Comparative Placentation

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updated:

July 4, 2002

Bongo
Tragelaphus eurycerus

Order: Artiodactyla
Family: Bovidae

1) General Zoological Data

Among the genus Tragelaphus (from Gr. tragos=he-goat, and elaphos=deer) with six species of the subgenus Tragelaphus, the bongo is the only member of the subgenus Boocerus. Occasionally, Boocerus eurycerus (eurus=broad, and keras=horn) is used as its species designation. This beautiful, large, striped brown East African antelope may weigh up to 220 kg. Males are significantly darker than females, and both sexes have slightly spiraled horns. It lives in dense forested regions (hence "Woodbucks") and is a browsing animal that makes up occasionally sizeable groups. The estrous cycle is described as being 21-22 days, with estrus lasting 3 days. The gestational length is between 282 and 287 days long, with single offspring weighing 18-22 kg born. First pregnancy is described as occurring at 27 months, and the longevity in captivity is 19+ years. Two subspecies are listed by Nowak (1999). Numerous animals are being bred well in several zoological gardens, including the San Diego Zoo. Although the animal is not endangered, it is not frequently seen. The relation between the Tragelaphinae was studied with an evaluation of the cytochrome b gene (Matthee & Robinson, 1999). These authors found no justification for the generic status of Boocerus. Ralls (1978), who published a detailed review of this species, stated that no direct antecedent to this species is known from the fossil record. She suggested that it represents a recent lineage of tragelaphines. Tragelaphinae may have derived from presumed common ancestors with the nilgai and may subsequently have immigrated to Africa from Asia. Their ultimate origin is still disputed, however. Speculations and recent findings are summarized by Thenius (1969). Petit et al. (1994) have constructed a putative phylogeny from their cytogenetic findings. As many other species of African antelopes, bongos have an unusual chromosomal structure. Tragelaphines possess a fusion between the Y-chromosome and a common (#13) autosome.

		Bongos at the San Diego Zoo.

		Bongos at the San Diego Zoo.

2) General Gestational Data

The singleton newborn weighs around 20 kg. While twins may occur, I am not aware of any reports, and Ralls (1978) also rules out the possibility of twins. Gestational length has been studied by Xanten (1972). It is around 280+ days in length. Bent & Reason (1998) found that more female than male calves were born in captivity.

Successful embryo transfer of bongo blastocysts into the common eland (Taurotragus oryx) has been reported by Dresser (1986).

3) Implantation

Early stages of implantation and placental development have not been recorded to my knowledge.

4) General Characterization of the Placenta

The placenta displayed in the next photographs comes from the delivery of a stillborn term calf that died during delivery from dystocia. The placenta is polycotyledonary with 125 cotyledons. These are arranged in four major rows. They measured between 2 and 10 cm in diameters, and 0.5 cm in thickness. Toward the tubal ends of the sac, the cotyledons became progressively smaller. Most were pale, while 1/3 was deeply congested. The placenta weighed 1,340 kg and measured 155 cm in greatest length and 83 cm in greatest diameter. The female stillborn calf was also unusually heavy (24.5 kg). Another placenta received fresh weighed 1,600 g and had 153 large cotyledons. It was similar in other respects.

		Delivered bongo placenta, maternal aspect. Note the four rows of cotyledons.

		Another bongo placenta, more elongate and showing cotyledons with much different colors (stillbirth).

		Higher magnification of the cotyledons with congestion and other without blood.

		Amnionic surface of this stillborn's placenta with numerous finely granular, yellow, areas of squamous metaplasia.

Hradecky et al. (1987) compared the structure of cotyledons and villi of various artiodactyl species, including those of eland and bongo. The number of cotyledons was similar to that reported here, and the villous structure of eland and bongo was sufficiently similar to explain the successful embryo transfer among these animals. They emphasized that one needs to study villi of specified regions in the cotyledons for meaningful comparisons. The villi were described as being 10 mm long, slightly branched and covered with a cuboidal trophoblast. In subsequent contributions, these authors provided better morphologic descriptions and illustrations of the varied species' placentas (1988). They emphasized that, while the basic structure and development of cotyledons of bovids is very similar, differences in structure exist that need to be considered for potential embryo transfers.

Aside from the cuboidal trophoblast that covers the villi, binucleate cells are abundant. This special type of trophoblast was discussed extensively in the chapter on sheep.

		Single cotyledon of delivered term bongo placenta with chorionic surface.

		Cross-section of cotyledonary surface of term bongo placenta. Moderate branching of villi is evident.

		Term bongo placental surface villous architecture.

	5) Details of fetal/maternal barrier This is a typical epitheliochorial placenta. No significant differences exist to other ruminants.

		Higher magnification of trophoblastic surface of the villi. The binucleate cells are labeled, as are the fetal capillaries.

		Moderate magnification of term villous structure of bongo placenta.

		Villous branching of term bongo placenta.

6) Umbilical cord

The umbilical cord of one animal measured 10 cm in length (complete), contained four large blood vessels and a large allantoic duct. Verrucae are present on the cord's surface and consist of areas of squamous metaplasia. There is an abundance of smaller allantoic vessels scattered throughout the umbilical cord, many with heavy muscular coats. It is common to see these additional blood vessels emerging from the main blood vessels. The allantoic duct has a seemingly separate, thinner-walled vasculature. Its epithelium is transitional in appearance. This umbilical cord had no spirals.

		Portion of bongo umbilical cord with large allantoic vessel above, numerous small vessels and the allantoic duct.

7) Uteroplacental circulation

I am not aware of any detailed studies concerning the vasculature of uterus or placenta.

8) Extraplacental membranes

The amnionic sac is considerably smaller than the chorioallantoic sac. Its surface is studded with many areas of squamous metaplasia. The allantoic membrane (but not the amnion) has a delicate vasculature. There are no "free" membranes, other than those between the cotyledons. There is no decidua capsularis.

		Membranes with amnion and allantois.

	9) Trophoblast external to barrier There is no invasion of the uterus by trophoblast, so far as is known to date. 10) Endometrium The endometrium has typical caruncles that are arranged in parallel rows, as shown in the neonatal uterus of the specimen available to me.

		This is the opened uterine horn of a neonatal Bongo that displays the abundance of endometrial "caruncles" as yellow-green elevations.

		Histology of fetal uterus with caruncles at "C" and myometrium at "M".

11) Various features

The uterus is typically bicornuate. Placentophagy is common.

12) Endocrinology

The neonate I had for examination had a sizeable fetal zone of the adrenal gland. Its testis had no stimulation of the interstitial cell component. Congenital defects in thyroglobulin have resulted in familial goiter (Doi et al., 1990; Schiller et al., 1995). The deficiency leads to reproductive difficulties.

13) Genetics

This group of antelopes is chromosomally extraordinary in that it is characterized by the fusion of an Y-chromosome to an autosome (# 13). Hence, females have one more chromosome (a #13-chromosome) than males (Wurster, 1972; Benirschke et al., 1982; other literature on tragelaphines cytogenetics can there be found). This large study included 4 males and 10 females and gave consistent results that have since been verified. Thus, the male bongos have 33 chromosomes, the females have 34 chromosomes. The fused (Y/13) makes up 8% of the DNA. It had previously been misidentified in tragelaphines as representing the X-chromosome (Wallace, 1978). It is of further interest that, in normal females, there occur two morphotypes of the X chromosome: one large acrocentric (as in most tragelaphines) and a large submetacentric element. The short arm of this submetacentric is heterochromatic and has thus not evolved by pericentric inversion.

The implications for taxonomic relations and for an understanding of the presumed phylogeny of these antelopes has been discussed in excellent detail by Petit et al. (1997) whose putative lineage diagram is shown next. These authors did an extensive genetic study of four tragelaphine species, arranged the elements according to the standard bovine reference definitions, and had conclusive results.

		This putative phylogeny is arranged according to cytogenetic information with chromosome numbers (2n=males/females) and the types of fusions as arranged according to bovid karyotype agreement.

	Two hybrids with the sitatunga (Tragelaphus spekei) have been described from the Antwerp zoo (Gray, 1972). Their gestation lasted 309 days and Cesarean section was necessary for delivery. One female hybrid produced a female offspring when mated with a male sitatunga. 14) Immunology I am not aware of any immunological study in Tragelaphinae. 15) Pathological features One common illness in hoofed species, including the Tragelaphinae, is the occurrence of "white muscle disease", an acute skeletal myopathy that occurs especially after strenuous exercise and capture (hence it is often called "capture myopathy"). This has been aptly summarized by Heldstab & Ruedi (1980). A congenital defect of diaphragmatic hernia was identified in San Diego (see Benirschke et al., 1982). This neonate possessed one each of the two X-chromosome morphotypes. It is unlikely, however, that the different X-chromosome types were related to the anomaly. Tragelaphinae are apparently susceptible to develop a scrapie-like encephalopathy. This was reported twice in greater kudus by Kirkwood et al. (1992, 1994). In one case the disease may have been transmitted in utero. 16) Physiologic data There are no such studies on bongos. Methods of immobilization were discussed by Haigh (1976), and a Cesarean section has been described by Bush et al. (1973). Pospisil et al. (1984) reported hematological values on these species. They were generally similar to those of humans. 17) Other resources Cell strains from many specimens of this species and related tragelaphines are available from CRES at the Zoological Society of San Diego. 18) Other remarks - What additional Information is needed? More placentas need to be studied to better understand the length of the umbilical cord, weights, and possible diseases. It is especially important to obtain more rapidly fixed material than was possible for me to obtain. Acknowledgement Most of the animal photographs in these chapters come from the Zoological Society of San Diego. I appreciate also very much the help of the pathologists at the San Diego Zoo. References Benirschke, K., Kumamoto, A.T., Esra, G.N. and Crocker, K.B.: The chromosomes of the bongo, Taurotragus (Boocerus) eurycerus. Cytogenet. Cell Genet. 34:10-18, 1982. Bent, N. and Reason, R.: A preliminary study of sex ratios in captive=-born ruminants. Int. Zoo Yb. 36:223-228, 1998. Bush, M., Montali, R.J., Gray, C.W. and Neeley, L.M.: Cesarean section in a Bongo antelope. J. Amer. Vet. Med. Assoc. 163:552-553, 1973. Doi, S., Shifrin, S., Santisteban, P., Montali, R.J., Schiller, C., Bush, M. and Grollman, E.F.: Familial goiter in bongo antelope (Tragelaphus eurycerus). Endocrinology 127:857-864, 1990. Dresser, B.L.: Embryo transfer in exotic bovids. Intern. Zoo Yearbook 24-25:138-142, 1986. Gotch, A.F.: Mammals - Their Latin Names Explained. Blandford Press, Poole, Dorset, 1979. Gray, A.P.: Mammalian Hybrids. A Check-list with Bibliography. 2nd edition. Commonwealth Agricultural Bureaux Farnham Royal, Slough, England, 1972. Haigh, J.C.: The immobilization of bongo (Boocerus eurycerus) and other African antelopes in captivity. Vet. Rec. 98:237-239, 1976. Heldstab, A. and Ruedi, D.: The occurrence of myodystrophy in zoo animals at the Basle Zoological Garden. Pp. 27-34, In, The Comparative Pathology of Zoo Animals, R.J. Montali and G. Migaki, eds., Smithsonian Institution Press, Washington, D.C., 1980. Hradecky, P., Benirschke, K. and Stott, G.G.: Implications of the placental structure compatibility for interspecies embryo transfer. Theriogenology 28:737-746, 1987. Hradecky, P., Mossman, H.W. and Stott, G.G.: Comparative histology of antelope placentomes. Theriogenology 29:693-714, 1988. Hradecky, P., Mossman, H.W. and Stott, G.G.: Comparative development of ruminant placentomes. Theriogenology 29:715-729, 1988. Kirkwood, J.K., Wells, G.A., Cunningham, A.A., Jackson, S.I., Scott, A.C., Dawson, M. and Wilesmith, J.W.: Scrapie-like encephalopathy in a greater kudu (Tragelaphus strepsiceros), which had not been fed ruminant-derived protein. Vet. Rec. 130:365-367, 1992. Kirkwood, J.K., Cunningham, A.A., Austin, A.R., Wells, G.A. and Sainsbury, A.W.: Spongiform encephalopathy in a greater kudu (Tragelaphus strepsiceros) introduced into an affected group. Vet. Rec. 134:167-168, 1994. Matthee, C.A. and Robinson, T.J.: Cytochrome b phylogeny of the family Bovidae: resolution within the alcelaphini, antilopini, neotragini, and tragelaphini. Mol. Evol. 12:31-46, 1999. Nowak, R.M.: Walker's Mammals of the World. 6th ed. The Johns Hopkins Press, Baltimore, 1999. Petit, P., Vermeesch, J.R., Marynen, P. and de Meurichy, W.: Comparative cytogenetic study in the subfamily Tragelaphinae. Proc. 11th Europ. Coll. Cytogenet. Domest. Anim. Pp. 109-113, 1994/5. Pospisil, J., Kase, F., Vahala, J. and Mouchova, I.: Basic haematological values in antelopes - II. The hippotraginae and the tragelaphinae. Comp. Biochem. Physiol. A 78:799-807, 1984. Ralls, K.: Tragelaphus eurycerus. In, Mammalian Species, No. 111, 1-4, 1978. Amer. Soc. Mammal. Schiller, C.A., Montali, R.J., Doi, S. and Grollman, E.F.: Clinical and morphologic findings of familial goiter in bongo antelope (Tragelaphus eurycerus). Vet. Pathol. 32:242-249, 1995. Thenius, E.: Stammesgeschichte der Säugetiere (einschliesslich der Hominiden). In Handbuch der Zoologie, J.G. Helmcke, D. Starck and H. Wermuth, eds. Vol. 8/2:369-722, 1969, Walter de Gruyter & Co., Berlin. Wallace, C.: Chromosomal evolution in the antelope tribe Tragelaphini. Genetica 48:75-80, 1978. Wurster, D.H.: Sex-chromosome translocations and karyotypes in bovid tribes. Cytogenetics 11:197-207, 1972. Xanten, W.A. Jr.: Gestation period in the bongo (Boocerus eurycerus). J. Mammal. 53:232, 1972.

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