1) General zoological data of species
The term "spider monkey" is used loosely here, as I well appreciate the difficulty in taxonomy. Konstant (1985; 1986) has stated that this designation best, or most properly, applies for Ateles geoffroy,i but that "spider monkey", has now been used for many other, similar-appearing, animals. They are all characterized by their prehensile tail, their body size and black feet. A comprehensive review of these animals was published by Kellogg and Goldman (1944), to be followed by many others. Still, much controversy on taxonomy exists.
This characteristically South American platyrrhine group of species is widely distributed through the Amazon basin and most of Central America. It is composed of many species and/or subspecies that differ greatly in color and some minor other features. Mittermeier (1986) discussed their distribution and status of endangerment in some detail. Despite a lack of publicity, a number of these species/subspecies are critically endangered (Konstant and Mittermeier, 1985). Schneider (2000) compared DNA databases of the major groups of South American primates (Atelidae, Pitheciidae, Cebidae) and further defined their relationships.
Spider monkeys are extremely nimble, prehensile-tailed animals and are often exhibited in zoological parks. They are very social animals. Often large groups travel in the trees of the rainforest. More often, they form smaller family groups. An extensive literature exists on these species that can be accessed through Nowak's book (1999) and the publication by Mittermeier (1986). A clear differentiation among the great array of phenotypes displayed by these animals has been difficult. A crisper designation of phenotypes was attempted by Konstant & Mittermeier (1985; 1986) when they discussed the need for subspecific recognition because of their chromosomal differences and their many different phenotypes. The importance of this was stressed especially for their captive management. They depicted these different phenotypes in color pamphlets (1985) but the work that was meant to come to a unifying agreement was never completed. The same can be said about the many chromosomal forms that are displayed by spider monkeys from different regions. There are many inversions and translocations, which have not found universal acceptance in their correlation with agreed-upon designations. Nor are they used for a more meaningful management (de Boer, 1974). One reason for the difficulty is that the precise origin of many zoo specimens is unknown, and fieldwork with cytogenetic techniques is problematic. More information on recent phenotype/genotype correlation is found below under the section on genetics. For the understanding of placentation all this is not problematic as the reproductive features of all Ateles species is much the same.
2) General gestational data
|Spider monkeys of obviously different types at Children's Zoo of the San Diego Zoo, many years ago. This sort of picture is now only rarely seen.|
|Spider monkeys with their prehensile tails at the San Diego Wild Animal Park; this is Ateles belzebuth.|
Few studies have been undertaken on spider monkey implantation. Wislocki (1930) had the best specimens, but they were still insufficient to know details. Implantation in the uterus simplex occurs similar to that in macacs, with one lobe presumably located anterior, the other posterior in the uterus. The bridging vessels run horizontally from one lobe to the other but only in one segment of membranes, not bilaterally. The larger lobe ("primary") usually has the cord insertion. One of our specimens deviated from that rule.
4) General characteristics of placenta
The spider monkey has a bilobed placenta and the lobes are subdivided into smaller lobules. It is thus cotyledonary and hemochorial in the type of its barrier function.
|Delivered placenta from spider monkey pregnancy at term. The placenta is bilobed but many smaller lobular dubdivisions are present in the "primary" lobe. There is meconium staining and the "bridging vessels" course only on one side of the membranes.|
Invasive trophoblast is mostly limited to the decidua and is composed of sheets of extravillous trophoblast that characteristically surround the maternal decidual arteries, rather than invading them. The placental villi are much more trabecular than those of man and cercopithecids, as was already mentioned by Mossman (1987). In that respect, the spider monkey placenta is more similar to that of callithricids (marmosets and tamarins). In some areas, particularly near the maternal surface, the villi have a near filiform appearance. Young placentas have larger villi with a rounder appearance and possess foci of hematopoiesis, "blood islands", in their fetal capillaries, much as the callithricids have. These are not found at term, however.
5) Details of barrier structure
This is a characteristic hemochorial placenta. The maternal blood circulates in the intervillous space (IVS) and surrounds the villi with their syncytial surfaces. Syncytial "buds" are commonly found on the villous surfaces and one would expect that, as in humans, they would often detach and land in the maternal lung, as happens in humans.
|The "filiform", trabecular nature of the villi is more pronounced near the placental floor (left) than higher up in the placenta (below left).|
|The "filiform", trabecular nature of the villi is more pronounced near the placental floor (above left) than higher up in the placenta (left).|
|Term spider monkey villous tissue with little blood in the intervillous space (common). The red blood cells are all contained in the fetal circulation. Multinucleated syncytiotrophoblast covers all villi and forms "knots" (center) that often detach. Cytotrophoblast cannot be discerned at term in paraffin material.|
|Immature placenta of stillborn fetus with 39 g placenta. Villi are larger than at term and contain foci of hematopoiesis (dark elements). Rare cytotrophoblastic cells can be identified.|
|Filiform villi on right attach to a large deposit of "X-cells" which has a cystically degenerated center. Such X-cell cysts are common in human placentas and contain major basic protein which is the secretory product of X-cells.|
6) Umbilical cord
There were four umbilical vessels in addition to a large allantoic duct in all but two of our placentas. These had only single arteries, thus altogether only three blood vessels. They were associated with normal fetuses. The allantoic duct may have a good urothelial lining or it may be atrophied. In one cord the duct was apparently occluded. The duct was usually central but in some sections the large fetal vessels "hang" into the sac on broad strands of Wharton's jelly.
The cords measured between13 and 30 cm in length (average 23 cm), had occasional right twists, but generally were not twisted much.
|Sections of two different umbilical cords to show the slit-like allantoic duct (left) and the large duct with "hanging" blood vessels in the ductal space.|
|Sections of two different umbilical cords to show the slit-like allantoic duct and the large duct with "hanging" blood vessels in the ductal space.|
7) Uteroplacental circulation
The general vasculature of the placental/uterine system has not been described in detail in this species. Gruenwald (1972) had one specimen and believed the spider monkey placenta to resemble so much that of the squirrel monkey that appropriate inference can be drawn from their study. He made reference to the fact that several maternal arteries enter the fetal lobules. The decidua basalis has, however, large maternal spiral arterioles that are typically surrounded and only slightly invaded by extravillous trophoblast.
|Placental "floor" with large maternal decidual blood vessel at left, surrounded by trophoblast. At "T" is the basal layer of extravillous trophoblast, next to the villous attachment (right). Note the invasion of the decidua by darker trophoblastic cells.|
8) Extraplacental membranes
An unusual feature of spider monkey placentas is their large allantoic sac, an exceptional feature in higher primate placentas (Miller & Benirschke, 1982; 1985). It was found in all of the placentas that we have had available. In contrast to artiodactyla, there was not the universal vascularization of the allantoic membrane. Fluid was expressed from the filled allantoic sac through the umbilical duct, and it was thus assumed to be fetal urine. In a specimen of howler monkey, neither allantoic sac nor a duct was found.
|At left is a section from the margin of the placenta with the attachment of the membranes. Note the dark cells (extravillous trophoblast) that surround the maternal blood vessel.|
|At left is a section of membranes to show the amnion (left) and allantoic sac (center).|
The decidua shows frequently much degeneration, frank yellow necrosis and hemorrhage. This is true for the decidua basalis as well as for the decidua capsularis. In the membranes, of course, travel the thick-walled fetal blood vessels that connect the lobes.
The amnion is cuboidal to slightly columnar, especially when there had been meconium discharge. In that case there is some degeneration of the amnionic epithelium and the columnar appearance becomes more striking. Meconium-laden macrophages can be found as in the human membranes after the discharge of meconium.
Trophoblast external to barrier
15) Pathological features
|Term placenta with "amnionic sac infection", i.e. chorioamnionitis and funisitis. This shows the fetal surface with emigration of polymorphonuclear leukocytes from the mother in the intervillous space (IVS) and from the fetus' surface vessel. The migration is always towards the surface where the chemotactic agent (bacterium etc.) resides.|
|Maternal surface of spider monkey placenta showing two central areas of retroplacental hemorrhage (abruptios) in the larger lobe.|
That abortion occurs in wild animals has been shown with fecal steroid determination in the study by Campbell et al. (2001).
Other relevant features and need for future studies
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Cell lines from: http://www.sandiegozoo.org/conservation/cres_home.html. Please direct your inquiries to Dr. Oliver Ryder (firstname.lastname@example.org).
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