (2008) 484e491

Fig. 2. A. Placental labyrinth showing large fetal artery entering from the surface and branching towards the endometrium. B. Part of the labyrinth and an
endometrial projection containing sections of a maternal artery. C. Endometrium with clusters of large cells and a large maternal vessel (mv) surrounded by
decidualized stromal cells. D. Clusters of large cells interposed between the maternal vessel and the labyrinth. Scale bars ¼ 80 mm (A, B), 35 mm (C), 22 mm
(D). M. schliemanni (A, C, D); M. aurita (B).

Examination of the ultrastructure of the labyrinth illus-
trated that the maternal endothelial cells had abundant rough
endoplasmic reticulum (Figs. 4 and 5). Beneath these cells
was a thick but irregular basement membrane with occa-
sional discontinuities where the trophoblast cells occasion-
ally abutted the endothelium. The trophoblast cells that
surrounded the maternal capillaries were large cells coupled
by distinct junctions (Fig. 5). They had a small amount of
rough endoplasmic reticulum that had a distinct content
but were not otherwise particularly rich in organelles. The
basal lamina underlying the trophoblast was thinner and
more regular than that underlying the maternal endothelium.
Although the fetal capillaries did not indent the trophoblast
surrounding maternal vessels, they were directly apposed to
the trophoblast with little or no intervening connective
tissue.
The folds at the lateral margins of the placental disk fre-
quently had two layers of trophoblast (Fig. 6A), and occa-
sional masses of syncytiotrophoblast were found in this
location. Some peculiar tubular-appearing structures were
also present (Fig. 6A,B). These structures had an outer layer
of cuboidal trophoblast cells and a tall inner layer of cells ad-
jacent to maternal blood. The inner layer of cells showed ev-
idence of fusion and had a band of heavy-staining material in
a subapical position, which by TEM was amorphous and was
not membrane-bound (not shown).
At the cranial end of the placenta were folds of columnar
trophoblast surrounding maternal blood (Fig. 6C,D). Many
 A.M. Carter et al. / Placenta 29 (2008) 484e491 487

Fig. 4. Placental labyrinth showing two maternal capillaries with enlarged

cuboidal endothelial cells and each with a thick, irregular basement membrane
(short arrows). There are occasional discontinuities in the basement membrane
where the trophoblast cells (troph) abut the endothelium. Note the fetal capil-
lary at upper left. Scale bar ¼ 6.4 mm. M. schliemanni.

vascularized, and was situated over a layer of low cuboidal lu-

minal epithelial cells that had numerous large vacuoles
(Fig. 7A). A few endometrial glands were found in some of
the decidua basalis underlying the peripheral aspects of the

Fig. 3. A. Confluence of maternal vessels (mv) in the junctional region

between labyrinth and endometrium. B. Detail of the labyrinth showing the
basophilic endothelium of maternal capillaries (mat cap) and fetal capillaries
(fet caps) with more squamous endothelium. C. Detail of the labyrinth show-
ing maternal and fetal capillaries and the paler trophoblast cells (troph). Scale
bars ¼ 54 mm (A), 13 mm (B, C). M. schliemanni.

of the cells composing these trophoblast sacs contained in-

gested erythrocytes. Other patches of columnar cells with
ingested erythrocytes were also found continuous with
more typical regions of the labyrinth at this end of the pla-
centa and constituted part of the irregular haemophagous
Fig. 5. Detail of the labyrinth showing maternal endothelial cells with
region. abundant rough endoplasmatic reticulum (rer) and part of two trophoblast
The chorioallantois extending peripherally from the placen- cells (troph) with few organelles but distinct junctions (short arrow). Note
tal disk had a simple single layer of trophoblast, was the capillary at lower right (long arrow). Scale bar ¼ 3.0 mm. M. schliemanni.
488 A.M. Carter et al. / Placenta 29 (2008) 484e491

Fig. 6. A. Folds of bilaminar trophoblast at the margin of the placental disk (arrow). Several tubular structures are formed from some of these folds. A section of the
peripheral allantois is at lower left. B. Parts of two tubular structures from the margin of the disk. They are surrounded by a thin connective tissue containing fetal
capillaries. There is then an outer layer of cuboidal trophoblast cells (outer troph) and an inner cell layer (inner troph) that includes a band of darkly staining
material. The lumen of each tube contains maternal blood, slightly shrunken away from the trophoblast surface. C. Cranial folds encompassing maternal blood
with patches of columnar trophoblast cells that contain ingested erythrocytes (haemophagous cells). D. Detail of a haemophagous region showing columnar tro-
phoblast cells with ingested erythrocytes. Scale bars ¼ 140 mm (A), 13 mm (B), 54 mm (C), 34 mm (D). M. schliemanni.

disk, but the rest of the basal decidua and the parietal decidua
were remarkably free of such structures.
The largely collapsed yolk sac was similar to that seen in
many species of bats, including vespertilionids. The robust ba-
sophilic endodermal cells lining the remnants of the yolk sac
cavity formed a continuous layer of cuboidal to columnar cells
(Fig. 7B). Between these and the mesothelial cells was a small
amount of fetal connective tissue and numerous capillaries.
The overlying mesothelial cells, rather than being squamous,
formed a continuous cuboidal layer but were not as basophilic
as the endothelial cells.
4. Discussion
The female genital tract and placentation of Myzopoda spp.
share some characters with all bats, have one unique feature
and fail to support either of the current hypotheses on the phy-
logenetic position of Myzopodidae.
The presence of a cellular trophoblast layer in an endothe-
liomonochorial placental relationship is found in other bats
such as Natalus (Natalidae) and Saccopteryx (Emballonuridae)
[3] and also in the kangaroo rat Dipodomys [11] and African
elephant Loxodonta [12]. Both endotheliochorial placentae
with cellular trophoblast and those with syncytial trophoblast
show regions where maternal endothelium and trophoblast
contact one another through a variably thick basement
membrane. The situation in Myzopoda, however, is relatively
simple in showing short blunt contacts. The presence of
such contacts in all endotheliochorial placentae suggests that
such regions function in information signaling between mater-
nal and fetal organisms. The trophoblast layer in Myzopoda
was not indented by the fetal capillaries, as is usually found
in later stages of placentation in other species with endothelio-
chorial placentae.
The structure of the margins of the placental disk was quite
interesting. Only in the cranial region did peripheral tropho-
blast folds develop haemophagous areas. In the rest of the
disk, some of the folds had two layers of trophoblast which
for the most part were closely apposed but in other areas
formed tubular-appearing structures that had a unique inner
syncytiotrophoblast layer often encompassing maternal blood.
Such structures have not been described in any other bat, and
their functional significance is not apparent. A developmental
series might provide better clues both as to their possible func-
tion and as to whether or not the placental labyrinth per se was
initially endotheliodichorial before becoming endotheliomo-
nochorial as occurs in Natalus and Saccopteryx [3].
The general pattern of maternal blood entering from
projections into the placenta and returning to regions be-
tween such projections and that of fetal blood branching
off arteries extending well into the placenta to return via
capillaries to the fetal surface suggests only partial counter-
current flow. The pattern could be studied better by vascular
casts to determine the definitive relationships of maternal and
fetal vessels.
 A.M. Carter et al. / Placenta 29 (2008) 484e491
Fig. 7. A. Chorioallantois peripheral to the disk. Above is chorionic mesoderm
with fetal capillaries. A single layer of basophilic trophoblast cells is apposed
to the uterine epithelial cells (ut epithelium), which appear vacuolated. Blood
vessels (bv) are seen in the endometrial stroma. B. Portion of the yolk sac. The
endoderm adjacent to the collapsed lumen comprises large, columnar, baso-
philic cells. The connective tissue between the endoderm and the pale cuboidal
mesothelial cells is sparse but well vascularised. Scale bars ¼ 13 mm (A),
34 mm (B). M. schliemanni.
4.1. Phylogenetic implications
There is general agreement to recognize four superfamilies
of microbats [1,6,8,13]. These are currently Rhinolophoidea,
Emballonuroidea, Noctilionoidea and Vespertilionoidea.
Recent phylogenies based on DNA sequence analysis place
Myzopoda either in Noctilionoidea [1] or Vespertilionoidea
[6]. However, alternative topologies, including an association
of Myzopoda with Emballonuridae and Nycteridae, cannot
be rejected on the basis of molecular data [6].
Noctilionoidea is well supported in cladistic analyses of de-
velopmental data [14,15]. Two of the character transforma-
tions supporting this group are orientation of the vulva in an
anterior-posterior direction and enlargement of the clitoris
[15,16]. Like most other bats, Myzopoda has transverse orien-
tation of the vulva and a small clitoral pad. Five additional
characters that support Noctilionoidea are concerned with
early development. They include development to the blasto-
cyst stage within the Fallopian tube, features of implantation,
and amniogenesis by cavitation [15]. Thus, it would be
489
necessary to have a developmental series of Myzopoda in order
to complete the comparison.
Abundant interstitial gland tissue is a consistent feature of
Vespertilionoidea [15] although it also occurs in Thyroptera
[17], placed in the Noctilionoidea. In contrast, interstitial
gland tissue was quite sparse in Myzopoda.
Emballonuridae is supported by two derived character
conditions: the absence of an allantoic vesicle at all stages
of development and the presence of a haemophagous region
within the placenta [15]. Myzopoda had no allantoic vesicle
at the stage examined but it is not known whether it is
always absent or is lost in the course of gestation as occurs
in most other bats [15]. Haemophagous regions are com-
prised of columnar trophoblast with the ability to engulf ma-
ternal erythrocytes and free their contained iron for use by
the fetus [18]. They are a feature of placentation in many
mammals [18], but among bats are seen only in Myzopoda
and in Emballonuridae, where they have been found in six
different genera [19].
Endotheliochorial placentation, with retention of the
maternal capillary endothelium in late pregnancy, is another
consistent feature of Emballonuridae [15]. In noctilionoids
and most vespertilionoids the minimum interhaemal barrier
at term is haemochorial, although the placenta is endothelio-
chorial in Natalus, which is assigned to Vespertilionoidea [4].
For mammals as a whole, this particular character has proven
difficult to resolve by cladistic analysis [20]. It can be re-
solved for bats only under the assumption of accelerated
character transformation, but endothelial placentation then
appears as a character transformation on the lineage of Em-
ballonuroidea [15].
Thus none of the characters we have examined offer
support for inclusion of Myzopoda in Noctilionoidea [1] or
Vespertilionoidea [6] (Table 2). There is, however, some
support for an alternative scenario that includes Myzopoda
with Emballonuridae and Nycteridae [6]. This includes
the nature of the interhaemal barrier and the presence of
a haemophagous region. To further examine this hypothesis
we would need to examine a full developmental series of
Myzopoda. In addition a study of placentation in Nycteridae
is greatly overdue.
Little is known about the reproductive biology of Myzo-
poda spp. The two pregnant specimens were caught in Sep-
tember and October. Each bore a single embryo, as do most
bats. Both embryos were in the left horn but in one the corpus
luteum was found in the right ovary. Asymmetry of the repro-
ductive tract, usually with the right side dominant, is common
in bats and may be an ancient feature [21], but the character
conditions are quite variable [15].
In conclusion, we have studied definitive placentation in
Myzopoda and describe some tubular structures of unknown
function that are unique to the genus. Several features of pla-
centation, especially the interhaemal barrier, which is endothe-
liomonochorial, and the presence of a haemophagous region
are coherent with an association of Myzopodidae with Embal-
lonuridae. No support was found for alternative hypotheses
that include the Myzopodidae in Noctilionoidea or
490 A.M. Carter et al. / Placenta 29 (2008) 484e491

Table 2
Comparison of reproductive tract and placentation in Family Myzopodidae with Superfamilies Noctilionoidea, Vespertilionoidea and Emballonuroidea
Charactera Myzopodidae Noctilionoidea Vespertilionoidea Emballonuroidea
Vulva (1) Transverse orientation Anterior-posterior orientation Transverse orientation Transverse orientation
Clitoris (2) Small clitoral pad Elongated clioris Small clitoris Small clitoris
Uterine morphology (3) Bicornuate Bicornuate with evolutionary Bicornuate Unresolved: bicornuate or
transformation to simplex uterus duplex uterus
Ovarian interstitial Sparse Sparse Abundant Sparse
gland tissue (4)
Definitive yolk sac (16) Partially inverted Partially inverted Partially inverted Gland-like with
reduced lumen
Allantoic vesicle (17) Absent in late Absent in late gestation Unresolved: absent in late Rudimentary throughout
gestation gestation or rudimentary gestation
throughout
Location of definitive Mesometrial Lateral to mesometrial with Facing uterotubal junction Lateral to mesometrial
placenta (18) several evolutionary transformations with evolutionary transformation
to antimesometrial
Gross form of placenta (19) Single disc Single disc Single disc with evolutionary Single disc
transformations to double disc
Overall structure of placenta Labyrinthine Labyrinthine Labyrinthine Labyrinthine
Interhaemal barrier (20) Endotheliochorial Haemochorial Haemochorial with evolutionary Endotheliochorial
transformation to endotheliochorial
in Natalus
Type of trophoblast in One layer of Two layers: syncytio- and Unresolved One layer of cyto- or
barrier (21) cytotrophoblast cytotrophoblast syncytio-trophoblast
Intrasyncytial membrane Not applicable Present Present Not applicable
Number of umbilical Two arteries and Two arteries and one vein Two arteries and one vein Two arteries and one vein
vessels one vein
Haemophagous regions (22) Present Absent Absent Present
Endometrial stroma Decidua present Decidua present Decidua present Decidua present
Number of offspring (23) One One One with transformation One
to two or more
Pubic nipples (25) Absent Absent Absent Absent
a
Numbers in brackets refer to characters in Carter and Mess [15]. Unnumbered characters were not phylogenetically informative in that study.

Vespertilionoidea. Further studies including early develop-
mental stages might throw light on the phylogenetic affinities
of this interesting family.
Acknowledgements
We thank Dr. Thomas N. Blankenship for stimulating dis-
cussions. The financial support of The Carlsberg Foundation
is gratefully acknowledged (AMC). Fieldwork associated
with the collection of these specimens was supported by grants
from the John D. and Catherine T. MacArthur Foundation,
Volkswagen Foundation and Beneficia Foundation (SMG).
We are grateful to the Malagasy authorities for permits to con-
duct these field programs.
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