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The reproductive organs of the male spotted skunk (Spilogale putorius).

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The Reproductive Organs of the Male Spotted
Skunk (Spilogale putorius)
Department of Biological Sciences, University of Idaho,
MOSCOW,Idaho 83843
A relatively well developed prostrate is the only accessory sex gland
present in the spotted skunk (Spilogale putorius). The distal end of the vas deferens
is quite glandular, but there is no distinct ampullary swelling. The gross morphology
of this species is compared with that of several other members of the family Mustelidae.
Hamlett's review of delayed implantation ( ' 3 5 ) stimulated considerable work
with several members of the weasel family
(Mustelidae) exhibiting this phenomenon.
However, most investigators have concerned themselves with various aspects of
the female reproductive tract or cycle. The
gross anatomy of the male reproductive
system and/or testicular cycle of Mustela
furo (Allanson, '32), M. frenata (Wright,
'47), M . emzinea (Deanesly, '35), M. nivalis (Hill, '39), Meles meles (Neal and
Harrison, ' 5 8 ) , Taxidea taxus (Wright,
'69), and Spilogale putorius (Mead, 'GSa,b)
have been described. However, few complete morphological and histological descriptions of the entire male reproductive
tract of members of this interesting family
are available and no descriptions of the
anatomy of the male reproductive tract of
any of the subfamily Mephitinae have been
Mead ('68a,b) demonstrated that western forms of the spotted skunk (Spilogale)
breed in the fall and exhibit a 180 to 200
day period of delayed implantation,
whereas eastern forms of this genus breed
in the spring. The gestation period of the
latter population is not precisely known,
but delayed implantation must be of exceedingly short duration, as in the mink,
if it occurs at all. Since the reproductive
cycles and karyotypes of eastern and western forms are distinctly different (Hsu and
Mead, '69), it was of interest to look for
differences in the morphology of the male
reproductive organs similar to those described by Mossman, Lawlah and Bradley
('32) in the family Sciuridae. Therefore a
ANAT. REc., 167: 291-302.
thorough study of the male reproductive
system of eastern and western spotted
skunks was undertaken and the observations compared with those of other members of this family.
Complete reproductive tracts of eight
male spotted skunks, representing three
subspecies (S. p . gracilis, S . p . latifrons,
and S . p . ambarualis) collected at various
times throughout the reproductive cycle,
were preserved in AFA (alcohol, formalin
and acetic acid) or 10% formalin and
stored in 70% ethyl alcohol. The gross
anatomy of each specimen was diagramed
and measurements made with a millimeter
rule. Appropriate tissues were dehydrated
in a graded series of ethyl alcohol,
cleared in methyl salicylate, embedded in
paraffin and sectioned at 6 p . The prostate,
urethra and penis of two specimens were
serially sectioned. The 0s penis was decalcified in Jenkin's fluid prior to dehydration and sectioning. Tissues were stained
with Groat's tetrachrome stain or Verhoeffs
elastin stain. All cytological measurements
were made with an ocular micrometer.
The gross anatomy of the reproductive
tract of the male spotted skunk is illustrated in figure 1. No gross differences in
the morphology, with the exception of the
baculum (Mead, '67), or histology of
the male reproductive tracts of the eastern
and western populations were detected.
Received Jan. 21, '70. Accepted Feb. 17, '70.
Fig, 1 Dorsal and lateral views of the male reproductive system of Spibgale. B., baculum; C.,
crus; E., epididymis; G.P., glans penis; M.U., muscular urethra; P., prostate; U., ureter; U.B., urinary bladder; V., vein.
Cyclic changes in the testes and epididymides have been described for this species
(Mead, '68a,b); therefore, further descriptions of these organs will be omitted.
Vas deferens
The vasa deferentia pass dorsal and
parallel to the epididymides and then extend cranially for a short distance after
passing through the inguinal canal. They
then loop over the ureters and continue
caudally to the prostate. Upon entering the
dorsal surface of the prostate, they proceed diagonally to about the midpoint of
the latter gland before turning abruptly to
open onto the surface of the colliculus
seminalis. There is no gross external enlargement at the distal end of the vas
deferens to form an ampulla similar to that
encountered in other species of mustelids
(table 1 ) .
Three distinct layers (mucosa, tunica
muscularis, and adventitia) are readily observed in cross sections of this organ (fig.
2). The mucosa is thrown into several
longitudinal folds. Its epithelium is tall
(24-45 p ) pseudostratified columnar. Some
but not all of its cells bear steriocilia. Occurrence and distribution of the steriocilia
were not extensively studied but it appears
that their condition is not constant
throughout the year. Blebs of cytoplasm
occur on the luminal surface of the epithelium of specimens taken during the breeding season. In some regions of the vas deferens some of the oval-shaped basal cells
are much larger than others and contain
large amounts of clear staining cytoplasm.
These cells frequently occur in clusters
which resemble glands. Within the prostate the lumen of the vas deferens appears
to be slightly expanded and the epithelial
lining contains many crypts. Some crypts
are lined with large cells (12 L L )not too unlike those previously described; others are
hollow (fig. 3 ) . This region of the vas deferens is undoubtedly homologous to the ampullae of other species. There is an abrupt
change in the luminal epithelium of the
vas deferens from pseudostratified columnar to transitional approximately 800
from its distal end. Each vas deferens
opens laterally into the prostatic urethra
via a narrow slit (approximately 15-20
wide) (fig. 4 ) .
The lamina propria beneath the luminal
epithelium is represented by a thin band
of longitudinally arranged elastic fibers interspersed among a sparse network of loose
connective tissue. A distinct muscularis
mucosa is lacking.
The tunica muscularis consists of a
prominent inner layer of circularly arranged and a thinner outer longitudinally
arranged layer of smooth muscle. A thin
adventitia composed of dense connective
tissue forms the outermost covering. A
serosa is lacking.
A well developed prostate gland completely surrounds the urethra and is firmly
attached to it. Its size varies from 7 X 7 X 3
Summary of the anatomy o f the vas deferens and prostate gland o f
various male mustelids
Vas deferens
Species 1
Prostate 2
Ampulla Ampulla
present absent developed developed
Mustela nivalis
Mustela erminea
Mustela frenata
Mustela furo
Mustela vison
Lutra canadensis
Lutra lutra
Galictes s p .
Spilogale putorius
Mustela lutreola
Tnxidea taxus
Meles meles
Hill, '39
Heidt, '69
Leydig, 1850
Mead, present study
Allanson, '32
Mead, present study
Hansson, '47
Disselhorst, '04
Wright, '69
Owen, 1868
Disselhorst, '04
Mead, present study
Leydig, 1850
Disselhorst, '04
Disselhorst, '04
Mead, present study
1 All scientific names used in this table with the exception of Galictes, are those in current usage.
2 For the purposes of this classification, a well developed prostate means that the glandular epithelium which surrounds the urethra i s developed to such an extent that it forms a distinct and readily
visible organ during the breeding season.
mm to 11 X 16 X 9 mm (length, breadth,
thickness) attaining its largest size during
the breeding season. The dorsal surface,
which is in close apposition to the rectum,
is slightly concavo-convex. The lateral surfaces gently taper in toward the mid ventral margin and are convex as is the ventral
surface, except for a small region near the
junction with the urinary bladder (fig. 1).
Although there is a slight mid ventral indentation in the surface of the prostate of
some specimens, there is no histological
evidence that this gland is truly bilobed.
The prostate is enveloped by a tough
capsule composed of a thin outer layer of
dense regular connective tissue and an
inner layer of smooth muscle. No elastic
fibers were observed in the capsule, as have
been described in the human prostate.
Trabeculae composed of connective tissue
and smooth muscle radiate from the
prostatic urethra and unite with the capsule (fig. 5). These structures carry nunierous blood vessels and nerves from the
capsule to the deeper portions of the gland.
Nerve ganglia are abundant beneath the
capsule and in the trabeculae. The prostate
is composed of numerous compound
tubulo-alveolar glands which are situated
between the trabeculae. The glandular epithelium vanes from simple cuboidal to
very tall pseudostratified columnar. Its
height is in part correlated with testicular
activity. Specimens whose testes contained
spermatozoa generally had tall simple
columnar epithelium containing vesicular
cytoplasm and basal nuclei. The apical
ends of some of the cells stained bright
orange and contained large clear vacuoles.
The glandular epithelium of anestrous
males was generally cuboidal or low columnar and there was an increased amount
of stroma in such glands. The condition
of the glandular epithelium is also apparently related to the secretory state of the
gland, as the height of the epithelium was
observed to vary from low columnar to
very high columnar within the same alveolus. The terminal duct of each prostatic
gland penetrates the submucosa and mucosa of the prostatic urethra and empties
into the lumen of the latter organ at any
point on its circumference (fig. 5). The
diameters of these ducts are usually
smaller than those of the secretory tubules
and they are lined by simple cuboidal or
low columnar epithelium.
No corpora amylacea were observed in
any of the specimens even though one
animal was three years old.
Prosta tic urethra
The prostatic urethra of this species is
8 to 10 mm long. The mucosa consists of
an epithelium and a lamina propria with
10 to 15 longitudinal folds (figs. 5, 6 ) .
Much of the lumen is lined by transitional
epithelium but distally the lining grades
from patches of stratified low columnar
to stratified squamous. A thick submucosa
(200 to 250 p ) , consisting of dense connective tissue and an elaborate network of
elastic fibers, comprises the bulk of this
organ. Elastic fibers from the latter layer
extend a short distance into the trabeculae
of the prostate (fig. 5). A thin longitudinal
band of smooth muscle extends about one
third the length of the organ near the
neck of the bladder, but a distinct tunica
muscularis is absent in the more distal
regions of this duct.
A short longitudinal swelling occurs in
the mid dorsal wall, the colliculus seminalis, which contains the distal ends of the
vasa deferentia and the utriculus prostaticus (fig. 4). The latter courses between the vasa deferentia for a distance
of 850 to 900 p and opens into the prostatic uretha just distal to the vasa deferentia. It is lined by pseudostatified columnar epithelium and is enveloped by a
thin band of loose connective tissue and
several layers of smooth muscle,
Muscular urethra
The muscular urethra is about 12 mm
long and extends from the caudal margin
of the prostate to the base of the penis.
The lumen is lined with stratified squamous and stratified low columnar epithelium. In some specimens a thin layer of
loose connective tissue, corresponding to
the lamina propria, is thrown into longitudinal folds. In others, the latter layer
is absent or so reduced as to be indistinguishable from the adjacent thick layer
of dense connective tissue and extensive
network of fine elastic fibers which is
present in all specimens. The tunica
muscularis is exceedingly well developed
and consists of several layers of striated
muscle. In mid sagittal sections a narrow
band of longitudinally arranged muscle
fibers originates at the base of the dorsal
portion of the prostate and extends caudally. The insertion of this muscle was
not observed but it most likely is the base
of the penis. Only circular (innermost)
and oblique (outermost) skeletal muscles
were noted in parasagittal sections. However, cross sections of this organ reveal
the presence of paired longitudinal muscles which course along the lateral margins. An adventitia of loose connective
tissue which helps to bind several large
arteries, veins, and nerves to the dorsolateral walls, provides the outer covering
of this organ.
The glans penis, which is completely
ensheathed by the prepuce, is 13 to 25 mm
in length. A long slender baculum with a
small hollow core is embedded in the glans
dorsal to the urethra. The shape of the
baculum varies depending upon the age
and subspecies of the animal (Mead, ’67).
The outer surface of the glans and the
opposing walls of the prepuce are lined
with stratified squamous epithelium.
The reproductive system of male mustelids is relatively simple, the prostate
being the only recognized accessory sex
gland. Table 1 summarizes the condition
of the vas deferens and prostate in a
number of mustelids. These organs exhibit
striking differences in the species studied
Penis and penile urethra
to date.
The penis is about 35 to 40 mm in
The prostate of the spotted skunk is
length. The root of the penis (radix penis) clearly the largest and best developed of any
is firmly attached to the caudal margins species in table 1. It forms a pronounced
of the ischii by connective tissue, The swelling which projects well above the
bulbous ends of the crura are likewise general outline of the muscular urethra
attached to the ischium by the bulbo- and at all times of the year. Mustela frenata
ischiocavernous muscles. The latter origi- and M . erminea represent an intermediate
nate on the ventrolateral margins of the condition in which the prostate becomes
crura and insert on the ischial tuberosi- greatly enlarged during the breeding seaties. Cross sections through the radix penis son (fig. 9). It is interesting to note that
reveal paired corpora cavernosa (fig. 8). Hill (’39) found no obvious prostate in M .
At the point where the crura become nivalis. One might arrive at a similar conabruptly constricted, the corpora cavernosa clusion if reproductive tracts of the other
unite but remain partially separated for a weasels were examined during anestrus
short distance by an incomplete median as the prostatic region of a sexually inacseptum of connective tissue. The tunica tive specimen of M . frenata exhibited no
albuginea is composed of dense wavy col- swelling. Cross sections of this region relagenous fibers, but lacks elastic fibers. The vealed the presence of extremely involuted
inner walls of the tunic give rise to num- patches of glandular tissue. Lesser deerous branching trabeculae composed of grees of swelling occur during the rut in
smooth muscle and connective tissue, the other species listed in table 1. Hansthereby dividing the interior of each crus son’s photograph (’47) of the reproductive
into a labyrinth of blood sinuses.
tract of a sexually active mink ( M .v i s o n )
The sharp flexure of the penis at the clearly illustrates a swollen prostatic redistal margin of the pelvis causes the gion, whereas the anestrus specimen I exurethra. which is wedged within a groove amined was totally devoid of any swelling.
formed by the ventral margins of the Absence of such swelling during rut is not
crura, to lie ventral to the penis. The penile necessarily indicative of “a poorly develurethra contains a well developed corpus oped prostate” as the prostatic tissue of a
spongiosum (fig. 7) and its lumen is lined sexually active otter (Lutra canadensis)
with stratified squamous epithelium. A which I examined was well developed;
slight dorsal depression between the crura however, the alveoli were not as closely agis occupied by paired nerves and arteries. gregated as in the weasels. The same may
An adventitia of connective tissue forms be true for other species such as Taxidea
the outer covering of the penis at this level. in which the gland is more diffuse. Wright
('69) found glandular elements in the neck
of the bladder and in the urethra of the
American badger which he interpreted to
be scattered prostatic tissue.
The terminal end of the vas deferens
of mustelids also exhibits a dichotomy in
its morphology. Vasa deferentia of most
weasels and the American badger (Wright,
'69) have well developed swellings (ampullae), whereas the other species studied
do not. Ampullae of sexually active specimens of M. frenata are about 1.2 X 1.0
mm in diameter and are composed of numerous compound tubulo-alveolar glands
lined with simple columnar epithelium. According to Heidt ('69) only poorly developed ampulliform swellings occur in M.
nivalis, although he does not state whether
he examined specimens trapped during
the breeding season. Faint swellings can
be observed in Hansson's photograph of
the reproductive tract of M .vison and similar swellings have been described by Leydig (1850) in the European mink (M.
lutreola). No distinct ampullae were observed in any of the spotted skunks but
the distal portions of the vasa deferentia
are quite glandular and the same may
be true for other species which lack
definite ampullae.
Several investigators such as Mossman,
Lawlah and Bradley ('32) have cited the
utility of the anatomy of male reproductive organs in taxonomic and evolutionary
problems. But the paucity of data regarding the morphology of mustelid reproductive organs and the universal lack of accessory sex glands other than the prostate
tend to make any comments on these parameters of little value at this time.
I am deeply indebted to my wife for
her technical assistance in preparing the
slides and illustration; to Dr. H. W. Mossman for his helpful suggestions in the
preparation of the manuscript; and to Dr.
P. L. Wright for the loan of his slides of
the prostate gland of the badger. The research was supported by a grant from NIH
(HD 04021-02).
Allanson, M. 1932 The reproductive processes
of certain mammals. 111.-The reproductive cycle
of the male ferret. Proc. Roy. SOC. B., 110:
Deanesly, R. 1935 The reproductive processes
of certain mammals. 1X.-Growth and reproduction in the stoat ( M u s t e l a e r m i n e a ) . Phil. Tran.
Roy. SOC.London, B., 225: 459492.
Disselhorst, R.
1904 Ausfuhrapparat und Anhangsdrusen der mannlichen Geschlechtsorgane. Oppel's Lehrbuch d. vergleich. mikrosk.
Anat., Bd. 4. Jena.
Hamlett, G. W. D. 1935 Delayed implantation
and discontinuous development in the mammals. Quart. Rev. Biol., 10: 432447.
Hansson, A. 1947 The physiology of reproduction i n mink ( M u s t e l a vison, Schreb.) with
special reference to delayed implantation. Acta
Zoologica, 28: 1-136.
Heidt, G. A. 1969 Ontogeny of the least weasel
( M u s t e l a nivalis L.), Ph. D. dissertation, Michigan State Univ., 102 pp.
Hill, M. 1939 The reproductive cycle of the
male weasel (Mustela nivalis). Proc. Zool. SOC.
London, B., 109: 481-512.
Hsu, T. C., and R. A. Mead 1969 Mechanisms
of chromosomal changes in mammalian speciation. In: Comparative Mammalian Cytogenetics.
K. Benirschke, ed. Springer-Verlag New York
Inc., N. Y.,pp. 8-17.
Leydig, F. 1850 Zur Anatomie der mannlichen
Geschlechtsorgane und Analdriisen der Saugetiere. Zeitschr. fur wiss. Zoologie, 11: 1-57.
(as cited by Disselhorst and Oudemans)
Mead, R. A. 1967 Age determination i n the
spotted skunk. J. Mammal., 48: 606-616.
1968a Reproduction in eastern forms
of the spotted skunk (genus Spilogale) J. Zool.,
London, 156: 119-136.
1968b Reproduction in western forms
of the spotted skunk (genus Spilogale) J.
Mammal., 49: 373-390.
Mossman, H. W., J. W. Lawlah and J. A. Bradley
1932 The male reproductive tract of the sciuridae. Am. J. Anat., 51: 89-155.
Neal, E. G., and R. J. Harrison 1958 Reproduction in the European badger ( M e l e s m e l e s ) .
Trans. Zool. SOC.London, 29: 67-130.
Oudemans, J. T. 1892 Die accessorischen Geschlechtsdriisen der Saugetiere. Natuurkunkije
Verhandelingen van de Hollandsche Maatschap.
pij der Wetenschappen. 3de Verz., Dee1 5, 2de
Stuk. 1887-1892.
Owen, R. 1868 The Anatomy of Vertebrates,
11, Mammals. Longmans, Green & Co., London.
Wright, P. L. 1947 The sexual cycle of the
male long-tailed weasel ( M u s t e l a f r e n a t a ) . J.
Mammal., 28: 343-352.
1969 The reproductive cycle of the
male American badger, T a x i d e a taxus. .T. Reprod. Fert., Suppl., 6: 435-445.
Cross section through the vas deferens of Spilogale putorius lntifrons
404 trapped on 8 February. Note the enlarged basal cells in the
mucosa. x 150.
Longitudinal section through the distal end of the vas deferens of
Spilogale putorius ambarvalis 1106 killed on 8 May illustrating the
crypts, some of which are glandular and others (upper left) are
hollow. x 810.
Cross section through the colliculis seminalis of Spilogale putorius
gracilis 1067 killed on 22 November. Note the terminal ends of the
vasa deferentia opening Iaterally into the lumen of the prostatic
urethra. x 158.
Cross section through the prostalic urethra of Spilogale putorius
grucilis 1067. Note the extensive distribution of dark staining elastic
fibers radiating into the trabeculae from the prostatic urethra. Numerous prostatic ducts can be seen entering the urethra a t many places
on its circumference. x 46.
Rodney A. Mead
Cross section through the prostate of Spilogale putorius ambarvalis
1106 illustrating the vasa deferentia (lateral) and uterus masculina
(central). Although this specimen was killed during the height of
the breeding season ( 8 May) and had sperm in its testes the glandular epithelium of the prostate was cuboidal and the glands were not
fully developed. x 44.
Cross section through the penile urethra of Spilogale putorius Zatif r o m 1110 illustrating the well developed corpus spongiosum. x 49.
Cross section through the radix penis and muscular urethra of Spilogale putorius gracilis 1067. x 10.
Cross section through the prostate and ampullae of a sexually active
long-tailed weasel (M. f r e n a t a ) . x 21.
Rodney A. Mead
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spilogale, putorius, malen, skunk, organy, reproduction, spotted
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