Elsevier

Placenta

Volume 24, Issue 6, July 2003, Pages 598-617
Placenta

Placentation in the African Elephant (Loxodonta africana): II Morphological Changes in the Uterus and Placenta Throughout Gestation

https://doi.org/10.1016/S0143-4004(03)00102-4Get rights and content

Abstract

The gross and microscopic development of the zonary endotheliochorial placenta in the African elephant was studied in 22 gravid uteri that ranged in gestational stage from 0.5 to 20.6 months. The conceptus only ever occupies one horn of the uterus and is associated with 2–5 large corpora lutea that persist in the ipsilateral ovary throughout gestation. Initially, the trophoblast in the equatorial region of the conceptus completely replaces the lumenal epithelium of the endometrium to which it is apposed. Blunt upgrowths of endometrial stroma then develop, each closely invested by trophoblast, and containing the capillaries that will vascularize this maternal component of the resulting placental band. With advancing gestation the lamellate stromal upgrowths increase markedly in length and become much thinner, thereby bringing the trophoblast into intimate contact with the endothelium of the maternal capillaries. They also become folded or pleated to increase the total area of intimate feto-maternal contact. At the lateral edges of the placental band the lamellae bend over towards the endometrium to form a blind cleft. Leakage of blood into this area creates haemophagous zones in which phenotypically specialized trophoblast cells phagocytose the blood components.

The presence of large resorbing blood clots and circumferential scars in the uteri of three post parturient animals initiated the hypothesis that, when the standing elephant gives birth at term, the passage of the 120 kg fetus through the vagina may wrench the placenta off the endometrium by severing its very narrow maternal placental hilus. The resulting intrauterine haemorrhage may then play a role in preventing further conception for around 2 years.

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.

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