A grey seal (Halichoerus grypus) pregnancy.
Keywords: grey, seal, pregnant, placenta, gonads
Halichoerus grypus.
General references:
Atkinson S. 1997. Reproductive biology of seals. Reviews of reproduction 2:175-194
Bones D.J. et al 1995. Does male harassment all females contribute to reproductive synchrony in the grey seal by affecting maternal performance? J. Behav Ecol Sociobiol. 36; 1-10.
Hewer H.R. and Backhouse 1968K.M. Embryology and fetal growth of the grey seal Halichoerus grypus. J. Zoo., London. 155; 507-533.
The grey seal
(link to image of live animal) is also known as the Atlantic grey seal or the Horsehead seal.
The total length from the tip of the nose to the tip of the hind pinnae of our specimen was approximately 52 cm. Using a published regression curve, this gave us
an estimated total gestational age of approximately 240 days or a placental gestational age (subtracting 100 days for diapause) of approximately 135 days. Our fetus weighed 2.17 kg. In one case, Hewer H.R. and Backhouse K.M. calculated a 2.5 kg fetus as having a placental gestation length of approximately 148 days. This correlates well with our estimate of active gestation in this case.
Remarkable features of this tract and the pregnancy were as follows:
The remarkably was short vagina, only seven or 8 cm long.
The external cervical os appeared to have a bilobed structure with a dorsal and ventral portion. This is referred to as a genital lock or the hymeneal folds. To this author (with experience in land mammals) it appeared to be a caudal portion of a very elongated cervical canal (15 cm caudal to cranial) because the area between the hymeneal folds and the uterine lumen was occluded by extremely viscous gel. The function of the hymeneal fold is not clear but because it contains smooth muscle cells is is thought to seal the penis within the vaginal during underwater breeding; the usual method of copulation in seals.
The external urethral orifice opened just caudal to the hymeneal fold, adding credibility to the idea that the hymeneal fold is analogous to the hymen in land mammals, because that is where the urethra enters the vagina in land mammals. This also means that there is no clear delineation between a vestibule and the cranial portion of the vagina.
The external urethral orifice was extremely difficult to locate at its outlet. It could only be delineated by catheterizing the bladder and passing a set of forceps caudally, into the urethra (as seen above) leading into the vagina.
The bladder itself was elongated, narrow and pointed at its most cranial extent (the pointed structure seen below).
The body of the uterus was very short, only about 3 cm caudal to cranial and the horns were long, giving the uterus a Y shape, similar to that of a domestic ruminant. In the image above,
a denotes the vestibule
, b, the tubular part of the tract between the hymeneal folds and the cervix itself,
c, the body of the uterus,
d, the "non-pregnant" horn and
e, the pregnant horn.
There was no obvious development of a middle uterine (or uterine) artery but
a thick band was present at the most cranial portion of the mesometrium, apparently part of the suspensory system for the uterus. One is left to speculate if an especially stable mesometrium is important in this species during pregnancy to prevent torsion during the twisting and diving motions of a seal that is hunting.
The pregnancy lay entirely in the right uterine horn,
supported by a corpus luteum in the right ovary. The left uterine horn was empty, not obviously involved in the pregnancy. The ovaries were visible in the non-dissected specimen i.e. they were
not totally enclosed in bursae like those of domestic bitches. The unopened uterus is seen below.
There was no obvious follicle development within the ovaries apart from a few follicles that were 1 to 2 mm in diameter (very small). This image shows an oocyte in a small follicle, raised on a cumulus oophorus, as is found in land mammals:
Interestingly, there were several obvious corpora albicanti in the ovaries. They are shown below, containing masses of coiled hyaline-like strands. This made them easy to identify; very different in appearance to corpora albicantiof domestic animals.
Corpora albicanti endure for long periods of time in the ovaries and are therefore used to distinguish between mature and immature captured females.
The gross anatomy of placentation was most similar to that of the domestic carnivores i.e. zonary in nature but the zone of placentation appeared to be proportionally wider (compared to the length of the fetus) than the zone in domestic carnivores.
The zonary placenta is obvious in the image below. Note that the amnion is still intact. The chorion has been ruptured to exposed the amnion and in doing so the allantois has been destroyed (the allantois lies in the space between the chorion and amnion). The three major intra-amniotic umbilical vessels (one vein and two arteries) split into four or five smaller vessels just after leaving the body wall of the fetus. This can be seen through the amnionic membrane in the image below. Many vessels traverse the space between the umbilical area of the amnion and the zonary placenta (the exocelom).
During normal birth, the allantochorion ruptures, releasing allantoic fluid. The amnion ruptures later. This is evident by viewing the image below, where the allantochorion (A-C) has ruptured but the head of the seal is still contained within the amnion.
On initial examination it appeared to the author as though the amnion would probably rupture early during the birth process in seals, preventing neonatal asphyxiation. This assumption was based on the short intra-amniotic umbilical cord (about 7 cm long) and the small exocelom i.e. the space between the umbilical portion of the chord and the zonary placenta. However, a video recording of a sea lion giving birth illustrated that the amnion could stretch for some distance and the placenta could detach suddenly, allowing the amnion to cover the fetal head in the immediate neonatal period. This may explain why fetal asphyxiation can indeed occur in pinnipeds. In attended zoo births therefore, manual rupturing of the amnion by an attendant may be important.
The fetus was in cranial longitudinal presentation with its anterior pinnae in shoulder flexion. In sea lions about 40% of pups are born in posterior presentation therefore posterior presentation may be consistent with normal birth in seals as well.
The image below shows the seal with the endometrial face of the zonary placenta exposed . The pink tissue on either pole of the zonary placenta is the allantochorion. The pale yellow tissue adjacent to the hind flippers is amnionic membrane.
This image below shows the histology of the placentation of the grey seal. This zonary placentation is extremely intimate and well vascularized like that of land carnivores. However it is impossible to delineate the maternal and fetal components in the absence of immunohistochemistry
As for domestic carnivores, the chorion distal to the zone of placentation on either pole of the zonary placenta was very loosely attached to the endometrium but as expected, the connection in the zonary placentation was very intimate and secure.
As for domestic carnivores, there was no distinct extra amnionic umbilical cord, only multiple vascular attachments to the inside of allantois in the zonary placenta. At this stage of developmet (~ 135 days of placental gestation) a large, cavernous remnant of the yolk sac was still present in the exocelom, once again reminiscent of the situation in domestic carnivores.
The image below shows that
the preputial opening of the fetus was very small indeed but concealed
a relatively thick, cavernous type of penis. In the mature male an os penis (baculum) is present. It was not yet evident in this fetus.
The ventral aspect of the penis did not appear to have an attached ventral frenulum and at least the most cranial portion was free from the prepuce, similar to the situation in a newborn foal (but not other domestic animals).
The testicles lay
subcutaneously within a vaginal tunic, oriented with the tail of the epididymis situated caudal, and slightly lateral to the head of the epididymis.
According to Hewer H.R. and Backhouse K.M., testicular descent had occurred in one fetus at approximately 100 days of gestation; after about a third of the duration of pregnancy. In our fetus (at approximately 135 days of gestation) testicular descent had also occurred, meaning that the testicles had descended through the inguinal canals into their normal subcutaneous locations. Sea lions and other Otoriid seals have scrotums but
in Phocid seals there is no scrotum.
The clearly define umbilical arteries are visible on either side of the bladder (being stretched by the glovedhand) and the lobulated kidneys in this species, remotely reminiscent of bovine kidneys but
unlike those of any domestic animal.
Notes on the grey seal
The grey seal has a lifespan of approximately 35 years. Mature bulls can weigh as much as 310 kg. By contrast, the cows are much smaller; weighing about two thirds the weight of males.
Breeding seasons vary but most breeding occurs in the fall and early winter i.e. these seals are
short day breeders. Reports of gestation length of vary between about 300 days and 365 days, meaning that the pups are born in the late fall to early winter as well. Data from Sable Island
in Nova Scotia suggests that pupping begins in early January and that after only three weeks of lactation, females are bred again. However, such short lactation is only true of Phocid seals i.e true seals with no pinnae. Otoriid seals with external pinnae such as sea lions, lactate for much longer, some for more than a year.
The pupping/birth site is traditionally referred to as a "
rookery". The average birth weight at about 350 days gestation in 74 pups was approximately 14.7 kg
After fertilization, development continues through to the blastocyst stage and at that point, development of the embryo virtually ceases i.e it enters
a state of diapause that last for about 100 days. Interestingly, there is no glandular development in the uterine wall during this time, despite the presence of a large vesicular corpus luteum (CL). At the end of embryonic diapause however, the corpus luteum does become larger, suggestion that activation is occurring. It is tempting to suggest that prolactin plays a role here (as it does in some cases of diapause) but that does not appear to be the case. At the time of reactivation, the uterus begins to undergo hyperplasia in the region of the embryo. Apparently this is only visible in primiparous seals, being obscured by enlargement from earlier pregnancies. After the blastocyst has enlarged considerably, the zona disappears and implantation begins.
The CL of pregnancy produces progesterone through gestation but the placenta does as well, so it is not clear if a seal pregnancy will abort after ovariectomy (as in the case in domestic carnivores, pigs and goats).
