Foetal age determination and development in elephants

Abstract

Elephants have the longest pregnancy of all mammals, with an average gestation of around 660 days, so their embryonic and foetal development have always been of special interest. Hitherto, it has only been possible to estimate foetal ages from theoretical calculations based on foetal mass. The recent development of sophisticated ultrasound procedures for elephants has now made it possible to monitor the growth and development of foetuses of known gestational age conceived in captivity from natural matings or artificial insemination. We have studied the early stages of pregnancy in 10 captive Asian and 9 African elephants by transrectal ultrasound. Measurements of foetal crown-rump lengths have provided the first accurate growth curves, which differ significantly from the previous theoretical estimates based on the cube root of foetal mass. We have used these to age 22 African elephant foetuses collected during culling operations. Pregnancy can be first recognized ultrasonographically by day 50, the presumptive yolk sac by about day 75 and the zonary placenta by about day 85. The trunk is first recognizable by days 85-90 and is distinct by day 104, while the first heartbeats are evident from around day 80. By combining ultrasonography and morphology, we have been able to produce the first reliable criteria for estimating gestational age and ontological development of Asian and African elephant foetuses during the first third of gestation.

Figure 1

(a) Foetal growth curves based on ultrasound measurements. The ultrasound data (SE1–19) show the relationship between true gestation age and crown–rump length (CRL). Crown–rump length (open square), biparietal diameter (open up triangle), thoracic diameter (open circle) and femur length (open down triangle) are plotted against foetal age. (b) Evaluation of existing models for the determination of foetal age. The foetal specimens (WB1–6 and EF1–16) have been aged using our formula (3.4) (solid line), the formulae by Huggett/Widdas (filled down triangle) and Craig for under 138 days (open up triangle) and Craig for over 140 days (filled up triangle), respectively.

Figure 2

Sonographic milestones. (a) Embryonic vesicle (Ev) at day 50. (b) An early embryo at day 74 of gestation. (c) Three-dimensional reconstruction of an embryo at 97 days of gestation with its yolk sac (Ys). The eyes (Ey) and the beak-like trunk (Tr) are clearly depicted. The placenta (Pl) is well developed. (d) Three-dimensional reconstruction of an early foetus of 102 days of gestation showing the physiological midgut herniation (Mh). The right ear (Ea), the typical trunk (Tr) and one fore limb (Fl) are easy to recognize. (e) At 108 days of gestation, the echogenic plexus choroideus (Pc) already fills most of the lateral ventricle. The trunk (Tr) is positioned between the fore limbs. (f) Characterization of foetal circulation at day 126 of gestation. The foetal heart (He), arteria vertebralis (Av) and umbilical vessels (Uv) are outlined by colour Doppler flow. (g) Lateral position of the foetus at 133 days of gestation. (h) In the later stages of pregnancy, here at day 303 of gestation, the allantoic pustules (AP) protrude into the allantoic cavity. Scale bars, 1 cm.

Figure 3

African savannah elephant embryo and foetuses. (a) EF1 (60 days of gestation). a, amnion; ba, branchial arches; fl, fore limb; h, heart; oe, optic evagination; s, somites; ta, tail; t, trunk. Scale bar, 0.25 cm. (b) EF4 (81 days of gestation). (c) EF5 (92 days of gestation). (d) EF6 (97 days of gestation). (e) Dorsal aspect of EF6 (100 days of gestation) showing the extent of neural tube development. (f) EF7 (103 days of gestation). (g) EF11 (150 days of gestation). (h) EF16 (167 days of gestation). Scale bars, 1 cm. Panel (a) from Gaeth et al. (1999).