The Pelvis of the Free-tailed Bat: Sexual
Dimorphism and Pregnancy Changes
E. S. CRELIN A N D E. V. NEWTON
Department of Anatomy, Y a k University School of Medicine,
New Haven, Connecticut
ABSTRACT
There are constant morphological differences between the bony pelves
of adult males and females that constitute a sexual dimorphism. A convexity along
the caudal border of the ischiopubic ramus and a bony projection bordering the pubic
joint are present only in the male. The pubic joint in the male is a typical symphysis,
whereas in the female it consists of an interpubic ligament interconnecting the coxal
bones. The ligament contains an abundance of elastic fibers interspersed among collagenous fibers. The disparity between the size of the pelvic birth canal of the pregnant bat and the single full-term fetus is so great that during parturition the interpubic ligament stretches to more than 15 times its original length.
The present experiment was designed to
determine the features that constituted a
bony pelvic sexual dimorphism and the
pelvic changes occurring during pregnancy
in the free-tailed bat.
Weigert's resorcin-fuchsin elastic stain
that stained elastic fibers blue-black to
black, collagenous fibers pink to red, cell
nuclei blue to black, and muscle yellow.
MATERIALS AND METHODS
There is no significant difference between the male and female in the size of
the bony pelvis. The features constituting
a bony pelvic sexual dimorphism are few.
The caudal border of the ischiopubic ramus
in the male has a distinct bony convexity
that is lacking in the female (figs. 3, 5).
The pubic joint of the male is a typical
pubic symphysis (figs. 2, 11) . The ends of
the coxal bones at the joint are less than
1 mm apart and capped with hypertrophic
hyaline cartilage that is continuous with
a compact lamina of fibro-elastic cartilage
in the center of the joint. The dense articular capsule of the male pubic symphysis
contains both collagenous and elastic fibers
(fig. 11). A projection of coxal bone at the
symphysis in the male is absent in the female (figs. 3, 5). Instead of a pubic symphysis in the adult female the ends of the
coxal bones at the pubic joint are interconnected by an interpubic ligament (figs. 4,
6, 7, 9). The ligament is attached directly
to an irregular surface of the coxal bones
at the joint (figs. 5, 9). Its outer part is a
mcdification of the articular capsule sur-
A total of 43 free-tailed bats (Tadarida
brasiliensis cynocephala, LeConte) were
captured in their wild state. Five were
adult males, six were nonpregnant adult females, and 32 were pregnant females in all
stages of an 11 to 12 week pregnancy. Five
of the latter were sacrificed shortly after
parturition, whereas the others were sacrificed at different stages of the pregnancy
period. At autopsy the pelves of all of the
bats were exposed. If an interpubic ligament were present it was cleaned and
measured in situ. The bony pelves were
then excised and stripped of attached soft
tissue. Quantitative and qualitative studies
were made on each pelvis to determine the
features that constituted a bony pelvic
sexual dimorphism similar to those made
on mouse and rat pelves (Crelin, '60;
Bernstein and Crelin, '67). The pelves of
two males, three nonpregnant females, five
pregnant females, and two post partum
females were prepared as dried whole
mounts. The pubic joint portion of the
coxal bones with its interconnecting cartilage or ligament was excised from the remaining bats and fixed, decalcified and
embedded in paraffi?. The tissues were
sectioned serially at 7 LI and stained with
ANAT. REC., 164: 349-358.
RESULTS
Received Jan. 27, '69. Accepted Mar. 10,'69.
1 This investigation was supported in whole by
Public Health Service Research p n t AM 09499-14
from the National Institute of Arthritis and Metabolic
Diseases.
349
350
E. S. CRELIN AND E. V. NEWTON
rounding the fibro-elastic cartilage of the
male symphysis. In the female it is a long
sheath of fibrous connective tissue containing an abundance of elastic fibers (figs. 10,
12, 13). The elastic fibers of the capsular
portion blend with those of the stroma of
the abdominal wall and pelvic musculature
that attaches to the ligament. Deep to the
capsular portion there is an intermingling
of bundles of elastic and collagenous
fibers (fig. 14). As the core of the ligament
is approached the elastic fibers become
fewer in number. The core consists almost
entirely of collagenous fibers. Osteoclasts
are present along the irregular surface of
the coxal bones where the ligament attaches.
The interpubic ligament was approximately the same length in the early pregnant bats as it was in the late pregnant
ones. Its average length was 1.75 mm
(range 1.10-2.35 mm) in all of the females, including the post partum females.
The bony pelvic birth canal consists of the
two coxal bones that articulate with the
sacrum posteriorly and with each other anteriorly through the interpubic ligament
(fig. 1 ). The widest diameter of the bony
birth canal was in the transverse interacetabular plane in all of the females and
averaged 3.35 mm (range 3.00-4.00 mm).
Since the widest diameter of the five newborn bats was in their caudal truyk region
and averaged 16.00 mm (range 15.5016.20 mm), it was calculated that the interpubic ligament had to increase in length
Fig. 1 A diagram of the actual size of the
bony birth canal of a nonpregnant free-tailed bat
is shown in A. The increase in lenzth of the interpubic ligament necessary for the birth canal
to accommodate a full-term fetus is shown in B.
S, sacrum; C, coxal bone; L, interpubic ligament.
during parturition by 15 times or more
(figs. 1, 7, 8).
DISCUSSION
In the literature search nothing was
found describing the presence of a bony
pelvic sexual dimorphism in the free-tailed
bat. Vaughn ('59) reported on the anatomy
of three other species of bats (Eumops,
Myotis, and Macrotus) in some detail, including illustrations, without describing a
bony pelvic sexual dimorphism. Even so,
such a dimorphism is probably universal
in bats. The anatomy of the rat has been
reported in great detail for many years and
yet it wasn't until relatively recently that
a bony pelvic dimorphism was described
(Crelin and Brightman, '57).
The dimorphic features of the bony pelvis of the bat presumably occur during
development under hormonal influence.
In the mouse and rat the chief causative
factor of development is gonadal testostercne (Crelin, '60; Crelin and Blood, '61;
Bernstein and Crelin, '67). The type of
pelvis that develops in the absence of the
gonads in the mouse and rat is the female
type, therefore, gonadal estrogen has no
influence on the shaping of the pelvis during development. However, at puberty the
ends of the coxal bones at the pubic joint
undergo some resorption in the mouse due
to the influflence of estrogen (Crelin, '54c;
Gardner, '36). Estrogen at puberty presumably induces the resorption of the coxal
bones where the interpubic ligament attaches in the female free-tailed bat.
Hamre et al. ('28) studied the pelvis of
the bat, Myotis lucifugus, and found that a
typical pubic symphysis was present in
males and immature females, whereas an
interpubic ligament was present in sexually mature females. They reported that
during pregnancy the ligament increased
greatly in thickness and width. They concluded that the transformation of the pubic
symphyseal tissue into an interpubic ligament was associated with the attainment
of sexual maturity in the female, somewhat similar to the occurrence in the
guinea pig (Talmage, '47). This is quite
different in the mouse where the transformstion of symphyseal tissue into a ligament does not occur until duriqg the first
pregnancy (Crelin, '54b; Crelin and Koch,
351
BAT PELVIS
Crelin, E. S. 1954a Prevention of innominate
bone separation during pregnancy in the
mouse. Proc. SOC. Exp. Biol. and Med., 86:
22-24.
1954b The effects of androgen, estrogen and relaxin on intact and transplanted
pelves i n mice. Am. J. Anat., 95: 47-73.
1954c The effects of estrogen and relaxin on the pubic symphysis and transplanted
ribs in mice. Anat. Rec., 120: 23-32.
1960 The development of bony pelvic
sexual dimorphism in mice. Ann. N. Y. Acad.
Sci., 84: 879-512.
1963 The development and hormonal
response of the autotransplanted interpubic
joint i n mice. Anat. Rec., 146: 149-163.
Crelin, E. S. and D. K. Blood 1961 The influence of the testes on the shaping of the bony
pelvis in mice. Anat. Rec., 140: 375-379.
Crelin, E. S . and M. W. Brightman 1957 The
pelvis of the rat: its response to estrogen and
relaxin. Anat. Rec., 128: 467483.
Crelin, E. S . and W. E. Koch 1965 Development of mouse pubic joint in uivo following
initial differentiation in uitro. Anat. Rec., 153:
161-171.
Gardner, W. U. 1936 Sexual dimorphism of
the pelvis of the mouse, the effect of estrogenic
hormones upon the pelvis and upon the develI
.
Anat., 59:
opment of scrota1 hernias. Am. .
459483.
Gersh, I. and H. R. Catchpole 1960 The nature of ground substance of connective tissue.
Perspectives in Biol. and Med., 111: 282-319.
Hall, K. 1947 The effects of pregnancy and
relaxin on the histology of the pubic symphysis
in the mouse. J. Endocrin., 5: 174-182.
1960 Relaxin. J. Reprod. Fertil., I :
368-384.
Hamre. C.. R. K. Meyer and S. J. Martin 1928
Sexu'al dimorphism- of the symphysis pubis of
the bat Myotis Zucifugus (Miller). Anat. Rec.,
41: 60-61.
Horn, E. H. 1958 Effects of feeding thiouracil
and/or thyroid powder upon pubic symphyseal
separation in female mice. Endocrinology, 63:
481-486.
Sherman, H. B. 1937 Breeding habits of the
free-tailed bat. J. Mammal., 18: 176-187.
Steinetz, B. G. and B. L. Beach 1963 Hormonal
requirements for interpubic ligament formation. i n hvuouhvsectomized mice. Endocrinology, 72: fflL776.
Steinetz, B. G., J. P. Manning, M. Butler and V.
ACKNOWLEDGMENTS
Beach 1965 Relationships of growth horThe authors thank Dr. R. J. Stephens
mone, steroids and relaxin in the transformation of pubic joint cartilage to ligament i n hyand Dr. 0. W. Henson for procuring the
pophysectomized mice. Endocrinology, 76: 876bats. Dr. Henson also assisted in the liter882.
ature search.
Talmage, R. V. 1947 Changes produced in the
symphysis pubis of the guinea pig by the sex
LITERATURE CITED
steroids and relaxin. Anat. Rec., 99: 91-113.
Bernstein. P. and E. S . Crelin 1967 Bony pelvic Vaughan, T. A. 1959 Functional morphology
of three bats: Eumops, Myotis, Macrotus. U. of
sexual dimorphism in the rat. Anat. Rec.; 157:
Kansas Pub., Museum of Nat. Hist., 12: 1-153.
517-526.
'65; Hall, '47). The ligament of the mouse
is also quite different from that of the
free-tailed bat in that it is relatively very
much shorter in length and not very elastic during parturition (Crelin, '54b). In
addition, the formation of a ligament is
not essential for parturition to occur in
the mouse (Crelin, '54a).
The formation of the interpubic ligament in the bat is without doubt induced
and controlled by hormones. Exactly what
hormones has yet to be determined. In the
mouse it is a combination of estrogen,
relaxin, thyroxin and somatotropin (Crelin, '54b; Hall, '60; Horn, '58; Steinetz and
Beach, '63).
Although the increase in length of the
ligament during parturition in the bat is
essentially a stretching phenomenon, the
ground substance in which the collagenous
and elastic fibers are embedded must be in
a less dense, colloid-poor, water-rich phase
to allow the shifting of position and the
sliding of the bundles of collagenous fibers
in relationship to each other as the ligament is stretched. Again, this is undoubtedly the result of the influence of hormones as it is in the mouse (Crelin, '63;
Gersh and Catchpole, '60; Steinetz et al.,
'65).
The passing out of the single newborn
bat from each mother was not witnessed in
the present experiment. Sherman ('37)
observed that it takes place in about a
minute and a half in this species. Not only
does the resistance of the mother's pelvic
structures have to be overcome during parturition in the free-tailed bat, but the force
of gravity as well. The mother hangs in
the usual upside-down position while the
baby is born tail-end first.
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~
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PLATE 1
EXPLANATION OF FIGURES
2
Ventral view of the bony pelvis of a n adult male. The arrow indicates the pubic symphysis. x 5.
3 Lateral view of the bony pelvis of a n adult male. A projection of
bone (P) at the pubic symphysis and a convexity ( C ) along the
caudal border of the ischiopubic ramus are indicated. X 5.
4
Ventral view of the bony pelvis of an adult nonpregnant female.
Arrows indicate the ends of the two coxal bones interconnected by
an interpubic ligament. X 5.
5 Lateral view of the bony pelvis of a n adult nonpregnant female. The
irregular surface of the pubic portion of the left coxal bone ( P )
where the interpubic ligament is attached is indicated. The pubic
spine (S) is where the psoas minor muscle inserts and is the same
in both sexes. X 5.
6
352
Ventral view of the bony pelvis of a pregnant female. Arrows indicate the ends of the two coxal bones interconnected by a n interpubic ligament. x 5.
BAT PELVIS
PLATE 1
E. S. Crelin and E. V. Newton
353
PLATE 2
EXPLANATION OF FIGURES
7 A newborn bat is shown in its folded condition below the bony pelvis
of its mother. The arrow passes behind the interpubic ligament to
indicate the route the newborn took through the pelvic birth canal.
The newborn and pelvis are magnified exactly the same to show the
great disparity between the size of the pelvic birth canal and the newborn free-tailed bat. X 3.
8
354
A full-term fetus, removed by Caesarian section and unfolded, is
placed next to its mother to show the relatively large size of the fetus.
BAT PELVIS
E. S. Crelin and E. V. Newton
PLATE 2
355
PLATE 3
EXPLANATION OF FIGURES
9
Section of the ends of the coxal bones ( B ) and attached interpubic
ligament (L) from a pregnant bat. X 35.
10 Section of the free border of an interpubic ligament showing the
capsular portion ( C ) containing an abundance of elastic fibers. X 400.
11
Section of the pubic symphysis from a n adult male. Indicated are
the articular capsule ( C ) of the joint, the hypertrophic hyaline
cartilage (H) lining the end of the coxal bone (B), and the compact
lamina of fibro-elastic (FE) cartilage in the center of the joint. x 60.
12 Tangential section of the dense layer of elastic fibers in the capsular
portion of a n interpubic ligament. x 500.
13
Section of the periphery of the capsular portion of a n interpubic ligament showing loosely-arranged elastic and collagenous fibers. X 500.
14 Section deep to the capsular portion of a n interpubic ligament showing bundles of elastic fibers (arrows) interspersed among dense
bundles of collagenous fibers. X 500.
356
BAT PELVIS
E. S. Crelin and E. V. Newton
PL.\TTE 3
357
Автор
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