Placentation in the African Elephant (Loxodonta africana): II Morphological Changes in the Uterus and Placenta Throughout Gestation
Introduction
Almost 40 years ago J. S. Perry and the late E. C. Amoroso gave an elegant and detailed description of the fetal membranes and placenta of the African elephant (Loxodonta africana), using material gathered from eight pregnant uteri harvested during routine culling in Uganda in the 1950s and 1960s (Perry, 1953; Amoroso and Perry, 1964; Perry, 1974). Prior to that time, information on pregnancy in the elephant had been limited to sporadic accounts in captive animals of births, untoward abortions and post mortem findings following death during pregnancy (Owen, 1868; Chapman, 1880; Assheton, 1906; Cooper, Connell and Wellings, 1964). Since then, attention has tended to focus more on ovarian function and peripheral plasma hormone profiles (Hanks and Short, 1972; Ogle, Braach and Buss, 1973; McNeilly et al., 1983; Brannian et al., 1988; Plotka et al., 1988; de Villiers, Skinner and Hall-Martin, 1989; Hodges et al., 1994, Hodges et al., 1997; Heistermann, Trohorsch and Hodges, 1997; Heistermann, Fieß and Hodges, 1997; Hodges, 1998) in cycling and pregnant females. In addition, Laws (1969)published an excellent account of the ecology and population dynamics of elephants in East African wildlife parks, Moss (1983)and Poole (1996)have written extensively on elephant behaviour, reproductive parameters and family life and van Aarde, Whyte and Pimm (1999)recently described the dynamics of the elephant population in Kruger National Park.
Amoroso and Perry (1964)described the differentiation of the extraembryonic membranes in the young elephant conceptus, including the unusual division of the allantois into four distinct compartments. They noted that the initially spherical conceptus lodged within one of three or four lateral grooves of the star-shaped endometrial lumen in one uterine horn and that, as the conceptus expanded, the outermost trophoblast cells appeared to erode and replace the lumenal epithelium of the endometrium over a considerable area of the chorion. Subsequently, a typical zonary placenta began to develop in just the equatorial region of the now ovate conceptus and this became essentially similar in architecture to the zonary placenta of canids, felids and the mink (Amoroso, 1952; Enders, 1957; Mossman, 1987; Wooding and Flint, 1994). Furthermore, the elephant placenta also had a diffuse haemophagous region under the lateral edges of the placental band in which trophoblast cells phagocytosed leaked maternal blood components (Amoroso and Perry, 1964). This haemophagous zone was similar to that found in the hyaena placenta but differed significantly from the sharply defined haemophagous sacs that develop in the placentae of the dog and mink (Steven, 1975; Steven and Morriss, 1975; Burton, 1982).
We were afforded a similar opportunity to study the development and architecture of the elephant placenta by examining and sampling gravid uteri recovered from adult female elephants being culled professionally in the Kruger National Game Park in South Africa. We recorded the gross appearance and general development of the zonary placenta and other fetal membranes and related these to gestational stage based on fetal weight (Craig, 1984). We also recovered pieces of placenta, fetal membranes, fetal gonad, endometrium and other fetal and maternal tissues for endocrinological studies (Allen et al., 2002), and for microscopic and immunohistochemical examinations. In this paper we summarize our gross, light microscopic and ultrastructural observations and, through these, attempt to describe the development and functioning of the elephant fetoplacental unit throughout gestation.
Section snippets
Recovery of specimens
For 2 weeks in each of three successive years (1993 to 1995 inclusive) three of the authors joined the annual cull of elephants in the Kruger National Game Park in the Western Transvaal region of South Africa. An accurate aerial census of total elephant numbers in the whole park was carried out annually and, based on the results, between 350 and 450 elephants were selected for culling in one of four main divisions of the Park (van Aarde, Whyte and Pimm, 1999). Each day one whole family group,
Anatomy of the uterus and ovaries
The bicornuate uterus shows some similarity to that of the horse in that the two horns are relatively straight and they diverge laterally from each other within the broad ligament (Figure 1, Figure 2a). Beyond this gross appearance, however, there are some marked contrasts. First, the body of the elephant uterus is shorter than its counterpart in the horse and is therefore not unlike that of the dromedary camel (Figure 1; Skidmore, Wooding and Allen, 1996). This means that the horns, joined to
Discussion
This study confirmed and extended the earlier findings of Amoroso and Perry (1964)on the development of the elephant placenta and it revealed some other unusual and interesting features of elephant placentation. First, the incredible toughness of the endometrial stroma combined with intense myometrial tone in the non-pregnant animal presumably creates the markedly star-shaped uterine lumen which results in tight apposition of the epithelial surfaces in the lateral branches of the star (Figure 2
Acknowledgements
We are extremely grateful to Dr Ian Whyte, Mrs Colleen Wood and all the other members of the Population Control Unit in Kruger National Park for much practical help in gathering samples and for great kindness and hospitality. We are also grateful to Marlena Ford, Martin Houpt and Domenic Moss for expert technical assistance. John Fuller kindly prepared the diagrams. The Sir Philip Oppenheimer and the Sunley Charitable Trusts gave generous financial support.
References (50)
Placental uptake of maternal erythrocytes: a comparative study
Placenta
(1982)Endocrinology of the ovarian cycle and pregnancy in the Asian (Elephas maximus) and African (Loxodonta africana) elephant
Anim Reprod Sci
(1998)- et al.
Implantation and early placentation in the one-humped camel (Camelus dromedarius)
Placenta
(1996) - et al.
Co-localization of vascular endothelial growth factor and its two receptors Flt-1 and KDR in the mink placenta
Placenta
(2001) - et al.
Culling and the dynamics of the Kruger National Park African elephant population
Anim Conserv
(1999) - et al.
The origin of the equine endometrial cups. II. Invasion of the endometrium by trophoblast
Anat Rec
(1973) - et al.
Placentation in the African elephant, Loxodonta africana. I. Endocrinological aspects. Reproduction
Suppl
(2002) - Amoroso EC (1952) In Marshall's Physiology of Reproduction (Ed.) Parkes AS. 3rd edn, vol. 2, p. 126. London: Longmans...
- et al.
The foetal membranes and placenta of the African elephant (Loxodonta africana)
Proc Roy Soc B
(1964) The morphology of the ungulate placenta, particularly the development of that organ in the sheep, and notes upon the placenta of an elephant and hyrax
Proc Roy Soc B
(1906)
Short and long phases of progesterone secretion during the oestrous cycle of the African elephant (Loxodonta africana)
J Reprod Fert
The placenta and generative apparatus of the elephant
J Nat Acad Sci
Distributions of VEGF and its binding sites at the maternal fetal interface during gestation in pigs
Reproduction
Placenta of the Indian elephant, Elephas indicus
Science
Foetal mass and date of conception in African elephants: a revised formula
Afr J Sci
Expression of VEGF and placental growth factor in conceptus and endometrium during implantation
Mol Human Reprod
Histological observations of the chorioallantoic placenta in the mink
Anat Rec
The origin of the equine endometrial cups. III. Light and electron microscopic study of fully developed equine endometrial cups
Anat Rec
Growth and Development of Mutton Qualities in the Sheep
The formation and function of the corpus luteum in the African elephant (Loxodonta africana)
J Reprod Fert
Assessment of ovarian function in the African elephant (Loxodonta africana) by measurement of 5α-reduced progesterone metabolites in serum and urine
Zoo Biol
Progestin content and biosynthetic potential of the corpus luteum of the African elephant (Loxodonta africana)
J Reprod Fert
Concentrations of the 5α-reduced progestins, 5α-pregnane-3,20 dione and 5α-pregnane-3α-ol-20-one in luteal tissue and circulating blood and their relationship to luteal function in the African elephant, Loxodonta africana
Biol Reprod
Handbook of Veterinary Obstetrics
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The distribution of small preantral follicles within the ovaries of prepubertal African elephants (Loxodonta africana)
2011, Animal Reproduction ScienceCitation Excerpt :Our finding that the numbers of small follicles in the left and right ovaries of a prepubertal elephant are similar allows reliable estimation of the number of small follicles per elephant in cases where only one ovary is available, even if it is not known whether it is from the left or right side of the animal, which of its surfaces is medial or lateral and which of its poles is cranial or caudal. The number of small follicles in the ovaries of pregnant animals can also now be estimated by using the ovary contralateral to the gravid uterine horn, which usually contains many fewer, if any, of the large accessory CL which are such a prominent feature of elephant pregnancy (Allen et al., 2003). During culling of elephant for management purposes the collection of scientific samples is not usually a priority which can result in a significant delay until access is gained to the reproductive tract.
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2010, Animal Reproduction ScienceCitation Excerpt :Similarly, Stansfield (2010) reports multiple luteal structures of varying size in the ovaries of culled pregnant and non-pregnant adult females. But perhaps most puzzling is the invariable finding of 2–5 large (3–5 cm diameter) pendulous corpora lutea clustered together usually, but not invariably, on the ovary ipsilateral to the gravid horn of the uterus (Hodges, 1998; Allen et al., 2003; Stansfield, 2010). These are much bigger than the diameter of any recorded cyclic follicle (Hodges, 1998) and they are composed of khaki-coloured homogeneous luteal tissue which actively converts radioactively-labelled cholesterol and pregnenolone to 5α-reduced progestagens (Fig. 18b; Hodges et al., 1994).