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Pronghorn (Antilocapra americana)
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Order: Artiodactyla
Family: Antilocapridae
1) General Zoological Data
This single member of the genus is widely distributed over the American west and northern Mexico. In the distant past, thirteen species of antilocapridae were found in North America, this is the only remaining species of this genus, with five recognized subspecies. They are well known for their speed and also difficulty in keeping healthy in zoological parks. Longevity in captivity is 12+ years. They are said to be the only animal with both horn and antler, having a hollow horn over a protrusion of bone. Their name derives from the short prong at the distal antler. Beintema et al. (2003) sought gene for ribonuclease gene sequences and were unable to detect the seminal-type ribonuclease in pronghorn, apparently having completely deleted in pronghorn, presenting difficulties for phylogenetic assignment. Indeed, Nowak (1999) summarized recent information on relationship to other taxa that suggests they be comprised with cervids under the superfamily Cervoidea. They weigh up to 70 kg, males being larger than females. Both have antlers. Neonates weigh from 3-5.78 kg (Hayssen et al.1993). A comprehensive review of all aspects of this species has been published by one the best experts on pronghorn, O'Gara (1978).
Aerial surveys of the population in Wyoming, for instance, were conducted by Johnson et al. (1991) with several herd sizes over 300 animals being detected. In Mexico, however, the three subspecies of pronghorn are considered to be significantly endangered with only a few thousand animals remaining (Ceballos & Navarro, 1991). This is especially true for the subspecies of Baja California.
Pronghorn antelope.
2) General Gestational Data
Wislocki & Fawcett described four mid-pregnant uteri, but a more comprehensive study of female reproduction was undertaken by O'Gara (1969). He indicated that between three to seven ova developed into expanded blastocysts, twins resulted as a general rule. The expanding tip of the proximal, normally implanted gestational sac pierced by the necrotic tip of its membranes the distal embryonic sac, thus eliminating excess implantation. Gestation is around 250 days with singletons in the first pregnancy and twins born thereafter in more than 50% of pregnancies. Triplets have also been reported. Transuterine migration occurs. Neonates suffer high mortality from predation. Possible monozygotic twins occur (see section on pathology).
3) Implantation
A few macroscopic descriptions of young implantations have been detailed by O'Gara (1969) but histology is needed. I have had available only one mid-pregnant uterus containing twins, made available by the Los Angeles zoo many years ago. The photographs come from that specimen.
4) General Characterization of the Placenta
This is a typical polycotyledonary, epithelio-chorial placenta, similar to most other ungulates. The placenta has are an average of 92 (flat) cotyledons and the membranes meet in midline around 50-75 mm length (O'Gara, 1969). Anastomoses between fetal circulations are most uncommon. The distal tip of the membranes is necrotic. There is, however great variation in the number of placentomes developing, from 46 to 180 (O'Gara, 1969). Weights are not available of placentas and only volumes of cotyledons have been ascertained by O'Gara (1969).
Implanted pronghorn cotyledon with uterus below and chorionic membrane above.
Cross section through cotyledon showing the complex network of maternal tissue and villi interdigitating.
5) Details of fetal/maternal barrier
This is typically epitheliochorial with cuboidal trophoblast and a moderate number of binucleate trophoblast. Villi contain relatively little connective tissue. They are diffusely interposed between major uterine trabeculae.
A network of broad endometrial connective tissue (center) interdigitates with villous extensions. Flat section through implanted cotyledon.
Horizontally cut villus with cylindrical trophoblast abutting the endometrium (below).
Fetal surface of implanted pronghorn placenta with purple tips of maternal tissue seen between the paler villi.
Maternal surface of the same implanted cotyledon showing the broad extensions of endometrial connective tissue spanning up and villi in between. There are numerous glands at the base between the maternal blood vessels.
6) Umbilical cord
The cord attaches nearer the cervix than the utero-tubal junction (Mossman, 1987), but there are no descriptions or measurements of umbilical cords in any of the descriptions listed here.
7) Uteroplacental circulation
No studies are found in the literature.
8) Extraplacental membranes
The peripheral tip towards to oviductal end of amnion/allantois usually becomes necrotic (yellow-cheesy) from lack of allantoic vasculature and "acts as a lethal weapon in intra-uterine competition" (O'Gara, 1969). Mossman (1987) described the allantois as a "long, narrow, tubular allantoic cavity".
Chorion and (little) amnion at right, vascularized allantois at left.
9) Trophoblast external to barrier
There is no uterine invasion by trophoblast.
10) Endometrium
The uterus is bicornuate; a cervical mucus plug develops during gestation. (O'Gara, 1969). Normally four rows of caruncles develop, although O'Gara (1969) found five uteri without caruncles in his large series. There is no true decidua. Between cotyledons, the endometrial glands continue to be active.
The edge of a cotyledon (right) with endo/myometrium between the cotyledons. Numerous endometrial glands with sparse openings into uterine lumen.
11) Various features
There is neither a subplacenta nor other unusual features of placentation.
12) Endocrinology
I have not been able to identify any studies on endocrinology of pronghorn.
13) Genetics
Pronghorns have 58 acrocentric chromosomes (Wurster & Benirschke, 1967; Hsu & Benirschke, 1969). Hybrids are unknown. Dain (1977) studied the replication pattern of the sex chromosomes and found it to be larger than the "normal" 5% of genome; they detected late-labeling portions of both X and Y that were in excess of the 4.7% for the "regular" X chromosome. Gallagher et al. (1994) compared the band homologies of several Bovidae, including the pronghorn and found cattle and pronghorn to be most similar. A study of satellite DNA was undertaken by Denome et al. (1994). Murray et al. (1995) were able to use mitochondrial D-loop variation for the species identification among many different ungulates. Lee et al. (1994) were able to differentiate some subspecies by allozyme analysis in a large population from different areas; their study of mtDNA variation however was less informative.
Karyotypes male and female pronghorns.
14) Immunology
The serological studies conducted are listed in the next section.
15) Pathological features
O'Gara (1969) depicted a "teratomas" which I believe to be more likely an acardiac fetus (his fig. 17). In personal communications with the author I learned that another observer had identified several same-sex pronghorn twin fetuses with vascular anastomoses of their placental circulations, suggesting that MZ twins may occur; thus, acardiacs would be a good possibility. Griner (1983) autopsied 25 pronghorn and the difficulty with immobilization is shown in his data. "Lumpy jaw" and various infections, as well as "white muscle disease" were other causes of death. He also saw one squamous cell carcinoma of the oral mucosa with metastases. Experimental high selenium diets had no significant impact on captive pronghorn (Raisbeck et al., 1996). An apparent copper deficiency in hand-reared fawns disappeared after copper supplementation (Miller et al., 2001). Polioencephalomalacia in some Saskatchewan wild pronghorn (after grain ingestion) was attributed to thiamine deficiency by Wobeser et al. (1983).
Numerous studies of infectious agents have been undertaken in captive and wild pronghorn. They can be separated into three categories:
1) Parasites: Dubey (1980; 1981) identified Sarcocystis and Toxoplasma in pronghorn. Kuttler (1984) found Anaplasma marginale. Kingston et al. (1990) identified Entamoeba bovis in the feces of pronghorn fawns. Simmons et al. (2002) identified natural infection with Parastrongylus tenuis in four captive animals of Nebraska that led to euthanasia.
2) Viruses: Stauber et al. (1980) surveyed for antibodies in 104 adult and 42 fawns and found antibodies to bovine infectious diarrhea, infectious bovine rhinotracheitis, parainfluenza, bovine adenovirus 7 & 3 and anaplasma, but none to brucella, bluetongue or epizootic hemorrhagic disease. Jessup (1985) studied antibodies against two orbiviruses (bluetongue) and found it uncommonly. Bluetongue infection, however, caused epidemic losses in Wyoming during epidemics of 1976 and 1984 (Thorne et al., 1988). Infection by mosquito-borne Malpias spring virus was demonstrated by Clark et al. (1988). A survey of antibodies to malignant catarrh fever virus in several ruminants by Li et al. (1996) found none in pronghorn but it was present in several other wild ungulates. A large outbreak of epizootic hemorrhagic disease killed numerous pronghorn (Brodie et al., 1998). Experimental infection with contagious ecthyma virus yielded oral lesions but had only a "limited clinical response" and was not thought to impact wild populations (Lance et al., 1983).
3) Bacteria: Griner (1983) already indicated losses from salmonellosis. Deaths due to infection with Pasteurella multocida has been reported from Oregon and Montana (Dunbar et al., 2000). Brucella abortus found in Yellowstone bison rarely colonizes pregnant pronghorn according to the survey by Elzer et al. (2002). An important description of fusobacteriosis comes from Edwards et al. (2001). These recently captured animals were housed in a pen previously used by cattle. Following a rain, pododermatitis developed with rapid sepsis due to Fusobacterium necrophorum ensuing.
16) Physiologic data
Hand-rearing and study of nutrition were studied in considerable detail by Schwartz et al. (1976). Diarrhea and joint problems were major side effects of some diets. Because of significant declines of pronghorn populations in Oregon, Dunbar et al. (1999) studied numerous parameters of fawns and adult animals, without finding a significant change to explain the decline. Baker et al. (1998) studied diet supplements and their digestive efficiency of several American ruminants, including the pronghorn. Hematologic values and blood chemistry were studied by Clemens et al. (1987). Pronghorn were found to have significantly higher selenium levels than bison and deer. Problems with tranquilization of pronghorn were amply studied by Pusateri et al. (1982) who found dosing with diazepam and promazine-HCl difficult. In efforts to find a "model" for the study of sickle cell disease, Dhindsa et al. (1975) studied sera of deer and pronghorn. They found low alkaline phosphatase levels in pronghorn. Mossman & Duke (1973) stated that the ovaries of pronghorn do not differ much from other ungulates and depicted (their fig. 6.98) the two types of luteal cells they identified.
17) Other resources
Cell strains of fibroblasts are available from CRES at the San Diego Zoo by contacting Dr. Oliver Ryder at oryder@ucsd.edu.
18) Other remarks - What additional Information is needed?
Timing of implantation and early microscopic studies are needed, as well as endocrine studies.
Acknowledgement
The animal photograph in this chapter comes from the Zoological Society of San Diego. I appreciate also very much the help of the pathologists at the San Diego Zoo.
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Baker, D.L., Stout, G.W. and Miller, M.W.: A diet supplement for captive wild ruminants. J. Zoo Wildl. Med. 29:150-156, 1998.
Beintema, J.J., Breukelman, H.J., Dubois, J.Y. and Warmels, H.W.: Phylogeny of ruminants secretory ribonuclease gene sequences of pronghorn (Antilocapra americana). Mol. Phylogenet. Evol. 26:18-25, 2003.
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Affiliation of the authors at the time of publication
Department of Reproductive Medicine and Pathology, School of Medecine, University of California, San Diego, CA, USA.
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