Observations on the Vasculature of the Reproductive Tract in Some Australian Marsupials C. S. LEE AND J. D.OSHEA Department of Veterinary Reclinical Sciences, Uniuersity ofMelbourne, Parkuille, Victoria3052. Australia
ABSTRACT The origin, distribution and structure of the blood vessels of the female reproductive tract and the testis of the brush possum (Trichosurus. vulpecula) were studied using latex and silicone rubber casting and histological techniques. Latex casts of the vessels of the female tract were also studied in five macropod species- Macropus giganteus, M. eugenii, M. agilis, Megaleia rufa and Thylogale billardierii and in the common wombat (Vombatus ursinus). The female reproductive tract in the brush possum was supplied and drained by four major sets of paired vessels-ovarian, cranial urogenital, caudal urogenital, and internal pudendal arteries and veins. These vessels formed substantial anastomoses with one another on each side of the midline, and also across-the-midline anastomoses. The proximal part of the ovarian artery ran in close apposition to the ovarian vein, which received one or more large uterine branches. In its distal portion the ovarian artery gave rise to a leash of small, tortuous ovarian branches, which wound around and between the plexiform ovarian veins. The testicular arteries and veins in this species also ran in close apposition to one another. Both arteries and veins branched into many smaller, mildly tortuous, parallel vessels in the spermatic cord, which reunited before entering the testis. The blood vessels of the reproductive tract in all of the macropod species studied, and in the common wombat, were basically similar to those of the brush possum. The intimate structural relationships between ovarian arteries and veins, and their ovarian branches, in these marsupials are suggestive of specializations for counter-current exchange between venous and arterial blood. However, in contrast to those of the testicular vessels where heat exchange is a demonstrated function, their physiological significance remains unknown. The blood vessels supplying and draining the testis have been studied in detail in many species of eutherian and marsupial mammals (Harrison, '49; Barnett .and Brazenor, '58). Particular interest in the testicular vessels has derived from their demonstrated role in countercurrent heat exchange (Setchell, '70; Waites, '70). More recently, considerable interest has been shown in the vasculature of the female reproductive tract, and particularly the ovary, in eutherian mammals (Del Campo and Ginther, '72, '73, '74; Ginther et al., '74; Lee and OShea, '76). This interest has been stimJ . MORPH., 154: 95-114.
ulated by recent evidence that these vessels may play a role in the local transfer of a luteolytic hormone, shown a t least in some , (Goding et al., species to be prostaglandin F '72; McCracken et al., '721, from the uterus to the ovary. In this connection it has been suggested that a correlation exists between he presence of venous and arterial pathways common to the ovary and uterus, and the occurrence of a unilateral uterine luteolytic mechanism (Del Campo and Ginther, '72). Apart from some early data on the main branches of the aorta and caudal vena cava (Beddard, '09; Pearson, '401, the blood vessels
95
96
C. S. LEE AND J. D. O’SHEA
to the reproductive tract in female marsupials do not appear to have been described. The arrangement of these vessels is, however, of interest, since it has been shown that hysterectomy is without effect on the duration of the oestrous cycle in a t least two species of marsupial, namely Didelphys virginiana (Hartman, ’25) and Trichosurus uulpecula (Clark and Sharman, ’65). Although comparable data on other marsupials are not available, a uterine luteolytic mechanism appears a n unlikely evolutionary development in the many species in which the duration of the oestrous cycle exceeds that of pregnancy, which have been listed by Tyndale-Biscoe (”73) and Tyndale-Biscoe et al., (“74). This paper reports data on the blood vessels of the female reproductive tract in the brush possum (Trichosurus uulpecula), five species of macropod marsupials, and the common wombat (Vombatus ursinus). Some observations on the blood vessels of the testis in the brush possum are also presented. MATERIALS AND METHODS
ital pressure via cannulae either into the aort a or directly into the various arterial or venous branches to the reproductive tract. Because of difficulties in filling the veins with latex, resulting from the high incidence of valves, the veins in some specimens were filled with the animal’s own blood by ligating the caudal vena cava before injecting latex into the aorta. In the other species studied, latex casts were prepared by direct injections into vessels of the reproductive tract. In male brush possums, latex injections were made either via the aorta or directly into the testicular artery or vein. After ligation a t the site of injection, all specimens were fixed in 10%formalin and subsequently either dissected, cleared in a 1:3 mixture of ethyl alcohol and methyl salicylate, or (in the case of latex casts only) macerated in 20% sodium hydroxide a t 5OOC. Histology Blood vessels for histological examination, which were obtained from three female and three male brush possums, were fixed in 10% buffered neutral formalin and embedded in paraffin. Single or serial sections were prepared and stained with haematoxylin and eosin (H and E), van Gieson’s stain or Verhoeffs elastic stain. In female animals the ovarian vessels were sectioned a t multiple (generally 6)sites extending from their origin a t the aorta and caudal vena cava to their point of entry into the ovary. In males, the testicular vessels were sectioned both in their intra-abdominal segments and at various points along the spermatic cord.
A total of 23 female and 7 male brush possums (Trichosurus uulpecula) were studied. Most of these animals were adults, and all were estimated to be over one year old. Histories were unknown, but 14 of the females had pouch-young of various ages. These animals were killed by an intraperitoneal overdose of pentobarbitone immediately or shortly before the preparation of casts or the fixation of tissues as described below. Female reproductive tracts, with their major blood vessels attached, were obtained from carcasses of individuals of the following RESULTS species: eastern grey kangaroo (Macropus Trichosurus vulpecula giganteus)-3 specimens, tammar wallaby (M. eugenii)-2, agile wallaby (M.agi1i.s)- 1, red Female There were four major sets of paired arkangaroo (Megaleia rufu)- 1, rufous bellied wallaby (Thylogale bil1ardierii)- 1, common teries and veins supplying the reproductive tract (figs.1,2),which have been designated: wombat (Vombatus u r s i n d - 4 . (1) ovarian artery and vein; (2) cranial uroGross anatomy genital a. and v; ( 3 ) caudal urogenital a. Vessels of the reproductive tract and pelvic and v.; (4) internal pudendal a. and v. The inregion in female brush possums were studied ternal pudendal artery and vein, which supeither in uninjected, formalin-fixed specimens plied the major vessels to the cloaca1 region, or following the preparation of vascular casts were supplemented by anastomotic vessels deeither in situ or after removal of the genital rived from branches of the external iliac tract from the animal. Casts were prepared artery and vein. Although these four sets of using latex rubber (‘‘Latex,” Dunlop Rubber vessels were consistently demonstrable, therz Co., Melbourne, Australia) or silicone rubber were many individual variations in the detail C‘Microfil”MV- 112, Canton Biomedical Prod- of their arrangement, including variations in ucts Inc., Colorado, U.S.A.)injected under dig- origin, branching and anastornotic connec-
REPRODUCTIVE TRACT I N MARSUPIALS
7 Fig. 1 Diagrammatic representation of ventral view of the female genital tract of the brush possum, showing the four major blood vessels supplying the tract. Veins appear pale grey and arteries black. 0, ovary; U, uterus: MV, median vagina; LV, lateral vagina; B, bladder; US, urogenital sinus;C, cloaca; OV, ovarian vessels: AU, cranial urogenital vessels; PU, caudal urogenital vessels; IP, internal pudendal vessels.
tions, and the presence of duplication of any one or more of the vessels.
Origin and distribution of vessels to the genital tract. The Ovarian Arteries (figs. 2 , 3) arose from the aorta close to one another (fig. 41, or occasionally by a common trunk, approximately two-thirds of the way from the origin of the renal arteries to that of the external iliac arteries. In most cases the right ovarian artery ran initially around the left side of the caudal vena tava and then crossed from left to right beneath its ventral surface (fig. 5). On each side, the artery then ran postero-laterally beneath the peritoneum before turning postero-ventrally and entering the cranial part of the broad ligament. Throughout the greater part of its length it ran along the surface of the ovarian vein, to which it was closely apposed (fig. 5).As i t approached the ovary, the artery underwent a series of branchings over a short distance, producing a leash of small ovarian branches of relatively uniform caliber (fig. 3), and then continued to supply branches to the Fallopian
97
tube and uterus. An additional, usually single, branch t o the ureter arose a t the same level in some cases, but more often arose independently, closer to the aorta and a t about the level where the ureter crossed dorsally over the ovarian vessels. There were additional minor branches to the tissues of the broad ligament. Up to the point of major branching, the artery ran a relatively straight course, showing little tortuosity (figs. 2-51. The first few millimeters of the many branches running to the ovary were also almost straight. Beyond this point, however, these branches, z 6 - 1 2 in number, showed a marked tortuosity incorporating many U- or S-shaped bends and regions of spiralling which continued after these vessels entered the substance of the ovary (fig. 3). These arteries branched infrequently and showed occasional anastomoses with one another and with branches running to the Fallopian tube or uterus. They also wound intimately around and between the branches of the venous plexus draining the ovary (fig. 2). The Fallopian tube and nearby areas of the broad ligament were supplied by one or more small, less convoluted branches, while a further group of small terminal branches of the ovarian artery ran to the cranial tip of the uterus (fig. 3). These also showed less tortuosity than those to the ovary. On reaching the tip of the uterus, the major uterine branches ran a convoluted or spiralling course along the mesometrial and antimesometrial borders of the uterus, and terminated by forming end-to-end anastomoses with similar branches from the cranial urogenital artery (fig. 1 ) . Along their courses these mesometrial and antimesometrial branches gave off, at right angles, many small spiralling branches which ran around the surfaces of the horn and frequently anastomosed directly with comparable branches from the opposite border of the uterus (fig.2 ) . These encircling vessels in turn gave off many smaller branches which penetrated the deeper tissues of the uterine wall. The Ovarian Veins (figs. 2, 5) were considerably larger than the ovarian arteries. In each case, the area o f drainage corresponded closely to the region supplied by the ovarian artery, whose pattern of branching was closely paralleled. Thus, the ovarian vein was formed by the fusion of a plexiform group of small veins draining the ovary, several veins
98
C. S. LEE AND J. D. OSHEA
from the cranial end of the uterine horn, and many small veins draining the Fallopian tube, which frequently joined the uterine branches before these in turn joined the ovarian branches. A branch from the ureter joined the ovarian vein below the site of junction of its ovarian and uterine branches, and small branches from the tissues of the broad ligament entered a t many levels. As with the equivalent artery, the largest uterine branches of the ovarian vein ran along the mesometrial and antimesometrial borders of the uterine horns. The mesometrial branches were the larger. There were anastomoses between these branches of the ovarian vein and corresponding branches of the cranial urogenital vein, and also between branches running around the uterine horns from the main mesometrial and antimesom e t r i a l vessels. Although t h e u t e r i n e branches closely paralleled the equivalent arterial branches, they showed less convolution and spiralling. The ovarian vein terminated by joining the caudal vena cava a t a point close to the level of the origin of the ovarian arteries from the aorta (fig. 5). The External Iliac Arteries arose approximately 2 cm below the level of the ovarian arteries (fig. 4). A short distance further back the aorta terminated by giving rise to the paired Internal Iliac Arteries and the single midline Median Sacral Artery (fig. 5). This pattern of termination of the aorta was, however, variable, with instances seen of short common iliac arteries, or of the origin of the median sacral artery from one or the other of the internal iliac arteries (fig. 4). Immediately in front of the origin of the external iliac arteries from the aorta the caudal vena cava received a pair of branches draining the ventro-lateral area of the abdominal body wall (fig. 5). It then terminated immediately below the origin of the external iliac arteries, usually by dividing into two Common Iliac Veins. These in turn bifurcated into Internal and External Iliac Veins. The Median Sacral Vein arose either directly from the hind end of the caudal vena cava or, more commonly, as a branch of one or other of the common or internal iliac veins (fig. 5). The Cranial Urogenital Arteries arose as the first major branches of the internal iliac arteries (fig. 4). On each side, after a short course through the broad ligament, the artery bifurcated into a cranial and a caudal branch (fig. 2).
The cranial branch supplied the caudal part of the uterus. It provided one or more major uterine branches which ran anteriorly along the mesometrial border of the uterus, and a branch which crossed the dorsal surface of the caudal part of the uterus and turned anteriorly to run along the antimesometrial border. These mesometrial and antimesometrial branches anastomosed with the equivalent branches of the ovarian artery. The cranial branch of the cranial urogenital artery also provided the major vessels to the lateral and median vagina, and supplied one or more small branches to the ureter. The major vaginal vessels, like their counterparts in the uterine horns, ran close to the surface and showed a marked convolution or spiralling (fig. 2). The caudal branch (fig. 2) extended obliquely across the ventrolateral aspect of the caudal portion of the lateral vagina, and gave rise to the major vessels supplying the bladder (fig. 1). It also supplied branches to the cranial part of the urogenital sinus, minor branches to the caudal parts of the vagina, and a small contribution to the terminal part of the ureter. The corresponding Cranial Urogenital Veins were formed by the junction of cranial and caudal branches which accompanied the equivalent branches of the cranial urogenital arteries, and drained the regions supplied by these arteries. The cranial urogenital veins terminated by joining the internal iliac veins (fig. 5 ) . Following the origin of a large, dorsally directed branch (fig. 4) extending between the ilium and the vertebral column immediately caudal t o the ilio-sacral articulation, and supplying muscles in the gluteal region, the next major branch of the internal iliac artery was usually the Caudal Urogenital Artery (fig. 4). This vessel ran a slightly convoluted, posteriorly-directed course along the side of the urogenital sinus, to which it provided the major supply, and extended to the cranial end of the cloaca (fig. 2). Minor anastomotic connections were present between branches of the caudal urogenital artery and branches of the cranial urogenital artery in the wall of the cranial part of the urogenital sinus. Across-the-middle anastomotic connections, often of substantial size, were present between arteries of the two sides a t all levels from the cranial end of the vagina to the caudal part of the urogenital sinus, involving branches of both the caudal and cranial
REPRODUCTIVE TRACT IN MARSUPIALS
urogenital arteries (fig. 2). Furthermore, small anastomoses were present between the cloacal branches of the caudal urogenital arteries and the cloacal vessels derived from the internal pudendal arteries. The Caudal Urogenital Veins arose from the internal iliac veins a t a similar level to that of the origin of the equivalent arteries (fig. 51, whose branching and distribution they closely followed. A vein equivalent to the artery to the gluteal muscles also joined the internal iliac vein usually below the point of origin of the caudal urogenital vein (fig. 5). The terminal branching of the internal iliac arteries and veins showed considerable individual variation. It did, however, include branches to the muscles on the inner surfaces of the pelvic girdle, branches extending towards the obturator foramen and sometimes anastomosing with obturator vessels derived from branches of the external iliac vessels, branches to a pad of fat present on each side of the cranial part of the urogenital sinus, and the internal pudendal arteries and veins. The Internal Pudendal Artery (fig. 4) on each side appeared to represent the most direct continuation of the internal iliac artery. This vessel ran in a postero-dorsal direction, extending deeply into and supplying branches to the musculature within the dorsal part of the pelvic wall. I t then passed dorsally and medially to the acetabulum between the pelvic bones and the vertebral column before turning ventro-medially and re-entering the caudal part of the pelvic cavity. Here its terminal branches supplied the wall of the cloaca and the clitoris (fig. 2). These terminal branches commonly also established anastomotic connections with branches of a vessel derived from the external iliac artery, approximately equivalent in its distribution to the medial circumflex femoral artery of many eutherian mammals (Getty, '75).Small anastomoses were also present with the terminal branches of the caudal urogenital artery. The Internal Pudendal Veinfollowed a similar course, and drained the regions supplied by the equivalent artery, forming a comparable set of anastomotic connections. Histology. The ovarian artery (fig. 6) had a thin intima with a well-defined internal elastic lamina, a thick media containing six to seven layers of circularly arranged smooth muscle, and a collagenous adventitia containing many elastic fibers. The corresponding vein (fig. 6) had a thin wall with a thin intima,
99
a media containing two to seven layers of smooth muscle cells, and a thicker collagenous and elastic adventitia containing occasional bundles of longitudinally oriented smooth muscle. In some instances the wall of the vein was distinctly thinner on the side facing the artery, mainly due t o a reduction in the amount of muscle in the adventitia. In most regions, a variable amount of loose collagenous connective tissue separated the ovarian artery and vein. However, there were sites where the adventitia of the artery was in direct contact with that of the vein, leaving a tissue barrier r l O O p m between the lumina of the two vessels. In the connective tissue between and around the ovarian artery and vein was a network of smaller blood vessels, nerves and lymphatic vessels. In the region close to the ovary, the ovarian arterial branches appeared to outnumber their venous counterparts (fig. 7). These arteries and veins were similar in structure to the main arterial and venous trunks described above. However, their walls were thinner and a t some of the many sites of close contact the tissue barrier between arterial and venous blood was as little as 20 fim (fig. 7). Ureteric vessels. In addition to branches from the ovarian and cranial urogenital arteries, the cranial part of the ureter was supplied by a branch arising from the renal artery a t a point close to the hilus of the kidney. Anastomoses between the branches from these three sources produced one or more main longitudinally-disposed arterial channels running parallel to the ureter and supplying many small branches to its walls. Similarly the ovarian and cranial urogenital venous branches to the ureter anastomosed with one another and anteriorly with a ureteric vein draining into the renal vein.
Male Origin and distribution of vessels to the testis. The paired Testiculur Arteries arose from the aorta a t a point approximately 2 cm above the level of origin of the external iliac arteries (fig. 9). On each side, the artery then ran posterolaterally beneath the peritoneum towards the inguinal canal. It initially ran a straight course and throughout the greater part of its length i t was closely apposed to the surface of the larger testicular vein. However, immediately before entering the inguinal canal it became mildly tortuous (fig. 9). Shortly after emerging from the inguinal canal to enter the
100
C. S.
LEE AND J . D. O’SHEA
stalk of the scrotum it underwent a series of branchings, giving rise to a rete mirabile consisting of a leash of -28 to 47 small arteries (fig. 10). These arteries were mildly tortuous, and parallel with one another, showed occasional anastomoses and intermingled with a similar number of parallel veins (fig. 9). On reaching the upper pole of the testis, these branches rejoined to form one or two main vessels which entered the substance of the testis via the caudal surface (fig. 10). Occasionally these main vessels rebranched, forming three or four smaller vessels which ramified over the caudal surface before entering the substance of the testis. In its course in the spermatic cord the rete mirabile gave rise to approximately three to eight relatively straight branches which extended separately to the epididymis (fig. 10). The Testicular Veins emerged as single vessels from the caudal end of the testis and extended along the cranial surface of the testis. As it passed up the spermatic cord, each vein gave rise t o a plexus consisting of approximately the same number of vessels as the leash of arteries but showing a greater degree of branching and anastomoses. These vessels were of uniform size and ran a tortuous course which closely paralleled that of the corresponding arterial branches (fig. 9). Shortly before entering the inguinal canal the veins rejoined to form a single vessel which finally opened into the caudal vena cava a t a point close t o the level of origin of the testicular arteries from the aorta (fig. 9). Histology. The wall of the testicular artery in its abdominal segment was composed of a thin intima with a well defined internal elastic lamina, a thick media incorporating six to seven layers of circularly disposed smooth muscle, and a moderately thick adventitia. Its venous counterpart had a thin intima, a media containing two to three layers of circular smooth muscle, and an adventitia of variable thickness. As with the ovarian vessels, there were also sites where the walls of the artery and vein were in close surface-tosurface contact. The surrounding connective tissue contained many smaller arteries and veins, nerpes and lymphatic vessels. In the spermatic cord, the testicular artery and vein, and the vas deferens, were surrounded by a thick collagenous sheath which was in turn incompletely surrounded by a longitudinally disposed skeletal muscular coat of
considerable thickness. The histological picture in the region of the testicular rete mirabile (fig. 8 ) correlated well with gross observations, there being an approximately similar number of arterial and venous branches of rather uniform size. The arteries here possessed a thin intima, a media containing 2 three layers of smooth muscle, and little if any adventitia. The veins had a very thin wall, comprised of a layer of endothelium and one to two layers of circular smooth muscle. These vessels, which were supported by a common mass of collagenous connective tissue, frequently came into close side-to-side contact with one another in localized regions (fig. 8). Other species Macropods Findings in each of the five species of macropod studied were closely similar, and these species are therefore considered together. The general distribution of vessels to the reproductive tract was similar to that in the brush possum. However, most tracts were obtained after removal from the animals, with the cloaca1 blood vessels cut off too short t o be studied adequately. All of these species possessed paired ovarian arteries and veins which ran in close relationship to one another, gave off branches to the Fallopian tube and uterus which anastomosed with branches of the cranial urogenital vessels, and supplied multiple (between 7 and 12) branches to the ovary (fig. 11).Cranial and caudal urogenital vessels were distributed in a similar way to those in the possum. Minor differences noted from the vessels in possums included: (a) The uterine branches of the ovarian vein were fewer (usually only 1) and somewhat larger than in the possum. (b) In at least one specimen of each of the red kangaroo and eastern grey kangaroo, the cranial and caudal urogenital vessels arose by common trunks (Common Urogenital Arteries and Veins) from the internal iliac vessels. In other specimens it was impossible to check this point because the vessels were severed too far along their courses to the genital tract. Vombatus ursinus
In the common wombat the pattern of vasculature of the female reproductive tract was again similar to that of the possum, although as in some macropods the cranial and caudal urogenital vessels arose by common trunks.
REPRODUCTIVE TRACT IN MARSUPIALS
There were only four or five ovarian branches of the ovarian artery (fig. 121, closely intertwined with the plexiform veins draining the ovary, and a substantial uterine branch joined the ovarian vein below the level a t which the ovarian branches arose (fig. 12). As in all of the above species, the ovarian artery ran closely along the surface of the ovarian vein in the region proximal to the origins of their major branches. DISCUSSION
Apart from the observations of Beddard ('09)on the major branches of the caudal vena cava, and of Pearson ('40) on the main branches of the aorta and venae cavae, there do not appear to be any previous published data on the pelvic vasculature in female marsupials. Since the terminology used in eutherian mammals is inappropriate because of marked differences in the anatomy of the urogenital system in marsupials (TyndaleBiscoe, '731, it has been necessary here to coin names-cranial and caudal urogenital arteries and veins-for the blood vessels supplying the tubular parts of the female reproductive tract. The main vessels to the cloaca1 region, being regarded a s approximately equivalent to the internal pudendal vessels of eutherian mammals, have been so named. With minor exceptions, a common pattern of vasculature of the female reproductive tract has emerged for all of the species studied here, representing three distinct families, Phalangeridae (T. vulpecula), Macropodidae (five macropod species), and Vombatidae (V. ursinus) (Tyndale-Biscoe, '73). However, further species from other groups of marsupials need to be studied to establish whether these observations are generally applicable to all marsupials. Among the vessels to the female tract described here, only the ovarian arteries and veins have been identified previously, and the earlier descriptions of these vessels do not accord with present observations. Beddard ('09) described anterior and posterior ovarian veins on each side, the anterior veins entering the renal veins and the posterior veins joining the posterior vena cava directly. Similarly, Pearson ('40) reported duplication of the ovarian arteries. With the exception of one specimen in which there was unilateral duplication of the ovarian artery, no cranial ovarian arteries or veins were observed in any of the possums studied here. I t is possible that indi-
101
vidual variation, which is a major feature of the arrangement of both arteries and veins in these animals, could account for this discrepancy. However, a more likely explanation is that Beddard ('09)and Pearson ('40) regarded the ureteric vessels, which anastomose with the ovarian and cranial urogenital vessels, as additional ovarian vessels. A common feature of the vasculature in all of the species studied here was the presence of numerous and substantial anastomoses between the several vessels supplying the reproductive tract on each side of the midline, together with across-the-midline anastomoses. Both veins and arteries showed these anastomoses, whose extent was such that an alternative blood supply would be likely to develop rapidly in the event that any single vessel was obstructed. Several points of interest were noted in relation to the arteries and veins supplying and draining the ovary. In all species there were substantial anastomoses between the ovarian vessels and branches of the cranial urogenital vessels supplying the uterus. From the size and disposition of the vessels concerned it would be predicted that the ovarian artery contributes to the blood supply of the uterus, and that a part of the uterine venous effluent passes to the caudal vena cava via the ovarian veins. Furthermore, the ovarian artery is closely attached to the surface of the ovarian vein, and a t least in the possum the histological relationship between these vessels is similar to that in the sheep (Lee and O'Shea, '76). On anatomical ground, therefore, these marsupials appear to satisfy the requirements for a local uterine luteolytic mechanism (Ginther, '74). However, since hysterectomy has been shown not to prolong the oestrous cycle in the brush possum (Clark and Sharman, ' 6 9 , such a mechanism presumably does not exist a t least in this species. Nor would a uterine luteolytic mechanism appear to be a logical evolutionary development, since in most marsupials so far studied the duration of the oestrous cycle exceeds that of pregnancy (Tyndale-Biscoe,'73). The possibility that these vascular relationships have some other function remains open. For example, von der Borch ('63) has shown that the uterine horn ipsilateral to the corpus luteum in non-pregnant specimens of the brush possum is heavier than the contralateral horn. This suggests the presence of a local hormonal effect of the ovary on the
102
C. S. LEE AND J. D. OSHEA
uterus, which could be accounted for by venoarterial transfer from ovarian venous blood t o ovarian arterial blood and thence via anastomotic connections to the ipsilateral uterine horn. At the level of the uterus there are no across-the-midline anastomoses and therefore a localized effect on the ipsilateral horn would be predicted. This possibility remains, however, purely hypothetical. The arrangement of the ovarian vessels distal to the point a t which their uterine branches arise is also noteworthy. As in many eutherian mammals, it is a t this level, closer to the ovary, that the most intimate relationship develops between the ovarian arteries and veins. In these marsupials, however, in contrast to eutherians, the ovarian artery gives rise to a large number of ovarian branches of rather uniform size. These arteries are closely intertwined with the veins draining the ovary, which form a plexus a t this level. Although the function of this vascular arrangement is not known, its structure is highly suggestive of a specialization for countercurrent exchange between arterial and venous blood. Since no data are available as to the nature, extent, or even the direction of any such exchange in female marsupials or eutherian mammals, it may be relevant to consider data on the function of the homologous and in many respects similar arterio-venous relationship in the vessels supplying the testis. As Harrison ('49) and Barnett and Brazenor ('581 have shown, a highly developed rete mirabile is present in the spermatic cord of many, though not all, marsupials. In relation to the brush possum, described here, both similarities and some differences are detectable between the ovarian and testicular vessels. Quantitatively, both in terms of numbers of arterial and venous branches and the length over which they are in contact, the testicular vessels greatly exceed the ovarian. Also the reuniting of the testicular arteries and veins to single or very small numbers of vessels close to the testis is absent in the ovarian vessels. Nonetheless, subject to these differences, the vascular arrangements of the ovary are distinctly similar to those of the testis. There is clear evidence that the rete mirabile in some macropod marsupials acts as a countercurrent heat exchanger to cool the arterial blood flowing into the testis (Setchell and Waites, '69). These authors also demonstrated that the branches of the internal spermatic artery act to dampen the pulse wave in
the testicular blood supply. Furthermore, Jacks and Setchell ('73) have demonstrated that substances in the blood (prostaglandin F,, testosterone and tritiated water) can pass from venous to arterial blood in the spermatic cord, although the physiological significance of such a process of transfer remains unknown. While there is no basis to suppose that heat exchange could be a function of the ovarian vessels, the exchange of substances in the blood is clearly worthy of investigation, particularly in the light of evidence that the corpus luteum may exert a local, unilateral effect on ovarian follicles in several eutherian species (Ginther, '74). I t seems reasonable to assume that the well-developed arterio-venous relationship in the ovarian pedicle in many eutherian and marsupial mammals is likely to serve some function. However, it is less easy to understand why such a close similarity exists between the ovarian and testicular vascular arrangements in many species, when a major proposed function in the male, namely heat exchange (Setchell, '70; Waites, '701, is presumably irrelevant in the female. This similarity is illustrated in eutherian mammals by comparison of the data of Harrison ('49) on the testicular vessels with data on the ovarian vessels in man (Delson et al., '491, rhesus monkey (Ginther et al., '741, guinea pig, rat, hamster, rabbit (Del Campo and Ginther, '721, horse, sheep, pig (Del Campo and Ginther, '73), dog and cat (Del Campo and Ginther, '74). In these species the extent of convolution of the testicular artery in the male appears generally to be mimicked, in lesser degree, by that of the ovarian artery. Thus, for example, in the sheep and pig there is a high degree of convolution in both male and female, while in man and the cat there is relatively little convolution in either sex. Although less information is available in relation to marsupials, the data presented here, together with those of Harrison ('49, '51) and Barnett and Brazenor ('58) confirm that distinct similarities between the two sexes exist a t least in relation to T. vulpecula, M. eugenii, T. billardierii, M. rufa, and K ursinus. No data on the testicular vessels of M.agilis or M. giganteus are available. If this tendency for similarity in the nature and arrangement of the testicular and ovarian vessels can be confirmed in a wider range of species, eutherian and marsupial, some explanation other than coincidence will clearly need to be considered. The development of a complex arteriove-
REPRODUCTIVE TRACT IN MARSUPIALS
nous relationship in the testicular vessels has been observed only in mammals, and within mammals is developed more commonly and to a much greater degree in those with scrota1 or inguinal testes (Setchell, ’70). It would appear likely, therefore, that this relationship has evolved primarily, though not necessarily exclusively, in conjunction with the function of cooling of the testes. Thus, assuming that the homologous vascular relationship in the ovary does serve some useful function unrelated to heat exchange, its occurrence could be construed as a form of evolutionary “opportunism” in the females of species in which natural selection has favored an increasingly complex arrangement of the testicular vessels in the males. ACKNOWLEDGMENTS
We are very grateful to Doctors Paul Presidente and Ray Butler, who made available to us many of the specimens used in this study. LITERATURE CITED Barnett, C. H., and C. W. Brazenor 1958 The testicular rete mirabile of marsupials. Aust. J. Zool., 6: 27-32. Beddard, F. E. 1909 On the postcaval vein and its branches in certain mammals. Proc. 2001. Soc., Land., I:
496-526. Clark, M. J.,and G. B. Sharman 1965 Failure of hysterectomy to affect the ovarian cycle of the marsupial Trichosurus uulpecula J. Reprod. Fert., 10: 459-461. Del Campo, C. H., and 0. J. Ginther 1972 Vascular anatomy of the uterus and ovaries and the unilateral luteolytic effect of the uterus: guinea pigs. rats, hamsters and rabbits. Am. J. Vet. Res., 33: 2561-2578. 1973 Vascular anatomy of t he uterus and ovaries and t h e unilateral luteolytic effect of the uterus: horses, sheep, and swine. Am. J. Vet. Res., 34: 305-316. 1974 Arteries and veins of uterus and ovaries in dogs and cats. Am. J. Vet. Res., 35: 409-415. Delson, B., S. Lubin and S. R. M. Reynolds 1949 Vascular patterns in the human ovary. Am. J. Obst. Gynec., 57:
-
842-853. Getty, R. 1975 Sisson and Grossman’s The Anatomy of th e Domestic Animals. Fifth ed. W. B. Saunders CO., Philadelphia, London and Toronto.
103
Ginther, 0. J. 1974 Internal regulation of physiological processes through local venoarterial pathways: a review. J. Anim. Sci., 39: 550-564. Ginther, 0. J., D. J. Diersche, S. W. Walsh and C. H. Del Campo 1974 Anatomy of arteries and veins of uterus and ovaries in rhesus monkeys. Biol. Reprod., I k205-219. Goding, J. R., I. A. Cumming, W. A. Chamley, J. M. Brown, M. D. Cain, J. C. Cerini, M. E. D. Cerini, J. K. Findlay, J. D. O She a and D. H. Pemberton 1972 Prostaglandin F b , “the” luteolysin in the mammal? Gynec. Invest., 2:
73-97. Harrison, R. G. 1949 The comparative anatomy of the blood.supply of the mammalian testis. Proc. 2001. SOC., 119: 325-334. 1951 Applications of microradiography: the testis. In: Microarteriography and Other Radiological Techniques Employed in Biological Research. A. E. Barclay, ed. Blackwell Scientific Publications. Oxford, pp. 89-91. Hartman, G. C. 1925 Hysterectomy and the oestrous cycle in the opossum. Am. J. Anat., 35: 25-29. Jacks, F.,and B. P. Setchell 1973 A technique for studying the transfer of substances from venous to arterial blood in the spermatic cord of wallabies and rams. J. Physiol., 233: 17P-18P. Lee, C. S., and J. D. OShea 1976 The extrinsic blood vessels of the ovary of the sheep. J. Morph.. 148: 287-304. McCracken, J. A.,J. C. Carlson, M. E. Clew, J. R. Goding, D. T. Baird, K. Green and B. Samuelsson 1973 Prostaglandin F b identified a s a luteolytic hormone in sheep. Nature: New Biology, 238: 129-134. Pearson, J. 1940 Notes on the blood system of the marsupiala. Pap. and Proc. Roy. %. Tasmania, 73: 77-94. Setchell, B. P. 1970 Testicular blood supply, lymphatic drainage, and secretion of fluid. In: The Testis. Vol. 1. A. D. Johnson, W. R. Gomes and N. L. Vandemark. eds. Academic Press, New York and London, pp. 101-239. Setchell, B. P., and G. M. H. Waites 1969 Pulse attenuation and countercurrent heat exchange in the internal spermatic artery of some Australian marsupials. J. Reprod. Fert., 20: 165-169. Tyndale-Biscoe, C. H. 1973 Life of Marsupials. Edward Arnold, London. Tyndale-Biscoe, C. H., J. P. Hearn and M.B. Renfree 1974 Control of reproduction in macropodid marsupials. J. Endocr., 63: 589-614. von der Borch, S. M. 1963 Unilateral hormone effect in the marsupial Trichosurus uulpecula. J. Reprod. Fert., 5:
447-449. Waites, G. M. H. 1970 Temperature regulation and the testis. In: The Testis. Vol. 1. A. D. Johnson, W.R.Gomes and N. L. Vandemark, eds. Academic Press, New York and London, pp. 241-279.
PLATE 1 EXPLANATION OF FIGURE
2
104
Dorsal view of partially cleared specimen of latex-injected female genital tract of the brush possum. Latex in arteries appears black, in veins white (right and left ovarian and right cranial urogenital veins only). 0, ovary; U, uterus; UR, ureter; V, vagina; US, urogenital sinus; C, cloaca; OA, ovarian artery; AU, cranial urogenital artery; 11, internal iliac artery; PU, caudal urogenital artery; IP, internal pudendal artery (which has become separated from internal iliac artery). Across-the-midline arterial anastomoses are present a t many sites (arrows). X 1.5.
REPRODUCTIVE TRACT IN MARSUPIALS C. S. Lee and J . D. OShea
PLATE 1
105
PLATE
2
EXPLANATION OF FIGURES
3 Latex cast of right ovarian artery from a brush possum. 0, ovary; U, cranial tip of uterus; OA. ovarian artery; OB, ovarian branches of ovarian artery; FB, branch to Fallopian tube; UB, branches to uterus. X 2.8. 4
Latex cast of aorta and branches to the genital tract and pelvic region in a female brush possum, ventral view. A, aorta; 0, ovarian artery; EI, external iliac artery; 11, internal iliac artery; AU, cranial urogenital artery; G, artery to gluteal region; PU, caudal urogenital artery; 1P. internal pudendal artery; MS, median sacral artery with two major branches. x 0.9.
5 Ventral view of caudal vena cava and pelvic veins filled with blood (dark), together with arteries filled with white latex, in a specimen from a female brush possum. PV, caudal vena cava; 0, ovarian vein; CI, common iliac vein; EI, external iliac vein; 11, internal iliac vein; AU, cranial urogenital vein; PU, caudal urogenital vein; G, vein to gluteal region; IP. internal pudendal vein; MS, median sacral vein. In this specimen there is no common iliac vein on the right side, and only a short one on the left. X 1.3.
106
REPRODUCTIVE TRACT IN MARSUPIALS C. S. Lee and J. D. OShea
PLATE 2
PLATE 3 EXPLANATION OF FIGURES
6 Section of ovarian artery (OA)and vein (OW, in the region proximal to origin of the ovarian branches in a female brush possum. A small vein (SV) is joining the ovarian vein a t left. H and E. X 120.
7 Section of ovarian branches of ovarian artery (A)and vein (V)not far from hilus of ovary in female brush possum. Close contact between arteries and a small vein is seen (arrows). H and E. X 120.
8 Section of many branches of testicular artery (A) and vein (V)in spermatic cord of male brush possum. Sites of arterio-venous contact are arrowed. Collagenous connective tissue (CT) separates arteries from veins in many places. H and E. X 120.
108
REPRODUCTIVE TRACT IN MARSUPIALS C. S. Lee and J. D. O'Shea
PLATE 3
109
PLATE 4 EXPLANATION OF FIGURES
9 Dissection of pelvic region of a male brush possum, showing origin and route of testicular vessels. B. bladder, P, prostate; T, testis; E,epididymis; PV,caudal vena cava; TV, testicular vessels in abdomen; IC, inguinal canal; TB, branches of testicular vessels in spermatic cord. Arteries injected with white latex, veins filled with blood and appearing black. X 0.9. 10 Latex cast of left testicular artery from a brush possum. T, testis; E, epididymis; TA,
testicular artery, abdominal portion; RM, rete mirabile of testicular artery in spermatic cord; EB, branches to epididymis. Note tha t the testicular artery again becomes single (arrow) before entering the testis. X 1.2.
110
REPRODUCTIVE TRACT IN MARSUPIALS D OShea
PLATE 4
C. S. Lee and J.
111
PLATE 5 EXPLANATION OF FIGURES
11 Partially cleared specimen of latex-injected female genital tract of eastern grey kangaroo, dorsal view. Arteries appear dark, veins white. 0, ovary; FT, Fallopian tube; U, uterus; V, vagina; OV, ovarian artery and vein; OB, ovarian branches of ovarian artery and vein; UB, uterine branch of ovarian vein; AU, cranial urogenital artery and vein. X 1.3. 12 Partially cleared specimen of latex injected female genital tract of common wombat,
dorsal view. Arteries dark, veins white. 0, ovary; FT,Fallopian tube; U, uterus; OV, ovarian artery and vein; OB, ovarian branches of ovarian artery and vein; UB, uterine branch of ovarian vein. x 1.1.
112
REPRODUCTIVE TRACT IN MARSUPIALS C. S. Lee and J. D. O'Shea
PLATE 5
113
ABSTRACT The origin, distribution and structure of the blood vessels of the female reproductive tract and the testis of the brush possum (Trichosurus. vulpecula) were studied using latex and silicone rubber casting and histological techniques. Latex casts of the vessels of the female tract were also studied in five macropod species- Macropus giganteus, M. eugenii, M. agilis, Megaleia rufa and Thylogale billardierii and in the common wombat (Vombatus ursinus). The female reproductive tract in the brush possum was supplied and drained by four major sets of paired vessels-ovarian, cranial urogenital, caudal urogenital, and internal pudendal arteries and veins. These vessels formed substantial anastomoses with one another on each side of the midline, and also across-the-midline anastomoses. The proximal part of the ovarian artery ran in close apposition to the ovarian vein, which received one or more large uterine branches. In its distal portion the ovarian artery gave rise to a leash of small, tortuous ovarian branches, which wound around and between the plexiform ovarian veins. The testicular arteries and veins in this species also ran in close apposition to one another. Both arteries and veins branched into many smaller, mildly tortuous, parallel vessels in the spermatic cord, which reunited before entering the testis. The blood vessels of the reproductive tract in all of the macropod species studied, and in the common wombat, were basically similar to those of the brush possum. The intimate structural relationships between ovarian arteries and veins, and their ovarian branches, in these marsupials are suggestive of specializations for counter-current exchange between venous and arterial blood. However, in contrast to those of the testicular vessels where heat exchange is a demonstrated function, their physiological significance remains unknown. The blood vessels supplying and draining the testis have been studied in detail in many species of eutherian and marsupial mammals (Harrison, '49; Barnett .and Brazenor, '58). Particular interest in the testicular vessels has derived from their demonstrated role in countercurrent heat exchange (Setchell, '70; Waites, '70). More recently, considerable interest has been shown in the vasculature of the female reproductive tract, and particularly the ovary, in eutherian mammals (Del Campo and Ginther, '72, '73, '74; Ginther et al., '74; Lee and OShea, '76). This interest has been stimJ . MORPH., 154: 95-114.
ulated by recent evidence that these vessels may play a role in the local transfer of a luteolytic hormone, shown a t least in some , (Goding et al., species to be prostaglandin F '72; McCracken et al., '721, from the uterus to the ovary. In this connection it has been suggested that a correlation exists between he presence of venous and arterial pathways common to the ovary and uterus, and the occurrence of a unilateral uterine luteolytic mechanism (Del Campo and Ginther, '72). Apart from some early data on the main branches of the aorta and caudal vena cava (Beddard, '09; Pearson, '401, the blood vessels
95
96
C. S. LEE AND J. D. O’SHEA
to the reproductive tract in female marsupials do not appear to have been described. The arrangement of these vessels is, however, of interest, since it has been shown that hysterectomy is without effect on the duration of the oestrous cycle in a t least two species of marsupial, namely Didelphys virginiana (Hartman, ’25) and Trichosurus uulpecula (Clark and Sharman, ’65). Although comparable data on other marsupials are not available, a uterine luteolytic mechanism appears a n unlikely evolutionary development in the many species in which the duration of the oestrous cycle exceeds that of pregnancy, which have been listed by Tyndale-Biscoe (”73) and Tyndale-Biscoe et al., (“74). This paper reports data on the blood vessels of the female reproductive tract in the brush possum (Trichosurus uulpecula), five species of macropod marsupials, and the common wombat (Vombatus ursinus). Some observations on the blood vessels of the testis in the brush possum are also presented. MATERIALS AND METHODS
ital pressure via cannulae either into the aort a or directly into the various arterial or venous branches to the reproductive tract. Because of difficulties in filling the veins with latex, resulting from the high incidence of valves, the veins in some specimens were filled with the animal’s own blood by ligating the caudal vena cava before injecting latex into the aorta. In the other species studied, latex casts were prepared by direct injections into vessels of the reproductive tract. In male brush possums, latex injections were made either via the aorta or directly into the testicular artery or vein. After ligation a t the site of injection, all specimens were fixed in 10%formalin and subsequently either dissected, cleared in a 1:3 mixture of ethyl alcohol and methyl salicylate, or (in the case of latex casts only) macerated in 20% sodium hydroxide a t 5OOC. Histology Blood vessels for histological examination, which were obtained from three female and three male brush possums, were fixed in 10% buffered neutral formalin and embedded in paraffin. Single or serial sections were prepared and stained with haematoxylin and eosin (H and E), van Gieson’s stain or Verhoeffs elastic stain. In female animals the ovarian vessels were sectioned a t multiple (generally 6)sites extending from their origin a t the aorta and caudal vena cava to their point of entry into the ovary. In males, the testicular vessels were sectioned both in their intra-abdominal segments and at various points along the spermatic cord.
A total of 23 female and 7 male brush possums (Trichosurus uulpecula) were studied. Most of these animals were adults, and all were estimated to be over one year old. Histories were unknown, but 14 of the females had pouch-young of various ages. These animals were killed by an intraperitoneal overdose of pentobarbitone immediately or shortly before the preparation of casts or the fixation of tissues as described below. Female reproductive tracts, with their major blood vessels attached, were obtained from carcasses of individuals of the following RESULTS species: eastern grey kangaroo (Macropus Trichosurus vulpecula giganteus)-3 specimens, tammar wallaby (M. eugenii)-2, agile wallaby (M.agi1i.s)- 1, red Female There were four major sets of paired arkangaroo (Megaleia rufu)- 1, rufous bellied wallaby (Thylogale bil1ardierii)- 1, common teries and veins supplying the reproductive tract (figs.1,2),which have been designated: wombat (Vombatus u r s i n d - 4 . (1) ovarian artery and vein; (2) cranial uroGross anatomy genital a. and v; ( 3 ) caudal urogenital a. Vessels of the reproductive tract and pelvic and v.; (4) internal pudendal a. and v. The inregion in female brush possums were studied ternal pudendal artery and vein, which supeither in uninjected, formalin-fixed specimens plied the major vessels to the cloaca1 region, or following the preparation of vascular casts were supplemented by anastomotic vessels deeither in situ or after removal of the genital rived from branches of the external iliac tract from the animal. Casts were prepared artery and vein. Although these four sets of using latex rubber (‘‘Latex,” Dunlop Rubber vessels were consistently demonstrable, therz Co., Melbourne, Australia) or silicone rubber were many individual variations in the detail C‘Microfil”MV- 112, Canton Biomedical Prod- of their arrangement, including variations in ucts Inc., Colorado, U.S.A.)injected under dig- origin, branching and anastornotic connec-
REPRODUCTIVE TRACT I N MARSUPIALS
7 Fig. 1 Diagrammatic representation of ventral view of the female genital tract of the brush possum, showing the four major blood vessels supplying the tract. Veins appear pale grey and arteries black. 0, ovary; U, uterus: MV, median vagina; LV, lateral vagina; B, bladder; US, urogenital sinus;C, cloaca; OV, ovarian vessels: AU, cranial urogenital vessels; PU, caudal urogenital vessels; IP, internal pudendal vessels.
tions, and the presence of duplication of any one or more of the vessels.
Origin and distribution of vessels to the genital tract. The Ovarian Arteries (figs. 2 , 3) arose from the aorta close to one another (fig. 41, or occasionally by a common trunk, approximately two-thirds of the way from the origin of the renal arteries to that of the external iliac arteries. In most cases the right ovarian artery ran initially around the left side of the caudal vena tava and then crossed from left to right beneath its ventral surface (fig. 5). On each side, the artery then ran postero-laterally beneath the peritoneum before turning postero-ventrally and entering the cranial part of the broad ligament. Throughout the greater part of its length it ran along the surface of the ovarian vein, to which it was closely apposed (fig. 5).As i t approached the ovary, the artery underwent a series of branchings over a short distance, producing a leash of small ovarian branches of relatively uniform caliber (fig. 3), and then continued to supply branches to the Fallopian
97
tube and uterus. An additional, usually single, branch t o the ureter arose a t the same level in some cases, but more often arose independently, closer to the aorta and a t about the level where the ureter crossed dorsally over the ovarian vessels. There were additional minor branches to the tissues of the broad ligament. Up to the point of major branching, the artery ran a relatively straight course, showing little tortuosity (figs. 2-51. The first few millimeters of the many branches running to the ovary were also almost straight. Beyond this point, however, these branches, z 6 - 1 2 in number, showed a marked tortuosity incorporating many U- or S-shaped bends and regions of spiralling which continued after these vessels entered the substance of the ovary (fig. 3). These arteries branched infrequently and showed occasional anastomoses with one another and with branches running to the Fallopian tube or uterus. They also wound intimately around and between the branches of the venous plexus draining the ovary (fig. 2). The Fallopian tube and nearby areas of the broad ligament were supplied by one or more small, less convoluted branches, while a further group of small terminal branches of the ovarian artery ran to the cranial tip of the uterus (fig. 3). These also showed less tortuosity than those to the ovary. On reaching the tip of the uterus, the major uterine branches ran a convoluted or spiralling course along the mesometrial and antimesometrial borders of the uterus, and terminated by forming end-to-end anastomoses with similar branches from the cranial urogenital artery (fig. 1 ) . Along their courses these mesometrial and antimesometrial branches gave off, at right angles, many small spiralling branches which ran around the surfaces of the horn and frequently anastomosed directly with comparable branches from the opposite border of the uterus (fig.2 ) . These encircling vessels in turn gave off many smaller branches which penetrated the deeper tissues of the uterine wall. The Ovarian Veins (figs. 2, 5) were considerably larger than the ovarian arteries. In each case, the area o f drainage corresponded closely to the region supplied by the ovarian artery, whose pattern of branching was closely paralleled. Thus, the ovarian vein was formed by the fusion of a plexiform group of small veins draining the ovary, several veins
98
C. S. LEE AND J. D. OSHEA
from the cranial end of the uterine horn, and many small veins draining the Fallopian tube, which frequently joined the uterine branches before these in turn joined the ovarian branches. A branch from the ureter joined the ovarian vein below the site of junction of its ovarian and uterine branches, and small branches from the tissues of the broad ligament entered a t many levels. As with the equivalent artery, the largest uterine branches of the ovarian vein ran along the mesometrial and antimesometrial borders of the uterine horns. The mesometrial branches were the larger. There were anastomoses between these branches of the ovarian vein and corresponding branches of the cranial urogenital vein, and also between branches running around the uterine horns from the main mesometrial and antimesom e t r i a l vessels. Although t h e u t e r i n e branches closely paralleled the equivalent arterial branches, they showed less convolution and spiralling. The ovarian vein terminated by joining the caudal vena cava a t a point close to the level of the origin of the ovarian arteries from the aorta (fig. 5). The External Iliac Arteries arose approximately 2 cm below the level of the ovarian arteries (fig. 4). A short distance further back the aorta terminated by giving rise to the paired Internal Iliac Arteries and the single midline Median Sacral Artery (fig. 5). This pattern of termination of the aorta was, however, variable, with instances seen of short common iliac arteries, or of the origin of the median sacral artery from one or the other of the internal iliac arteries (fig. 4). Immediately in front of the origin of the external iliac arteries from the aorta the caudal vena cava received a pair of branches draining the ventro-lateral area of the abdominal body wall (fig. 5). It then terminated immediately below the origin of the external iliac arteries, usually by dividing into two Common Iliac Veins. These in turn bifurcated into Internal and External Iliac Veins. The Median Sacral Vein arose either directly from the hind end of the caudal vena cava or, more commonly, as a branch of one or other of the common or internal iliac veins (fig. 5). The Cranial Urogenital Arteries arose as the first major branches of the internal iliac arteries (fig. 4). On each side, after a short course through the broad ligament, the artery bifurcated into a cranial and a caudal branch (fig. 2).
The cranial branch supplied the caudal part of the uterus. It provided one or more major uterine branches which ran anteriorly along the mesometrial border of the uterus, and a branch which crossed the dorsal surface of the caudal part of the uterus and turned anteriorly to run along the antimesometrial border. These mesometrial and antimesometrial branches anastomosed with the equivalent branches of the ovarian artery. The cranial branch of the cranial urogenital artery also provided the major vessels to the lateral and median vagina, and supplied one or more small branches to the ureter. The major vaginal vessels, like their counterparts in the uterine horns, ran close to the surface and showed a marked convolution or spiralling (fig. 2). The caudal branch (fig. 2) extended obliquely across the ventrolateral aspect of the caudal portion of the lateral vagina, and gave rise to the major vessels supplying the bladder (fig. 1). It also supplied branches to the cranial part of the urogenital sinus, minor branches to the caudal parts of the vagina, and a small contribution to the terminal part of the ureter. The corresponding Cranial Urogenital Veins were formed by the junction of cranial and caudal branches which accompanied the equivalent branches of the cranial urogenital arteries, and drained the regions supplied by these arteries. The cranial urogenital veins terminated by joining the internal iliac veins (fig. 5 ) . Following the origin of a large, dorsally directed branch (fig. 4) extending between the ilium and the vertebral column immediately caudal t o the ilio-sacral articulation, and supplying muscles in the gluteal region, the next major branch of the internal iliac artery was usually the Caudal Urogenital Artery (fig. 4). This vessel ran a slightly convoluted, posteriorly-directed course along the side of the urogenital sinus, to which it provided the major supply, and extended to the cranial end of the cloaca (fig. 2). Minor anastomotic connections were present between branches of the caudal urogenital artery and branches of the cranial urogenital artery in the wall of the cranial part of the urogenital sinus. Across-the-middle anastomotic connections, often of substantial size, were present between arteries of the two sides a t all levels from the cranial end of the vagina to the caudal part of the urogenital sinus, involving branches of both the caudal and cranial
REPRODUCTIVE TRACT IN MARSUPIALS
urogenital arteries (fig. 2). Furthermore, small anastomoses were present between the cloacal branches of the caudal urogenital arteries and the cloacal vessels derived from the internal pudendal arteries. The Caudal Urogenital Veins arose from the internal iliac veins a t a similar level to that of the origin of the equivalent arteries (fig. 51, whose branching and distribution they closely followed. A vein equivalent to the artery to the gluteal muscles also joined the internal iliac vein usually below the point of origin of the caudal urogenital vein (fig. 5). The terminal branching of the internal iliac arteries and veins showed considerable individual variation. It did, however, include branches to the muscles on the inner surfaces of the pelvic girdle, branches extending towards the obturator foramen and sometimes anastomosing with obturator vessels derived from branches of the external iliac vessels, branches to a pad of fat present on each side of the cranial part of the urogenital sinus, and the internal pudendal arteries and veins. The Internal Pudendal Artery (fig. 4) on each side appeared to represent the most direct continuation of the internal iliac artery. This vessel ran in a postero-dorsal direction, extending deeply into and supplying branches to the musculature within the dorsal part of the pelvic wall. I t then passed dorsally and medially to the acetabulum between the pelvic bones and the vertebral column before turning ventro-medially and re-entering the caudal part of the pelvic cavity. Here its terminal branches supplied the wall of the cloaca and the clitoris (fig. 2). These terminal branches commonly also established anastomotic connections with branches of a vessel derived from the external iliac artery, approximately equivalent in its distribution to the medial circumflex femoral artery of many eutherian mammals (Getty, '75).Small anastomoses were also present with the terminal branches of the caudal urogenital artery. The Internal Pudendal Veinfollowed a similar course, and drained the regions supplied by the equivalent artery, forming a comparable set of anastomotic connections. Histology. The ovarian artery (fig. 6) had a thin intima with a well-defined internal elastic lamina, a thick media containing six to seven layers of circularly arranged smooth muscle, and a collagenous adventitia containing many elastic fibers. The corresponding vein (fig. 6) had a thin wall with a thin intima,
99
a media containing two to seven layers of smooth muscle cells, and a thicker collagenous and elastic adventitia containing occasional bundles of longitudinally oriented smooth muscle. In some instances the wall of the vein was distinctly thinner on the side facing the artery, mainly due t o a reduction in the amount of muscle in the adventitia. In most regions, a variable amount of loose collagenous connective tissue separated the ovarian artery and vein. However, there were sites where the adventitia of the artery was in direct contact with that of the vein, leaving a tissue barrier r l O O p m between the lumina of the two vessels. In the connective tissue between and around the ovarian artery and vein was a network of smaller blood vessels, nerves and lymphatic vessels. In the region close to the ovary, the ovarian arterial branches appeared to outnumber their venous counterparts (fig. 7). These arteries and veins were similar in structure to the main arterial and venous trunks described above. However, their walls were thinner and a t some of the many sites of close contact the tissue barrier between arterial and venous blood was as little as 20 fim (fig. 7). Ureteric vessels. In addition to branches from the ovarian and cranial urogenital arteries, the cranial part of the ureter was supplied by a branch arising from the renal artery a t a point close to the hilus of the kidney. Anastomoses between the branches from these three sources produced one or more main longitudinally-disposed arterial channels running parallel to the ureter and supplying many small branches to its walls. Similarly the ovarian and cranial urogenital venous branches to the ureter anastomosed with one another and anteriorly with a ureteric vein draining into the renal vein.
Male Origin and distribution of vessels to the testis. The paired Testiculur Arteries arose from the aorta a t a point approximately 2 cm above the level of origin of the external iliac arteries (fig. 9). On each side, the artery then ran posterolaterally beneath the peritoneum towards the inguinal canal. It initially ran a straight course and throughout the greater part of its length i t was closely apposed to the surface of the larger testicular vein. However, immediately before entering the inguinal canal it became mildly tortuous (fig. 9). Shortly after emerging from the inguinal canal to enter the
100
C. S.
LEE AND J . D. O’SHEA
stalk of the scrotum it underwent a series of branchings, giving rise to a rete mirabile consisting of a leash of -28 to 47 small arteries (fig. 10). These arteries were mildly tortuous, and parallel with one another, showed occasional anastomoses and intermingled with a similar number of parallel veins (fig. 9). On reaching the upper pole of the testis, these branches rejoined to form one or two main vessels which entered the substance of the testis via the caudal surface (fig. 10). Occasionally these main vessels rebranched, forming three or four smaller vessels which ramified over the caudal surface before entering the substance of the testis. In its course in the spermatic cord the rete mirabile gave rise to approximately three to eight relatively straight branches which extended separately to the epididymis (fig. 10). The Testicular Veins emerged as single vessels from the caudal end of the testis and extended along the cranial surface of the testis. As it passed up the spermatic cord, each vein gave rise t o a plexus consisting of approximately the same number of vessels as the leash of arteries but showing a greater degree of branching and anastomoses. These vessels were of uniform size and ran a tortuous course which closely paralleled that of the corresponding arterial branches (fig. 9). Shortly before entering the inguinal canal the veins rejoined to form a single vessel which finally opened into the caudal vena cava a t a point close t o the level of origin of the testicular arteries from the aorta (fig. 9). Histology. The wall of the testicular artery in its abdominal segment was composed of a thin intima with a well defined internal elastic lamina, a thick media incorporating six to seven layers of circularly disposed smooth muscle, and a moderately thick adventitia. Its venous counterpart had a thin intima, a media containing two to three layers of circular smooth muscle, and an adventitia of variable thickness. As with the ovarian vessels, there were also sites where the walls of the artery and vein were in close surface-tosurface contact. The surrounding connective tissue contained many smaller arteries and veins, nerpes and lymphatic vessels. In the spermatic cord, the testicular artery and vein, and the vas deferens, were surrounded by a thick collagenous sheath which was in turn incompletely surrounded by a longitudinally disposed skeletal muscular coat of
considerable thickness. The histological picture in the region of the testicular rete mirabile (fig. 8 ) correlated well with gross observations, there being an approximately similar number of arterial and venous branches of rather uniform size. The arteries here possessed a thin intima, a media containing 2 three layers of smooth muscle, and little if any adventitia. The veins had a very thin wall, comprised of a layer of endothelium and one to two layers of circular smooth muscle. These vessels, which were supported by a common mass of collagenous connective tissue, frequently came into close side-to-side contact with one another in localized regions (fig. 8). Other species Macropods Findings in each of the five species of macropod studied were closely similar, and these species are therefore considered together. The general distribution of vessels to the reproductive tract was similar to that in the brush possum. However, most tracts were obtained after removal from the animals, with the cloaca1 blood vessels cut off too short t o be studied adequately. All of these species possessed paired ovarian arteries and veins which ran in close relationship to one another, gave off branches to the Fallopian tube and uterus which anastomosed with branches of the cranial urogenital vessels, and supplied multiple (between 7 and 12) branches to the ovary (fig. 11).Cranial and caudal urogenital vessels were distributed in a similar way to those in the possum. Minor differences noted from the vessels in possums included: (a) The uterine branches of the ovarian vein were fewer (usually only 1) and somewhat larger than in the possum. (b) In at least one specimen of each of the red kangaroo and eastern grey kangaroo, the cranial and caudal urogenital vessels arose by common trunks (Common Urogenital Arteries and Veins) from the internal iliac vessels. In other specimens it was impossible to check this point because the vessels were severed too far along their courses to the genital tract. Vombatus ursinus
In the common wombat the pattern of vasculature of the female reproductive tract was again similar to that of the possum, although as in some macropods the cranial and caudal urogenital vessels arose by common trunks.
REPRODUCTIVE TRACT IN MARSUPIALS
There were only four or five ovarian branches of the ovarian artery (fig. 121, closely intertwined with the plexiform veins draining the ovary, and a substantial uterine branch joined the ovarian vein below the level a t which the ovarian branches arose (fig. 12). As in all of the above species, the ovarian artery ran closely along the surface of the ovarian vein in the region proximal to the origins of their major branches. DISCUSSION
Apart from the observations of Beddard ('09)on the major branches of the caudal vena cava, and of Pearson ('40) on the main branches of the aorta and venae cavae, there do not appear to be any previous published data on the pelvic vasculature in female marsupials. Since the terminology used in eutherian mammals is inappropriate because of marked differences in the anatomy of the urogenital system in marsupials (TyndaleBiscoe, '731, it has been necessary here to coin names-cranial and caudal urogenital arteries and veins-for the blood vessels supplying the tubular parts of the female reproductive tract. The main vessels to the cloaca1 region, being regarded a s approximately equivalent to the internal pudendal vessels of eutherian mammals, have been so named. With minor exceptions, a common pattern of vasculature of the female reproductive tract has emerged for all of the species studied here, representing three distinct families, Phalangeridae (T. vulpecula), Macropodidae (five macropod species), and Vombatidae (V. ursinus) (Tyndale-Biscoe, '73). However, further species from other groups of marsupials need to be studied to establish whether these observations are generally applicable to all marsupials. Among the vessels to the female tract described here, only the ovarian arteries and veins have been identified previously, and the earlier descriptions of these vessels do not accord with present observations. Beddard ('09) described anterior and posterior ovarian veins on each side, the anterior veins entering the renal veins and the posterior veins joining the posterior vena cava directly. Similarly, Pearson ('40) reported duplication of the ovarian arteries. With the exception of one specimen in which there was unilateral duplication of the ovarian artery, no cranial ovarian arteries or veins were observed in any of the possums studied here. I t is possible that indi-
101
vidual variation, which is a major feature of the arrangement of both arteries and veins in these animals, could account for this discrepancy. However, a more likely explanation is that Beddard ('09)and Pearson ('40) regarded the ureteric vessels, which anastomose with the ovarian and cranial urogenital vessels, as additional ovarian vessels. A common feature of the vasculature in all of the species studied here was the presence of numerous and substantial anastomoses between the several vessels supplying the reproductive tract on each side of the midline, together with across-the-midline anastomoses. Both veins and arteries showed these anastomoses, whose extent was such that an alternative blood supply would be likely to develop rapidly in the event that any single vessel was obstructed. Several points of interest were noted in relation to the arteries and veins supplying and draining the ovary. In all species there were substantial anastomoses between the ovarian vessels and branches of the cranial urogenital vessels supplying the uterus. From the size and disposition of the vessels concerned it would be predicted that the ovarian artery contributes to the blood supply of the uterus, and that a part of the uterine venous effluent passes to the caudal vena cava via the ovarian veins. Furthermore, the ovarian artery is closely attached to the surface of the ovarian vein, and a t least in the possum the histological relationship between these vessels is similar to that in the sheep (Lee and O'Shea, '76). On anatomical ground, therefore, these marsupials appear to satisfy the requirements for a local uterine luteolytic mechanism (Ginther, '74). However, since hysterectomy has been shown not to prolong the oestrous cycle in the brush possum (Clark and Sharman, ' 6 9 , such a mechanism presumably does not exist a t least in this species. Nor would a uterine luteolytic mechanism appear to be a logical evolutionary development, since in most marsupials so far studied the duration of the oestrous cycle exceeds that of pregnancy (Tyndale-Biscoe,'73). The possibility that these vascular relationships have some other function remains open. For example, von der Borch ('63) has shown that the uterine horn ipsilateral to the corpus luteum in non-pregnant specimens of the brush possum is heavier than the contralateral horn. This suggests the presence of a local hormonal effect of the ovary on the
102
C. S. LEE AND J. D. OSHEA
uterus, which could be accounted for by venoarterial transfer from ovarian venous blood t o ovarian arterial blood and thence via anastomotic connections to the ipsilateral uterine horn. At the level of the uterus there are no across-the-midline anastomoses and therefore a localized effect on the ipsilateral horn would be predicted. This possibility remains, however, purely hypothetical. The arrangement of the ovarian vessels distal to the point a t which their uterine branches arise is also noteworthy. As in many eutherian mammals, it is a t this level, closer to the ovary, that the most intimate relationship develops between the ovarian arteries and veins. In these marsupials, however, in contrast to eutherians, the ovarian artery gives rise to a large number of ovarian branches of rather uniform size. These arteries are closely intertwined with the veins draining the ovary, which form a plexus a t this level. Although the function of this vascular arrangement is not known, its structure is highly suggestive of a specialization for countercurrent exchange between arterial and venous blood. Since no data are available as to the nature, extent, or even the direction of any such exchange in female marsupials or eutherian mammals, it may be relevant to consider data on the function of the homologous and in many respects similar arterio-venous relationship in the vessels supplying the testis. As Harrison ('49) and Barnett and Brazenor ('581 have shown, a highly developed rete mirabile is present in the spermatic cord of many, though not all, marsupials. In relation to the brush possum, described here, both similarities and some differences are detectable between the ovarian and testicular vessels. Quantitatively, both in terms of numbers of arterial and venous branches and the length over which they are in contact, the testicular vessels greatly exceed the ovarian. Also the reuniting of the testicular arteries and veins to single or very small numbers of vessels close to the testis is absent in the ovarian vessels. Nonetheless, subject to these differences, the vascular arrangements of the ovary are distinctly similar to those of the testis. There is clear evidence that the rete mirabile in some macropod marsupials acts as a countercurrent heat exchanger to cool the arterial blood flowing into the testis (Setchell and Waites, '69). These authors also demonstrated that the branches of the internal spermatic artery act to dampen the pulse wave in
the testicular blood supply. Furthermore, Jacks and Setchell ('73) have demonstrated that substances in the blood (prostaglandin F,, testosterone and tritiated water) can pass from venous to arterial blood in the spermatic cord, although the physiological significance of such a process of transfer remains unknown. While there is no basis to suppose that heat exchange could be a function of the ovarian vessels, the exchange of substances in the blood is clearly worthy of investigation, particularly in the light of evidence that the corpus luteum may exert a local, unilateral effect on ovarian follicles in several eutherian species (Ginther, '74). I t seems reasonable to assume that the well-developed arterio-venous relationship in the ovarian pedicle in many eutherian and marsupial mammals is likely to serve some function. However, it is less easy to understand why such a close similarity exists between the ovarian and testicular vascular arrangements in many species, when a major proposed function in the male, namely heat exchange (Setchell, '70; Waites, '701, is presumably irrelevant in the female. This similarity is illustrated in eutherian mammals by comparison of the data of Harrison ('49) on the testicular vessels with data on the ovarian vessels in man (Delson et al., '491, rhesus monkey (Ginther et al., '741, guinea pig, rat, hamster, rabbit (Del Campo and Ginther, '721, horse, sheep, pig (Del Campo and Ginther, '73), dog and cat (Del Campo and Ginther, '74). In these species the extent of convolution of the testicular artery in the male appears generally to be mimicked, in lesser degree, by that of the ovarian artery. Thus, for example, in the sheep and pig there is a high degree of convolution in both male and female, while in man and the cat there is relatively little convolution in either sex. Although less information is available in relation to marsupials, the data presented here, together with those of Harrison ('49, '51) and Barnett and Brazenor ('58) confirm that distinct similarities between the two sexes exist a t least in relation to T. vulpecula, M. eugenii, T. billardierii, M. rufa, and K ursinus. No data on the testicular vessels of M.agilis or M. giganteus are available. If this tendency for similarity in the nature and arrangement of the testicular and ovarian vessels can be confirmed in a wider range of species, eutherian and marsupial, some explanation other than coincidence will clearly need to be considered. The development of a complex arteriove-
REPRODUCTIVE TRACT IN MARSUPIALS
nous relationship in the testicular vessels has been observed only in mammals, and within mammals is developed more commonly and to a much greater degree in those with scrota1 or inguinal testes (Setchell, ’70). It would appear likely, therefore, that this relationship has evolved primarily, though not necessarily exclusively, in conjunction with the function of cooling of the testes. Thus, assuming that the homologous vascular relationship in the ovary does serve some useful function unrelated to heat exchange, its occurrence could be construed as a form of evolutionary “opportunism” in the females of species in which natural selection has favored an increasingly complex arrangement of the testicular vessels in the males. ACKNOWLEDGMENTS
We are very grateful to Doctors Paul Presidente and Ray Butler, who made available to us many of the specimens used in this study. LITERATURE CITED Barnett, C. H., and C. W. Brazenor 1958 The testicular rete mirabile of marsupials. Aust. J. Zool., 6: 27-32. Beddard, F. E. 1909 On the postcaval vein and its branches in certain mammals. Proc. 2001. Soc., Land., I:
496-526. Clark, M. J.,and G. B. Sharman 1965 Failure of hysterectomy to affect the ovarian cycle of the marsupial Trichosurus uulpecula J. Reprod. Fert., 10: 459-461. Del Campo, C. H., and 0. J. Ginther 1972 Vascular anatomy of the uterus and ovaries and the unilateral luteolytic effect of the uterus: guinea pigs. rats, hamsters and rabbits. Am. J. Vet. Res., 33: 2561-2578. 1973 Vascular anatomy of t he uterus and ovaries and t h e unilateral luteolytic effect of the uterus: horses, sheep, and swine. Am. J. Vet. Res., 34: 305-316. 1974 Arteries and veins of uterus and ovaries in dogs and cats. Am. J. Vet. Res., 35: 409-415. Delson, B., S. Lubin and S. R. M. Reynolds 1949 Vascular patterns in the human ovary. Am. J. Obst. Gynec., 57:
-
842-853. Getty, R. 1975 Sisson and Grossman’s The Anatomy of th e Domestic Animals. Fifth ed. W. B. Saunders CO., Philadelphia, London and Toronto.
103
Ginther, 0. J. 1974 Internal regulation of physiological processes through local venoarterial pathways: a review. J. Anim. Sci., 39: 550-564. Ginther, 0. J., D. J. Diersche, S. W. Walsh and C. H. Del Campo 1974 Anatomy of arteries and veins of uterus and ovaries in rhesus monkeys. Biol. Reprod., I k205-219. Goding, J. R., I. A. Cumming, W. A. Chamley, J. M. Brown, M. D. Cain, J. C. Cerini, M. E. D. Cerini, J. K. Findlay, J. D. O She a and D. H. Pemberton 1972 Prostaglandin F b , “the” luteolysin in the mammal? Gynec. Invest., 2:
73-97. Harrison, R. G. 1949 The comparative anatomy of the blood.supply of the mammalian testis. Proc. 2001. SOC., 119: 325-334. 1951 Applications of microradiography: the testis. In: Microarteriography and Other Radiological Techniques Employed in Biological Research. A. E. Barclay, ed. Blackwell Scientific Publications. Oxford, pp. 89-91. Hartman, G. C. 1925 Hysterectomy and the oestrous cycle in the opossum. Am. J. Anat., 35: 25-29. Jacks, F.,and B. P. Setchell 1973 A technique for studying the transfer of substances from venous to arterial blood in the spermatic cord of wallabies and rams. J. Physiol., 233: 17P-18P. Lee, C. S., and J. D. OShea 1976 The extrinsic blood vessels of the ovary of the sheep. J. Morph.. 148: 287-304. McCracken, J. A.,J. C. Carlson, M. E. Clew, J. R. Goding, D. T. Baird, K. Green and B. Samuelsson 1973 Prostaglandin F b identified a s a luteolytic hormone in sheep. Nature: New Biology, 238: 129-134. Pearson, J. 1940 Notes on the blood system of the marsupiala. Pap. and Proc. Roy. %. Tasmania, 73: 77-94. Setchell, B. P. 1970 Testicular blood supply, lymphatic drainage, and secretion of fluid. In: The Testis. Vol. 1. A. D. Johnson, W. R. Gomes and N. L. Vandemark. eds. Academic Press, New York and London, pp. 101-239. Setchell, B. P., and G. M. H. Waites 1969 Pulse attenuation and countercurrent heat exchange in the internal spermatic artery of some Australian marsupials. J. Reprod. Fert., 20: 165-169. Tyndale-Biscoe, C. H. 1973 Life of Marsupials. Edward Arnold, London. Tyndale-Biscoe, C. H., J. P. Hearn and M.B. Renfree 1974 Control of reproduction in macropodid marsupials. J. Endocr., 63: 589-614. von der Borch, S. M. 1963 Unilateral hormone effect in the marsupial Trichosurus uulpecula. J. Reprod. Fert., 5:
447-449. Waites, G. M. H. 1970 Temperature regulation and the testis. In: The Testis. Vol. 1. A. D. Johnson, W.R.Gomes and N. L. Vandemark, eds. Academic Press, New York and London, pp. 241-279.
PLATE 1 EXPLANATION OF FIGURE
2
104
Dorsal view of partially cleared specimen of latex-injected female genital tract of the brush possum. Latex in arteries appears black, in veins white (right and left ovarian and right cranial urogenital veins only). 0, ovary; U, uterus; UR, ureter; V, vagina; US, urogenital sinus; C, cloaca; OA, ovarian artery; AU, cranial urogenital artery; 11, internal iliac artery; PU, caudal urogenital artery; IP, internal pudendal artery (which has become separated from internal iliac artery). Across-the-midline arterial anastomoses are present a t many sites (arrows). X 1.5.
REPRODUCTIVE TRACT IN MARSUPIALS C. S. Lee and J . D. OShea
PLATE 1
105
PLATE
2
EXPLANATION OF FIGURES
3 Latex cast of right ovarian artery from a brush possum. 0, ovary; U, cranial tip of uterus; OA. ovarian artery; OB, ovarian branches of ovarian artery; FB, branch to Fallopian tube; UB, branches to uterus. X 2.8. 4
Latex cast of aorta and branches to the genital tract and pelvic region in a female brush possum, ventral view. A, aorta; 0, ovarian artery; EI, external iliac artery; 11, internal iliac artery; AU, cranial urogenital artery; G, artery to gluteal region; PU, caudal urogenital artery; 1P. internal pudendal artery; MS, median sacral artery with two major branches. x 0.9.
5 Ventral view of caudal vena cava and pelvic veins filled with blood (dark), together with arteries filled with white latex, in a specimen from a female brush possum. PV, caudal vena cava; 0, ovarian vein; CI, common iliac vein; EI, external iliac vein; 11, internal iliac vein; AU, cranial urogenital vein; PU, caudal urogenital vein; G, vein to gluteal region; IP. internal pudendal vein; MS, median sacral vein. In this specimen there is no common iliac vein on the right side, and only a short one on the left. X 1.3.
106
REPRODUCTIVE TRACT IN MARSUPIALS C. S. Lee and J. D. OShea
PLATE 2
PLATE 3 EXPLANATION OF FIGURES
6 Section of ovarian artery (OA)and vein (OW, in the region proximal to origin of the ovarian branches in a female brush possum. A small vein (SV) is joining the ovarian vein a t left. H and E. X 120.
7 Section of ovarian branches of ovarian artery (A)and vein (V)not far from hilus of ovary in female brush possum. Close contact between arteries and a small vein is seen (arrows). H and E. X 120.
8 Section of many branches of testicular artery (A) and vein (V)in spermatic cord of male brush possum. Sites of arterio-venous contact are arrowed. Collagenous connective tissue (CT) separates arteries from veins in many places. H and E. X 120.
108
REPRODUCTIVE TRACT IN MARSUPIALS C. S. Lee and J. D. O'Shea
PLATE 3
109
PLATE 4 EXPLANATION OF FIGURES
9 Dissection of pelvic region of a male brush possum, showing origin and route of testicular vessels. B. bladder, P, prostate; T, testis; E,epididymis; PV,caudal vena cava; TV, testicular vessels in abdomen; IC, inguinal canal; TB, branches of testicular vessels in spermatic cord. Arteries injected with white latex, veins filled with blood and appearing black. X 0.9. 10 Latex cast of left testicular artery from a brush possum. T, testis; E, epididymis; TA,
testicular artery, abdominal portion; RM, rete mirabile of testicular artery in spermatic cord; EB, branches to epididymis. Note tha t the testicular artery again becomes single (arrow) before entering the testis. X 1.2.
110
REPRODUCTIVE TRACT IN MARSUPIALS D OShea
PLATE 4
C. S. Lee and J.
111
PLATE 5 EXPLANATION OF FIGURES
11 Partially cleared specimen of latex-injected female genital tract of eastern grey kangaroo, dorsal view. Arteries appear dark, veins white. 0, ovary; FT, Fallopian tube; U, uterus; V, vagina; OV, ovarian artery and vein; OB, ovarian branches of ovarian artery and vein; UB, uterine branch of ovarian vein; AU, cranial urogenital artery and vein. X 1.3. 12 Partially cleared specimen of latex injected female genital tract of common wombat,
dorsal view. Arteries dark, veins white. 0, ovary; FT,Fallopian tube; U, uterus; OV, ovarian artery and vein; OB, ovarian branches of ovarian artery and vein; UB, uterine branch of ovarian vein. x 1.1.
112
REPRODUCTIVE TRACT IN MARSUPIALS C. S. Lee and J. D. O'Shea
PLATE 5
113
