Comparative Placentation

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Goeldi's Monkey
Callimico goeldii

Order: Primates
Family: Callitrichidae - Callicominidae(nae)

1) General Zoological Data

The Goeldi's monkey is one of the many South American tree-dwelling small primates in Amazonia whose ecology and general characteristics have been described in detail by Heltne et al. (1981). It is considered to be an endangered species. Although similar in size to marmosets and tamarins, these species differ in many respects. Goeldi's monkey for instance does not produce twins and has a third molar tooth, absent in marmosets and tamarins. This is but one reason why it is generally considered to be more primitive. It is presumed that the Goeldi's monkey, one of the "dwarf species", split off the ancestral stock of South American primates prior to the development of marmosets (Dutrillaux et al., 1988). These authors discussed the presumed phylogeny in detail. Martin (1992), who considered this problem in modern detail, felt nevertheless that the species should be classed with other callithricids, rather than in a placed into a separate family. That publication summarizes all the controversial views that pertain to the placement of this species with marmosets and tamarins into one monophyletic group. Some controversy, however, still exists in the appropriate assignment of this animal. Longevity of about 18 years.

		Goeldi's monkeys at San Diego Zoo.

2) General Gestational Data

Gestational length is approximately (150)-155 days with a singleton born. Twins occur only rarely in captivity. Newborns weigh between 30-50 g; adults are 393-860 g (Nowak, 1999).

3) Implantation

No studies of early implantation have been described for this species. The uterus is unicornuate.

4) General Characterization of the Placenta

Goeldi's monkey has a bidiscoid placenta with a villous, hemochorial implantation. The only report of its structure comes from Soma & Kada (1989) who observed two placentas. Both of these were from a stillborn animals and at least one pregnancy was deemed to have been premature, at 110 days gestation. One neonate weighed 56 g, the placenta weighed 4, and 5 g respectively and measured 2x2x06, 1.6x6x0.4 cm, and 2x2x0.4, 3x2x0.5 cm. The two lobes were separated by 2.4 and 4 cm of membranes. Both had infarcts and the decidual necrosis at the floor was pronounced. They described the structure as "trabecular - pseudolabyrinthine". The histologic slides shown here come from a third placenta that was kindly donated to me from the Brookfield Zoo, Chicago. It also was from a stillborn term fetus, but macroscopic details were not supplied. The features are entirely those as of the previous authors' observations.

		Placenta of Goeldi's monkey from publication of Soma and Kada (1989). The photograph was kindly supplied by Dr. Hiroaki Soma, Tokyo.

		Macroscopic appearance of Goeldi placenta with fused disks, one smaller than the other.

	5) Details of fetal/maternal barrier

		Surface of placenta with detached amnion and the chorion above, villous tissue below.

		Large chorioallantoic artery in chorion above, amnion at top left.

		Villous structure of Goeldi's monkey. Note the absence of hematopoiesis in the villi.

		The "floor" of a mature Goeldi's monkey placenta showing much decidual necrosis, and fibrin accumulation.

		Higher magnification of villous structure with sparse syncytium and no villous hematopoiesis.

In contrast to tamarins, none of the three placentas observed by Soma and Kada (1989) and those seen by myself had villous hematopoiesis. There is an unusual amount of basal decidual necrosis, similar to what is seen in tamarins. The villous structure is somewhat trabecular, but not so pronounced as that of tamarins. The trophoblast is single-layered by light microscopy at least in term placentas. It is likely, however, that electron microscopy would disclose cytotrophoblast underlying the syncytium. At the implantation site, numerous large "X-cells" (extravillous trophoblast) are present. No such deposits of extravillous trophoblast exist in the villous portion of the placenta, unlike that seen in simians.

6) Umbilical cord

The umbilical cords of the two placentas described by Soma & Kada (1989) were 1.5 and 2.5 cm in length and had four blood vessels. They were marginally inserted on one disk and connected to the other disk by large membranous vessels. Spirals and ducts of any kind were not described.

7) Uteroplacental circulation

No studies have been published.

8) Extraplacental membranes

The amnion is thin and avascular with a single layer of epithelium. One placenta had a tiny, yellow yolk sac remnant beneath the amnion. There is a small amount of decidua capsularis.

9) Trophoblast external to barrier

This has not been observed, as no implanted placenta has been described. The decidual arterioles present in my specimen, however had no trophoblastic infiltration, although extravillous trophoblast is amply present in the decidua basalis.

10) Endometrium

The decidua basalis has much apparently normal necrosis and fibrin deposition. Nevertheless, the intervillous circulation was intact in all three placentas.

		The "floor" of mature placentas always has a large amount of fibrin and fibrinoid accumulation, in addition to decidual necrosis. The blue cells are "X-cells" (extravillous trophoblast).

11) Various features

No other remarkable endometrial features have been recorded.

12) Endocrinology

Soma and Kada (1989) stained their placentas with anti-hCG antibodies and failed to demonstrate the presence of gonadotropins in that manner. Ziegler et al. (1990), on the other hand, identified urinary chorionic gonadotropins 18 days after presumed ovulation, with elevated titers remaining to day 45 days. The polyestrous animals have a cycle of 22-24 days, estrus lasting 7 days. Other endocrine studies come from Carroll et al. (1990) and Ziegler et al. (1990).

13) Genetics

Goeldi's monkeys have typically 48 chromosomes (Bender & Mettler, 1960; Chiarelli, 1980). Initially, a XX/XO sex determining mechanism was suspected (Hsu & Hampton, 1970). Subsequently the mystery was solved when a chromosomal error was described in a male animal. It had a fusion of the Y-chromosome to autosome # 23 (Dutrillaux et al., 1988). The animal appeared to be normal. The publication gives details of chromosomal banding patterns. A study of repetitive DNA provided additional support for the current phylogenetic position of this species (Montagnon, et al., 1993). Similar conclusions were also derived from the study of genes determining the v. Willebrand factor (Chaves, et al., 1999). No hybrids have been described.

14) Immunology

No studies are known to me.

15) Pathological features

Infarcts were present in two of the three placentas of stillborn fetuses. Callithrichids, including Goeldi's monkey, are extremely susceptible to infection with lymphocytic choriomeningitis virus (Asper et al., 2001). It is transmitted by wild mice and can be fatal with hepatitis. Pseudotuberculosis due to Yersinia pseudotuberculosis appears to be endemic at Jersey with death resulting in some animals (Bielli et al., 1999).

16) Physiologic data

I know of no data relevant to this section.

17) Other resources

Few cell lines are available from CRES through Dr. Oliver Ryder at: oryder@ucsd.edu

18) Other remarks - What additional Information is needed?

It would be helpful to have an implanted placenta described and one of live births. Moreover, the data on umbilical cord and endocrinology are woefully inadequate.

Acknowledgement

The animal photograph of this chapter comes from the Zoological Society of San Diego.

References

Asper, M., Hofmann, P., Osmann, C., Funk, J., Metzger, C., Bruns, M., Kaup, F.J., Schmitz, H. and Gunther, S.: First outbreak of callithrichid hepatitis in Germany: genetic characterization of the causative lymphocytic choriomeningitis virus strain. Virology 284:203-213, 2001.

Bender, M.A. and Mettler, L.E.: Chromosome studies of primates. II Callithrix, Leontocebus and Callimico. Cytologia 25:400-404, 1960.

Bielli, M., Lauzi, S., Pratelli, A., Martini, M., Dall'Ara, P. and Bonizzi, L.: Pseudotuberculosis in marmosets, tamarins, and Goeldi's monkeys (Callithrichidae/Callicominidae) housed at a European zoo. J. Zoo Wildl. Med. 30:532-536, 1999.

Carroll, J.B., Abbott, D.H., George, L.M., Hindle, J.E. and Martin, R.D.: Urinary endocrine monitoring of the ovarian cycle and pregnancy in Goeldi's monkey (Callimico goeldii). J. Reprod. Fertil. 89:149-161, 1990.

Chaves, R., Sampaio, I., Schneider, M.P., Schneider, H., Page, S.L. and Goodman, M.: The place of Callimico goeldii in the Callitrichine phylogenetic tree: evidence from von Willebrand factor intron II sequences. Mol. Phylogenet. Evol. 13:392-404, 1999.

Chiarelli, A.B.: The karyology of South American primates and their relationship to African and Asian species. Chapter 19, pp. 387-398 in, Evolutionary Biology of the New World Monkeys and Continental Drift. R. Ciochon and A.B. Chiarelli, eds. Plenum Press, NY 1980.

Dutrillaux, B., Lombardi, M., Carroll, J.B. and Martin, R.D.: Chromosomal affinities of Callimico goeldii (Platyrrhini) and characterization of a Y-autosome translocation in a male. Folia primatol. 50:230-236, 1988.

Heltne, P.G., Wojcik, J.F. and Pook, A.G.: Goeldi's monkey, Genus Callimico. Chapter 4, pp. 169-210, in Ecology and Behavior of Neotropical Primates, Vol. 1. A.F. Coimbra-Filho and R.A. Mittermeier, eds. Academia Brasileira de Ciências, Rio de Janeiro, 1981.

Hsu, T.C. and Hampton, S.H.: Chromosomes of Callithricidae with special reference e to an XX-'XO' sex chromosome system in Goeldi's marmoset (Callimico goeldii Thomas 1904). Folia primatol. 13:183-195, 1970.

Martin, R.D.: Goeldi and the dwarfs: the evolutionary biology of the small New World monkeys. J. Human Evol. 22:367-369, 1992.

Montagnon, D., Crovella, S. and Rumpler, Y.: Confirmation of the taxonomic position of Callimico goeldi (Paris). (Primates, Platyrrhini) on the basis of its highly repeated DNA patterns. Compte rendu Acad. Sci. III 316:219-223, 1993 Nowak, R.M.: Walker's Mammals of the World. 6th ed. The Johns Hopkins Press, Baltimore, 1999.

Soma, H. and Kada, H.: Placentation of the Goeldi's monkey, Callimico. 31. International Symp. Erkrankungen der Zoo- und Wildtiere, Dortmund. Akademie-Verlag, Berlin, pp. 93-98, 1989.

Ziegler, T.E., Snowdown, C.T., Warneke, M. and Bridson, W.E.: Urinary excretion of oestrone conjugates and gonadotrophins during pregnancy in the Goeldi's monkey (Callimico goeldii). J. Reprod. Fertil. 89:163-168, 1990.