/I B R.AFLY OF THE UNIVERSITY OF ILLINOIS 590.5 FI v. 35 cop. 3 NATURAL HISTORY 5* 3 PLACENTATION OF A PRIMITIVE INSECTIVORE ECHINOSORKX GYMNURA WALDEMAR MEISTER AND D. DWIGHT DAVIS FIELDIANA: ZOOLOGY VOLUME 35, NUMBER 2 Published by CHICAGO NATURAL HISTORY MUSEUM OCTOBER 7, 1953 History Library PLACENTATION OF A PRIMITIVE INSECTIVORE ECHINOSOREX GYMNURA WALDEMAR MEISTER AND D. DWIGHT DAVIS Curator, Division of Vertebrate Anatomy FIELDIANA: ZOOLOGY VOLUME 35, NUMBER 2 Published by CHICAGO NATURAL HISTORY MUSEUM OCTOBER 7, 1953 THE W 1? W53 PRINTED IN THE UNITED STATES OF AMERICA BY CHICAGO NATURAL HISTORY MUSEUM PRESS 5 5' 3 Placentation of a Primitive Insectivore Echinosorex gymnura INTRODUCTION The gymnure, variously called the "white shrew," "moon rat," or Ticus bulan (Malay), is an insectivore allied to the hedgehogs of Europe and Africa. In many respects Echinosorex (= Gymnura of authors) is more primitive than the hedgehogs, however; it is, in fact, one of the most generalized of living placental mammals. Its closest living relatives are the lesser gymnure (Hylomys) of the Malay Peninsula and the East Indies, the Philippine gymnure (Podogymnura) of southern Mindanao, and Neotetracus of western China and northern Indochina. Echinosorex is found in the Malay Peninsula, Sumatra, and Borneo. Nothing is known of the placentation and fetal membranes of Echinosorex beyond a brief and unsatisfactory account of an early stage by Hubrecht (1898). The placentation of the other three genera is wholly unknown. MATERIAL AND METHODS The material on which this study is based was collected by one of us (Davis) in 1950, during field work by the Bornean Zoological Expedition of Chicago Natural History Museum. The specimens came from the vicinity of Sandakan, North Borneo. They consisted of a gravid uterus containing two fetuses near term, and the entire body of a non-pregnant female. This material was preserved in 10 per cent formalin in the field and was transferred some months later to 68 per cent alcohol. Both specimens were dissected, using a 9X binocular microscope where necessary. Tissue from both uteri was embedded in celloidin and sectioned at thicknesses varying from 8 to 24 micra. Serial sections were cut at 20-24 micra from the central and lateral parts of the placenta. Fixation proved satisfactory for ordinary histo- logical study. All sections were stained with hematoxylin-eosin. 11 LIBRARY 12 FIELDIANA: ZOOLOGY, VOLUME 35 We are indebted to Dr. H. W. Mossman, of the Department of Anatomy, University of Wisconsin, for extremely helpful advice and criticism during the course of this work. OBSERVATIONS The Non-Gravid Uterus The uterus (pi. 4, fig. 2) is bicornuate, as in all insectivores that have been examined. It is a T-shaped organ, consisting of a short median body and two horns connected by a median fundus. In the undisturbed condition the horns are much flexed, and completely hide the corpus from ventral view. The organ measures about 25 mm. across the extended horns, each horn thus measuring about 12 mm. The corpus, which consists chiefly of the massive cervix, measures about 7-8 mm. in length. Wislocki (1940) states that the cervix is "very inconspicuous" in Solenodon. The ventral surface of the uterus is separated from the bladder by a shallow utero-vesical pouch of peritoneum. This recess extends over the proximal part of the vagina. The dorsal surface is sepa- rated from the rectum by a deep recto-uterine pouch, delimited on either side by the diaphragmatic folds. The recto-uterine pouch is very evident when the uterus is shifted ventrad, for the diaphrag- matic folds are then stretched and elevated. The uterus is connected to the pelvic walls by a broad ligament on each side. The broad ligament is a wide double-layered fold of peritoneum extending between the uterine horn and the ventro- lateral wall of the pelvis. Its free lateral edge contains the round ligament, a narrow, rather flat fibro-muscular band attached to the ventral surface of the horn. The round ligament is directed ven- trally, reaching the pelvic wall in the region of the inguinal canal. The two round ligaments form an angle of about 90, open ven- trally. The diaphragmatic fold, which is comparable to the recto-uterine fold of human anatomy, is a part of the broad ligament. It is a very long, double-layered peritoneal fold enclosing a fibro-muscular band, that extends from the dorsal surface of the uterine horn and the ovary to the body wall in the region of the kidney and dia- phragm. It is elongate triangular in outline. The suspensory liga- ment of the ovary cannot be distinguished as a separate structure distinct from the diaphragmatic fold. The ovarian ligament, be- tween ovary and uterus, is not well defined. MEISTER AND DAVIS: PLACENTATION OF INSECTIVORE 13 Ovary and oviduct. -The ovary (pi. 4, fig. 3) is a relatively small, flattened, bilobed body attached to the distal part of the uterine horn. It measures about 3 by 5 mm. The ovary, together with the oviduct, is completely encapsulated in an ovarian bursa, which is a part of the diaphragmatic fold. Wislocki (1940) described a slit-like opening through which the bursa communicates with the peritoneal cavity in Solenodon, but careful examination failed to reveal any such opening in Echinosorex; the ovary and oviduct appear to be completely sealed within the bursa. The oviduct is a rather short tube continuous with the uterine horn, situated in the part of the bursa closest to the uterus. It measures about 8-9 mm. in length. The tube is slightly coiled in S-shape. The infundibulum is spread flatly on the inner surface of the bursa. It has a flat, funnel-shaped form, and lies close to the medial pole of the ovary; its opening faces ventrad (pi. 4, fig. 3). Vagina. The vagina is about 25 mm. long, measured by a probe, with a maximum internal diameter of 5-6 mm. It is widest at the middle, becoming narrower proximally and distally. The walls are about one mm. thick. Between the wall of the vagina and the vaginal part of the cervix there are well-defined fornices that are deep laterally and ventrally, and shallow dorsally. In the distal half of the vagina the mucosa is thrown up into numerous longitu- dinal rugae, with a few transverse folds. The mucosa of the proxi- mal half, nearest the cervix, is smoother, with only a few indistinct rugae. The massive cervix protrudes deeply into the vagina. External genitalia and urethra. The introitus vaginae is situated 15 mm. below the anus. It is a short longitudinal slit surrounded by a roughly circular area of naked unpigmented skin. The edges of the opening are only slightly raised posteriorly, but anteriorly there is a prominent papilla-like elevation. The skin surrounding the introitus is much puckered. The urethra is about 15 mm. long, its external orifice situated below the introitus vaginae and about 4 mm. inside the urogenital opening. It does not form a special papilla. This most external part of the urogenital canal, which is lined with cornified epithelium, may be regarded as a poorly defined vestibulum. Histology of the Non-Gravid Uterus Fixation was less satisfactory than for the gravid uterus, although general histological structure was preserved. The right horn was sectioned transversely. The myometrium is composed of a thin 14 FIELDIANA: ZOOLOGY, VOLUME 35 outer layer of circular muscle fibers and a much thicker inner layer of more or less longitudinal fibers. The uterine vessels lie in the external third of the inner muscular layer but do not form any regular vascular sheet. In the endometrium the epithelial lining was lost through maceration, but it is preserved in the pregnant uterus close to the tip of the horn. It consists of tall simple columnar cells, apparently non-ciliated. Uterine glands penetrate the endo- metrial mesenchymal stroma out to the myometrium. They are cut in all directions in the sections and are not very densely dis- tributed. The histological structure of the uterus closely resembles that of Erinaceus as described by Deanesly (1934). The right ovary, enclosed in the ovarian bursa, was sectioned paral- lel to the long axis of the uterine horn, the cut crossing the ovi- duct. The bursa is composed of connective tissue similar to that of the uterine ligaments and is covered externally and internally with a layer of flat mesothelial cells. Some parts of the bursa contain adipose tissue, especially around the large ovarian vessels. The germinal epithelium of the ovary is of low cuboidal type. The medullary part of the ovarian stroma is relatively dense, the cortex more loose. Ovarian follicles are present in all stages of development, from primary up to large Graafian follicles containing eggs surrounded by follicular epithelium (pi. 6, fig. 8). The vesicu- lar follicles are surrounded by a follicular theca. Numerous corpora lutea are present. The oviduct has a relatively thin muscular wall and a much- folded mucosa covered with tall columnar epithelium (pi. 6, fig. 9). It is impossible to determine whether the epithelium is ciliated or not. A large epoophoron is situated near the proximal pole of the ovary, close to the fimbrial end of the oviduct. The Gravid Uterus The gravid uterus is much enlarged, containing two fetuses, one in each cornu (pi. 5, fig. 4). Judging from their size and state of development the fetuses were close to term. The crown-rump length is 71 mm. Each lay with its head in the part of the cornu adjacent to the uterine body, the rump occupying the ovarian end of the cornu. The trunk of the fetus is enclosed between the pla- centa dorsally and the yolk sac ventrally. The head is flexed, and the tail is curved along the body between the hind legs. The fetus is unpigmented and naked except for short vibrissae on the snout. MEISTER AND DAVIS: PLACENTATION OF INSECTIVORE 15 The eyes appear to be closed, and the ears are flattened against the head, their outlines indicated by semicircular wrinkles. The wall of the uterus is thin and extended, except at the ovarian end of the horn. Sections show that the part of the endometrium representing the decidua parietalis contains no glands or covering epithelium, these being lost in fusion with the decidua capsularis. At the ovarian end of the horn the walls are thicker, the endo- metrium is slightly folded, and glands and epithelium are present (pi. 6, fig. 7). The Placenta and Fetal Membranes The placenta is discoidal, is sharply circumscribed, and is at- tached to the antimesometrial wall of the uterine horn. Its diameter, measured over the convex surface, is about 40 by 55 mm. The umbilical cord is connected to the approximate center of the pla- centa, which is the thickest part of the structure (5-6 mm.). The thickness gradually decreases toward the margin, which is only slightly elevated above the lining of the uterus. The umbilical cord is relatively short, measuring 40-45 mm. in length; it is untwisted and oval in cross section. Both fetuses face away from the placenta, and the cord accordingly crosses the fetus, as shown in plate 5, fig. 4. The diameter of the cord close to the fetal body, after the vitelline vessels have joined it, is about 3 by 1.5 mm., measured on the slides. The vitelline vessels join the cord at a point about 10 mm. from the umbilical ring. The cord was sectioned about 5 mm. from the umbilical ring, after the vitelline vessels had joined it (pi. 6, fig. 10). There are five main blood vessels divided into two groups: two umbilical ar- teries and one umbilical vein, representing the allantoic group of vessels; and two vitelline vessels, an artery and a vein, representing the yolk sac vessels. These groups occupy opposite ends of the long diameter of the cord. All three umbilical vessels and the vitelline artery are filled with mature erythrocytes. The vitelline vein con- tains both mature non-nucleate and young nucleated erythrocytes. The thin allantoic duct lies between the umbilical arteries, close to the surface of the cord. It is lined with pyramidal cells with large vesicular nuclei, and has a narrow lumen. The lining endodermal cells are surrounded by a layer of spindle-shaped mesodermal cells. The stroma of the umbilical cord has a reticular structure, its density varying in different parts of the cross section. This tissue 16 FIELDIANA: ZOOLOGY, VOLUME 35 is acellular, and its structure evidently results from fixation of the jelly-like mass of the umbilical cord stroma (Wharton's jelly). A few cellular elements of fibroblastic nature, and some wandering elements, are scattered through the stroma. The epithelium cover- ing the cord is stratified, consisting of several layers of flattened amniotic cells. To return to the placenta, the endometrium separates easily from the myometrium, especially in the region of the decidua basalis. The sheets of the gestation sac (the fetal amnion and chorion and the maternal decidua capsularis) were so intimately fused that they could not be separated. It was also impossible to determine whether the decidua capsularis is complete or not. A large and very shrunken yolk sac (omphalopleure) is situated between the amnion and the chorion on the ventral side of the fetus. It is heavily folded, its surface is rough, and it completely covers the ventral surface of the fetus, lying just opposite' to the placenta (pi. 5, fig. 4) . The vitelline vessels from the yolk sac run in a separate cord that joins the umbilical cord close to the umbilical ring about 10 mm. from the ring in the right fetus and slightly closer in the left. Histology of the Placenta The chorio-allantoic placenta is of the hemoendothelial labyrin- thine type. It is composed of a relatively thin endometrial part, the decidua basalis (maternal), and a thick trophoblastic and allan- toic part (embryonic). No indication of a decidua capsularis was found. The decidua basalis is composed exclusively of connective tissue of the endometrial stroma, traversed by endometrial vessels. Uterine glands and uterine epithelium are wanting. There are a few epi- thelial cells around the edges of the placenta, but they are com- pletely absent elsewhere over the decidua. Afferent and efferent vessels in the endometrium communicate with blood channels in the trophoblast and with vessels in the myometrium. The endo- thelial lining of some afferent (arterial) endometrial vessels shows proliferation: the endothelial cells are taller, irregular in form, and project into the vascular lumen (pi. 8, fig. 19). The trophoblast is three or four times as thick as the decidua. It is composed of a massive spongy basal part in contact with the maternal endometrium, from which plate-like outgrowths project radially toward the inner (allantoic) surface of the placenta, forming the trabecular part of the trophoblast. Both basal and trabecu- MEISTER AND DAVIS: PLACENTATION OF INSECTIVORE 17 lar parts are of syncytial nature, although in some parts cellular structure, with definite boundaries between individual cells, is main- tained. Most of the cells are mononuclear, with large vesicular nuclei and very granular cytoplasm (pi. 6, fig. 11; pi. 7, fig. 12; pi. 9, fig. 22). The basal trophoblast contains numerous large blood channels, which have no endothelial lining (pi. 7, fig. 13). Arteries traversing this layer give off feeder channels that penetrate radially through the whole thickness of the placenta (pi. 9, figs. 22, 23). Venous channels, irregular and lacunar in form, are connected with the endometrial veins of the decidua and are filled with maternal blood (pi. 7, fig. 13; pi. 8, fig. 19). These large venous channels in turn open into a dense network of smaller trophoblastic channels, which communicate directly with the basal ends of the labyrinthine chan- nels of the trabecular trophoblast. The numerous blood channels give a spongy texture to the basal trophoblast, the "tropho-spongia" of Hubrecht. In the trabecular part of the trophoblast the plate-like out- growths interanastomose to form a network of labyrinthine chan- nels. These channels are in direct connection with the venous channels in the basal trophoblast on the basal side, and with the arterial feeder channels on the allantoic side, and are filled with maternal blood. The thickness of the trabecular plates varies in different parts of the trophoblast, but they are always thickest toward the basal trophoblast and thinner toward the allantoic surface. Giant cells.- Many groups of giant mononuclear cells occur in the trophoblast (pi. 7, fig. 13; pi. 8, figs. 18, 19). These are the mis- named "Deziduofracts" or "decidual cells" of Hubrecht. These cells have irregular outlines and large nuclei, and stain deeply with hematoxylin-eosin. They vary in size, but all are enormous com- pared with other cells in the surrounding syncytium. They occur chiefly in scattered clusters, usually of about a dozen cells, although the size of the clusters varies and occasional single cells are found. In the trophoblast the giant cells all lie adjacent to the decidua basalis; nowhere were they found in the deeper layers of the tropho- blastic proliferation, or in the decidua basalis. Large clusters of giant cells are also located in the lumen of many of the large venous channels lying in the zone of junction between the decidua basalis and the trophoblast. The form of the clusters clearly depends on the form of the channels they occupy, 18 FIELDIANA: ZOOLOGY, VOLUME 35 and they are strictly confined to the lumina of the channels. In some cases the vascular lumen is completely blocked by the cell mass, although a few blood elements are present among the giant cells. In other cases the lumen is only partially occluded, and ma- ternal blood is still present in the vessel. The size of these giant cells varies greatly, and some show degenerative changes in the nu- cleus and cytoplasm. The origin and significance of giant cells in the placenta have been much discussed (e.g., Mossman, 1937). Some authors have inter- preted them as arising from the vascular endothelium of the endo- metrial vessels, while others regard them as of trophoblastic origin. In our specimen of Echinosorex, giant cells are found exclusively in trophoblastic tissue (the venous channels have no endothelium). If they are of endothelial origin they would have had to migrate from the endometrial vessels into the trophoblastic tissue. Furthermore, in our specimen there is nothing to indicate that the giant cells arose in the vessels and then migrated into the trophoblast. Origin in situ from trophoblastic tissue seems far more likely in Echinosorex. We suggest that in Echinosorex, at least, the giant cells indicate degenerative changes taking place in the placenta as the time for parturition draws near. The allantoic vesicle lies adjacent to the inner surface of the tro- phoblast. It is a flattened structure of medium size extending to the edges of the placenta and is composed of mesenchymal tissue lined with a single layer of cuboidal endodermal epithelium (pi. 7, fig. 16). There are two sets of large allantoic vessels: a set of thick-walled vessels with narrow lumen, representing branches of the umbilical arteries; and a set of thin-walled vessels with large lumen, apparently belonging to the umbilical venous system. Small branches from the umbilical arteries and veins penetrate into the trophoblastic chan- nels, where they break up into numerous capillaries (pi. 7, fig. 17). Some capillaries run for a long distance as single vessels, but most of them branch and interanastomose to form vascular networks within the trabecular channels (pi. 7, fig. 15). These capillaries, bathed in maternal blood as they lie in the channels, represent the actual site of exchange between maternal and fetal circulations. The walls of the capillaries are composed of a single layer of endo- thelial cells; there is no visible trophoblastic layer covering them, and therefore the placenta of Echinosorex clearly shows the hemo- endothelial relationship between maternal and fetal circulations at MEISTER AND DAVIS: PLACENTATION OF INSECTIVORE 19 least at the stage represented by our specimen. This is especially evident in places where a bare capillary lies in a trophoblastic chan- nel that is not completely filled with maternal blood (pi. 7, fig. 14). In these places it is very evident that the barrier between fetal and maternal blood is represented only by the endothelium forming the capillary wall. The yolk sac consists of a large but very shrunken bilaminar omphalopleure representing the chorio-vitelline placenta. It is cov- ered with amnion on the outer surface, except the abembryonic surface, which is in contact with the chorion. The wall of the yolk sac consists of a thick splanchnopleuric mesenchyme lined with a single layer of endodermal cells and covered externally with mesothelium. The mesenchymal layer is well vas- cularized and is densely packed with young nucleated blood cells; apparently most of these are young erythrocytes. The splanchno- pleure is in fact so densely packed with young blood cells that in some places it is difficult to distinguish the mesenchymal structure (pi. 8, fig. 21). Thus, although the fetus is very close to term, the yolk sac still shows very active hemopoietic activity. The cavity of the yolk sac is everywhere lined with a single layer of large endodermal cells (pi. 8, fig. 21). It is impossible to determine in our material whether the abembryonic surface is underlain by a mesodermal layer, i.e. whether the yolk sac is inverted or not. The larger vitelline vessels, probably veins, are filled with eryth- rocytes. Most of these are non-nucleated mature cells, but young nucleated erythrocytes are also present. The smaller vessels contain a higher percentage of young nucleated cells. Numerous nucleated erythrocytes are also present in the vitelline vein in the umbilical cord. Maternal Circulation in the Placenta Figure 1 Maternal arterial blood is delivered to the trophoblastic laby- rinth through large feeder channels that, arising directly from the endometrial arteries, penetrate the whole thickness of the tropho- blast (pi. 9, figs. 22, 23). Upon reaching the allantoic surface of the placenta they turn at right angles and run parallel to the inner placen- tal surface (pi. 9, fig. 23). The channels paralleling the inner pla- cental surface form numerous connections with the allantoic ends of the labyrinthine channels in the trabecular part of the tropho- 20 FIELDIANA: ZOOLOGY, VOLUME 35 blast. Maternal blood, de-oxygenated in the labyrinthine channels, is returned to the maternal venous circulation via venous channels at the opposite (basal) ends of the labyrinthine channels. Thus within the trophoblastic channels maternal blood flows from the allantoic surface to the endometrial surface. Venous channel plate Fetal capillaries Labyrinthine channel (Maternal blood) Umbilical artery Allontoic vesicle FIG. 1. Diagrammatic section through placenta of Echinosorex gymnura to show relationships of fetal and maternal circulations. Fetal blood solid, maternal blood hatched. Are these vessels connecting the endometrial arteries with the labyrinthine channels true arteries, or are they channels of tropho- blastic origin? Their structure varies from level to level in the pla- centa. At the endometrial end the walls are thick and have an indefinite structure that stains deeply with eosin. The structure re- sembles sheets of fibrinous deposition, including only a few cellular elements in various stages of degeneration; these cells are apparently of trophoblastic origin. The boundary between the fibrinous walls MEISTER AND DAVIS: PLACENTATION OF INSECTIVORE 21 and the surrounding trophoblastic tissue is not clearly defined, and in some places the fibrinous masses penetrate into the spongy tro- phoblast (pi. 9, fig. 24). The deeper the vessels penetrate into the placenta the thinner the walls become; for the most part they dis- appear after the vessels leave the basal trophoblast and enter the trabecular trophoblast. The cells lining these vessels have no regular form, and some show a clear tendency toward proliferation. It is difficult to decide whether they are true endothelial cells or merely modified tropho- blastic cells. When they are traced along a vessel, from the basal toward the allantoic surface of the trophoblast, their structure more and more resembles that of flattened trophoblastic cells. The morphology of these vessels indicates that they are arterial placental channels, not arteries. The fibrinous deposition and the variation in form of the cells lining the lumen are probably degenera- tive changes to be expected in a full term placenta. The fetal capillaries occupying the trabecular channels carry embryonic blood and are surrounded by maternal blood. Within the channels the arterial blood of mother and fetus flows in opposite directions, which increases efficiency of exchange between maternal and fetal circulations (Noer, 1946). DISCUSSION The placenta and fetal membranes undergo continuous change from the time of early implantation until birth, and recent work has rightly emphasized the morphogenesis of these structures rather than description and comparison of selected stages. It is obvious, however, that the material required for proper study of morpho- genetic processes will never be available for more than a small frac- tion of mammalian types. For the vast majority of mammals we will probably never have more than the few random stages that happen to be preserved from time to time. These will continue to be important because knowledge, however detailed, of a handful of laboratory and semi-laboratory forms cannot supplant knowledge of as wide a variety of forms as possible what is gained in depth is lost in breadth. Echinosorex is a member of the order Insectivora. The insecti- vores are morphologically the most primitive of living placental mammals. Evidence from the fossil record supports the view that they truly represent the most ancient and conservative stock of the Eutheria, and that the unspecialized living members of the Asiatic 22 FIELDIANA: ZOOLOGY, VOLUME 35 Erinaceidae and the Madagascar! Tenrecidae differ little from their Eocene ancestors. Echinosorex is, in turn, one of the most general- ized of living erinaceids, and therefore one of the most generalized and primitive of living eutherian mammals. Interest in the placenta and fetal membranes of Echinosorex is threefold : (1) How does its placentation compare with that of other erinaceids? (2) How does the erinaceid type of placentation compare with that of other generalized insectivores, especially the Tenrecoidea? (3) Is the placentation of these lowly insectivores primitive and generalized in the same sense as the morphology of these creatures? Mossman (1937) has reviewed and summarized the enormous literature on placentation in mammals in an extremely valuable compilation. He regards the placenta and fetal membranes as the most conservative features of the body, and therefore ipso facto most trustworthy as indicators of true affinities among mammals. He presents a classification of mammals based exclusively on the morphology of the fetal membranes, but some of the relationships he adduces are so fantastically at variance with those indicated by all other evidence that they cannot be taken seriously. 1 What Moss- man's discussion does prove conclusively is that characters of the placenta and fetal membranes, like all other characters, must be in- terpreted in the light of data from all other sources. This is essen- tially the conclusion reached by Gerard (1934) after he had consid- ered the fetal adnexa in relation to other characters that have been used in determining inter-relationships among the Mammalia. Re- gardless of interpretation, however, Mossman's compilation and assessment of existing data are a monumental achievement that greatly simplifies further comparative work. At the time he wrote, Mossman had data for Erinaceus only from Hubrecht's old studies, and for the Tenrecidae only the data of Strahl and Grosser. There is still no modern study of Erinaceus, but Goetz's work on Tenrec (=Centetes) (1936) and Hemicentetes, (1937) and Wislocki's (1940) excellent study of Solenodon at mid- gestation are now available. Thus there are now data for one or more representatives of each of the three most primitive families of the Insectivora. 1 Most astonishing is his conclusion that the Lemuridae are "definitely related to the ungulates, probably most closely to the Perissodactyla, and are widely unrelated to the Primates." MEISTER AND DAVIS: PLACENTATION OF INSECTIVORE 23 Using the tabular form employed by Mossman, the data for Echinosorex (family Erinaceidae), Tenrec and Hemicentetes (family Tenrecidae), and Solenodon (family Solenodontidae) are as follows. Some interpretation of authors' descriptions has been necessary, especially for Goetz's works, which unfortunately are more discus- sions than descriptions. Implantation Orientation . Depth . . Decidua Echinosorex antimesometrial eccentric (fide Hubrecht)' no data for capsularis Amniogenesis no data Yolk sac Bilaminar omphalopleure . Chorio-vitelline olacenta . . large, persists to full term no data Tenrec Hemicentetes 1 "orthomeso- metrial" 3 eccentric 4 remnants of cap- sularis cavitation small, persists central blood si- nus with folded walls Solenodon 5 antimesometrial no data remnants of capsu- laris at mid-term no data large, persists abundant complex splanchnopleuric villi; no sinus Vascular splanchnopleure Chorio-allantoic placenta Shape large, hemopo- ietic, near term; no data on in- version discoidal small near term cup-shaped large, completely inverted cup-shaped Type. labyrinthine labyrinthine labyrinthine 7 r*^* Finer morphol-. . ogy hemoendothelial, hemochorial hemochorial at Location at least near term antimesometrial "orthomeso- mid-term antimesometrial Allantoic vesicle Size medium metrial" 1 large absent Permanence. . term term? absent at mid-term 1 Authority of Goetz. 1 Hubrecht (1898) and de Lange (1933, p. 169) also describe implantation in Erinaceus as eccentric, not interstitial as Mossman states. 3 Approximately halfway between mesometrial and antimesometrial. 4 Goetz (1937, p. 161) describes implantation as "intermediate between" superficial and interstitial. This is eccentric implantation. 5 Authority of Wislocki. 24 FIELDIANA: ZOOLOGY, VOLUME 35 As far as can be determined from Hubrecht's descriptions, Echi- nosorex seems not to differ from Erinaceus in any essential respect except in the intimacy of contact between chorion and maternal tissues. Hubrecht described this as hemochorial for Erinaceus, whereas it is definitely hemoendothelial in our specimen of Echino- sorex. The phylogenetic significance, if any, of this difference is difficult to assess. Mossman found that certain rodents achieve the hemoendothelial condition late in pregnancy, after passing through a hemochorial stage. It must be remembered, of course, that the hemoendothelial condition was unknown at the time Hubrecht wrote. The placentation of the Solenodontidae and Centetidae differs from that of the Erinaceidae in many respects, as shown in the table. The Solenodontidae and Centetidae also differ from each other, and Wislocki concluded that the placentation of Solenodon "reveals that its closest affinities are to the Soricidae." Goetz believed that the placentation of Hemicentetes indicates relationships to the Gar- ni vora, the manatee, and the Lemuridae on the one hand, and to the Reptilia on the other! The differences between Solenodon and the Tenrecidae are real, and certainly are far greater than those between Erinaceus and Echinosorex. There is no way of evaluating these differences, however, and we feel that Wislocki (like most others who have worked on the placenta) has over-emphasized dif- ferences and ignored equally real similarities. The astonishing rela- tionships, completely at variance with data from all other sources, that are often proposed on the basis of placental morphology indi- cate that a basis for valid interpretation has not yet been found. It is unreal and illogical to divorce placental characters from all other evidence and to insist on impossible relationships purely on the basis of placental data. It contributes nothing to an under- standing of the inter-relationships of mammals, and even less to an understanding of the phylogeny of the placenta. It suggests the equally dogmatic, and equally illogical, insistence on serological tests as the sole arbiter of relationships between organisms. Certainly it is impossible to postulate, on the basis of what is presently known of placentation in the primitive insectivores, the primary type of placentation in eutherian mammals. We feel that this may be partly due to the astonishing lack of any modern study of Erinaceus or an adequate description of any centetid. The per- sistence of hemopoiesis in the yolk sac until term in Echinosorex would appear to be a more primitive condition than in other mam- mals, in which such activity ceases early in pregnancy. MEISTER AND DAVIS: PLACENTATION OF INSECTIVORE 25 SUMMARY 1. The female reproductive organs of a non-gravid and a gravid Echinosorex gymnura are described. 2. The placenta and fetal membranes from a near-term preg- nancy are described. 3. The placentation of Echinosorex is very similar to that of Erinaceus, except that placentation is hemoendothelial in Echino- sorex (near term) and hemochorial in Erinaceus. 4. Placentation in the Erinaceidae differs in many respects from placentation in the Solenodontidae or Tenrecidae. 5. The placentation of the generalized insectivores is not primitive in the same sense that the adult morphology of these organisms is. 6. Any classification of the Mammalia based exclusively on characters of the fetal adnexa leads to impossible relationships. Placental characters must be evaluated in the light of data from comparative anatomy, embryology, and paleontology. 7. Any phylogenetic arrangement of the fetal adnexa that ignores the phylogeny of the organisms is artificial and mislead- ing. REFERENCES DEANESLY, RUTH 1934. The reproductive processes of certain mammals. Part VI: The repro- ductive cycle of the female hedgehog. Phil. Trans. Roy. Soc. London, (B), 223: 239-276, pis. 27-33. GERARD, POL 1934. La formation et la structure des annexes foetales peuvent-elles servir de base a une classification des mammiferes? Ann. Soc. Roy. Belgique, 64: 75-92, 13 figs. GOETZ, R. H. 1936. Studien zur Placentation der Centetiden. I. Eine Neu-untersuchung der Centetesplacenta. Zeitschr. Anat. Entwg., 106: 315-342, 16 figs. 1937. Studien zur Placentation der Centetiden. III. Die Entwicklung der Fruchthlillen und der Placenta bei Hemicentetes semispinosus (Cuvier). Zeitschr. Anat. Entwg., 108: 161-200, 22 figs. HUBRECHT, A. A. W. 1889. Studies in mammalian embryology. I. The placentation of Erinaceus europaeus, with remarks on the phylogeny of the placenta. Quart. Jour. Micr. Sci., 30: 283-404, pis. 15-27. 1898. La formation de la decidua reflexa chez les genres Erinaceus et Gymnura. Ann. Jardin Bot. Buitenzorg, Suppl. 2, pp. 159-167, pi. 9. 1909. Die Saugetierontogenese in ihrer Bedeutung fur die Phylogenie der Wir- beltiere. v+247 pp., 186 figs. Jena, G. Fischer. 26 FIELDIANA: ZOOLOGY, VOLUME 35 LANGE, D. DE 1933. Plazentarbildung. In Handbuch der vergleichenden Anatomie der Wir- beltiere, ed. by Bolk, Goppert, Kallius, and Lubosch. 6: 155-234. Berlin, Urban & Schwarzenberg. MOSSMAN, H. W. 1937. Comparative morphogenesis of the fetal membranes and accessory uterine structures. Carnegie Inst. Wash. Contr. Embryol., 26: 128-246, 12 figs., 24 pis. NOER, ROLF 1946. A study of the effect of flow direction on the placental transmission, using artificial placentas. Anat. Rec., 96: 383-389, 6 figs. WISLOCKI, G. B. 1940. The placentation of Solenodon paradoxus. Amer. Jour. Anat., 66: 497- 531, 1 fig., 7 pis. EXPLANATION OF PLATE 4 Fig. 2. Female urogenital system of Echinosorex gymnura, ventral view. X 2. Fig. 3. Left ovary and oviduct, ventral view. The bursa ovarica has been opened. X 7. Fieldiana: Zoology, Volume 35 Plate 4 _^l_ Rectum ! Plica diophrogmatica Ovanum in Bursa / ovorico Tuba uterine Cornu smistrum uteri Formx vaginae _ Plica vesicalis peritonii Bursa ovorica Infundibulum tubae uterinae Plica diaphragmotica Ovarium Tuba uterma Cornu uteri EXPLANATION OF PLATE 5 Fig. 4. Pregnant uterus, ventral view. Wall of right horn partly cut away to show topographic relations of fetus, placenta, and yolk sac. X 0.75. Fig. 5. Right uterine horn, cervix, and proximal part of vagina, ventral view. Fetus and yolk sac shifted from uterine cavity, placenta in situ. X 0.75. Fieldiana: Zoology, Volume 35 Plate 5 Cornu dextrum Corpus uteri Cornu sinistrum Heod of Fetus Wai! of uterus Umbilical cord Placenta YolK sac Amnion (part) Hind leg Placenta Loterol fornix Cervix Vagina Yolk sac EXPLANATION OF PLATE 6 Fig. 6. Cross section through wall of vagina of pregnant female; section taken from proximal half. X 40. Fig. 7. Section through wall of pregnant uterus at tip of horn, showing endo- metrium with epithelium and uterine glands, and a part of myometrium. X 40. Fig. 8. Section through ovary of non-pregnant female, showing primary and secondary follicles and corpora lutea. The ovarian bursa is visible on the left. X 40. Fig. 9. Cross section through distal part of oviduct of non-pregnant female. X 40. Fig. 10. Cross section through umbilical cord taken close to fetus, after vitelline vessels have joined the cord. Umbilical vessels at top, vitelline vessels at bottom. X 15. Fig. 11. Section through entire placenta, about halfway between center and margin. Maternal surface to right, fetal to left; endomyometrium split. The numbered rectangles indicate the approximate sites at which photographs at higher magnification were taken. X 4.5. Mian a: Zoology, Volume 35 Plate 6 EXPLANATION OF PLATE 7 Fig. 12. Section through spongy basal trophoblast (right) and trabecular trophoblast (left). The plate-like outgrowths forming labyrinthine channels are shown. Fetal capillaries are visible in the labyrinthine channels. X 40. Fig. 13. Venous channels, filled with maternal blood, in basal trophoblast. X 40. Fig. 14. Enlarged view of fetal capillary shown near top of figure 12. The bare capillary, without trophoblastic layer, is seen surrounded by maternal blood. X 168. Fig. 15. Interanastomosing fetal capillaries in trophoblastic channels. X 168. Fig. 16. Allantoic side of placenta showing large maternal arterial channel (center), with allantoic vessels to the left and below it. Allantoic vesicle at bottom of figure. X 40. Fig. 17. Fetal arteriole, from umbilical artery, in labyrinthine trophoblast. These vessels break up to form the fetal capillaries. X 40. Idiana: Zoology, Volume 35 Plate 7 EXPLANATION OF PLATE 8 Fig. 18. Giant cells blocking maternal venous channels at base of basal trophoblast. Endometrium at extreme right. X 45. Fig. 19. Same as figure 18. Maternal endometrial vessel with swollen endo- thelium at extreme right. X 45. Fig. 20. Section through yolk sac. Amnion at left. X 40. Fig. 21. Enlargement of section of figure 20 to show active hemopoiesis. The lobule is covered with single-layered mesothelium, and lined with large endo- dermal cells. X 168. eldiana: Zoology, Volume 35 Plate 8 EXPLANATION OF PLATE 9 Fig. 22. Section through entire placenta close to umbilical cord. Maternal surface at top, fetal surface at bottom. X 6. Fig. 23. Maternal arterial feeder channel penetrating trophoblast. X 15. Fig. 24. Cross section of maternal arterial feeder channel in spongy tropho- blast, showing lining of trophoblastic cells surrounded by fibrinous deposition. X 24. i'l( liana: Zoology, Volume 35 Plate 9 Publication 721