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.

Pair of bongos at San Diego Zoo.

Front view of female bongo.

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. Another placenta of a term, healthy neonate had 95 cotyledons (up to 9 cm in diameter), weighed 1,550 g and measured 15 x 40 cm in dimensions. Its cord was 17 cm long; still one more placenta of a 5 year old female who broke her neck was contained in the right horn of the uterus (3,720 g.) while the left horn was empty. It contained only 65 cotyledons. The male fetus weighed 6.6 kg and had a CR length of 57 cm. The umbilical cord was 16 cm long.

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.

Bongo fetus in right uterine horn. Described above.

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.

Fetal surface of one cotyledon in the bongo found dead in pregnant dam.

Maternal surface of one cotyledon in the bongo found dead in pregnant dam.

5) Details of Fetal/maternal Barrier

This is a typical ruminant relationship between maternal villous projections in between the fetal villi as shown in the previous slides.

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

he 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.