Comparative Placentation

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Squirrel Monkey
Saimiri sciureus

Order: Primates
Family: Cebidae

1) General Zoological Data

The squirrel monkey is widely used in research and has been classified as comprising 5 separate species by Wilson & Reeder (1992). Numerous subspecies or different names have been employed for this animal whose phenotype can differ appreciably between animals from different regions of the Amazon basin. There is also controversy, as some authors have comprised all squirrel monkeys in one species. The variability of karyotypes alone (deBoer, 1974) argues against such simplification, however. A more recent splitting of the group has been provided by Groves (2001) who gives detailed description of their phenotypes and distribution. Gotch (1979) stated that the name "Saimiri" derives from the Brazilian/Portuguese for small monkey.

This small South American cebid monkey weighs up to 1,000 g, is arboreal prefers insects, small reptiles and birds as well as fruit (see Lima & Ferrari, 2003), and is a diurnal animal. It associates in relatively large groups (over 100 animals) in the tropical rainforest and rarely comes to the floor of the forest. It is endowed with one of the largest brains for body size in primates (1/9th is CNS) and has been widely used in numerous experimental protocols. It has been useful especially in neural studies and for research into parasitology and virology. Many Primate Research Centers employ this anima for research, and so do many private laboratories. There is a huge literature on the results of many biological studies conducted in this species that has seen marked reduction in the wild and some subspecies of which are endangered now. Hof et al. (2002) who wrote about CNS aging of primates suggested that squirrel monkeys live more than 25 years.

	Squirrel monkey at San Diego Zoo.

	Squirrel monkey at San Diego Zoo.

2) General Gestational Data

Gestation lasts from 146-175 days and produces generally a single young. Twins are very uncommon. The newborn of this gestation weighed 140 g, but Hayssen et al. (1993) mentioned size up to 247 g.

3) Implantation

Dukelow et al. (1983) spent much effort to define the growth of preimplantation oocytes growth and effects on cleavage if in vitro fertilization after superovulation (16 h post hCG). They found no significantly increased aneuploidy as result of their manipulations. I have been unable to find publications on early implantation in this widely used species.

4) General Characterization of the Placenta

I have had only one delivered placenta available from a term infant that died neonatally. In addition, slides of a serially-sectioned implanted placenta were reviewed. The two placental disks, characteristic for this species and other cebidae, weighed 22 g and measured 5x4x0.5 cm each. Their surface vasculature was connected around the lateral aspect of the free membranes. This is a trabecular/villous placenta with hemochorial relationship to the maternal circulation. While Mossman (1987) mentioned the existence of villous hematopoiesis, none was found in the specimens I examined. The disks are infiltrated by a few large maternal arteries that have stiff walls, infiltrated by fibrinoid and are surrounded by syncytium (Luckett, 1974; Gruenwald, 1972).

	Complete lobe of squirrel monkey placenta with membrane carrying connecting vessel at right.

	The other disk of the same placenta, slightly thicker. Amnion at top.

5) Details of fetal/maternal barrier

The slender villi are covered by syncytiotrophoblast as seen in the next photograph. While there is cytotrophoblast below the syncytium, at term it is so delicate that it cannot be demonstrated.

Trabecular villous tissue of term squirrel monkey placenta. The large amount of closely placed syncytium is obvious.

6) Umbilical cord

The cord inserts near the center of one of the two disks. While this disk is often larger than the second one, that was not the case in this placenta. The cord had no twists and possessed two arteries, one vein and no ducts. It is covered by a very thin amnion. The length of umbilical cords in Saimiri was given as 8.5 cm by Spatz (1968).

7) Uteroplacental circulation

I am not aware of any fundamental research into the uterine vasculature of this species, other than the descriptions of flow to the placenta shown above.

8) Extraplacental membranes

The free membranes connecting the disks lack atrophied villi, unlike the condition in the human placenta. This, however, has been the case in most bilobed primate placentas. It carries the connecting vessels laterally between the two disks. The membranes have an inner single layer of epithelium without squamous metaplasia that is planted on a thin layer of connective tissue. It is loosely attached to the chorionic membrane that carries the blood vessels. Outside of the chorion is a small layer of cytotrophoblast and a very minimal amount of decidua capsularis. There are no vitelline or allantoic remnants.

	Membranes between lobes.

	Interconnecting blood vessel in the chorion between the two lobes.

9) Trophoblast external to barrier

Cytotrophoblast, equivalent to the "extravillous trophoblast" of human gestations superficially invades the decidua beneath the two disks and is also found to alter the maternal arterioles in a manner very similar to human placental sites. Deeper invasion does not occur.

Maternal spiral arteriole in decidua basalis. It shows infiltration of trophoblast with partial replacement of its wall.

10) Endometrium

There is complete decidual transformation of the endometrium and relatively few extravillous trophoblastic cells can be found deep in the endometrium. At the site of connection to the endometrium, numerous vacuolated extravillous trophoblastic cells are present intermixed with a small amount of fibrinoid.

Squirrel monkeys have no menstruation; instead, there is a well-defined estrus cycle. Ovaries have a large amount of interstitial gland tissue (Mossman & Duke, 1973).

The large central maternal artery referred to earlier is seen in the center above the site of implantation.

11) Various features

There is no subplacenta. The absence of atrophied villi in the free membranes remains unexplained.

12) Endocrinology

Wolf et al. (1977) studied the reproductive cycles and Tullner (1972) reviewed pregnancy hormones. Positive gonadotropin tests were obtained from 3-16 weeks of gestation. Urinary gonadotropins were positive for 7-8 weeks (see also Hodgen, 1979). Ainsworth et al. (1969) incubated squirrel monkey placental tissue with precursors and identified production of estrone and estradiol from androstenedione precursors and conversion of pregnenolone to progesterone. Davidson et al. (1979) described the exceptional seasonality of reproductive behavior in squirrel monkeys and the reaction of male testosterone levels on females.

13) Genetics

Squirrel monkeys have 44 chromosomes, but their fine details differ in animals from different regions. Thus, in the karyotypes shown below (Hsu & Benirschke, 1973), the male with 12 acrocentrics came from Leticia (Columbia), while the female with 10 acrocentrics was from Iquitos (Peru). Other variations have been delineated by deBoer (1974) and affect mostly the position of centromeres, i.e. the number of acrocentrics. Stanyon et al. (2000) who examined platyrrhines with chromosome paints suggested that many of the former banding interpretations and putative homologies to human chromosomes have to be re-evaluated. The same investigators (Neusser et al., 2001) later linked the squirrel monkey as a sister group to callithricids, as they share one derived syntenic association.

Hybrids have not been described to my knowledge and no direct crosses between the different cytotypes are known to me. It had once been speculated that the endangered Panamanian species (Saimiri oerstedii) might have been introduced or be a hybrid. The study by Cropp & Boinski (2000) has excluded this speculation.

Male and female karyotypes of animals from different regions (see text) and having different numbers of acrocentric.

14) Immunology

It is likely that such studies have been performed in Primate Research Centers, but I have not been able to access fundamental information.

15) Pathological features

The most important pathologic feature of squirrel monkeys undoubtedly is that all animals are infected with the Herpesvirus saimiri. This virus is not pathogenic for squirrel monkeys but, as was early recognized (Hunt et al., 1970), it causes usually fatal T-cell lymphoma in other primates, especially marmosets. Therefore, these animals should not be housed together. A detailed review of the genome and all other aspects of this virus are available from Fickenscher & Fleckenstein (2001). More recently, this virus is being considered as a potential agent for gene delivery into cells (Whitehouse, 2003).

Scott (1992) referred to a gastric carcinoma in a squirrel monkey; also a breast cancer was found in a male. Borda et al. (2000) described that 35% of Bolivian squirrel monkeys suffer a proliferative glomerulonephritis with deposits of immunoglobulins. Several squirrel monkeys were found to suffer an infectious gastritis, but Helicobacter pylori was not found (Khanolkar-Gaitonde et al., 2000).

Many animals are infected with a variety of trypanosome, including T. cruzi, and Ndao et al. (2000) caution handlers of New World monkeys to be cognizant of these parasites, as they can easily be infected by handling them or their products. Horizontal transmission of the lethal infection with Toxoplasma gondii was clearly demonstrated by Furuta et al. (2001). Squirrel monkeys have often been used for the study of malaria and with hopes of vaccine production. While infection may be achieved with some plasmodial species, they generally do not produce infectious gametocytes. More recently, Sullivan et al. (2003) showed that infection with Plasmodium inui shortti can infect the animals and produce gametocytes as well.

16) Physiologic data

Numerous physiological data are available. Thus, the diet of free-ranging monkeys was studied by Lima & Ferrari (2003); allelic frequency for x-linked color vision was studied in two species by Cropp et al. (2002); ABO blood groups were described by Corvelo et al. (2002). Squirrel monkeys exhibited group A (# 67) and AB (# 7). Cortisol secretion was determined by sampling saliva in chewed string of unrestrained squirrel monkeys by Tiefenbacher et al. (2003). They found the expected rise after SCTH and also determined normal daily rhythms. Numerous parameters of physiological importance (size, life span, hematology, seminal volume etc.) have been summarized and compared with other taxa in a table by Mather & Rushmer (1979).

17) Other resources

Cell lines were established by Scammell et al. (2001) and, later (2002) the same authors made a renal cell line because of the paucity of such material available for research. But the line was hyperdiploid (2n=52-57).

18) Other remarks - What additional Information is needed?

Descriptions of early implantation are virtually absent.

Acknowledgement

The animal photographs in this chapter come from the Zoological Society of San Diego.

References

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