Comparative Placentation

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Proboscis monkey
Nasalis larvatus

Order: Primates
Family: Cercopithecidae

1) General Zoological Data

This large, diurnal leaf- and fruit-eating monkey is resident of Borneo and Indonesia where it lives in sizeable troops. Their group size at foraging has been studied in some detail in Brunei by Macdonald (1982) who found up to 63 individual foraging together. This animal has a preference for mangrove swamps and is also known to be an excellent swimmer, often diving from great heights into water in order to forage. The composition of their largely herbivorous diet has been analyzed by Yeager et al. (1997). MacKinnon (1986) estimated that only 25,000 animals remained in Borneo. Some controversy has existed as to the most closely related Asian monkeys. Collura et al. (1996) have addressed this by studying the mitochondrial cytochrome b gene. This has suggested to them that proboscis monkeys "groups with the Asian langurs, rather than forming a sister taxon to all Asian and African colobines".

It has been challenging to keep proboscis monkeys in captivity for prolonged periods. They are currently only seen in Singapore and rarely in other zoos. This is a declining and severely endangered species. It is, of course, prominently known because of the large nose that grows to excessive proportions in males. Proboscis monkeys also have very long tails. Males weigh up to 22 kg; females are between 7 and 11 kg (Nowak, 1999). Their longevity is at least 23 years in captivity, and maturity is reached in males at about 7 years. Neonates are colored blue until about three months old.

		Male proboscis monkey at San Diego Zoo.

		Male proboscis monkey at San Diego Zoo.

		Female proboscis monkey with young, formerly at San Diego Zoo.

2) General Gestational Data

I have had two specimens available for study; both were immature. One was an abortus supplied by Dr. Heldstab of the Basel Zoo; the other was from a gestation at San Diego Zoo. The proboscis monkey has typically a single, initially blue fetus that delivers after about 166 days of gestation. The neonatal weight is around 450 g. It is of considerable interest, however, that Wislocki (1939) had examined the uterus of a proboscis monkey that contained twins, a male and female. Each had only a single placental disk, to which the cords were centrally implanted. The twins were monochorionic (!) with two amnions. There were, however, two corpora lutea, contained in the right ovary. Wislocki did not discuss whether the female twin was adversely affected by being co-twin to a male, nor whether there were vascular connections between the two placental circulations. The placenta was also not described further. The placental weight has not yet been determined, as no term placenta has yet been described.

3) Implantation

Only one early specimen (about 17 days) has ever been examined. This specimen of Selenka is depicted in a drawing that was kindly supplied to me by Patrick Luckett in 1977; it is depicted here. Luckett wrote that he disagreed with Hill's 1932 interpretation of this embryo's yolk sac formation (my arrows). Luckett considered this to represent the beginning of folding of the primary yolk sac in the initiation of the formation of the secondary yolk sac. No other stages are available and there is thus no resolution to this minor disagreement between two eminent placentologists.

		Drawing of Selenka's Keim S kindly supplied by Dr. W.P. Luckett in 1977.

		Immature fetus with uterus (left) and placenta in situ. The two lobes of the immature placenta are readily distinguished as being anterior and posterior in the uterus. The 15 cm cord is attached to the margin of one placental lobe.

4) General Characterization of the Placenta

This species has a bidiscoid placenta that has been described only once (Soma & Benirschke, 1977). It is the specimen shown above and came from the pregnant uterus of an animal that was bred at the San Diego Zoo. The mother had died from exposure to cold. The placenta is cotyledonary, villous and hemochorial. The trophoblast invades the decidua basalis, similar to that of other cercopithecids.

5) Details of fetal/maternal barrier

This placenta is a typical hemochorial (hemo-monochorial) villous organ that is constructed very much like that of all other higher primates. The amnion is closely attached to the chorion, whence the mesenchyma of the villous structures originate. The villi are surrounded by maternal blood that contacts the trophoblast directly. The outside trophoblast is syncytiotrophoblast; beneath this syncytium is the regenerative cytotrophoblast (the "Langhans" cells of human placentas) that produces the syncytium. The villi contain loose connective tissue with numerous macrophages (Hofbauer cells), and fetal capillaries. At least three orders of villous branching are readily identified. There are rare larger accumulations of extravillous trophoblast ("X-cells"). The only typical X-cells occur at the tips of the villi at the implantation site and there extend a very short distance into the decidua basalis. Rather large numbers of this extravillous trophoblast are seen at the site of implantation in early gestation. However, unlike human placentation, no real fibrinoid is produced at this site and there is also no obvious invasion of the maternal blood vessels. Rather, there is invariably a layer of amorphous decidual necrosis. In these early specimens, there are no infarcts. In older specimens of the numerous cercopithecids placentas that I have examined, including colobids, there have always been villous infarcts. At times they are rather numerous and sizeable. But they are not related to "atherosis" of humans, but are probably due to thrombosis.

		Main stem villi of the Basel proboscis monkey abortus.

		Typical villus with many Hofbauer cells (H), occasional fetal vessels (F.V.) and occasional cytotrophoblastic cells beneath the syncytiotrophoblast.

		Surface of midterm placenta with amnion on top, loosely attached to the chorion.

		Enlarged view of midterm villi with fetal blood vessels containing nucleated red blood cells and an obvious Langhans layer of cytotrophoblast. Microvilli are barely visible on the syncytium.

		Another villus with degenerating blood vessels and content. Better microvilli.

	6) Umbilical cord The cord of this fetus was 15 cm long and not appreciably spiraled; there was no cord or fetus in the first specimen. The cord contained two arteries and one vein. There were no ducts. The surface is a thin amnionic epithelium, without metaplastic changes.

		Male fetus 9 cm CR length, weighing 56 g, with 15 cm cord.

	7) Uteroplacental circulation This has not been studied but it is likely to be similar to that of macacs. See that chapter for details.

		Anchoring villi of aborted proboscis monkey placenta with extravillous trophoblast securing the adhesion to the decidual floor below.

		More anchoring villi with syncytium, X-cells and superficial infiltration of X-cells into decidua basalis.

		This implantation site show the thick layer of extravillous trophoblast that spew from the anchoring villi into the layer of degenerated decidua basalis.

8) Extraplacental membranes

The amnion is pressed against the chorion in which the fetal blood vessels are carried. The amnion is composed of a thin epithelium and a layer of connective tissue without vessels. More peripheral to the chorionic membrane is a thin layer of extravillous trophoblast, and then follows a small amount of decidua capsularis. There is no allantoic sac. Of interest is that the chorion laeve did not contain atrophic villi, as they are abundant in human placentas. This absence is similar to the condition found in macacs and other monkeys with bidiscoid placentas. You will find more discussion in the macac chapter on this absence of atrophied villi in the membranes.

9) Trophoblast external to barrier

There is an extensive shell of invading extravillous trophoblast ("X-cells"). It infiltrates the superficial layer of the decidua basalis but does not reach the myometrium.

10) Endometrium

The endometrium undergoes decidual changes very much like those that occur in human gestation. There is no basal layer of typical fibrinoid as seen in humans (the Rohr and Nitabuch layers); instead, a broad band of decidual necrosis is found here, as is true for other cercopithecids.

11) Various features

None.

12) Endocrinology

I know of no studies specifically directed to this species. Typically though, the fetus depicted above had the usual large fetal adrenal glands of primates that are due to the presence of a wide fetal zone (Soma & Benirschke, 1977). The adrenal glands were even larger than the kidneys. It is of interest that Wislocki (1939), who saw monochorionic twins in this species, does not mention any freemartin effect on the female fetus. Perhaps there were no vascular anastomoses between the twins, or perhaps the situation is similar to that of marmosets.

13) Genetics

The proboscis monkey has 48 chromosomes, and Giemsa banding has been done (Chiarelli, 1966; Hsu & Benirschke, 1975; Soma & Benirschke, 1975). Hybrids are unknown. One study on the cytochrome b mitochondrial gene has been published by Collura et al. (1996). In studies that employ chromosome painting, Bigoni et al. (2003) found complex rearrangements to explain the unique karyotype of this unusual animal. It may not, as had been suspected, be most ancestral of colobids. Further studies of related taxa are imperative.

Male and female karyotypes of proboscis monkey from Hsu & Benirschke, 1975.

14) Immunology

The deaths of proboscis monkeys at San Diego were frequently due to infection with cryptococci, but it is not known whether this is due to an immune deficiency.

15) Pathological features

Cryptococcosis has been a significant cause of mortality in San Diego. Pulmonary acariasis due to Pneumonyssus simicola was also common in the animals of our zoo (Griner, 1983). In the Frankfurt Zoo, where many animals have been kept in the past, intestinal parasites were an initial problem.

16) Physiologic data

Few studies other than the brief description of the partitioned stomach that is so characteristic of these leaf-eaters are published (Soma & Benirschke, 1977).

17) Other resources

Some cell strains are available from CRES at the San Diego Zoo by contacting Dr. Oliver Ryder at: oryder@ucsd.edu.

18) Other remarks - What additional Information is needed?

Term placentas have not been described. Thus, the weight of the mature placenta and the length of term umbilical cords are unknown. No endocrine studies have been conducted and they are needed.

Acknowledgement

The animal photographs in this chapter come from the Zoological Society of San Diego. I appreciate also very much the help of the pathologists at the San Diego Zoo.

References

Bigoni, F., Stanyon, R., Wimmer, R. and Schempp, W.: Chromosome painting shows that the proboscis monkey (Nasalis larvatus) has a derived karyotype and is phylogenetically nested with asian colobines. Amer. J. Primatol. 60:85-93, 2003.
Chiarelli, B.: The chromosome complement of Nasalis larvatus (Wurm 1781). Experientia 22:797, 1966.

Collura, R.V., Auerbach, M.R. and Stewart, C.B.: A quick, direct method that can differentiate expressed mitochondrial genes from their nuclear pseudogenes. Curr. Biol. 6:1337-1339, 1996.

Griner, L.A.: Pathology of Zoo Animals. Zoological Society of San Diego, San Diego, California, 1983.

Hill, J.P.: The developmental history of the primates. Philosoph. Trans. B. 221:45-178, 1932.

Hsu, T.C. and Benirschke, K.: An Atlas of Mammalian Chromosomes. Springer-Verlag, New York. Vol. 9, Folio 449, 1975.

Luckett, W.P.: Comparative development and evolution of the placenta in primates. Contrib. Primatol. 3:142-234, 1974.

Macdonald, D.W.: Notes on the size and composition of groups of proboscis monkey, Nasalis larvatus. Folia Primatol. 37:95-98, 1982.

MacKinnon, K.: The conservation status of nonhuman primates in Indonesia. Chapter 8 in, Primates - The Road to self-sustaining Populations, K. Benirschke, ed. Pp.99-126, Springer-Verlag, NY, 1986.

Nowak, R.M.: Walker's Mammals of the World. 6th ed. The Johns Hopkins Press, Baltimore, 1999.

Selenka, E.: Entwickklung des Gibbons (Hylobates und Siamanga). Fortsetz. Stud. Entw. Gesch. Tiere 8:173-208, 1900.

Soma, H., Benirschke, K. and Robinson, P.: The chromosomes of the Proboscis monkey (Nasalis larvatus). Chromosome Information Service 17:24-26. 1974

Soma, H. and Benirschke, K.: Observations on the fetus and placenta of a proboscis monkey (Nasalis larvatus). Primates 18:277-284, 1977.

Wislocki, G.B.: Observations on twinning in marmosets. Amer. J. Anat. 64:445-483, 1939.

Yeager, C.P., Silver, S.C. and Dierenfeld, E.S.: Mineral and phytochemical influences on foliage selection by the proboscis monkey (Nasalis larvatus). Amer. J. Primatol. 41:117-128, 1997.