Hanuman Langur Presbytis (Semnopithecus) entellus

Order: Primates

Family: Cercopithecidae

1) General Zoological Data

There are 15 species of Presbytis, according to Nowak (1999), all distributed over southern Asia. Hanuman langurs form large groups in India and in several adjacent countries. They are mostly folivorous and inhabit trees but they also walk often on the ground as well. The designation Semnopithecus is preferred by some, but Presbytis is perhaps even more frequently used as well. Nowak (1999) stated that Hanuman langurs are now endangered because of an encroaching human expansion. Many zoos have kept this species, at least for some time, but their maintenance has its challenges and the colonies have often died out. Often this can be attributed to their folivory and inadequate food supply. Gotch (1979) stated that "Hanuman" is a Hindu word for a monkey god. Presbytis refers to an old man, while entellus comes from a figure in Virgil's Aeneid.

Family group of Hanuman langurs at San Diego Zoo's Wild Animal Park. Note the extraordinary length of the tails.

2) General Gestational Data

The estrous cycle is 24 - 30 days and estrus lasts 5-6 days. Births occur at any time during the year. Gestation is from 190-210 days (Roonwal & Mohnot, 1977). Singleton births are the rule, but twins have also been observed. The weight at birth is around 500 g, and longevity may be beyond 25 years (Nowak, 1999).

3) Implantation

I am not aware of any studies of early implantations in Hanuman langurs. Those for Douc langurs and, especially for the rhesus monkey, can be found under the relevant chapters. Burton (1980), on the other hand, had the opportunity of studying two Presbytis obscura(Dusky Leaf Monkeys) uteri in early gestations and also referred to an old publication by Selenka. Placentation in that species is likely to be similar to the Hanuman langur gestation, thus these may be guide posts. The large size of the blastocyst and its superficial nature of implantation were highlights of the observations by Burton (1980). He also remarked on the then still absent decidualization and highlighted the proliferation of endometrium lateral to the invasion of trophoblast. Cytotrophoblast is also described as infiltrating superficial maternal blood vessels.

4) General Characterization of the Placenta

I have had over 20 Hanuman langur placentas available for study; some came from term gestations, a few were from spontaneous abortions. Some placentas were bilobed, a few had only a single lobe. All placentas had some old infarcted lesions. Normally, I expect that this animal would have a bilobed placenta, with the umbilical cord inserting on the larger lobe. The absence of a second lobe also occurs in about 15% of rhesus monkeys (see that chapter) and usually does not threaten the gestation. The average lobe of the placenta measures 8 -12 cm in diameter at term and is between 0.5 and 1 cm in thickness. The combined weight of the lobes, without cords and membranes, is given in the table that follows (see also Benirschke, 1982).

This is a villous placenta with hemochorial relation to the maternal system.

Bilobed immature placenta of Hanuman langur, with cord insertion on the larger left lobe.

Cross sections of mature Hanuman langur placenta showing the large number of infarcts, not unusual and not leading to fetal demise.

5) Details of fetal/maternal barrier

This is a mono-hemochorial relationship with the maternal blood surrounding all villi, very similar to the placenta of other catarrhine monkeys. The villi are covered mostly by syncytiotrophoblast; occasional cytotrophoblastic cells lie beneath the syncytium and border the basement membrane. Syncytial "knots" (or sprouts) occur frequently and are prominent at term. They may detach and be swept away in the intervillous maternal blood, as is normally the case in human placentas.

Immature villi of Hanuman placenta showing nucleated red blood cells in the fetal capillaries.

Base of implanted immature placenta, PAS stain. A broad villous connection (by extravillous trophoblast) anchors the villi to the fibrinoid of Nitabuch.

Same placenta at higher magnification. The avascular villous cores are covered with fibrinoid rather than trophoblast in the anchoring site.

Same section in Giemsa stain. Note that there is virtually no decidual penetration by trophoblast.

6) Umbilical cord

The umbilical cord of Hanuman langurs has normally three blood vessels, 2 arteries and one vein, and there is no patent allantoic duct. Occasionally, single umbilical arteries occur, as is true of +/- 1% of human placentas. Rarely, atrophied remnants of the allantoic duct may be found. There is no surface squamous metaplasia. The variety of observed cord lengths in my material will be seen in the preceding table. Other observations are available in Bolk's contribution (1900) and the paper by Starck (1957).

Cross section of typical umbilical cord of Hanuman langur. Vein is at top left.

7) Uteroplacental circulation

No special studies have been conducted in langurs, but it is reasonable to assume this to be very similar to the vascular supply of rhesus monkeys which is reviewed in that chapter. Occasional major maternal arteries in the decidua basalis have infiltration with cytotrophoblast, as is shown next. No really extensive modulation of maternal vessels occurs, however.

Large uterine decidual artery with minimal cytotrophoblast infiltration at its outside.

8) Extraplacental membranes

Burton (1980) stated that there is no decidual transformation in the young placentations he observed in Presbytis obscura. There is, however, extensive decidual transformation in mature placentas and I have been repeatedly surprised at the large quantity of decidua capsularis in the membrane rolls that were prepared from placentas. As is true in other cercopithecids, there are no atrophying villi in the membrane rolls' decidua capsularis, as are common features of ape and human placentas. The decidua capsularis is rich in vessels and endometrial glands and it contains no evidence of trophoblast infiltration. The amnion is thin and avascular. The epithelium is single-layered and lacks squamous metaplasia. There is no allantoic sac. The yolk sac does not persist.

Membrane roll and sections of umbilical cords of Hanuman langur. The large vessels that cross between lobes are seen in the membrane roll.

A "membrane roll" of the free membranes between disks. Note the thick decidua capsularis and absence of atrophied villi. Amnion is outside.

Membranes under higher magnification. Amnionic epithelium at top, with its avascular connective tissue, artifactually separated from the thin chorion which is underlain by a very small layer of cytotrophoblast. Most of the tissue is highly vascular decidua capsularis.

9) Trophoblast external to barrier

There is virtually no trophoblastic infiltration of the decidua basalis. Only very few trophoblastic cells are found in the maternal vessels that supply the intervillous space. Such an infiltration is commented upon only in the early implantation stages of Presbytis obscura that Burton (1980) was able to study.

10) Endometrium

As mentioned earlier, Burton (1980) found little decidual transformation around the implantation site in early gestation. He remarked on the extensive endometrial secretory activity adjacent, but not below the implantation site and on the adjacent endometrial proliferation. In later gestation, however, there is extensive decidual transformation that is especially evident in the decidua capsularis of the membrane rolls.

11) Various features

There is no subplacenta.

12) Endocrinology

David & Ramaswami (1969) studied the menstrual cycle over many cycles and found it to vary widely in length, with an average of 26.8 days. They correlated this also with vulvar swelling and vaginal cornification. Progesterone metabolites were ascertained in the urine of cycling and pregnant Hanuman langurs by Shandilya et al. (1976a). Pregnanediol was the principal metabolite during pregnancy and it rose a day after ovulation and reached its peak on day 17 of the cycle. All three major estrogens were identified in the urine of cycling and pregnant langurs (Shandilya et al., 1976b). All rose significantly during gestation. Sialic acid levels were determined in various reproductive organs of male and female langurs in an effort to pinpoint the day of ovulation (Shandilya et at., 1977). It was not truly effective in doing so. Ramaswami (1975), in a comprehensive review of Hanuman langur reproductive biology, stated that there is a "pregnancy Presbytis gonadotropin", but gave no further details and levels are not yet known. Maston & Ruvola (2002) studied the genes for the subunits of chorionic gonadotropin and found that man has 7 unique clones, while Presbytis has 6. They also provided a tree for the evolution of the LH ß duplication, the CGß gene, and derived macacs and colobines as a group from a common ancestor.

13) Genetics

Presbytis spp. all have 44 chromosomes that are very similar among the various species; an example of Presbytis senex, the purple-faced langur, is shown following the one on Hanuman langurs (Hsu & Benirschke, 1977; see also Zneimer et al., 1979; Sharma & Kakati, 1967). A number of hybrids have been alluded to, but few have lived long enough to ascertain their possible fertility (Gray, 1972), at least this is not remarked upon. Sharma & Gupta (1973) suggested an autosomal/X-chromosomal translocation to have occurred in a specimen they studied; the photograph, however, is not convincing. Banding studies of two Presbytis species and macacs were published by Ponsa et al. (1983).

Karyotypes of male and female Presbytis entellus, 2n-44.

Karyotypes of male and female Presbytis senex.

14) Immunology

I know of no studies other than the serologic surveys of experimental nature reviewed in the next section.

15) Pathological features

There has been an active breeding colony of Hanumans at San Diego Zoo's Wild Animal Park in the past. A significant problem there had been the occurrence of intestinal perforation with peritonitis. It was attributed to the spines of Acacia salignum, a plant the animals loved to consume; but they suffered the peritonitis. Since discontinuing this diet, the problem disappeared (Ensley et al., 1982). A few cases of stillbirth and abortion have occurred, almost all of them associated with major placental infarction. Additionally, villitis of unknown etiology ("VUE") has occurred, and we have also seen acute villitis due to bacilli. VUE is a relatively common entity that leads to growth restriction in human gestations and is currently not fully understood (Benirschke & Kaufmann, 2000). Griner (1983) described an insignificant cestode infestation, lobar pneumonia, and glomerulosclerosis in his review of primate mortality at San Diego Zoo. Walker et al. (1973) were able to show in Presbytis cristatus the induction of scrub typhus with rickettsemia but no development of antibodies. They conjectured that this tree-dwelling species was more susceptible than other monkeys because of their lack of exposure to the vector. Mycobacterium bovis was isolated from a dusky langur (Presbytis obscurus) with splenic and intestinal lesions (Himes et al., 1982). The infection was acquired from a group of newly imported fennec foxes that were housed in the same facility. Benveniste & Todaro (1977) isolated a d-type retrovirus from the genome of two langur species. David and Ramaswami (1967) reported right renal hypoplasia in a female animal. Scott (1992) depicted acute myocarditis (Fig. 7.2) and old pleurisy (Fig. 7.3) in langurs.

Typical, sharply circumscribed infarct (left) of term Hanuman langur placenta.

Decidua basalis with large maternal blood vessel showing fibrinoid replacement of its muscular wall. This is similar to minor changes of the decidual arteriopathy in cases of human pre-eclampsia.

Chronic villitis ("VUE") of langur placenta.

Acute necrotizing villitis in langur villi, Gram stain. Not black organisms and necrosis of villous core. Fetal demise.

Acute, infectious villitis and "intervillositis" in abortus.

Complete hyalinization of villi in stillborn, aborted Hanuman langur gestation.

Complete cross section through the immature placenta of abortion specimen; no cause was identified. Chorion is above.

16) Physiologic data

Most important for the maintenance of langurs in captivity has been their unusual (leaf-demanding) diet. This has been one reason for the difficulty of maintaining many species of these langurs in captivity, and to keep them healthy. Bauchop & Martucci (1968) made the most important observations regarding this matter. While it had been known that the stomach contents of the leaf-eaters may weigh as much as 15-20% of the body weight and that their abdomens are often markedly protuberant, the true ruminant-like digestion of leaves had not been appreciated before their study. They showed that the stomach is partitioned and that there is a typical groove ("Magenstrasse"), not unlike that of ruminants. But these monkeys do not ruminate. Huge numbers of specific anaerobic, and few aerobic bacteria digest the leafy material and produce volatile fatty acids, probably their most important energy requirement. These authors also suggested from their experiments that fresh alfalfa was eagerly consumed and that animals subsequently thrived on it after initial starvation.

The maintenance under laboratory conditions has also been explored for the silvered leaf monkey, Presbytis cristatus, by Walker et al. (1974). Diarrhea, often due to salmonellosis, was their main concern, but methemoglobinemia also occurred. Various hematologic values are available in that publication. David & Ramaswami (1971) described in considerable detail the reproductive organs of males and females and noted the similarity to the human anatomy in several systems. The ovulation apparently is associated with considerable hemorrhage and the blood is contained in the cystic corpus luteum (Ramaswami, 1975). He also stated that, unlike the rhesus monkey, the cervix is straight and not spiraled.

17) Other resources

Several cell strains of Hanuman langurs are available from CRES at San Diego Zoo by contacting Dr. Oliver Ryder at oryder@ucsd.edu.

18) Other remarks - What additional information is needed?

The reason for the frequent occurrence of placental infarcts is currently not understood although minor vascular changes occur. Early stages of implantation and placental development of Hanuman langurs are lacking. Better knowledge of the endocrine status of gestation, especially of gonadotropins, would be helpful.

Acknowledgement

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