Greater Kudu (Tragelaphus strepsiceros)

Order: Artiodactyla

Family: Bovidae

1) General Zoological Data

This beautiful African species has elegant, spiraled horns in the grey males; females do not have horns. A relevant web site gives the following information: "The range of the Greater Kudu extends from the east in Tanzania, Eritrea and Kenya into the south where they are found in Zambia, Angola, Namibia, Botswana, Zimbabwe and South Africa. They have also been introduced in small numbers into New Mexico. Their habitat includes thick bushveld, rocky hillsides, dry riverbeds and anywhere with a constant supply of water". The evolutionary relationships of various bovid taxa were described with cytochrome b mtDNA data by Hassanin & Douzery (1999) and Matthee & Robinson (1999). More recently, Hernández Fernández & Vrba (2005) have summarized the relationships and constructed trees that include the kudu, eland and related species, and Gatesy et al. (1997) aligned the Bovini with Tragelaphinae by mtDNA studies of Artiodactyla.

Gotch (1974) derived the name ‘tragos (Gr) from he-goat, elaphos (Gr) a deer, strepho (Gr) I twist, keras (Gr) horn; kudu (koodoo) is the Hottentot name for this animal.

The longevity of the greater kudu in captivity is 23 years according to Jones (1993) and Weigl (2005), but Mentis (1972) summarized literature that gives longevity of 7 - 15 years in the field. Males weigh between 190 and 270 kg, while females weigh between 120 and 210 kg.

Male greater kudu at San Diego Zoo's Wild Animal Park.

Female greater kudu at San Diego Zoo's Wild Animal Park.

Female greater kudus at San Diego Zoo.

2) General Gestational Data

Single young are the rule (Hayssen et al., 1993) and gestation is estimated to be 7 - 9 months with neonates weighing 16 kg (Nowak, 1999). The smaller female fetus shown below was found at necropsy as a singleton that measured 9 cm in crown-to-rump length. It was located in the right uterine horn but the placenta extended into the left horn as well. The normal length of gestation is 212 - 214 days (Mentis, 1972; Hayssen, V. et al., 1993). The usually single neonate weighs ≈15 kg (Hayssen et al. (1993).

3) Implantation

Early stages of implantation are not recorded. Implantation occurs on flat caruncles with a typical epitheliochorial, cotyledonary type of placenta evolving. Hradecky (1983) described implantation in right and left uterine horns but has found many more cotyledons (55 and 70) than seen in our immature specimen (21). He described four rows of caruncles and observed cotyledons to develop in the lesser horn as well. Mossman (1987) indicated that the placenta attaches mesometrially and that placentation is superficial. Carter (2008) provided suggestions as to how to access Mossman’s collection.

4) General Characterization of the Placenta

I have had one pregnant uterus available that came from a female that was euthanized after sustaining severe injuries in fights. In its right uterine horn the dam contained a single female fetus weighing 2,900 g (normally 16,000 g at term!) that had a 37 cm CR length. After removing the fetus, the uterus and placenta together weighed 1,650 g. There were 21 flat cotyledons measuring up to 7 cm in width and 0.8 cm in thickness. The cord had a mesometrial central attachment and measured 13 cm in length. A single corpus luteum was present in the right ovary; several small cysts were present in the left ovary. The placenta differs little from that of the lesser kudu (see that chapter) except for the smaller number of cotyledons that were found at least in this single specimen. Hradecky et al. (1988b) depicted the dense band of connective tissue that separates the villous tissue from the endometrium.

In addition to this specimen, Dr. P. Hradecky made available some slides of term placentas which he described in publications here annotated. The histology of these specimens is also here presented.

A second and much younger implanted gestation came from Dr. Moresco at UC Davis. It is a similar and typical polycotyledonary, epitheliochorial placenta whose cotyledons are arranged in four rows and implantation occurred in either horn. At term, the delivered organ of the generally similar common eland weighs ≈1,100 g (Hayssen et al., 1993). Hradecky (1983) saw 142 and 155 cotyledons in two placentas available to him; they were arranged in four rows, as are the cotyledons. Turner (1879) found more than 100 cotyledons. In addition, an attached placenta was studied.

Intact uterus with empty horn in mid-portion at right.

Fetus still in the amnion; allantoic sac with urine at top. Cervix at bottom left.

Opened uterus with cervix at bottom right. The left horn is seen behind the rear legs.

Fetal kudu attached to placenta in utero, specimen from UC Davis.

Second fetal kudu attached to placenta in utero.

Composite of two sections of large, flat cotyledon with adjacent membranes, implanted on myometrium (bottom).

One cotyledon implanted on myometrium (bottom). Note foci of squamous metaplasia on amnion (right and left).

Edge of implanted term kudu cotyledon with intercotyledonary endometrium at bottom right.

Another implanted term cotyledon donated by Hradecky.

Placentome of term kudu gestation showing the dense "band" that separates the villous structures from the endometrial glands.

Implantation site of term cotyledon. Note the variably structured bands of connective tissue above the more loosely constructed endometrium.

Placentome of greater kudu (Fig. 9 from Hradecky et al. 1988b).

Villous tissue as shown by Hradecky et al. (1998b).

Implanted immature cotyledon in the right uterine horn. The pale tissue are fetal villi, the darker red areas are maternal septa. The dark blue mass corresponds to that shown previously by Hradecky (1988b).

Implanted cotyledon in left horn and apposition of membranes to uterine wall.

Maternal septa in red, fetal surface above, pale villi are covered by trophoblast.

This cross section of a term placenta shows the interlacing maternal septa and villi in their central compartments.

5) Details of fetal/maternal barrier

This is a typical epithelio-chorial placenta with long strands of maternal connective tissue separating the long, slender villi. The single-layered trophoblastic epithelium has a very large number of binucleate cells. Microvilli extend from the trophoblastic surface. The uterine epithelium in this specimen is single-layered and intact, albeit somewhat autolyzed. No trophoblastic infiltration into the endometrium occurs. Some trophoblastic cells have small yellow granular inclusions, but it is not clear that they are not artifacts of fixation. There is no subchorial "hematophagous region", as seen in so many other species. The finer histologic features of the kudu placentome were described by Hradecky et al. (1988a). They measured the term villi to be 7 mm long and branched and somewhat different from those of the eland. The septa and epithelia are also described in this contribution. Hradecky et al. (1988a) described that thee villous surfaces were more ‘corrugated’ than those of the eland. They described that: a) "the covering epithelium was 10 to 15 µm thick and was composed of polygonal; cells with visible boundaries and round nuclei"; and further b) "the crypt lining was 5 µm thick, had dark spindle-shaped nuclei, and varied between syncytial and cellular types".

Interdigitation of immature villus (center) with maternal septa (left, right). Two large binucleate cells are present. Minute granules of yellow pigment are found in some trophoblast.

Relationship between trophoblast of central villus and maternal septa in term placenta.

Another representation of the interdigitating villi and septa of a term kudu caruncle. Binucleate trophoblast at arrows. There is only epithelium-to-epithelium contact between fetal and maternal tissues - no ingrowth.

Maternal septum above with epithelial mitosis in endometrial epithelium.

Maternal tissue above; villus below with binucleate cell and one giant trophoblastic nucleus.

6) Umbilical cord

The cord of this specimen measured 13 cm in length, had four large blood vessels and a central allantoic duct. In addition to these large chorioallantoic vessels there are numerous small vessels but they are not specifically congregated around the allantoic duct. There were numerous small surface granules composed of squamous metaplasia. The allantoic duct is lined with a flat urothelium.

Central insertion of 13 cm cord with minimal spiral and numerous amnionic squamous granules on the surface.

Cross section of umbilical cord. Note diffuse squamous metaplasia on surface and central allantoic duct. Numerous small blood vessels are present in addition to the four large vessels.

7) Uteroplacental circulation

No details have been described.

8) Extraplacental membranes

The amnion had numerous small foci of squamous metaplasia; the allantoic sac contained yellow urine without hippomanes. The membranes extended into the empty left sac, but there were no implanted cotyledons in that horn. The composition of amnionic and allantoic fluid of term kudu was described by Hradecky (1984). It included volume and pH values.

Amnion with focus of squamous metaplasia.

Trophoblast covers the membranes between the cotyledons.

Attachment of membranes to endometrium (left). Allanto-amnion at right.

Second specimen. Endometrium at left, direct attachment of allantois (small vessels in the center) and amnion at right. Second specimen.

9) Trophoblast external to barrier

There is no infiltration of the basal endometrium.

10) Endometrium

The cervical canal was filled with dense, yellow mucus and was firmly closed.

No true decidua was found.

Section through the unused uterine horn.

Cross section of empty uterine horn in pregnant uterus showing one caruncle at top left. It also displays the dense band at the base of endometrium described by Hradecky (1988b).

11) Various features

There are no other unusual features in this gestation. There is an ovarian bursa (Mossman & Duke, 1973).

12) Endocrinology

The role of hormone production (placental lactogen) by the trophoblastic binucleate cells was explored by Wooding (1982). Atkinson et al. (1993) explored the glycoprotein production in ovine placentas by these cells. No other endocrine information is available. The ovaries of the second specimen measured 24&23 x 14&15 x 10&5 mm.

Ovary with corpus luteum (left) and corpora albicantia (red) of second specimen.

Section of ovary with corpus luteum at bottom left.

13) Genetics

Greater kudu males have 31 chromosomes, females have 32 chromosomes. This discrepancy is due to a translocation between an autosome and the Y-chromosome (Wallace & Fairall, 1967, 1967; Wurster, 1972; Hsu & Benirschke, 1971). Hybrids between greater kudu and eland have been described (Gray, 1972; Jorge et al., 1976). The latter hybrid reported at least was sterile. Gallagher & Womack (1992) also studied the translocations of many bovid species, including the kudu and suggested that speciation may have been the result of translocation with isolation of resultant karyotypically rearranged individuals.

The lesser kudu has 38 chromosomes and is remarkable because of its fusion chromosome; both X and Y chromosomes have compound fusions, and we believe they are with the same autosome (# 13). Petit et al. (1994/5) also studied the relationships of these unusual animals. Both views are presented at the end in a "pedigree" of possible developments over time. The finding of translocations in both sex chromosomes contrasts with that of many other African ungulates that have only an X/A translocation, but possess a normal Y chromosome. These species thus have different numbers in males and females (Benirschke et al., 1980). Other views of evolutionary relationships, resulting from mtDNA studies, were presented by Matthee & Robinson (1999) and Hassanin & Douzery (1999).

The hybrid and its parents are shown below. Since both species have the same chromosome number, the sterility is likely to be due to the different sizes and shapes of chromosomes and derived by inversions, as detailed by Jorge et al. (1976). Gallagher & Womack (1992) also studied the translocations of many bovid species, including those in the greater kudu and suggested that speciation may have been the result of translocations with subsequent isolation of resultant karyotypically rearranged individuals (see also Wurster et al., 1972). The putative differences in karyotypic banding pattern arrangement between eland and kudu are shown in the next photograph.

In addition, Petit et al. (1994/5) studied the relationships of these African animals. Both views are presented at the end in a "pedigree" of possible developments over time. The finding of translocations in both sex chromosomes contrasts with that of many other African ungulates that have only an X/A translocation, but possess a normal Y chromosome. These species have different numbers in males and females (Benirschke et al., 1980). Other views of evolutionary relationships, resulting from mtDNA studies, were presented by Matthee & Robinson (1999) and Hassanin & Douzery (1999). They are, however, still controversial as pointed out by Willows-Munro et al. (2005) who studied nuclear DNA introns. Nersting & Arctander (2001) examined the phylogeography of kudu and impala. Ralls et al. (1979) suggested on very sparse data that inbreeding may lead to increased mortality.

Chromosomes of male and female kudus (From Hsu & Benirschke, 1971).

Possible relationship of tragelaphines (from Benirschke et al., 1980).

Eland (m) x kudu (f) hybrid (Jorge et al., 1976).

This putative phylogeny is arranged by Petit (1995) according to cytogenetic information with chromosome numbers (2n=males/females) and the types of fusions as arranged according to bovid karyotype agreement.

Different banding arrangements of chromosomes from eland and kudu (Jorge et al., 1976).

14) Immunology

I am not aware of any publications.

15) Pathological features

Griner (1983) reports on autopsies of 20 greater kudus. Six died from trauma, four had neonatal malnutrition, one had capture myopathy. Two kudus had pulmonary tuberculosis, another had malnutrition from dental malocclusion and periodontitis. Post partum endometritis was seen in another female, another died from what appeared to be "bluetongue", although no virus was cultured, and large numbers of Trichuris led to emaciation of yet another animal.

Tuberculosis in kudus has been reported a number of times; thus, Himes et al. (1976) reported on four cases occurring in a zoo. Keet et al. (2001) found five cases in the Kruger National Park, and Bengis (2001) found an infected animal in a commercial ranch close to the park. Also, rabies has been reported by several authors (Barnard & Hassel, 1981; Hübschle, 1988). Barnard et al. (1982) transmitted the lethal virus experimentally via nasal and buccal instillations. Foot-and-mouth disease was described from Botswana by Letshwenyo et al. (2006). Several authors have identified and commented upon bovine spongiform encephalopathy in kudus (Kirkwood et. al, 1990, 1992, 1994; Cunningham et al., 1993, 2004). Flach et al. (2002) studied a variety of artiodactyls from Whipsnade for gamma herpesvirus, causative agent of malignant catarrhal fever and found in some animals, including kudus. Toxoplasma antibodies were found in 2 of 10 kudus from Zimbabwe by Hove & Mukaratirwa (2005). Numerous parasites have been identified in kudus and their identity can be found in papers by: McCully et al. (1967); Boomker (1982); Boomker et al. (1989, 1991); Zieger et al. (1998); Fellis et al. (2003).

An intraosseous liposarcoma led to fractures in a kudu, as reported by Raubenheimer et al. (1990). Chittick et al. (2002) reported a remarkable abnormality in two neonate kudus - Ichthyosis congenita (also referred to as harlequin ichthyosis); they had the same sire and the lethal anomaly is believed to be recessively inherited.

16) Physiologic data

Pospisil et al. (1984) provided data on blood counts in kudu as well as several other antelopes. Hradecky (1982) studied the uteri of a variety of antelopes in zoos and found the kudu to possess a Uterus bicornis similar to that of cattle. In a later publication (1984), he studied the composition of two kudu "fetal fluids" (amnionic and allantoic separately) of specimens 20 and 54 cm long. Interestingly, they differed considerably from one another. The two hemoglobin components of kudu (Hb A and Hb B) were studied by Rodewald et al. (1985) who sequenced the complete amino-acid chains. They found much homology with cattle hemoglobin. The nature of myosin heavy chain isoforms was studied in several African ruminants, including the kudu, by Kohn et al. (2007). The response to fever from pneumonia was the topic of a study by Hetem et al. (2008), while Owen-Smith (1997) studied the energy balance during foraging. Hagey et al. (1997) described the changes in bile acid composition with age a many bovids.

17) Other resources

Cell strains of this and several other animals as well as related tragelaphines are available from CRES by contacting Dr. Oliver Ryder at: oryder@ucsd.edu.

18) Other remarks - What additional Information is needed?

Early stages of implantation are not on record and more endocrine data are needed.

Acknowledgement

The animal photographs in this chapter come from the Zoological Society of San Diego. Some slides of a term placenta from a greater kudu were donated by Dr. Petr Hradecky.