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Ruffed Lemur Species
Varecia variegata

Order: Primates
Family: Lemuridae

1) General zoological data of species

There are numerous lemur species, all from Madagascar (Malagasy Republic) or from the Comoro Islands. They vary greatly in appearance but the surviving species vary only slightly in size. Many species have become extinct in the recent past (Ziswiler, 1967). I have had experience with ruffed lemurs, (Varecia spp.), ring-tailed lemurs (Lemur catta), and with black lemurs (Lemur macaco). Their placentation is generally similar and for that reason only one species will be dealt with here in some detail.

All lemurs are significantly endangered. This is one reason why so many breeding colonies exist in zoos of various countries. Most notably, lemurs are well represented in the Vincennes Zoo of Paris and at the Primate Research Center of Duke University, Durham, North Carolina. There are some exceptionally rare species at those locations. The management of lemurs in captivity has been aptly discussed by Puschmann (1989).

The body weight of lemurs is around 2,000 g; they have long tails and thick fur. Lemurs are mostly arboreal forest dwellers (Nowak & Paradiso, 1983) and most are primarily diurnally active; a few other species not discussed here are more nocturnal. They often occur in sizeable groups and are largely vegetarian. There is an abundant literature on these well-studied prosimians.

2) General gestational data

In Madagascar (Malagasy Republic), lemurs mate from April to June and have a gestational length of about 4½ months (black lemurs 127 days; ring-tailed lemurs 136 days or less; ruffed lemurs 90-102 days). The ruffed lemurs (Varecia spp.) have been grouped with the genus Lemur in the past but now they are separated as comprising a different genus, Varecia. They are also somewhat heavier than most of the other species. The estrous cycle is 30 days in length in ring-tailed lemurs, with estrus around 6 days. Multiple offspring are much more common in ruffed lemurs, while singletons are the rule in ring-tailed lemurs. Longevity of ring-tailed lemurs is 19 years (Bogart et al., 1977).

The litter size varies appreciably, especially in ruffed lemurs where triplets and quadruplets occur. The weight of the placenta in ruffed lemur is around 20 g (perhaps incomplete) and the placenta has a diameter of 3.5 x 1.5 cm and is 1 cm in thickness. The newborns weigh around 80-90 g, while "cattas" (ring-tailed lemurs) weigh only 15-20 g at birth with a placenta of about 7-8 g.
  Black and white ruffed lemur (Varecia variegatus).
3) Implantation

Early embryonic/placental stages of these species have not been described. Mossman (1987), however, suggested that implantation occurs in an antimesometrial location. The final location of the diffuse lemur placenta is one throughout the bicornuate uterus.
  Delivered placenta of black and white ruffed lemur. At left is the cervical area (C).
  Terminal villi of mature placenta from black and white ruffed lemur. Note the peripheralization of fetal capillaries beneath the single-layered trophoblast
  Complete cross sections of mature placenta from black and white ruffed lemur.
  The maternal myometrium.
4) General characteristics of placenta

Lemurs have a diffuse, villous placenta that occupies the entire bicornuate uterus. The nidation is superficial (Mossman, 1987). Their placenta is epitheliochorial and it has a large allantoic sac. There is no invasive trophoblast.

5) Details of barrier structure

This is a typical epithelio-chorial type of placentation with villi merely approximating the uterine epithelium. They are superficially attached to the undamaged uterine epithelium. The trophoblastic surface of villi is underlain by a capillary network.

  Trophoblastic surface beneath the chorionic plate of lemur.
6) Umbilical cord

The umbilical cord contains three blood vessels. In addition there is a large allantoic duct that connects the bladder with the allantoic sac. It is a short cord, about 10 cm in length and 0.3 cm in width. Cords may have some keratiniziation of the amnionic surface.
  Cross-section of mature lemur umbilical cord. Two arteries, one vein and a large allantoic duct.
7) Uteroplacental circulation

There is no description of these features in the literature.

8) Extraplacental membranes

A large allantoic sac is present that is connected to the bladder by a wide allantoic duct of the umbilical cord. Since this is a diffuse placenta, there are no free membranes. Thus, there is also no decidua capsularis.

  Membranes with amnion at left. It exhibits some squamous metaplasia. The thin allantois is at right and its membrane carries the allantoic blood vessels. Numerous pigmented macrophages are present in these membranes.
9) Trophoblast external to barrier

There is no extravillous trophoblast, and giant cells are not present. There is also no maternal vascular trophoblastic infiltration or invasion.

10) Endometrium

There is no decidualization of the endometrium. In postpartum uteri, hemosiderin granules are found in the endometrium.

11) Various features

There is neither subplacenta nor evidence of metrial glands.

12) Endocrinology

No gonadotropins have been identified in lemurs.
Urinary estrogens were monitored during pregnancy by Shideler et al. (1983). Total urinary estrogen excretion rose significantly during gestation until they reached values 1,000 times of those at estrus. Estrone was the major secretory product.

13) Genetics

The chromosome number of lemurs is variable; some are here listed: Lemur catta 2n=56; Lemur coronatus 2n=46; Lemur fulvus albifrons 2n=60; Lemur f. fulvus 2n=48; Lemur macaco 2n=44; Varecia variegata 2n=46; Hapalemur g. griseus 2n=54; Hapalemur griseus olivaceus 2n=58; Cheirogaleus major 2n=66; Cheirogaleus medius 2n=66 (Hsu & Benirschke, 1975).

Hybrids of many lemur species have been recorded by Gray (1972). The two ruffed lemur species (red and the black & white ruffed lemurs) hybridize fertilely in captivity. Among the other lemuridae, the hybrids have not been recorded as being fertile.
A variety of genetic diseases have been described in ruffed lemurs. Naked lemurs (hairless) have occurred in a London colony. We have described "sunken chest" (Pectus excavatum) as an inherited deformity with little illness. Massive skeletal abnormalities may also be inherited.

14) Immunology

I know of no studies that relate to immunological investigations.

15) Pathological features

In captivity, lemurs often develop generalized hemosiderosis and, consequent to hepatic fibrosis, they may suffer from neoplasms of the liver and bile ducts. These afflictions have been attributed to a greater avidity for iron absorption, as apparently they are unknown in freshly captured animals (Gonzales et al., 1984).

Pectus excavatum is inherited in ruffed lemurs, and so may be their multiple skeletal anomalies that have been observed in our colony. We have also seen an acute bacterial infection of the pregnant uterus with acute villitis and death of the superficial endometrium (Benirschke et al., 1985). Worley & Stalis (2002) identified a hepadnavirus in the livers of two black and white ruffed lemurs that died with acute hepatitus.

Although we have often looked for parasites, we have not detected any in the three species studied.

16) Physiological data

I know of no blood flow studies before and during pregnancy. We have studied the absorption of iron in ruffed lemurs and found the ruffed lemur to have a great avidity for dietary iron. This, we interpreted to be the result of their dependence in nature on tannic acid-containing food such as tamarind fruit (Gonzales et al., 1984). Administration of tea instead of water has reduced this problem in captivity.

17) Other resources

Cell strains of many species of lemurs and related taxa are available from CRES at the Zoological Society of San Diego.

18) Other data to be accumulated

It would be of interest to know whether all lemurs have the same placentation with allantoic sacs. There is need for a better understanding of the genetics of the congenital anomalies we observed including their possible relationship to inbreeding.


CRES at: http://www.sandiegozoo.org/conservation/cres_home.html. Please direct your inquiries to Dr. Oliver Ryder (oryder@ucsd.edu).

Benirschke, K.: Pectus excavatum in ruffed lemurs (Lemur [Varecia] variegatus). XXII Internatl. Symp. über die Erkrankungen der Zootiere. Arnhem, Holland, May. Akademie-Verlag, Berlin, pp. 169-172, 1980.

Benirschke, K., Kumamoto, A.T. and Bogart, M.H.: Congenital anomalies in Lemur variegatus. J. Med. Primatol. 10:38-45, 1981.

Benirschke, K. and Miller, C.J.: Weights and neonatal growth of ring-tailed lemurs (Lemur catta) and ruffed lemurs (Lemur variegatus). J. Zoo Anim. Med. 12:107-111, 1981.

Benirschke, K., Miller, C., Ippen, R. and Heldstab, A.: The pathology of prosimians, especially lemurs. In: Advances in Veterinary Sciences and Comparative Medicine. Vol. 30. Academic Press, Inc. pp. 167-208, 1985.

Bogart, M.H., Cooper, R.W. and Benirschke, K.: Reproductive studies of Lemur m. macaco, Lemur variegatus subcinctus and Lemur v. ruber. Internat. Zoo Yrbk. 17:177-182, 1977.

Gonzales, J., Benirschke, K., Saltman, P., Roberts, J. and Robinson, P.T.: Hemosiderosis in lemurs. Zoo Biol. 3:255-265, 1984.

Gray, A.P.: Mammalian Hybrids. Second edition. A Check-List with Bibliography. Commonwealth Agricultural Bureaux, Farnham Royal, Slough, UK, 1972.

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

Mossman, H.W.: Vertebrate Fetal Membranes. MacMillan, Hound mills, UK, 1987.

Nowak, R.M. and Paradiso, J.L.: Walker's Mammals of the World, Vol. II. 4th edition. The Johns Hopkins University Press, 1983.

Puschmann, W.: Zootierhaltung. Vol. 2 Säugetiere. VEB Deutscher Landwirtschaftsverlag, Berlin, 1989.

Shideler, S.E., Czekala, N.M., Benirschke, K. and Lasley, B.L.: Urinary estrogens during pregnancy of the ruffed lemur (Lemur variegatus). Biol. Reprod. 28:963-969, 1983.

Worley, M.B. and Stalis, I.H.: Detection of virus-like particles in the liver of black an white ruffed lemurs with hepatitis. J. Wildl. Dis. 38:258-265, 2002.

Ziswiler, V.: Extinct and Vanishing Animals. Springer-Verlag, New York, 1967.

Other lemur species from the San Diego Zoo

  Ring-tailed lemur (Lemur catta).
  Red ruffed lemur (Lemur/Varecia variegatus ruber).
  Black lemur (Lemur macaco), male is black, female is pale.
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