CRETAN GOAT
Capra aegagrus cretica

Order: Artiodactyla
Family: Bovidae

1) General zoological data of species

This species of wild goat, one of eight such species, lives on steep rocky cliffs on the island Theodoru, north of Crete. It is characterized by the knobby, long (four feet), curved horns that are smaller in females. It also has a pronounced, pendulous chin beard. But for goats in general, "there is much controversy regarding the systematics of this genus…" (Nowak & Paradiso, 1983). Adult Cretan goats (also referred to as Cretian goats) weigh 20-30 kg. with considerable variation upward. It is estimated that some 200 varieties of domestic goat have evolved (Keisler, 1998).

Since this species is so similar to domestic goats, no other Capra species will be presented in these pages.

Nowak (1999) stated that domestication of goats began about 8,000 years ago, with C. aegagrus being the ancestral species. More recently, Luikart et al. (2001), using mtDNA studies, estimated divergence taking place about 10,000 years ago, but with three different lineages serving as the domestic goat ancestors.

2) General gestational data

Breeding colonies of Cretan goats are now found in only few zoos, even though this is a spectacular animal and was the presumed ancestor of domestic goats. The San Diego Zoo has long bred this species and has much experience with it. The length of gestation is 148-160 days, with twins being born most commonly. Singletons are frequent, but triplets occur only rarely. Sexual maturity in males occurs at 1½ years, in females around 2½ years, much depending on their environment and nutrition. Maximum life span is about 22 years. Newborns weigh around 1.5-2.0 kg. The placenta at term weighs 200g.

3) Implantation

Implantation of caprine (Bovidae) placentas occurs over the uterine "caruncles" in their bicornuate uterus and, less intimately, over the rest of the uterine surface onto the intercotyledonary endometrium. The early attachment phases of ungulates (especially that of bovine and ovine species) have been documented by excellent electronmicroscopic studies of King et al. (1982). The first attachment of the goat blastocyst is mesometrial with trophoblast and future villi interdigitating with the endometrium in the caruncles (Wimsatt uses the wonderful term of "increscence" for this apposition). These regions of altered endometrium are arranged in rows whose origin has been traced by Mossman (1987). The concave cotyledons thus develop and occupy both horns. In between the cotyledons there is contact between trophoblast and endometrium and, in the "areolae" (over the orifices of endometrial glands), much secretion of "uterine milk" occurs, secretions that are perhaps used for fetal nutrition.

4) General characteristics of placenta

This chapter will concentrate on the goat placenta only. Even though the goat placenta is similar to that of the sheep, there is sufficient reason for treating the sheep placenta in a separate chapter. Moreover, sheep and goat have occasionally hybridized and therefore must have similar placentation. But the sheep needs a separate chapter because the sheep is so often used in experimental studies, and so much more is known about its physiology and structure than of goat pregnancies.

In the Cretan goat we found a multi-cotyledonary placenta with 65 cotyledons that are arranged in rows. These follow the disposition of the endometrial caruncles. Most of the Bovidae have very similar placentas (Mossman, 1987, Kaufmann, 1983, King et al., 1982) and end up having an allegedly epitheliochorial placentation (at least between the cotyledons), with variably shaped cotyledons. These regions, however, are now considered to have a syndesmochorial fetal/maternal relationship. Implantation is thus relatively superficial over large stretches, and it is more complex in the cotyledons where some endometrial epithelium is being replaced by syncytium. Irregular foci of bleeding from maternal capillaries exist, with incorporation of released pigments into the trophoblast.

Another specimen of a term, normal delivery became available in May, 2002. It weighed 170g, measured 62 x 14 cm and had 48 cotyledons measuring from 1-3 cm in diameters. It was otherwise identical and is depicted next.

5) Details of barrier structure

The original classification of the sheep (and therefore goat) placenta as being an epitheliochorial organ is no longer considered to be correct. The autoradiographic studies by Wooding et al. (1981) supersede the older information, as will be seen. The ovine/caprine placenta must now be considered (as far as the cotyledons are concerned) as syndesmochorial organs. The intercotyledonary regions, however, remain epitheliochorial.

The most controversial aspect perhaps of sheep/goat, for that matter ungulate, placentation has been the origin of the syncytium that lines the crypts of the cotyledons, and the nature of the binucleated cells. Binucleate cells are clearly trophoblastic in origin and are now know to produce the placental lactogen. Amoroso (1952) had already considered them to be precursors of the syncytial "plaques" found in the cotyledons. The autoradiographic study by Wooding et al. (1981) convincingly showed that the syncytium has a trophoblastic origin and that it is not derived by fusion with endometrial epithelium, as was once thought. Presumably, the binucleate cells initiate the process of fusion and subsequent migration, and they continue to do so during the entire pregnancy. Moreover, the fact that there are no mitoses in the syncytium, while they do occur in the cellular trophoblast, supports this notion. Thus, the syncytium is much like other fusion-induced cells, but Wooding (1984) showed that some fusion with maternal epithelium produces trinucleate hybrid cells as well. These cells are quite specific, and secretion of the lactogen-containing granules (perhaps to maintain gestation) is described in this paper. He emphasized that there is no immune reaction as the result of maternal epithelial erosion and this fusion ("hybridization" of cells).

Fine structural analysis of ruminant placentas often shows square osmiophilic or needle-shaped inclusions in the rough endoplasmic reticulum of trophoblast. Presumably these represent crystallized protein aggregates whose function remains unknown (Anderson & Cheville, 1986).

6) Umbilical cord

The umbilical cords available have been around 10 cm in length and 1 cm in diameter. There are four blood vessels and a large allantoic duct that is surrounded by numerous smaller blood vessels. There are no spirals of the cord. Regions of squamous metaplasia are common on the surface of the umbilical cord.

7) Uteroplacental circulation

This has been studied primarily in sheep and the reader should refer to Wimsatt (1950) and the chapter on sheep. Apparently, one artery is projected into each villous stem where it branches and forms capillaries; these then turn then into venules. Makowski (1968), however, also using goat placentas to examine the vascular flow of cotyledons, observed the absence of a true countercurrent blood flow, as had been expected. He assumed that arterial sphincters under hormonal control regulate the fetal cotyledonary flow because he was unable to identify neural mechanisms.

8) Extraplacental membranes

The multicotyledonary placenta of artiodactyla has no true "free membranes", aside from the intercotyledonary stretches of allantochorion. Otherwise there is only the specialized region of allantoic cavity that is closely applied to the amnion and chorion and contains mostly fetal urine with a high content of fructose.

The structure of the sheep amnion was described in some detail by Bautzmann & Schröder (1955). They found a single-layered squamous epithelium with occasional pearls ("warts" - see also Naaktgeboren & Zwillenberg, 1961), and an absence of smooth musculature. Of course, these authors (my anatomy teachers) were most interested in the membranes because of their earlier studies of bird membranes. They showed these to possess a muscular network for "circulation of fluid". In sheep, there was a complex fibrocyte network instead, that connected the amnion with the allantoic sac. This, in turn, was rich in water and was assumed to allow much expansibility of this sac.

The contribution by fetal urine to the allantoic fluid has been critically studied by Ross et al. (1988), but only in sheep. Most allantoic fluid derives from fetal urine, as we showed with Barron by cannulating the fetal urachus. Despite the fact that urination is said to decrease toward term, the allantoic sac remains quite large. Allantoic fluid also differs much in its composition from amnionic fluid, the latter receiving less urine and having an equilibrium with fetal lung fluid, through swallowing and inhalation. Much allantoic fluid (fetal urine) is being resorbed by the allantoic vasculature of this membranes. As indicated, this was apparent when we placed catheters into the allantoic duct of sheep and allowed all urine to escape; gradually the fetus stopped urination, which then became of ever-higher osmolality. Urination only resumed after water was injected into the allantoic sac. Hippomanes are present in the allantoic sac.

The intercotyledonary membranes and their relation to the uterus have been best studied by Davies & Wimsatt (1966) who defined the regions of the so-called "areolae". These areas are located atop the orifices of endometrial glands and are presumed to be an important zone of nutritional transfer to the fetus. This is the site of "uterine milk" production by the endometrium. The remainder shows a close approximation of the microvillous surfaces of endometrial epithelium and cellular trophoblast. There is no decidua capsularis.

9) Trophoblast external to barrier

There is no extravillous trophoblastic invasion.

10) Endometrium

There is no decidualization.

11) Various features

There is no subplacenta.

12) Endocrinology

The reproductive physiology and nutritional influences on reproduction of does have been superbly summarized by Keisler (1998). The length of the estrous cycle is about 19-21 days; offspring are born usually only yearly. PGF2", produced by the uterus, lyses the corpus luteum; this consequently leads to a fall of progesterone. When pregnancy is established, the placenta produces PSPB (Pregnancy Specific Protein B), whose function is unknown; placental lactogen and other products are also secreted. PSPB is used for pregnancy testing. After 60 days of gestation, the placental progesterone production is adequate enough to support pregnancy. Later in pregnancy, the adrenal/pituitary axis takes over the endocrine support, and delivery can be induced by injection of adrenal steroids (cortisol). Conversely, hypophysectomy (in sheep fetuses) or specific cranial anomalies (anencephaly), lead to postmaturity. Later in gestation, PGE2 is produced.

13) Genetics

Goats have 60 chromosomes, as do the many specimens of Cretan goats studied at CRES of the Zoological Society of San Diego.

Studies of mtDNA by Luikart et al. (2991) found divergence of goat and cattle to have occurred about 200,000 years ago, while goat domestication is estimated as having taken place about 10,000 years ago, but originating from three independent lines of ancestors.

It has occasionally been possible to hybridize sheep and goats, and an extensive literature exists about these attempts (Gray, 1972). Most fetuses abort by two months; their chromosome number is 57, in between the sheep (54) and that of the goat (60). In a large series of experiments, Dent et al. (1971) showed with electronmicroscopy that the trophoblast of the hybrids is normal and implantation appears to proceed normally. There was, however, an extensive accumulation of platelets in the maternal blood vessels and endothelial swelling to the point of occlusion with hemorrhage ensuing between 34 and 38 days. These authors suggested that this is akin to an immunological rejection of the fetal hybrid implant. Domestic goat and Cretan goats "hybridize" with fertile offspring. Occasional female sheep x goat hybrids have been fertile (Bunch et al. (1976), when bred back to Barbados sheep, resulting in animals with 55 chromosomes.

14) Immunology

MHC molecules, NK cells, and other specific cell populations have apparently not been studied much in goats. Hemolysins were found in sheep x goat hybrid pregnancies but were not considered to have caused the abortions (Tucker et al., 1971). Immunization of goats against sheep antigens reduced the length of fetal survival from six to three weeks (McGovern, 1973).

15) Pathological features

The findings at autopsy of adults have shown that Cretan goat deaths were usually due to trauma (aggression) and also attributed to old age with blindness; only occasional infections have occurred. Fetal or neonatal deaths have been attributed to poor nursing of twins, "stress", and occasional congenital anomalies (renal agenesis). Infections are uncommon, except for males who may suffer Brucella epididymitis with sterility ensuing. This organism also causes abortion by infecting the placenta. Anderson & Cheville (1986) showed large numbers of organisms in these placentas within the rough endoplasmic reticulum of the cytotrophoblast but absent from the binucleated cells.

16) Physiological data

Physiological parameters have been extensively explored, but mostly in sheep, and the reader should refer to that chapter for details and references. Fetal carbohydrate availability consists most of fructose, as opposed to glucose of other species.

17) Other resources

The San Diego Zoo has a thriving colony of these animals from which animals cell cultures are available through CRES.

18) Other relevant features and additional needs for information

More knowledge of the length of umbilical cords would be desirable and whether pathologic features can be identified. The precise mechanism leading to the abortion of sheep x goat hybrids should be better understood.

References

Amoroso, E.C.: Placentation. In, Marshalls Physiology of Reproduction. 3rd ed. A.S. Parkes, ed. Longmans, London. 1952. Chapter 15, pp. 127-311.

Anderson, T.D. and Cheville, N.F.: Ultrastructural morphometric analysis of Brucella abortus-infected trophoblasts in experimental placentitis. Amer. J. Pathol. 124:226-237, 1986.

Bautzmann, H. and Schröder, R.: Vergleichende Studien über Bau und Funktion des Amnions. Z. Zellforsch. 43:48-63, 1955.

Bunch, T.D., Foote, W.C. and Spillett, J.J.: Sheep-goat hybrid karyotypes. Theriogenology 6:379-385, 1976.

Cell cultures are available from CRES at: www.sandiegozoo.org/CRES

Davies, J. and Wimsatt, W.A.: Observations on the fine structure of the sheep placenta. Acta anat. 65:182-223, 1966.

Dent, J., McGovern, P.T. and Hancock, J.L.: Immunological implications of ultrastructural studies of goat x sheep hybrid placentae. Nature 231:115-117, 1971.

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

Kaufmann, P.: Vergleichend-anatomische und funktionelle Aspekte des Placenta-Baues. Funkt. Biol. Med. 2:71-79, 1983.

Keisler, D.H.: Sheep and Goats. In, Encyclopedia of Reproduction, Vol. 4, E. Knobil and J.D. Neill, eds. Academic Press, San Diego, pp. 479-492.

King, G.J., Atkinson, B.A. and Robertson, H.A.: Implantation and early placentation in domestic ungulates. J. Reprod. Fertil. Suppl. 31:17-30, 1982.

Naaktgeboren, C. and Zwillenberg, H.H.L.: Untersuchungen über die Auswüchse und an der Nabelschnur bei Walen und Huftieren, mit besonderer Berücksichtigung des europäischen Hausrindes. Acta Neerl.-Scand. 4:31-60, 1961.

Luikart, G., Gielly, L., Excoffier, L., Vigne, J.D., Bouvet, J. and Taberlet, P.: Multiple maternal origins and weak phylogeographic structure of goats. Proc, Natl. Acad. Sci. USA 98:5927-5932, 2001.

Makowski, E.L.: Maternal and fetal vascular nets in placentas of sheep and goats. Amer. J. Obstet. Gynecol. 100:283-288, 1068.

McGovern, P.T.: The effect of maternal immunity on the survival of sheep x goat hybrid embryos. J. Reprod. Fertil. 34:215-220, 1971.

Mossman, H.W.: Vertebrate Fetal Membranes. MacMillan, Houndmills, 1987.

Nowak, R.M.: Walker's Mammals of the World, Vol. II. The Johns Hopkins University Press, Baltimore, 1999.

Ross, M.G., Ervin, M.G., Rappaport, V.J., Youssef, A., Leake, R.D. and Fisher, D.A.: Ovine fetal urine contribution to amniotic and allantoic compartments. Biol. Neonat. 53:98-104, 1988.

Tucker, E.M., McGovern, P.T. and Hancock, J.L.: Serological investigations into the cause of death of goat x sheep hybrid fetuses. J. Reprod. Fertil. 27:417-425, 1971.

Wimsatt, W.A.: New histological observations on the placenta of the sheep. Amer. J. Anat. 87:391-458, 1950.

Wooding, F.B.P.: Role of binucleate cells in fetomaternal cell fusion at implantation in the sheep. Amer. J. Anat. 170:233-250, 1950.

Wooding, F.B.P., Flint, A.P.F., Heap, R.B. and Hobbs, T.: Autoradiographic evidence for migration and fusion of cells in the sheep placenta: Resolution of a problem in placenta classification. Cell Biol. Internat. Reports 5:821-827, 1981.