White-faced Capuchin Monkey (Cebus albifrons albifrons)

Order: Primates

Family: Cebidae

1) General Zoological Data

Six species are recognized according to Nowak (1999), all from Central or South America and these are further subdivided by Groves (2001). In general, their physiological and pathological parameters appear to be very similar. The evolutionary split of catarrhines and platyrrhines (25-35 MYA) was inferred by Courseaux et al. (2003) from the duplicated euchromatic segments. Many experimental colonies are kept in Primate Research Centers and by private individuals. They are easily trained animals that are sometimes also used to support handicapped persons. Apparent infanticide has been reported by Manson et al. (2004). Adults weigh between 1,000 and 4,000 g and possess a moderately useful prehensile tail (Lemelin, 1995).

White-fronted capuchin monkey at San Diego Zoo.

Mother and infants whose placenta is here described.

2) General Gestational Data

Gestation lasts 160-180 days and ends with the birth of a singleton weighing 200-250 g. Twinning has been reported in 2.4% of captive colonies of C. apella by Leighty et al. (2004). 45% of these twins will die neonatally, as compared to 16% of singletons but subsequently they do well. Longevity is up to 45-55 years. Neonatal growth and other reproductive phenomena have been examined by Fragaszy & Adams-Curtis (1998). Sperm migration through the uterus was approximately one hour (Ortiz et al., 1995).

3) Implantation

This placenta is said to have an antimesometrial implantation but one lobe locates anteriorly, the other on the posterior wall of the unicornuate uterus. Membranous vessels connect the two lobes.

4) General Characterization of the Placenta

I have had one placenta available for study; it weighed 63 g. This was a two-lobed, discoid, hemochorial placenta with long, slender villi, resembling those of spider monkeys. The villi are also referred to as being trabecular. In contrast to the callithricid monkeys, no hematopoietic foci were found in this placenta. The cord inserted marginally on the major lobe and vessels traversed in the membranes to the other lobe. Its appearance is like that described by Soma (1978) and Young (1972). This placenta was meconium-stained, although the neonate survived.

Capuchin placenta, courtesy H. Soma, Tokyo.

Complete cross section of one lobe of capuchin placenta with fetal surface above.

5) Details of fetal/maternal barrier

The surface of the mature villi is covered with syncytiotrophoblast that is bathed in maternal intervillous blood. In the term placenta there is no cytotrophoblast visible although fine-structurally it must be present. The villi contain few macrophages, the "Hofbauer" cells, and are otherwise made of delicate connective tissue.

Capuchin placental relationship to intervillous circulation.

Mature villi surrounded by maternal intervillous blood.

6) Umbilical cord

The capuchin umbilical cord has variable insertion sites. It contains two arteries and two veins, in addition to a small allantoic duct, but smaller vessels as in ungulates are absent. Young 1972) described fusion of the two veins in the middle of the cord in one case. Spatz (1968) found the cord to be 10 cm long. The small ducts, mostly the allantoic duct, may be present but that is apparently very variable. The vitelline duct is usually diminutive.

7) Uteroplacental circulation

No studies are known to me, except that Ramsey (1982) stated that Cebidae do not possess spiral arterioles in the endometrium.

This is from the margin of the capuchin placenta with the degenerating (due to meconium) amnion above. The membranes extend to the right but have no atrophic villi.

8) Extraplacental membranes

The amnion is avascular and it is pressed against the underlying chorion. The amnion is avascular, the chorion carries the large fetal vessels. The amnionic epithelium is single-layered and squamous. Foci of squamous metaplasia may be present. Decidua capsularis was not seen in this placenta and there were no atrophic villi as are seen in the membranes of human placentas. The outer surface of the chorion is covered by a thin layer of cytotrophoblast, so-called "X-cells". There was no allantoic sac in this placenta but Young (1972) reported its presence in 5 of 6 C. apella placentas. Persistent yolk sacs are uncommon, as are remnants of their ducts.

The edematous nature of the membrane and the degenerating amnionic epithelium are due to meconium toxicity.

9) Trophoblast external to barrier

I have not had an implanted placenta available for study. Thus, whether trophoblast invades the deciduas basalis is not known to me; however, Mossman (1987) stated it to be absent. In comparing this placenta with other cebid placentas, the basal infiltration would also have to be a shallow one. In this delivered placenta there was no decidua shed; the "floor" consisted of extravillous trophoblast ("X-cells") only. It was accompanied by some syncytial cells. Ramsey (1982) stated that there is a pronounced "epithelial plaque" at the periphery of cebid placentas; my specimen had merely extravillous trophoblast. This could conceivably be mistaken as epithelium.

10) Endometrium

The decidual transformation is apparently minimal and spiral arterioles are said to be absent (Ramsey, 1982).

Placental floor of delivered placenta; it consists mostly of extravillous trophoblast with little fibrinoid and no decidua.

11) Various features

There are no specific unusual features in capuchin placentas.

12) Endocrinology

The placenta produces chorionic gonadotropin. Postnatal testosterone and the production of other androgens was studied by Rey et al. (1995). An interesting study of adrenal cortisol production was undertaken by Torres-Farfan et al. (2004). They found that fetuses whose mothers are exposed to constant light (and thus induced melatonin suppression) had no effect on fetal DHAS production (as inferred from maternal estradiol levels). Newborns, however, of these mothers had twice as much plasma cortisol. Thus, melatonin (and its regulation by light) affects fetal and neonatal cortisol levels.

The menstrual cycle is 18-22 days long and implantation occurs on day 5 after ovulation (Jones et al., 2001). These authors studied the endometria and found glands deep in the myometrium, and Muc1 expression on epithelial surfaces. A variety of endocrine studies were done on small quantities of urine; thus by Nagle et al. (1979; 1980; 1983; 1989), Lasley et al. (1980), Czekala et al. (1981), Hodges et al. (1979; 1981) and Castellanos & McCombs (1968).

13) Genetics

Capuchin monkeys have usually had 54 chromosomes and they have been studied extensively by de Boer (1974) who provided the chromosomes shown below. The one exception (2n=52 in a C. capucinus ) was studied by Egozcue et al. (1967 – cited by de Boer), but it lacks confirmation to date. Numerous hybrids between the various species were recorded by Gray (1972). Garcia et al. (1999) studied the "constitutive heterochromatin" (C-bands) of capuchins and chimpanzees and compared these with human chromosomes. They found widely scattered amounts of centromeric heterochromatin as opposed to little variation of the noncentromeric regions. In a later study (2002), these authors compared capuchins and spider monkeys with ZOO-FISH. Courseaux et al. (2003) studied segmental chromosome duplications of human #5 and drew evolutionary conclusions. Chiu et al. (1999) described the recruitment of gamma-globin genes in capuchins and marmosets.

Karyotypes of male and female Cebus albifrons (from Hsu & Benirschke, 1975).

14) Immunology

The immunological response to experimental infections has been recorded and is detailed under the next section. Ferrari et al. (2003) found that, while herpes virus (Epstein-Barr) immortalizes T-cells of tamarins, it did not do so in capuchin T-cells.

15) Pathological features

Two capuchins were reported as having oral squamous cell carcinomas (Grana et al., 1992). Renal lesions (glomerulonephritis and pyelonephritis) caused the death of 5 capuchins in Argentina (Borda et al., 2000). A variety of parasites have been identified in capuchins, thus mites from the auditory canal (Guerim et al., 2001) and intestinal nematodes (Durette-Desset et al., 2001). These animals have also been used for experimental studies of Chagas disease with its myocardiopathy (Samudio et al., 1999). The immunological response to the infection was followed precisely in that study. Similarly, leishmaniasis and the immunological response to that experimental infection were topics of study by Garcez et al., (1997; 2001). Griner (1983) found a capuchin to have died from a myocardial infarct. Occasional parasitic infections, respiratory and renal causes of death are also listed.

16) Physiologic data

There is much information on the social aspects, handedness, CNS development and CNS function, and also on various anatomical aspects of capuchin monkeys. It is suggested that the reader look in PubMed for appropriate listings. The hematology and blood chemistry values of C. apella were provided by Riviello & Wirz (2001).

17) Other resources

Some cell strains of capuchin monkeys are available from CRES by contacting Dr. Oliver Ryder at oryder@ucsd.edu.

18) Other remarks – What additional Information is needed?

Early implantation stages have not been recorded to my knowledge.

Acknowledgement

The animal photographs in this chapter come from the Zoological Society of San Diego. I am grateful to Dr. Hiroaki Soma for allowing me to show the macroscopic picture of the placenta he published in 1978.